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Open Access

Peer-reviewed

Research Article

Effects of Ready-to-Eat-Cereals on Key Nutritional and Health Outcomes: A Systematic Review

* E-mail: [email protected]

Affiliations University Medical Center Groningen, University of Groningen, Center for Medical Biomics, Groningen, The Netherlands, Nutrition Reviewed, Murnau, Germany

Affiliation Cereal Partners Worldwide, Lausanne 1008, Switzerland

• Marion G. Priebe, 
• Jolene R. McMonagle

• Published: October 17, 2016
• https://doi.org/10.1371/journal.pone.0164931
• Reader Comments

In many countries breakfast cereals are an important component of breakfast. This systematic review assesses the contribution of consumption of ready-to eat cereal (RTEC) to the recommended nutrient intake. Furthermore, the effects of RTEC consumption on key health parameters are investigated as well as health promoting properties of RTEC.

The Cochrane Central Register of Controlled Trials, MEDLINE, EMBASE and CINAHL have been searched up till 16 th of June 2015. Randomized controlled trials were excluded if RTEC were used during hypocaloric diets, if RTEC were eaten at other times than breakfast and if breakfasts included other products than RTEC, milk and fruit. Observational studies were excluded when “breakfast cereals” were not defined or their definition included cooked cereals. From cross-sectional studies only data concerning energy and nutrient intake as well as micronutrient status were used.

From 4727 identified citations 64 publications met the inclusion criteria of which 32 were cross-sectional studies, eight prospective studies and 24 randomized controlled trials. Consumption of RTEC is associated with a healthier dietary pattern, concerning intake of carbohydrates, dietary fiber, fat and micronutrients, however total sugar intake is higher. Persons consuming RTEC frequently (≥ 5 times/week) have a lower risk of inadequate micronutrient intake especially for vitamin A, calcium, folate, vitamin B 6, magnesium and zinc. Evidence from prospective studies suggests that whole grain RTEC may have beneficial effects on hypertension and type 2 diabetes. Consumption of RTEC with soluble fiber helps to reduce LDL cholesterol in hypercholesterolemic men and RTEC fortified with folate can reduce plasma homocysteine.

One of the review’s strengths is its thorough ex/inclusion of studies. Limitations are that results of observational studies were based on self-reported data and that many studies were funded by food-industry.

Consumption of RTEC, especially of fiber-rich or whole grain RTEC, is implicated with several beneficial nutritional and health outcomes. The effect on body weight, intestinal health and cognitive function needs further evaluation. Of concern is the higher total sugar intake associated with frequent RTEC consumption.

Citation: Priebe MG, McMonagle JR (2016) Effects of Ready-to-Eat-Cereals on Key Nutritional and Health Outcomes: A Systematic Review. PLoS ONE 11(10): e0164931. https://doi.org/10.1371/journal.pone.0164931

Editor: Jacobus van Wouwe, TNO, NETHERLANDS

Received: June 2, 2016; Accepted: October 4, 2016; Published: October 17, 2016

Copyright: © 2016 Priebe, McMonagle. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the paper and its Supporting Information files.

Funding: This systematic review was sponsored by Cereal Partners Worldwide, Lausanne 1008, Switzerland. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: JRM is an employee of Cereal Partners Worldwide, Lausanne 1008, Switzerland. MGP received payment from Cereal Partners Worldwide for conducting the systematic review. This does not alter our adherence to PLOS ONE policies on sharing data and materials.

Introduction

Extensive research has been shown that eating breakfast compared to skipping breakfast results in improved macro- and micro-nutrient intake and status [ 1 ], can reduce the risk of weight gain [ 2 ] and has beneficial effects on cognitive and academic performance [ 1 ; 3 ] and development of diseases such as type 2 diabetes [ 4 ] and cardiovascular diseases [ 5 ; 6 ]. In many countries breakfast cereals (BC) are considered the main component of a balanced breakfast. A considerable number of studies are conducted to investigate the impact of the consumption of BC on nutritional and health benefits [ 7 – 12 ]. In addition, several reviews summarize their effects on either specific health outcomes [ 13 ; 14 ] or comprehensively on nutritional and health benefits [ 15 ]. The group of BC comprises many different cereal products and can be divided roughly into cooked cereals, like porridge type breakfasts, and ready-to-eat cereals (RTEC) or “cold” breakfast cereals like corn flakes and muesli. It is obvious that nutritional and health benefits depend on the composition of the breakfast meal. Many observational studies do not differentiate between RTEC and cooked cereals and in intervention trials BC are often either only part of breakfast or consumed not only for breakfast. To obtain more specifically information on nutritional and health benefits of cereals consumed at breakfast it is necessary to consider the specific composition of BC while summarizing and evaluating the available evidence. Therefore, in this systematic review, studies are included that investigate the effect of RTEC only and an attempt is made to relate their specific composition to specific health benefits.

Two questions are addressed:

• To what extent does consumption of RTEC contribute to the recommended nutrient intake of children, adolescents and adults?
• What are the effects of RTEC consumption on key health parameters in healthy persons as well as in persons at risk of disease and what are health promoting properties of RTEC?

Data from all available observational cohort studies and (randomized) controlled trials (RCTs) have been systematically reviewed and summarized. “Key health parameters” assessed were outcomes related to energy metabolism, weight management, cardiovascular health, digestion/gut health, immune function, performance, bone growth and development. RCTs compared either the health effect of consuming different amounts of RTEC or different types of RTEC (e.g. high- vs low-fiber RTEC). Data from cross-sectional studies have not been considered for assessing the effect on health parameters due to their limited strength of evidence.

A protocol of this systematic review is available as supporting information ( S1 Protocol ). The Preferred Reporting Items for Systematic reviews and Meta-Analyses (PRISMA) and the guidelines for the Meta-analysis of Observational Studies in Epidemiology (MOOSE) were followed [ 16 ; 17 ]. The PRISMA and MOOSE checklists are available as supporting information ( S1 and S2 Checklists). Due to the low number and the diversity of the studies addressing one specific health outcome a meta-analysis was not carried out.

Data sources and literature search

The Cochrane Central Register of Controlled Trials, MEDLINE, EMBASE and CINAHL have been searched with no time limit and no language restriction on 26 th of February 2014 by MGP (investigator). The following MEDLINE search strategy has been used and adapted for the other electronic databases searched: 1) Breakfast OR fortified OR ready-to-eat, 2) Cereal OR cereals, 3) 1 AND 2. No specific search items have been used for nutritional and health outcomes as we aimed for a wide range. The search was updated with the identical search-strategy on 16 th of June 2015. In addition, the reference lists of all included studies and of review articles have been searched in order to identify additional studies of interest. The title and abstract of each record of the search have been assessed by two reviewers (MGP, JRM) independently. Studies have been rejected if the article, based on the abstract, definitely did not meet the review's inclusion criteria, otherwise the full text of the study has been obtained and screened. Abstracts for which no full text papers were available were excluded. Differences between reviewers' results have been resolved by discussion. Studies were included if they were RCTs or prospective studies and if they assessed energy and nutrient intake or outcomes related to energy metabolism, weight management, cardiovascular health, digestion/gut health, immune function, performance, bone growth and development. Cross-sectional studies were included if they assessed energy intake, nutrient intake and micronutrient status. RTEC were defined as “a cereal food that is processed to the point where it can be eaten without further preparation, as in boxed cereals”, thus cold cereals were defined to be RTEC. RCTs were excluded if they assessed breakfast skippers vs breakfast eaters, if RTEC were used as meal replacer or during hypocaloric diets, if RTEC were eaten at other times than breakfast, if breakfasts included other products than RTEC, milk and fruit and if breakfasts differed in carbohydrate content in studies comparing postprandial blood glucose and/or insulin. Observational studies were excluded when “breakfast cereals” were not defined or the definition of “breakfast cereals” included cooked cereals. From cross-sectional studies only data concerning energy and nutrient intake as well as micronutrient status were used.

Data extraction process and assessment of risk of bias

From original reports of the studies data were extracted by one reviewer (MGP) according to pre-designed extraction forms which were validated and used already in a similar systematic review [ 18 ]. From RCTs the following data were extracted:

• General information: title, authors, country, year of publication, funding, duplicate publication;
• Trial characteristics: design, duration, randomizations, concealment of allocation, blinding, checking of blinding;
• Intervention: length of intervention, dietary advice/diet provided, comparison interventions;
• Participants: population, exclusion criteria, number (total, per compared groups), age, gender, health condition; diagnostic criteria used to define health condition, similarity groups at baseline, assessment of compliance, withdrawals/losses to follow-up;
• Outcomes: outcomes specified above (primary and secondary outcomes of the studies);
• Results: for outcomes and times of assessment (including a measure of variation), intention-to-treat analyses.

The following data were extracted from cohort studies:

• General information: title, authors, country, year of publication, duplicate publication;
• Study characteristics: design, dates of enrolment, follow-up;
• Exposure: type, type of measurement, validation of measurement, time-points measurements;
• Outcome: type, criteria used, type of measurement, validation of measurement;
• Participants: number, characteristics;
• Results: total number of cases, cases in group with lowest and highest intake, results of outcome, confounders adjusted for.

Risk of bias of RCTs and the methodological quality of prospective and cross-sectional studies were evaluated by one reviewer (MGP). The Cochrane Collaboration’s tool for assessing risk of bias [ 19 ] was used for the appraisal of RCTs. The following seven items were assessed and rated as “low”, “high” or “unclear risk” of bias: random sequence generation, allocation concealment, blinding participants and personnel, blinding of outcome assessment, incomplete outcome data, selective reporting and other bias. As “other bias” the appropriateness and methodology (washout period, analysis) of the cross-over design in cross-over studies was examined. For the assessment of the quality of observational studies the following criteria were examined [ 18 ]: methods for selecting study participants, number of appropriate confounders investigated and adjusted for; quality of method used to assess dietary intake, e.g. food frequency questionnaire with/without validation, quality of method used to assess outcome measures: e.g. self-report with/without validation, or direct measurement/medical records and additional for prospective studies: duration/completeness of follow-up.

Description of studies

The results of the literature search and the progress through the different stages of the review process are depicted in the PRISMA flow diagram ( Fig 1 ). A total of 64 publications (all published in English) met the inclusion criteria, of which 32 were cross-sectional studies [ 7 ; 9 ; 20 – 49 ], eight prospective studies [ 8 ; 50 – 56 ] and 24 RCTs [ 10 – 12 ; 57 – 77 ].

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https://doi.org/10.1371/journal.pone.0164931.g001

Characteristics of cross-sectional studies are presented in Table 1 , those of prospective studies in Table 2 and those of RCTs in Table 3 . The impact of RTEC consumption on nutrient intake was addressed in all cross-sectional studies as well as in three prospective studies (cross-sectional at baseline [ 51 ; 53 ] and prospectively [ 51 ]) and one RCT [ 11 ]. All RCTs and prospective studies assessed health parameters, which were risk factors for cardiovascular disease [ 10 ; 11 ; 52 ; 54 ; 56 ; 58 ; 62 ; 66 ; 68 ; 69 ; 71 ; 72 ; 77 ] and type 2 diabetes [ 50 ; 55 ; 59 ; 60 ; 64 ; 67 ; 70 ; 74 ], BMI/body weight/satiety/food intake [ 8 ; 11 ; 12 ; 51 ; 54 ; 57 ; 59 – 62 ; 65 ; 73 ; 76 ], digestion/gut health [ 10 ; 58 ; 69 ] and cognitive performance [ 53 ; 63 ; 75 ]. No publications were found assessing immune function and bone growth and development. The risk of bias for all individual RTCs is depicted in Fig 2 . Overall the RCTs had a low or unclear risk of bias. Based on the items assessed, all selected observational studies have been judged to be of appropriate methodological quality. As many studies (45 studies, Tables 1 – 3 ) were funded by food industry, funding is also reported together with the results.

Green (+) indicates low risk of bias; Red (-) indicates high risk of bias; and Yellow (?) indicates unclear risk of bias. NA: not applicable, * for cross-over studies only.

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https://doi.org/10.1371/journal.pone.0164931.t001

https://doi.org/10.1371/journal.pone.0164931.t002

https://doi.org/10.1371/journal.pone.0164931.t003

Nutritional benefits—associations and effects of interventions

One prospective [ 54 ] and 31 cross-sectional studies in different countries (15 in the USA [ 7 ; 23 ; 25 ; 27 – 29 ; 31 ; 32 ; 34 ; 36 ; 42 – 44 ; 47 ; 48 ], three in Canada [ 22 ; 24 ; 46 ], two each in Spain [ 33 ; 41 ], Ireland [ 37 ; 39 ], Australia [ 26 ; 45 ] and France [ 9 ; 38 ] and one each in Scotland [ 40 ], Cyprus [ 20 ], Greece [ 35 ], Malaysia [ 21 ] and Guatemala [ 30 ]) investigated the association between RTEC consumption and daily nutrient intake. From two prospective studies [ 51 ; 53 ] baseline data concerning RTEC consumption and daily nutrient intake were also used. One cross-sectional study assessed the impact of RTEC consumption on micronutrient status only [ 49 ].

23 studies included only children/adolescents [ 7 ; 20 – 23 ; 26 ; 27 ; 29 – 31 ; 35 ; 36 ; 38 – 41 ; 43 – 45 ; 47 – 49 ; 51 ], eight studies only adults [ 9 ; 24 ; 25 ; 28 ; 34 ; 37 ; 38 ; 53 ], one study children and adults [ 42 ] and in three studies the age-range comprised children/adolescents and adults [ 32 ; 33 ; 46 ] (categorized in “adult” studies). In cross-sectional studies frequency of RTEC consumption was mainly assessed with single and repeated 24-h dietary recalls ([ 20 – 24 ; 27 – 35 ; 42 ; 44 ; 47 ; 49 ] and [ 9 ; 26 ; 45 ] respectively) ( Table 1 ). In addition, food diaries of 14 [ 7 ; 25 ; 36 ], 7 [ 37 ; 43 ; 46 ] and 3 days [ 78 ] as well as 5 –and 7 day weighted food records were used [ 40 ; 41 ]. Two studies applied the dietary history method [ 38 ; 39 ]. Due to the variation in registration of food intake, comparisons of high or low frequency of RTEC consumption in these studies varies from 1 serving/day vs none to 7/14 day vs < 2/14 days. RTEC consumption at breakfast only was monitored in 20 studies [ 20 – 24 ; 26 ; 28 ; 29 ; 31 ; 32 ; 34 ; 38 ; 40 ; 41 ; 43 ; 45 ; 47 ; 48 ; 51 ; 54 ]. RTEC consumption during the whole day was assessed in 14 studies of which in four it was demonstrated that most of the RTEC were consumed at breakfast (Ireland: 91% [ 37 ], Spain: 67% [ 33 ], France: 89% [ 9 ], Guatemala: 93.2% [ 30 ]) and in three studies that a high percentage of the population was eating RTEC at breakfast (USA: 63% of 10 y olds and 65% of young adults [ 42 ] and 87,3% of 4–12 y old children [ 44 ], Greece: 60% of boys and 58% of girls [ 35 ]). As RTEC, based on these numbers, are predominately eaten at breakfast, all the studies were included. One RCT in adults examined the impact of substituting a traditional breakfast by RTEC on daily macronutrient consumption [ 11 ].

Associations of RTEC consumption with daily intake of energy, macronutrients, cholesterol, dietary fiber (DF) and sodium.

For summarizing cross-sectional data about the association between RTEC consumption and daily intake of energy, macronutrients, cholesterol, DF and sodium in children/adolescents, 33 data sets from 24 studies were available. More data sets per study were available when the investigators reported their results per sex and/or in several age groups ( S1 Table and Table 4 ). 18 of these studies were (in part) funded by food industry. Higher frequency (approximately ≥ 5 serving/week) of RTEC consumption in children/adolescents was associated with higher intake of DF, carbohydrates and total sugars in 75%, 65% and 63% of the data sets respectively and with lower intake of cholesterol and fat, expressed as total amount and as energy percentage in 83%, 50%, and 60% of the data sets respectively. Energy, saturated fat, sodium and protein intake was not associated with RTEC consumption in most data sets (in 77%, 75%, 81% and 86% respectively). Associations were similar in the 6 studies (9 data sets) [ 20 ; 21 ; 41 ; 43 ; 48 ; 51 ] with no food-industry related funding, except that total amount of fat was only reduced in 22% of the 9 data sets and dietary fiber intake was only higher in 25% of the 4 data sets in which it was measured. In the other data sets (78% and 75%) no difference of fat and dietary fiber intake was reported.

https://doi.org/10.1371/journal.pone.0164931.t004

For summarizing the results in adults 16 data sets from 12 studies were available ( S1 Table and Table 4 ). One of these studies [ 28 ] received no food-industry related funding. Higher frequency (approximately ≥ 5 serving/week) of RTEC consumption in adults was associated with higher intake of DF, carbohydrates and total sugars in 93%, 100% and 100% of the data sets respectively and lower intake of fat expressed as energy percentage (in 100% of data sets) but not if expressed as total amount. The associations of RTEC consumption with saturated fat and cholesterol intake were not consistent, whereas most data sets (62%) did not show an association with energy and protein intake.

One study (funded by food industry) investigated the association between RTEC consumption and daily intake of energy, macronutrients, cholesterol, DF and sodium prospectively [ 54 ] ( Table 2 ). In secondary analyses of a RCT, 8–10 y old children were followed for 7.5 y Higher frequency (3 vs 0 serving/3 days) of RTEC consumption at breakfast was associated in girls and boys with a higher percentage of energy intake from carbohydrates and protein as well as a lower percentage from total and saturated fats. In addition, an association with higher intake of DF and lower intake of cholesterol was found whereas energy and sodium intake was not related. For boys, but not for girls, RTEC consumption was associated with higher intake of total sugars.

Associations of RTEC consumption with the percentage of populations receiving inadequate amounts of vitamins and minerals.

17 studies (of which one [ 20 ] was not funded by food industry) investigated the association of frequency of RTEC consumption with the proportion of the population receiving inadequate vitamins and minerals, of which ten studies were conducted in children/adolescents [ 7 ; 20 ; 22 ; 23 ; 26 ; 27 ; 36 ; 39 ; 44 ; 47 ], five studies in adults [ 24 ; 25 ; 33 ; 37 ; 46 ] and two in both categories [ 32 ; 42 ] ( Table 1 ).

Inadequate micronutrient intake was defined as “below the estimated average requirement (EAR)” in ten studies [ 22 – 25 ; 27 ; 32 ; 36 ; 37 ; 44 ; 46 ], as “receiving less than two-thirds of the recommended dietary allowance (RDA)” in three studies [ 20 ; 33 ; 42 ] and as “consuming less than 100% of RDA, “consuming less than 80% of RDA”, “probability of not achieving 100% of EAR “and “percentage who did not achieve LRNI” in one study each [ 7 ; 26 ; 39 ; 47 ]. The EAR is defined as the intake adequate for 50% of the population, the RDA is the average daily dietary intake level that is sufficient to meet the nutrient requirement of nearly all (97 to 98 percent) healthy individuals and the LRNI is the amount estimated to meet the needs of 2.5% of the population with the lowest requirements.

The prevalence of inadequate vitamin and mineral intake by breakfast group (lowest vs highest RTEC consumption) for 14 micronutrients is given in S2 Table . 19 data sets were available for children/adolescents and 11 for adults. In 15 data sets it was assessed whether the prevalence of inadequacy between low and high RTEC consumers is significantly different.

Combining these results, significant reductions of prevalence of inadequacy associated with RTEC consumption were observed for all vitamins and minerals. Prevalence of inadequacy as well as magnitude of reduction varied depending on country, age group, sex and method of assessment ( S2 Table ).

To assess the nutrients for which the prevalence of inadequacy was reduced the most, those nutrients were scored which had the four highest reductions of inadequacy. In case that an equal percentage of reduction was observed for more micronutrients, all micronutrients were scored, thus more micronutrients per reduction level were possible ( S2 Table ). To reduce imbalance due to limited assessment of micronutrients, data of studies were excluded which reported less than eight micronutrients, resulting in 11 data sets for children and eight for adults. The scored micronutrients of different populations were then combined: data of adults in which significance was assessed (7 data sets), data of children in which significance was assessed (6 data sets), all adult and all children/adolescent data sets.

When using only data sets that assessed significance, in children/adolescents as well as in adults, reductions of prevalence of inadequacy due to RTEC consumption were highest for vitamin A (range: 7–21% and 5–37% respectively), calcium (17–39% and 6–40% respectively), folate (5–28% and 7–50% respectively), magnesium (7–11% and 4–26% respectively) and zinc (9% and 19–37% respectively). In adults, high reductions were also seen for vitamin B 6 (7–55%) and C (6–21%).

When combining all data sets, for children/adolescents as well as for adults consistently the greatest reductions of prevalence of inadequacy was observed for vitamin A (range: 7–28% and 5–37% respectively), calcium (17–39% and 6–43% respectively), folate (5–50% and 7–50% respectively), vitamin B 6 (31–37% and 7–55% respectively), magnesium (7–11% and 4–26% respectively) and zinc (9–15% and 19–37% respectively).

Associations of RTEC consumption with micronutrient status.

In two cross-sectional studies (of which one was funded by food industry [ 38 ]) micronutrient status (12 vitamins and minerals) was measured in populations with and without RTEC consumption [ 38 ; 41 ] ( Table 1 ). In Spanish and/or French children and adolescents consumption of RTEC was associated with higher plasma concentrations of vitamin A (0.10 μmol/l [ 41 ]), β-carotene (0.21 μmol/l [ 38 ]), serum folate (4.1 nmol/l [ 41 ]) and lower erythrocyte glutathione reductase (EGR, 0.07 [ 38 ; 41 ]) which indicates a better riboflavin status. In Spanish adults, a better thiamine and riboflavin status (erythrocyte transketolase 0.03, EGR 0.06) as well as higher β-carotene (0.25 μmol/l) and serum folate concentrations (30 μg/l) were found in the RTEC group [ 38 ].

Another study (no industrial funding) investigated the contribution of consumption of folic-acid enriched RTEC to folate and vitamin B 12 status in US children and adolescents [ 49 ] ( Table 1 ). Higher folate and vitamin B 12 concentrations were associated with consumption of enriched RTEC. However, only a very low percentage of this population (< 0.5%) had folate deficiency or low vitamin B-12 status, probably due to consumption of other grain products which are mandatory enriched with folate since 1996. The percentage of persons with marginally low folate and vitamin B-12 status decreased from 3.4% to 1.7% and from 9.6 to 6.6% respectively [ 49 ] due to additional consumption of RTEC.

The effect of RTEC consumption on macronutrient and DF intake.

In healthy adults substituting the habitual breakfast with RTEC (60 g for women/80 g for men) resulted in a higher percentage of energy from carbohydrates and a lower percentage from total and saturated fat [ 11 ] ( Table 3 ) in this study funded by food industry. Intake of energy, protein and cholesterol stayed the same. No effect on DF intake was observed, but the RTEC administered were relatively low in DF, providing 3 and 4 g DF/day for women and men respectively.

Health benefits—associations and effects of interventions

Associations of rtec consumption with risk factors for cardiovascular diseases..

One prospective study investigated the association of consumption of whole grain vs refined grain RTEC with incident heart failure in a large cohort of male physicians [ 56 ] ( Table 2 ). Decreased risk of heart failure was found for frequent consumers of whole grain RTEC (HR: 0.78 (95% CI 0.64–0.96) for 2–6 servings/wk; HR: 0.72 (95% CI 0.55–0.88) for ≥ 7 servings/wk) but not for those consuming refined RTEC.

Another prospective study investigated the association of consumption of whole grain vs refined grain RTEC with incident hypertension in a large cohort of male physicians [ 52 ] ( Table 2 ). Decreased risk of hypertension was clearly demonstrated for participants with a high consumption of whole grain RTEC (HR: 0.87 (0.81–0.94) for 2–6 servings/wk, HR: 0.80 (0.74–0.86) for ≥ 7 servings/wk), whereas the associations with consumption of refined RTEC was weak and not significant in all groups (HR: 0.86 (95% CI 0.76–0.98) for 2–6 servings/wk, HR: 0.86 (95% CI0.74–1.00) for ≥ 7 servings/wk).

One prospective study [ 54 ] ( Table 2 ) investigated the association between low and high RTEC consumption (0 vs 3 servings/3 days) on blood lipids in a group of 660 children, aged 8–10 years at baseline and with serum LDL cholesterol levels between the 80th and the 98th percentile for sex and age. In the high RTEC group total cholesterol was lower in boys (0.10 mmol/l) but not in girls. LDL cholesterol was lower in boys (0.07 mmol/l) but in girls lower HDL cholesterol (0.05 mmol/l) was observed.

The two prospective studies reporting decreased risk of heart failure and hypertension were not funded by food industry [ 56 ; 52 ], whereas the last described prospective study [ 54 ] which was funded by food industry showed mixed results on blood lipids in children.

Effects of RTEC consumption on risk factors for cardiovascular diseases.

Two RCTs, one in children (overweight or at risk of overweight 6- to 12-year-old Mexican children [ 62 ]) and one in Finnish adults [ 11 ] investigated whether increased consumption of RTEC results in a reduction of blood lipids ( Table 3 ).

Twelve weeks of RTEC consumption (≈ 33 g, different corn and rice based types) resulted in an increase in HDL concentrations (as compared to baseline and the control group) when combined with nutritional education [ 62 ] in children. The changes of other lipid parameters, however, were not different.

In adults with serum cholesterol concentrations above 5.0 mmol/l, six weeks of consumption of RTEC (60 g for women/80 g for men) mainly in the morning instead of the habitual Finnish breakfast resulted in a reduction in total cholesterol by 2.5% (0.16 mmol/l) which was partly due to a reduction in HDL cholesterol (LDL was not measured) [ 11 ]. Intake of saturated fat and total fat was decreased by 2.5 and 5.5 energy% respectively.

Both studies were (partially) funded by the food industry and showed mixed results on the parameters investigated.

The effect of RTEC enriched with different types of DF on blood lipids was investigated in five RCTs [ 10 ; 58 ; 69 ; 71 ; 72 ] ( Table 3 ).

Six week consumption of DF-enriched RTEC providing 5.8 or 11.9 g soluble fiber/day consistently lowered total cholesterol and LDL (by 5.9 or 3,5% and 5.7 or 5.7% respectively) in persons with hypercholesterolemia consuming a low-fat diet [ 71 ; 72 ]. The effective soluble fiber was mainly derived from psyllium whereas soluble fiber from pectin [ 72 ] or wheat bran [ 71 ] did not have a significant cholesterol lowering effect.

Three other, more short-term (3–4 wk), RCTs in healthy volunteers [ 10 ; 58 ; 69 ] investigated the effect of RTEC rich in various DF (inulin-enriched vs inulin-free, whole grain wheat vs wheat bran-based, whole grain maize vs refined maize) on various lipid parameters. No effect on total and HDL cholesterol was found, only the inulin-enriched RTEC (9 g inulin/day) was able to reduce LDL cholesterol compared to baseline (by 0.35 mmol/l, 8.3%) but not to control. However, concentrations of triacylglycerols were reduced compared to baseline and to control (by 0.23 mmol/l, 27.4%) [ 69 ].

Four RCTS were industrial funded, of which two [ 71 ; 72 ] showed positive effects on blood lipids and two no effects [ 10 ; 58 ]. Another RCT [ 69 ], without industrial funding, showed mixed effects.

Three RCTs [ 66 ; 68 ; 77 ] investigated the effect of folate-fortified RTEC on plasma homocysteine (tHcy) ( Table 3 ). It was found that cereals fortified with 200 μg per portion could increase plasma folate concentrations by about 12 nmol/l and lower tHcy by about 1 μmol/l in populations selected based on high plasma tHcy concentrations (≥ 10 μmol/l, [ 68 ]) or not consuming vitamin supplements and RTEC [ 77 ]. Consumption of RTEC with 200 μg folate in combination with other vitamins did not result in different effects [ 77 ]. Homocysteine lowering effects were most effective in subjects with lowest plasma folate concentrations and highest baseline tHcy (tHcy reduction- 1.58 μmol/l and -1.87 μmol/l respectively) [ 77 ]. Venn et al [ 68 ] also tested fortification with 100 and 300 μg folate/portion and found similar tHcy results, concluding that 100 μg folate would be sufficient in population with ≥ 10 μmol /l plasma tHcy. Consumption of RTEC enriched with 440 μg folate in combination with RDA amounts of vitamin B 6 and B 12/portion resulted in small differences in plasma folate (7,5 nmol/l) and homocysteine (-0.4 μmol/l) in a population with in general already relatively high baseline folate and low homocysteine concentrations [ 66 ]. In addition, the reduction of the percentage of persons with high homocysteine (>10.4 μmol/l for women or 11.4 μmol/l for men) was greater in the supplemented group (13% to 3.2%) compared to the control group (10.4% to 7.3%). All three RCTs were funded by industry and showed a positive effect of the intervention.

Associations of RTEC consumption with BMI/weight gain.

One prospective study in adults demonstrated that men consuming at least one portion of RTEC/day gained on average 0.59 and 0.46 kg less body weight after 8 and 13 years respectively than men consuming RTEC rarely [ 8 ] ( Table 2 ). They also had a decreased risk of 22% and 12% to become overweight during 8 and 13 years of follow-up. Associations were also examined for whole grain and refined grain RTEC intake separately but these were not different.

Two prospective studies investigated the relationship between consumption of RTEC and BMI in children with a follow up of 7.5 [ 54 ] and 3 years [ 51 ] ( Table 2 ). Both studies were secondary analyses of RCTs with 8–10 year old children including either both intervention groups [ 54 ] or the control group only [ 51 ]. Lower BMI was associated with more frequent RTEC consumption in both sexes in low-income minority children in one study [ 51 ] (every day of RTEC consumption decreased BMI by 2 percentiles), but only in boys in the other (BMI 20.4 vs 20.1, 0–3 times RTEC/week respectively) [ 54 ].

Negative associations of frequent RTEC consumption with body weight gain were found in all three RCTs, two of which [ 8 ; 54 ] were funded by food industry.

Effects of RTEC consumption on body weight, satiety and food intake.

Two RCTs, one in children (overweight or at risk of overweight [ 62 ]) and one in adults [ 11 ] investigated whether increase of consumption of RTEC results in a reduction in body weight ( Table 3 ). Twelve weeks of RTEC consumption (≈ 33 g, different corn and rice based types) in combination with nutritional education not only prevented the weight gain observed in the other groups but it decreased weight (mean -1.01 kg) and body fat gain (0.8%) [ 62 ]. As these changes were different to that observed after the RTEC intervention without nutritional education, it can be assumed that nutritional education is responsible for this positive effect.

In adults, six weeks of consumption of RTEC (60 g for women/80 g for men) mainly in the morning instead of the habitual Finnish breakfast did not result in change in body weight (secondary objective) [ 11 ].

Both RCTs were funded by food industry and showed no effect of RTEC consumption (alone) on body weight reduction.

Seven RCTs [ 12 ; 57 ; 59 ; 61 ; 65 ; 73 ; 76 ] examined the effect of low DF vs high DF RTEC and/or wholemeal RTEC [ 65 ] on postprandial satiety and five of them also on subsequent energy intake [ 12 ; 57 ; 59 ; 61 ; 73 ] ( Table 3 ). The amount of DF administered with the high DF RTEC varied between 2.3 g and 33 g whereas the control RTEC contained 0–4 g. The types of DF were wheat bran [ 12 ; 61 ; 65 ; 73 ], b-glucan [ 59 ; 76 ] and 2 types of arabinoxylans (AX): hydrolysed wheat bran AX and unhydrolysed flax AX [ 57 ]. Visual analog scales were applied in most studies to measure satiety and/or appetite and a questionnaire in one trial [ 73 ]. Three trials reported a significant difference in satiety/appetite measures. The degree of hunger was lower after ingestion of high versus low DF RTEC [ 73 ]. Furthermore, the average appetite score was highest after the high bran RTEC [ 12 ] and the ß-glucan RTECs resulted in a lower combined appetite score independent from dose [ 59 ].

Positive effects on satiety/appetite measured were found in two industrial funded [ 12 ; 59 ] and one not industrial funded RCT [ 73 ]. No effects were found in three industrial funded RCTs [ 57 ; 61 ; 76 ] and one RCT without industrial funding [ 65 ].

In two trials [ 12 ; 61 ] it was found that a large portion of RTEC (71 and 60 g) containing 33 and 28 g of mainly insoluble wheat fiber can reduce subsequent energy intake ( Table 3 ). After breakfasts providing the same energy, food intake at an early subsequent meal (75 min) was reduced by 160 kcal [ 12 ]. In the other trial the lower caloric value of the high DF RTEC was not compensated at lunch (3 h later) resulting in lower cumulative energy intake (93 kcal) [ 61 ]. In another trial [ 73 ] two experiments were conducted with RTEC containing different amounts of wheat bran. In the first experiment a significant difference in cumulative (breakfast and lunch 3.5 h later) energy intake (≈ 140 kcal) was found after the RTECs with the highest (22 and 20 g) compared to that with the lowest DF content (0 g). In the second experiment comparing the RTEC with the lowest and highest amount of DF, a decrease of energy intake at lunch and of cumulative energy intake was observed after the high DF RTEC (≈ 100 and 200 kcal respectively). In a trial with overweight women consumption of RTEC enriched with 15 g AX (19 g total DF) did not result in decreased energy intake at lunch (4 h later) nor decreased cumulative energy intake compared to the low DF RTECs (4 and 3 g DF) [ 57 ]. In addition, RTEC enriched with a low amount of β-glucan (2.3–5.9 g) did not result in lower energy intake at lunch (4 h later) in overweight persons [ 59 ].

Positive effects of consumption of fiber-rich RTEC on subsequent food intake were found in two RCTs [ 12 ; 61 ] funded by food industry and one RCT without industry-related funding [ 73 ], whereas the other two funded RCTs [ 57 ; 59 ] showed no effect. One RCT (industry funded) investigated the effect of modifying the processing procedure of wheat flakes (sour-dough prefermentation, steam cooking omission, reduction sucrose content) on satiety. Modified wheat flakes successfully reduced hunger feelings at 120, 150 and 180 min after ingestion compared to conventionally produced wheat flakes and white wheat bread [ 60 ] ( Table 3 ). The test meals had similar energy content and differed slightly in macronutrient and DF composition.

Associations of RTEC consumption with development of type 2 diabetes.

One prospective study investigated the association between RTEC (cold breakfast cereals) consumption and incident diabetes in male physicians [ 55 ] ( Table 2 ). Decreased risk of diabetes was clearly demonstrated for participants with a high consumption of whole grain RTEC (HR: 0.76 (95% CI 0.66–0.87) for 2–6 servings/wk, HR: 0.60 (95% CI 0.50–0.71) for ≥ 7 servings/wk), whereas the associations with consumption of refined RTEC were not significant in all groups (HR: 0.69 (95% CI 0.53–0.90) for 2–6 servings/wk, HR: 0.95 (95% CI 0.73–1.3) for ≥ 7 servings/wk) [ 55 ].

Another prospective study investigated the association between consumption of whole grain foods and incident diabetes in women [ 50 ] ( Table 2 ). Analyses of HR of specific whole grain foods showed decrease risk of diabetes for high consumption of whole grain breakfast cereals ((HR: 0.71 (95% CI 0.62–0.82) for 5–6 servings/week and HR: 0.66 (95% CI 0.55–0.80) for ≥ 1/day).

Both these prospective studies showing associations between high consumption of whole grain RTEC and decreased risk of diabetes were not industry funded.

Effects of RTEC consumption on risk factors for type 2 diabetes.

Two RCTs examined to what extent postprandial insulinemia is changed in response to RTEC with different content of DF and different GI [ 64 ; 74 ] ( Table 3 ). 136 g whole grain wheat RTEC enriched with corn bran (GI: 49, 50 g available carbohydrates, 63.5 g DF) compared to 60 g low DF RTEC (GI: 125, 50 g available carbohydrates, 2 g DF) consumed with water reduced postprandial the 2h-AUC of insulin by 50% in healthy volunteers [ 64 ]. Half the portion of those RTEC was administered with milk in the other trial in which 2h-AUC of insulin was only decreased (by 14%) in volunteers with high fasting insulin but not in those with normal insulin values [ 74 ]. Both those industrial funded RCTs found positive effects of fiber-rich RTEC on postprandial insulinemia.

Two RCTs investigated whether addition of soluble fiber to RTEC with the same carbohydrate content results in decreased postprandial glucose and insulin responses [ 59 ; 70 ] ( Table 3 ). In overweight volunteers, corn based RTEC with 4–6 g oat β-glucan did not reduce blood glucose but only decreased the 2h-AUC insulin by 14–17% compared to RTEC without β-glucan [ 59 ]. In healthy volunteers, however, addition of 4.5 g soluble fiber from guar gum to wheat RTEC decreased both the 2 h- AUC glucose and insulin by 47% and 34% respectively compared to control [ 70 ]. The industry funded RCT [ 59 ] found mixed results of consumption of RTEC rich in soluble fiber on postprandial glucose and insulin, whereas the RCT without industry-related funding [ 70 ] found reduction of both parameters.

One RCT (food-industry funded) investigated the effect of modified processing of wheat flakes (sourdough pre-fermentation, suppressing steam cooking) and reduced sucrose content on GI and insulinemic index (reference food was white wheat bread) [ 60 ] ( Table 3 ). The GI of modified whole wheat flakes and standard whole wheat flakes was not different. However, the 90 min and 180 min insulinemic index of the modified flakes was decreased by 20 and 12% respectively.

Another RCT (food-industry funded) investigated whether the low GI of a DF-rich RTEC is caused by a slower rate of appearance of starch-derived glucose (Ra gluc , reflecting starch digestion) or a higher glucose uptake from the blood by tissues (Rd gluc ) [ 67 ] ( Table 3 ). The Ra gluc of the high GI RTEC and low GI RTEC was not different. However, the Rd gluc at 30–60 min was 31% higher after the low GI RTEC which was associated with a 125% higher 0–30 min insulin response. It was hypothesized that the higher protein content of the low GI RTEC (11 g) contributed to the higher insulin response and thereby increased Rd gluc which could explain the low GI despite the same rate of starch digestion.

Effect of RTEC consumption on the composition of the colonic microbiota and on bowel function.

One RCT (without industry-related funding) investigated the effect of 4-wk consumption of inulin-rich (9 g inulin/day) compared to inulin-free RTEC on the composition of the microbiota using selective growth media [ 69 ] ( Table 3 ). It was found that the amount of bifidobacteria was higher after the inulin-rich RTEC compared to control, but only after correction for total anaerobes.

Two RCTs (food-industry funded) investigated the effect of 3-wk consumption of one portion whole grain RTEC/day on the composition of the microbiota with fluorescence in situ hybridization [ 10 ; 58 ] ( Table 3 ). One trial compared whole wheat RTEC (48 g, 5.7 g DF) to a wheat- bran based RTEC (48 g, 13 g DF) [ 10 ], whereas the other compared whole grain maize RTEC (48 g, 7 g DF) to refined maize RTEC (48 g, 0.4 g DF) [ 58 ]. In both trials, only whole grain RTEC consumption increased the amount of Bifidobacterium spp. compared to baseline. The increase in Bifidobacterium spp compared to control, however, was only significantly different in the wheat RTEC trial [ 10 ]. In this trial, also the numbers of Lactobacillus/Enterococcus were higher after the intervention with whole wheat RTEC compared to that with the wheat bran based RTEC.

The same three trials, which assessed the effect of DF-rich RTEC on the composition of the microbiota [ 10 ; 58 ; 69 ] ( Table 3 ), monitored also bowel function as secondary outcome. A daily increase of DF in form of 9 g inulin or 7 g maize fiber did not change bowel habits [ 58 ; 69 ]. During the intervention with wheat-bran based RTEC stool frequency was increased compared to that with whole wheat RTEC, and frequency of soft stools and flatulence increased [ 10 ]. Consumption of whole wheat RTEC resulted in more formed stool [ 10 ]. Consumption of DF-rich RTEC did not have an effect on bowel habits in one industrial funded RCT [ 58 ] and one without industry-related funding [ 69 ]. Another industrial funded RCT [ 10 ] reported improved bowel habits.

Association between RTEC consumption and cognitive decline.

One prospective study (food-industry funded) investigated the association between frequency of RTEC consumption and cognitive decline in elderly subjects over 11 years [ 53 ] ( Table 2 ). Daily consumers of RTEC had a pattern of cognitive decline similar to infrequent consumers.

Effect of RTEC consumption on acute cognitive performance.

One RCT in children [ 75 ] and one in adolescents [ 63 ] investigated the effect of RTEC with low and high GI on acute cognitive performance ( Table 3 ). The low GI RTEC (GI 30 [ 63 ] and 42 [ 75 ]) provided a lower amount of energy and carbohydrates, but higher amounts of protein than the high GI RTEC (both GI 77). In children, after the low GI RTEC secondary memory performance was better and decline in accuracy of attention was attenuated. Speed of attention and memory as well as working memory was not affected by GI [ 75 ]. In adolescents verbal episodic memory tasks were performed under divided attention which measured immediate, short-delay and long-delay memory [ 63 ]. No differences were found comparing the raw data scored after high and low GI RTEC consumption. However, when calculating remembering/ forgetting indices for each participant, it was shown that high GI RTEC improved long-delayed memory. Both RCTs were without industry-related funding and showed either positive [ 75 ] or negative effects [ 63 ] of consumption of low GI RTEC on specific cognitive tasks.

Nutritional benefits

Frequent consumption (≥ 5 servings/week) of RTEC compared to low or no RTEC consumption consistently has been associated with a healthier dietary pattern in children and adults in most studies demonstrating a higher consumption of carbohydrates, DF and a reduction of total fat intake and cholesterol (only for children). Thus, current dietary recommendations are more likely to be met by RTEC consumers.

As many RTEC are fortified with micronutrients, it is not surprising that intake of those micronutrients is increased in RTEC consumers. However, increased micronutrient consumption is only relevant in case that micronutrient intake is below the nutritional recommendations. For this reason, we assessed the impact of RTEC consumption on micronutrient inadequacy. Our results show that the reduction of prevalence of inadequacy associated with frequent RTEC consumption is greatest for vitamin A, calcium, folate, vitamin B 6, magnesium and zinc. These results are mainly derived from surveys conducted in the US, Canada and Australia.

These data demonstrate that RTEC, due to fortification, DF content and by stimulating milk intake, can play an important role in reducing the prevalence of micronutrient inadequacy.

Of concern is the total sugar intake which was positively associated in children and adults with frequent RTEC consumption in most studies. Higher consumption of total sugar, which is the sum of free sugars, intrinsic sugars and milk sugars, can be partly explained by higher lactose intake due to an increase in milk consumption. However, it can also partly be due to the sugar content of RTEC (defined as “free” sugar) and dietary recommendations are to decrease ‘free’ sugar intake to less than 10% of the total daily energy consumption [ 79 ; 80 ]. The current intake in some European countries and the US exceeds 10 energy% especially in children [ 81 – 83 ].

Analysis of different RTEC of leading brands in the US market showed that the mean sugar content of 142 types of RTEC was 28.1 g/100 g in 2006 but decreased to 24.8 g/100 g (mean of 151 types) in 2011 [ 84 ]. Even though this is a move in the right direction 24.8 g/100 g is still high. According to the color-coded Traffic Light System for classifying nutrients in solid foods of the Department of Health UK products containing >22.5 g/100 g would be colored red, indicating that this is not a healthy choice [ 85 ]. From this study it cannot be derived whether reductions were predominantly made in RTEC marketed to children or those not marketed to children (generic). This is of interest because it was shown that RTEC for children contained more sugar than generic RTEC (36 g/100 vs 23 g/100 g respectively in the US [ 86 ]; 28.2 g/100 g vs 18.1 g/100 g respectively in Germany [ 87 ]). Interestingly, in a RCT it was shown that children consuming either low-sugar or high sugar cereals did not differ in how much they liked the cereal [ 79 ]. Even though children added sugar to the low-sugar cereal they consumed half the amount of the sugar children in the high-sugar cereal group consumed. They were also more likely to put fresh fruit on their cereal as compared to the children in the high-sugar cereal group. This indicates that low-sugar RTEC are accepted by children and that the benefit of enhanced micronutrient intake due to RTEC consumption does not necessarily need to be accompanied by high sugar intake.

Health benefits

Risk factors for cvd..

Prospective studies that examined associations of low and high consumption of RTEC with health outcomes mostly differentiated between whole grain and refined grain RTEC. No studies were found that investigated associations of whole grain RTEC with cardiovascular disease directly. However, the associations with hypertension [ 52 ] and heart failure [ 56 ] were assessed and a decreased risk of 20 and 28% respectively was found. The inverse association of whole grain RTEC consumption with hypertension is consistent with that of a number of studies investigating associations with whole grain intake in general (women 0.89 [ 88 ], men 0.81 [ 89 ], young adults 0.83 HR [ 90 ]) whereas the magnitude of effect on heart failure was not comparable with that of a study examining the association with whole grain intake in general (0.93 HR [ 91 ]). Beneficial effects of whole grain products are related mainly to the bran fraction of the grain and its high content of micronutrients, like magnesium and zinc, and bioactive components, like phytic and ferulic acid, many having antioxidant properties [ 92 ; 93 ]. Magnesium is one of the micronutrients linked to the prevention of hypertension [ 93 ; 94 ] and oxidative stress is involved in the pathophysiology of cardiovascular disease and heart failure [ 95 ; 96 ]. Furthermore, it is postulated that synergetic effects can occur as different components of whole grain act together to beneficial influence processes involved in development of disease [ 92 ].

In addition, hypocholesterolaemic properties of whole grain have been postulated that are mainly ascribed to viscous soluble fiber [ 97 ]. Reductions in total cholesterol and LDL were seen due to psyllium-enriched RTEC [ 71 ; 72 ] but not with wheat bran RTEC in hypercholesterolemic men [ 71 ]. In normocholesterolemic persons RTEC based on whole grain maize [ 58 ], whole grain wheat and wheat bran [ 10 ] did not affect blood lipids. This is in agreement with the findings of a recent meta-analysis summarizing results of lipid-lowering effects of whole-grain interventions in apparently healthy [ 98 ]. Whole grain products based on wheat did not consistently exert lipid lowering effects in contrary to products based on barley and oat [ 48 ]. Psyllium fiber, like fiber in oat and barley, are soluble whereas wheat or corn fiber are mainly insoluble, which can explain these results.

Elevated plasma concentrations of homocysteine are suggested to be an additional risk factor for the development of cardiovascular disease [ 99 ], although not consistently [ 100 ]. Higher plasma folate concentrations are implicated with lower homocysteine [ 101 ] as well as a reduced risk of developing CVD [ 102 ]. Three studies consistently demonstrated that consumption of RTEC fortified with folate could increase plasma folate concentration and lower plasma homocysteine [ 66 ; 68 ; 77 ]. The effects were most pronounced in persons with low plasma folate and high homocysteine concentrations.

In summary, studies investigating whether RTEC consumption can reduce the risk of development of CVD addressed different risk factors. Prospective studies suggest that consumption of whole grain RTEC may reduce the risk of hypertension and heart failure, which so far has not been assessed in RCTs. RCTs demonstrated that RTEC with soluble fiber from psyllium have lipid lowering potency and folate-enriched RTEC can reduce plasma homocysteine concentrations. These prospective studies did not have industrial funding, whereas the effect of psyllium and folate-enriched RTEC were only investigated in RCTs which were industrial funded.

Weight gain/BMI, satiety and food intake.

Lower weight gain (0.59 and 0.46 kg during 8 and 13 y respectively) and a lower risk of becoming obese (22 and 12%) was associated with frequent RTEC consumption in men without being different between refined and whole grain RTEC [ 8 ]. The magnitude of effect was similar in two prospective studies that examined the association between whole grain food and refined grain food intake [ 103 ; 104 ]. Consumption of whole grain food resulted in 0.49 kg less weight gain during 8 y in men [ 103 ] and 0.39 kg less weight gain during 12 y in women [ 104 ]. In contrary to the RTEC study [ 8 ] refined grain intake was associated with an increase in weight in women (0.43 kg during 12 y) [ 104 ]. However, differences in weight gain found in these studies are quite small and its health impact is difficult to judge.

In 8–10 y old children frequency of RTEC consumption was associated with slightly lower BMI in boys in two prospective studies [ 51 ; 54 ] but in girls only in one study (low-income minority children) [ 51 ]. These studies did not differentiate between types of RTEC. Similar associations between BMI and consumption of breakfast cereals in general (9–10 y girls [ 105 ]) or whole grain foods (13–15 y old boys and girls [ 106 ]) were found, with no sex-related differences. Explanations for these beneficial effects postulated are the more healthy eating pattern of RTEC consumers with increased intakes of whole grain, DF and reduced fat or increased satiety [ 51 ; 54 ] and higher insulin sensitivity in case of whole grain consumers [ 106 ]. Results of two RCTs [ 11 ; 62 ] investigating the effect of high vs low RTEC consumption on body weight do not substantiate results from prospective studies. However, in both trials RTEC with a low content of DF were administered and one was of relative short duration.

Other RCTs explored the effect of DF-rich RTEC on postprandial satiety and food intake. From these trials it seems that postprandial satiety and/or appetite is not affected by higher DF content of RTEC, as only three from seven studies reported a decrease [ 12 ; 59 ; 73 ]. However, consumption of wheat bran RTEC decreased energy intake at a subsequent meal in normal weight subjects [ 12 ; 61 ; 73 ].

In summary, consumption of RTEC (all types) is associated with modest reduction in weight gain or BMI in adults and children in prospective studies, which so far is not substantiated with RCTs. There are indications that RTEC enriched with wheat bran can decrease energy intake at a subsequent meal in normal weight persons, with RCTs without industry-related funding showing similar results as industrial funded RCTs. However, long term RCTs are needed to demonstrate that this results in decreased weight gain. Furthermore, it seems of great interest to not only assess body weight but also fat mass as the results of a recent meta-analyses demonstrated that whole grain interventions can decrease fat mass, despite no effect on body weight [ 107 ].

Type 2 diabetes and risk factors.

Consumption of whole grain RTEC 2–6 times weekly was associated with a decreased the risk of the development of type 2 diabetes by 24% and 29% and ≥ 7 servings/week by 40 and 43% [ 55 ; 50 ]. These finding are consistent with that of studies investigating associations with total whole grain intake (0.79 HR [ 108 ], 0.67 [ 109 ], 0.72 [ 110 ]). Increased intake of bran-derived micronutrients like magnesium and zinc as well as bioactive components may contribute to beneficial effects [ 92 ; 93 ]. Magnesium for example, plays an important role in insulin sensitivity [ 94 ; 111 ; 112 ] and recently the property of zinc to influence synthesis, secretion and the action of insulin has become clear [ 113 ]. In addition, chronic low-grade inflammation and oxidative stress are factors involved in the development of type 2 diabetes, which can be alleviated by certain micronutrients as well as by bioactive compounds,—possibly through synergistic action [ 92 ].

Reduction of postprandial glucose and/or insulin concentrations are considered beneficial as repeated high glucose concentrations and related high insulin concentrations can lead to decreased insulin sensitivity and β-cell function in susceptible persons [ 114 ; 115 ]. Reductions of postprandial glucose and insulin concentrations have been demonstrated for viscous soluble fiber [ 116 ]. The property of RTEC enriched with soluble fiber to decrease postprandial glucose and insulin was shown for guar gum (4.5 g) in healthy [ 70 ], whereas in overweight persons only the insulin response was reduced after RTEC with oat b-glucan [ 59 ].

Evidence from prospective studies, which were all without food-industry related funding, indicates a reduced risk of development of type 2 diabetes due to consumption of whole grain RTEC. However, RCTs investigating the effect of whole grain versus refined grain RTEC on risk factors related to the development of type 2 diabetes are needed to draw a definite conclusion. Addition of soluble fiber seems a promising strategy to reduce not only postprandial glucose but also insulin concentrations (independent from funding sources) and deserves further evaluation. Lower postprandial insulin response is considered beneficial because this would be less demanding for the pancreatic β-cells [ 115 ] and could play a role in preventing insulin resistance [ 117 ]. In addition, more recently, diets with a low insulin load were reported to be associated with lower body fat during puberty [ 118 ] and with lower energy intake in obese adolescents with features of insulin resistance and/or prediabetes [ 119 ].

Strengths and Limitations

This review provides a comprehensive overview of nutritional and health effects that are related to the consumption of RTEC and has identified specific favorable characteristics. One of the review’s strength is the careful selection of studies, excluding studies with cooked cereals or those in which cereals were not defined. In addition, RCTs were not considered in which RTEC were administered at several occasions during the day or breakfasts included other products than RTEC, milk and fruit. This enables us to draw conclusion on the properties of RTEC only. Data about nutritional benefits were derived from large, national representative surveys conducted in a number of different countries in many age-groups, which aids generalizability of results. There are some limitations of this review and the body of evidence. Evidence for nutritional and health benefits is partly derived from observational studies in which dietary data are self-reported. These studies are more prone to bias and confounding than RCTs, therefore results have to be interpreted with caution. For assessing health benefits, however, only prospective studies and no cross-sectional studies, which lack temporal relationship, have been used. As prospective studies were mainly conducted in the US generalizability of these results is uncertain. A large number of studies (45) were (partly) funded by food-industry, which can introduce reporting bias. As we examined and discussed the results also in view of funding sources, we can conclude that reporting bias seems less likely what concerns the prospective studies and most RCTs.

Frequent consumption of RTEC (≥ 5 servings/week) as compared to no or low RTEC consumption is associated with a healthier dietary pattern, concerning intake of carbohydrates, DF, fat and micronutrients, however total sugar intake is higher. The impact of frequent RTEC consumption on inadequacy of micronutrient intake is highest for vitamin A, calcium, folate, vitamin B 6, magnesium and zinc.

Evidence from prospective studies suggests that whole grain RTEC may have beneficial effects on hypertension and type 2 diabetes. These protective effects seem biological plausible, however, to prove a causal relationship RCTs are needed that assess the effect of whole grain versus refined grain RTEC on hypertension and risk factors for type 2 diabetes.

Consumption of RTEC with soluble fiber from psyllium helps to reduce LDL and total cholesterol in hypercholesterolemic men. RTEC fortified with folate have the potency to reduce plasma homocysteine especially in persons with low folate and high homocysteine plasma concentrations. Addition of soluble fiber to RTEC could aid in reducing postprandial glycaemia and insulinemia but more studies are needed to draw a final conclusion. The effect of RTEC on body weight, intestinal health and cognitive function needs further evaluation.

Supporting Information

S1 checklist. prisma checklist for the reporting of systematic reviews of randomized controlled trials..

https://doi.org/10.1371/journal.pone.0164931.s001

S2 Checklist. MOOSE checklist for the Reporting of Meta-analyses of Observational Studies.

https://doi.org/10.1371/journal.pone.0164931.s002

S1 Protocol.

https://doi.org/10.1371/journal.pone.0164931.s003

S1 Table. Differences in daily intake of energy, macronutrients, cholesterol, dietary fiber and sodium of frequent versus low/no RTEC consumers.

https://doi.org/10.1371/journal.pone.0164931.s004

S2 Table. Percentage of population with daily intake of micronutrients below recommended intake by frequency of RTEC consumption.

https://doi.org/10.1371/journal.pone.0164931.s005

Author Contributions

• Conceptualization: JRM MGP.
• Data curation: MGP.
• Formal analysis: MGP.
• Funding acquisition: JRM.
• Investigation: MGP JRM.
• Methodology: MGP.
• Validation: MGP.
• Visualization: MGP.
• Writing – original draft: MGP.
• Writing – review & editing: JRM MGP.
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• Research article
• Open access
• Published: 19 January 2017

A description of interventions promoting healthier ready-to-eat meals (to eat in, to take away, or to be delivered) sold by specific food outlets in England: a systematic mapping and evidence synthesis

• Frances C. Hillier-Brown 1 , 2 ,
• Carolyn D. Summerbell 1 , 2 ,
• Helen J. Moore 1 , 2 ,
• Wendy L. Wrieden 2 , 3 , 4 ,
• Jean Adams 4 , 7 ,
• Charles Abraham 5 ,
• Ashley Adamson 2 , 3 , 4 ,
• Vera Araújo-Soares 2 , 4 ,
• Martin White 4 , 7 &
• Amelia A. Lake 2 , 6  

BMC Public Health volume  17 , Article number:  93 ( 2017 ) Cite this article

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Ready-to-eat meals (to eat in, to take away or to be delivered) sold by food outlets are often more energy dense and nutrient poor compared with meals prepared at home, making them a reasonable target for public health intervention. The aim of the research presented in this paper was to systematically identify and describe interventions to promote healthier ready-to-eat meals (to eat in, to take away, or to be delivered) sold by specific food outlets in England.

A systematic search and sift of the literature, followed by evidence mapping of relevant interventions, was conducted. Food outlets were included if they were located in England, were openly accessible to the public and, as their main business, sold ready-to-eat meals. Academic databases and grey literature were searched. Also, local authorities in England, topic experts, and key health professionals and workers were contacted. Two tiers of evidence synthesis took place: type, content and delivery of each intervention were summarised (Tier 1) and for those interventions that had been evaluated, a narrative synthesis was conducted (Tier 2).

A total of 75 interventions were identified, the most popular being awards. Businesses were more likely to engage with cost neutral interventions which offered imperceptible changes to price, palatability and portion size. Few interventions involved working upstream with suppliers of food, the generation of customer demand, the exploration of competition effects, and/or reducing portion sizes. Evaluations of interventions were generally limited in scope and of low methodological quality, and many were simple assessments of acceptability.

Conclusions

Many interventions promoting healthier ready-to-eat meals (to eat in, to take away, or to be delivered) sold by specific food outlets in England are taking place; award-type interventions are the most common. Proprietors of food outlets in England that, as their main business, sell ready-to-eat meals, can be engaged in implementing interventions to promote healthier ready-to-eat-food. These proprietors are generally positive about such interventions, particularly when they are cost neutral and use a health by stealth approach.

Peer Review reports

Ready-to-eat meals (to eat in, to take away, or to be delivered) sold by specific food outlets that, as their main business, sell ready-to-eat meals, are often more energy dense and nutrient poor compared with meals prepared and eaten at home [ 1 ]. Furthermore, the consumption of ready-to-eat meals sold by food outlets is associated with higher energy and fat, and lower micronutrient intake [ 2 ], and eating takeaway or fast food is associated with excess weight gain and obesity [ 3 , 4 ].

The popularity and prevalence of eating ready-to-eat meals sold by food outlets has risen considerably over the last few decades in many high and middle income countries [ 5 – 7 ]. For example, around one fifth to one quarter of the UK population eat takeaway meals at home at least once per week [ 7 ]. There is some evidence that food outlets selling takeaway meals and fast foods are clustered in areas of deprivation [ 8 ]. Ready-to-eat meals sold by food outlets, particularly in deprived areas, are therefore a reasonable target for public health intervention [ 9 ].

A systematic review of the world literature on the impact of such interventions [ 10 ] identified only 13 interventions (12 in peer review publications), 11 of which were based in the US and one each in Canada and South Korea. The review found a limited range of practices that food outlets were asked to change as part of the intervention; all interventions included signage and labelling to promote healthful food options, several promoted more healthful cooking methods, and only one introduced new healthful menu options. The authors summarised the impact of these 13 interventions as being promising.

Since March 2011 the Department for Health (England), through the ‘Public Health Responsibility Deal’, has worked with a number of national and regional chain food outlets operating in England to promote healthier ready-to-eat meals. Chain food outlets ‘sign up’ to the nutrition guideline and pledge to implement a range of interventions to promote the sale of healthier ready-to-eat meals. Many of these interventions have used ‘health by stealth’ approaches, e.g. reformulation (particularly salt reduction, the removal of trans fats, and calorie reductions), and removing condiments from tables in sit-in eateries. Other interventions have focused on promoting smaller portion sizes (for example through re-packaging, or offering smaller options in addition to regular size meals), and providing consumers with better nutritional information (for example calorie labelling on menus) [ 11 ].

However, there are very few independently owned food outlets signed up to the Responsibility Deal despite the fact that there is a Local Responsibility Deal (see https://responsibilitydeal.dh.gov.uk/local-partners/ [ 12 ]) which the Department of Health (England) has been encouraging local authorities to promote to businesses in their area. This is of particular concern because the nutritional quality of food sold by independent food outlets is, in general, less healthy than that sold by chain food outlets [ 1 ]. Also, owners of these outlets, particularly those in deprived areas, appear to be less willing to engage in health-promoting interventions [ 13 , 14 ]. A range of interventions are currently being championed by local government in England to promote healthier ready-to-eat foods sold by independent food outlets, but these tend to be poorly catalogued and described [ 15 ]. Indeed, our work with this review and others has shown that information on applied public health research questions relating to the nature and range of public health interventions, as well as many evaluations of these interventions, may be predominantly, or only, held in grey literature and grey information [ 16 ]. In addition, the evidence base around the development, implementation and effectiveness of these interventions is unclear and scattered. Together, these problems make it hard for those planning, designing and delivering new interventions to build on previous learning.

The research presented in this paper, and a related ‘sister’ review ([ 17 , 18 ]), attempt to fill these evidence gaps. Our related ‘sister’ review found that the evidence is dominated by interventions in national and multinational chain food outlets operating in North America; only one intervention from the UK was identified. This ‘sister’ review of the effectiveness of such interventions was restricted to evaluations of interventions which include an assessment of impact/outcome that were conducted anywhere in the world, identified through academic database searches and published in peer review publications. In contrast, the paper reported here includes a description of relevant interventions in England and, where available, evaluations of interventions which include an assessment of process, acceptability, cost, and/or impact/outcome conducted, identified through academic database and grey literature searches and information from various contacts.

The aim of the research presented in the current paper, therefore, was to systematically identify interventions to promote healthier ready-to-eat meals (to eat in, to take away, or to be delivered) sold by specific food outlets in England. Where possible, we aimed to describe the type of interventions, and summarise information on their content and delivery. In addition, for those interventions which had been evaluated, we aimed to summarise information from these evaluations.

We conducted a systematic search and mapping of the evidence, and an evidence synthesis, using methods adapted from standard systematic review techniques [ 19 , 20 ], of interventions to promote healthy ready-to-eat meals (to eat in, to take away, or to be delivered) sold by specific food outlets in England.

Inclusion criteria

The specific food outlets we included were those that, as their main business, sold ready-to-eat meals and beverages, and were openly accessible to the general public. Supermarkets and general food stores selling ready-to-eat meals (e.g. salad boxes and sandwiches) were not included, but cafes and restaurants within supermarkets and other retail stores selling ready-to-eat meals were. Food outlets which would otherwise meet the inclusion criteria, but provided ready-to-eat meals free of charge (e.g. community based lunch clubs for the elderly or homeless), were excluded. We also excluded food outlets which are not openly accessible to the general public, including those based in schools and universities, workplaces, and health or social care institutions: the effects of interventions to promote the sale of healthier meals in these food environments has previously been reviewed, e.g. [ 21 – 23 ].

We did not specifically exclude food outlets where the only option was to eat in, and as such we ran the risk of including interventions targeted at ‘high end’ restaurants.

The categorisation of types of food outlets to be included was developed using previous work on this topic area by Lake et al. [ 24 , 25 ]. This work identified various categories of food outlets, of which nine were deemed relevant for this review (see Additional file 1 ). Food outlets targeted by the interventions included in this review were mapped onto these 9 categories of food outlets; some food outlets mapped onto more than one category.

Our knowledge of the evidence base in this area comes from our sister review [ 18 ], where after searching the bibliographic databases we identified just one uncontrolled study conducted in England [ 26 ] (included in this article as Award 34). Given the aim of the present review was to provide an inclusive and comprehensive list and description of relevant interventions, we did not set any inclusion criteria based on how or where information about relevant interventions (or evaluations of them) was reported, or methodological quality of this information. For example, we considered assessments of acceptability of the intervention (by the project team, the food proprietor and staff, or the customer) as evaluations for the purpose of this review.

Systematic search and mapping

Bibliographic databases, research and trial registers, and grey literature, were searched for relevant information between December 2013 and January 2014 (by FHB and HJM); see Table  1 for more information. In addition, between January and March 2014, a list of people were contacted (via social media, email, routine newsletters, magazines, bulletins and websites, by FHB) asking for relevant information. These included key contacts in all 353 local authorities in England, topic experts, and relevant health professionals and workers; see Additional file 2 for more information.

All bibliographic and grey literature searches were performed by FHB or HJM. All search results from the academic literature were screened for relevance by FHB, AAL, HJM or CDS. All search results from the grey literature were screened for relevance by FHB. Responses to information requests were screened for relevance by FHB. Any instances of uncertainty were resolved through discussion with AAL.

Given that information about some interventions was reported from more than one source (Fig.  1 ), in different formats and by different people, a careful mapping of interventions was conducted by FHB. Areas of uncertainly were resolved through discussion with AAL. Information on the name, location, type, aim and description of the intervention, and the intervention team, was extracted for each intervention. For data extraction, we developed, piloted, and used a data extraction pro forma. Where we had just a small amount of information, for example from an email correspondence or a brief article on a website, we chose to include all available information. Data extractions were conducted by FHB, AAL, CDS or WLW and checked by FHB and AAL. Any discrepancies were resolved by CDS.

Systematic search and mapping of interventions to promote healthier ready-to-eat meals (to eat in, take away, or delivered) sold by specific food outlets in England: flow diagram

Evidence synthesis

Two tiers of evidence synthesis took place, depending on data availability. Where enough information was available to assess the type, content and delivery of the intervention (Tier 1), this information was systematically extracted onto a pro forma, and details were sent to the relevant contacts to check for accuracy and completeness. Examples of ‘enough information’ in this context were ‘calorie labelling and reformulation’ (Non-award intervention, No 11) for content, and ‘information was provided to the food outlet’ (Non-award intervention, No 2) for delivery. A summary of this information is presented as a narrative synthesis.

Where interventions had been evaluated, regardless of the extent or methodological quality of the evaluation (Tier 2), information on the design, methods and results of these evaluations were also extracted onto the pro forma and details sent to the relevant contacts to check for accuracy and completeness. A summary of this information is presented in Table  2 in this paper, and a narrative synthesis is presented.

The systematic search and mapping identified 75 relevant interventions, and these were included in the Tier 1 synthesis (Fig.  1 ) and are listed in Additional file 3 . For completeness, interventions we identified that sounded relevant from their titles, but were excluded because there was insufficient information to assess the type, content and delivery of the intervention, are listed in Additional file 4 . Data collected for the Tier 1 evidence synthesis are reported in Additional file 5 and summarised in Additional file 6 .

Type of interventions

The single distinguishing factor around which interventions could be reasonably categorised was whether or not they were awards. ‘Award’ type interventions were defined as those that involved an assessment of food outlet practice(s) targeted by the intervention using pre-defined criteria, together with some sort of accreditation if the food outlet met the criteria. Of the 75 interventions, 43 were awards of which 14 were based on the Charted Institute of Environmental Health‘s Healthier Catering Commitment (HCC) for London [ 27 ]. The remaining 32 non-award interventions were heterogeneous in nature.

Nutrient/food group targets

This information is provided in Additional file 5 , under aims or intervention description. Awards often included multiple nutrient targets for change and assessment of intervention success (e.g. fat, salt, and sugar content of meals on sale) and usually had levels of award (e.g. bronze, silver, gold). In contrast, most ‘non-award’ interventions focused on changing specific nutrients (e.g. salt or fat). Awards usually targeted a broad range of food outlets, whereas most non-award interventions focused on specific types of food outlets (e.g. Fish and chip shops or sandwich shops).

Project funding

Information about funding for the projects team, and associated intervention costs for the food outlet proprietor, and sustainability of this funding, was available for 18 interventions (data not reported). Funding was usually described as being time-limited, and sourced from existing local government budgets. Although the available information is limited, sustainable funding routes appear uncommon.

Intervention delivery costs for the food outlets

Some information on set up and running costs was provided for a third ( n  = 25) of the interventions and eight provided detailed values. This information is not reported in detail here due to its sensitive nature. Where details were provided, the delivery of most interventions was reported as being cost neutral to the food outlet businesses.

Type and location of food outlet targeted

Forty-nine of 75 interventions were not targeted at any specific type of food outlet, and 24 were targeted at takeaways only. One intervention was targeted at an independent café that primarily offered an eat in option. Another intervention was targeted at the eat in aspect of food outlets which could be considered as low to reasonable cost, fast service cafes, restaurants and pubs (for example Jamie’s Italian, Nando’s, Frankie and Benny’s, McDonald’s and Weatherspoons). These two interventions were classified as sit-in eateries for the purpose of this review. In seven cases it was clear that interventions were specifically targeted at independent food outlets. Thirteen interventions were targeted at food outlets in deprived areas, and seven interventions were targeted at food outlets very close to schools.

Project teams

This information is provided in Additional file 5 , under details of intervention team, expertise and award accredited by. The majority (54 of 75) of project teams involved in the promotion of the intervention to the food outlets were local government environmental health officers in partnership with other professionals. These included: trading standards staff, public health professionals, dietitians and community nutritionists. Awards were mostly accredited by local government environmental health, food safety and/or trading standards officers. Twenty-one (of 75) project teams were non-governmental organisations, independent nutritionists, or ‘not for profit’ organisations.

Description of support provided by the project team to the food outlets proprietors and their staff

A key feature of award type interventions was, as expected, the process of accreditation by the project teams (all 43). For many interventions (48 of 75), particularly award type interventions, one assessment at a single point in time of the food outlet practices by the project team against a pre-determined criteria was conducted. In practice, this involved the food outlet signing up to the intervention, then in some cases (32 of 48) being sent or signposted to relevant support information, and then assessed by the project team. The re-assessment of practices post intervention was only clearly reported in one award-type intervention and five non-award type interventions.

Support provided included standard leaflets or booklets, ( n  = 31), personalised support or feedback for the staff and proprietor ( n  = 28), training for the staff and proprietor ( n  = 15), and equipment provision ( n  = 11). Few interventions involved the project team working upstream with suppliers of food to the food outlet ( n  = 6), for example to enable the businesses to source equipment or healthier ingredients which they could use as alternatives (e.g. low-fat mayonnaise, low-fat spread, a different type of cooking oil), or generating customer demand ( n  = 2). By generation of customer demand, in this context, we mean the process by which project teams create or reinforce customer desire for healthier food options through education and/or encourage or support customers to ask for healthier options in food outlets so that this desire is communicated.

We did not identify any evidence of project teams working with businesses to encourage them to provide healthier ready-to-eat meals through the creation of competition with other food outlets, but we did find one intervention where the effects of competition were explored by the project team [Non-award 20]. By competition, in this context, we mean the process by which food outlets could market the healthier ready-to-eat meals on their menus as a competitive advantage in comparison with the (less healthy) options available from their direct competitors. These marketing strategies are commonly used in business [ 28 ], and have been used as part of interventions to increase the sale of healthier food [ 29 ].

Description of the practices that food outlets were asked to change as part of the intervention

The most common practice targeted by interventions was adapting existing cooking practices, including recipe reformulation and changing ingredients used (in 45 of 75 interventions). The removal of ‘unhealthy options’ was only clearly reported in seven interventions, but adding ‘healthier’ food or drink options, for example fruits and vegetables, low or no sugar drinks, and smaller portion size options alongside regular portions, was clearly reported in about half of cases ( n  = 37). Marketing and promoting healthy options, or that the business was participating in health promotion interventions, was reported in 26 interventions. Eighteen interventions included a focus on providing suitable options for children. Sixteen interventions clearly reported using menu labelling.

Six interventions clearly reported targeting reductions in portion size. Nine interventions included the provision of verbal or printed information for customers, above and beyond generic information included in the menus.

Intervention evaluation

Thirty interventions were included in the Tier 2 synthesis (results shown in Additional file 7 , and summarised in Table  2 ). The 30 evaluations included an assessment of the 1) process, 2) acceptability, 3) cost and/or 4) impact/outcome of the interventions. These assessments were focussed on the project team, the food outlet, and/or the customer. We also included a note of whether the evaluation included any information about issues relating to working upstream with suppliers, favouring a health by stealth approach, and the generation of customer demand.

Evaluation study design

Sixteen of the 30 evaluations included post-intervention assessment only, and two only included pre-intervention assessment (e.g. baseline information on interest, and perceptions of acceptability and feasibility, of the intervention by the food outlet proprietor). Ten evaluations included a pre- and post-intervention assessment. Two evaluations included a control group: one including post-intervention assessments only [Award 26], and one both pre- and post-assessments [Non-award 28]).

Evaluation methods

Overall, the methods used to collect data were poorly described but appeared mainly qualitative. Most evaluations collected information about the experiences and perceptions of the food outlet proprietors of interventions. Some also collected information on customer and the project team’s views about the intervention. Data was most commonly collected through surveys using postal questionnaires which were designed by the project teams. Face to face or telephone interviews were used in some evaluations, often as part of feedback and follow-up visits, and a focus group (with customers) was used in one evaluation [Non-award 31].

Fifteen of the 30 evaluations were of award-type interventions, of which five were based on the HCC [ 27 ]. Six of the 30 evaluations were of interventions targeted at take-away food outlets, three at food outlets near schools, four at independent food outlets, and seven at food outlets in areas of deprivation.

Evaluation findings

Process ( n   = 5): Five evaluations included an assessment of process.

Difficulties in assessing nutritional composition of foods served: One evaluation [Non-award 9] that planned to assess the effect of interventions on nutritional composition of food sold highlighted a number of problems. Takeaway outlets, particularly independently owned food outlets serving predominately Chinese and Indian dishes, do not commonly document recipes. Even when recipes are documented, the absence of many ingredients from popular nutritional analysis software packages meant that the nutritional composition of dishes (and any changes, as a result of the intervention) could not be determined. Although laboratory based analysis of dishes are possible and attractive to local authorities, they were prohibitively expensive in many cases.

Process issues perceived by food outlet proprietors primarily stemmed from underlying concerns that interventions would have negative effects on the acceptability of food for their customers, and sales. One evaluation [Award 25] of interventions in independent takeaway food outlets highlighted the relatively high turnover of staff working in these outlets which resulted in limited and patchy knowledge of the intervention.

Acceptability ( n   = 26) : Twenty six evaluations included an assessment of the acceptability of the intervention; four from the perspective of the project team, 21 from the perspective of the food outlets, and 11 from the perspective of the customers.

From the perspective of the project team , the acceptability and success of the intervention was, in part, dependent on project team’s skills and knowledge. The project team’s ability to be both positive and enthusiastic about the intervention, and their personal interest in healthier lifestyles, were deemed to be important factors. The ability of the project team to build rapport and trusting relationships with food outlet proprietors was also considered important for success. Promoting the intervention to food outlet proprietors and their staff, to the point where they agreed to take part, often required a higher time commitment than originally planned. Evaluations highlighted the perceived need for multi-disciplinary approaches; in most cases this meant the inclusion of a qualified nutritionist or dietitian, in addition to environmental health officers, in the project team. The evaluation team for one intervention [Award 27] perceived the fact that including a former chef, who had worked in a similar type of food outlet to the ones targeted, in the project team was key to the success of the intervention.

From the perspective of the food outlet owners, managers and staff members , most (17 of 21) were positive about interventions. Overall, they particularly favoured interventions that did not affect the cost, palatability or portion size of the food served, and those which they felt were the easiest to implement. For example, mobile roadside cafés [Non-awards 15, 16 and 17] and a sandwich shop intervention [Non-award 28] reported that the changes to practice they found easiest to implement (and liked very much) were using healthier versions of standard ingredients (e.g. lower fat mayonnaise or spread) and using healthier cooking practices (e.g. draining food on kitchen roll before service; removing visible fat from bacon).

Two evaluations of interventions [Awards 6 and 41] found that food outlet proprietors reported benefits to staff health and knowledge. Also, two evaluations of interventions [Awards 6 and 10] found that food outlets perceived value in the public recognition associated with awards, which they thought improved customer satisfaction and confidence as well as attracting more customers.

One evaluation [Award 6] reported that food outlet proprietors raised initial concerns about food wastage as a result of adding healthier alternatives to their menus, and these then failing to sell. However, two other evaluations [Award 15 and Non-Award 28] experienced a decrease in waste in practice. Also, one evaluation [Award 6] reported that businesses had difficulties in training staff in new cooking and food preparation techniques.

One evaluation concluded that the intervention [Award 43] was acceptable in restaurants and cafes, but not takeaways, and three evaluations concluded that, overall, the intervention [Awards 25 and 34, and Non-award 24] was not acceptable to the food outlets. The main criticism around Award 25 was that this intervention had come to an end; for Award 34 the criticisms focussed on those changes which were perceptible to the customer, and for Non-award 24 the criticisms focussed around the use of the new 5-hole salt shaker which had resulted in customers taking longer to salt their food and increased queues in their outlets.

From the perspective of the customers interviewed for eight of the 11 evaluations, they were in favour, overall, of the intervention, and particularly liked the increase in choice of healthier options’. However , in some cases [Awards 26 and 42, and Non-award 31] customers appeared to lack awareness of intervention, regardless of whether or not they were publicised. In one evaluation, some customers complained about the intervention [Award 2] along the lines of a ‘nanny state’.

One evaluation [Award 40] reported that customers did not feel that the intervention would make any difference to what they bought from the food outlet, and two evaluations [Non-awards 24 and 26] received negative views about the interventions from customers. In both cases, the intervention was a 5-hole salt shaker; some customers complained about the ‘lack of taste’ and longer queues due to it taking longer for customers to salt their food.

Overall , there was not enough information to determine if certain types of food outlets were more willing to participate in interventions. However, two evaluations contacted businesses who had not taken part in interventions [Award 20 and Award 26]. Reasons for not taking part included lack of time and interest in receiving an award, lost or unreceived invitations to take part, and too much concern about the potential effect of interventions on food palatability and sales. One evaluation [Award 27] reported that food outlets in deprived areas found it particularly challenging to generate profits and that interventions and project teams had to be sensitive this.

There was also not enough information to determine whether interventions were more effective in some type of food outlets compared with others. However, one evaluation of an award [Award 43] reported that engagement by restaurants, sandwich shops and cafes was higher than by takeaways, for two reasons. First, because the former typically did not have to make substantive changes to achieve award criteria, or the criteria (e.g. focusing on frying practice) were not relevant. Second, takeaways, where more frying took place, were often reluctant to change frying practices due to concerns about the potential impact on food palatability.

Cost ( n   = 10): Ten evaluations included an assessment of the cost of the intervention, all of which were from the perspective of the food outlets. Six food outlets reported an increase in profits and four food outlets reported no change. One evaluation of an intervention targeting mobile food outlets [Non-award 16] reported a saving in oil used due to the use of the small oil spray bottle for frying which was provided by the project team. Another evaluation of a 5-hole salt shaker intervention [Non-award 27] reported a saving in salt used.

Impact/outcome ( n   = 21): Twenty one evaluations included an assessment of the impact/outcome of the intervention; none from the perspective of the project team, 19 from the perspective of the food outlets, and three from the perspective of the customers.

Eighteen of the 19 evaluations found that the interventions had a positive impact from the perspective of the food outlet; one evaluation [Non award 16] found negligible impact. The project team who evaluated Non award 16 conducted nutrition sampling and analysis of meals offered by two of the food outlets involved in the intervention. In one case they found that the reduction in fat content of fried food was offset against larger portions being served. In another case, the only change that had been implemented was the use of wholemeal bread for white bread.

The positive impact reported in 18 of the evaluations related to the practices that food outlets were asked to change as part of the intervention (as listed in Additional file 6 ). Although a little unclear overall, it appears that certain practices which took a health by steal approach were more commonly implemented (see below).

One evaluation of an intervention that targeted independent takeaway food outlets [Award 25] included long term (3 year) follow up results. Challenges associated with a relatively high turnover rate of businesses, and staff working in food outlets, were identified. Although many of the staff reported little memory of the intervention at follow-up, all of the businesses still trading under the same owner at 3 years (80%) had sustained at least some of the changes made as a result of the intervention.

Two of the interventions [Awards 29 and 30] were perceived to have had a positive impact from the perspective of the customers, particularly in terms of their awareness and purchasing of meals that had been identified as ‘Healthier choices’ on the menu. One intervention [Non-award 31] which focussed on calorie labelling was perceived to have had a negligible impact because many of the customers struggled with, and didn’t appreciate, the calories labelling.

Working upstream with suppliers ( n  = 3): Three businesses reported experiencing difficulties sourcing healthier ingredients and foods from suppliers. One business specifically reported difficulties sourcing lower fat spreads and mayonnaise [Award 34], and another business had similar difficulties sourcing tinned tuna in spring water (Non-award 17).

Favouring a health by stealth approach ( n = 10): Ten businesses reported favouring a health by stealth approach to interventions. In general, they found that changing ‘like-for-like’ more acceptable compared with changes that would be more perceptible to the customer. Specific examples mentioned included using lower fat spread or lower fat mayonnaise for their full fat alternatives, using a healthier oil, and using a 5-hole salt shaker instead of their usual salt shakers.

Generation of customer demand ( n  = 3): Three businesses reported the generation of customer demand as a result of implementing the intervention. Their customers reported that they liked the fact that there were more healthier choices on the menu. One evaluation of an intervention [Award 41] reported that they were selling more water and diet drinks now that these are more prominently displayed in their outlet.

Summary of findings

To our knowledge this is the first systematic mapping and evidence synthesis of interventions to promote healthier ready-to-eat-food sold by specific food outlets in England. We identified 75 interventions with information on content and delivery. Evaluations were conducted on 30 these 75 interventions. The majority (43 of 75) of interventions were awards, which tended to be aimed at a broad range of food outlets and target multiple nutrients for change. In contrast, non-award interventions tended to be aimed at independently owned foot outlets and target specific nutrients.

The majority of project teams who promoted the uptake of interventions by food outlets were local government workers, and most commonly they were environmental health officers. Funding for the projects was usually time-limited, and the delivery of interventions tended to be cost-neutral to the food outlets.

Food outlets were offered a range of support, including in some cases training and provision of new equipment. The most common practice targeted by interventions was adaptation of existing cooking practices. Adding ‘healthy meal’ options, smaller portion size options, menu labelling, and healthier choices on children’s menus, were also popular. There was some evidence to suggest that if interventions can be implemented there is a strong likelihood that changes to food outlet practices will be maintained.

Evaluations predominately focused on acceptability of interventions to business owners. Evaluation findings suggest that successful delivery and implementation of these interventions requires a substantial time commitment from the project team with key personal skills and knowledge. Businesses were more likely to engage with cost neutral interventions which were relatively easy to implement, and those which offered imperceptible changes to price, palatability and portion size. Some businesses did find difficulties in sourcing healthier ingredients at affordable prices.

Strengths and limitations of methods

We used novel and systematic methods to search for relevant interventions and evaluations. By using these methods we identified over 100 relevant interventions. However, of course, we cannot be sure that we identified all relevant interventions. Building on the search methods used in this paper and that of Godin et al. [ 30 ], feasible and robust methods for applying systematic search strategies to identify web-based and desk-based information in the grey literature that are of relevance to public health are needed.

Our ability to draw conclusions was limited by the quality of reporting of information on intervention content and delivery available, and the limited scope and low methodological quality of evaluations. In nearly all cases, evaluation results were favourable about the intervention, but these findings need to be considered with some caution for two reasons. First, in all cases, evaluations were conducted to inform service delivery rather than as formal research. As such, evaluations were fit for practice, but were limited in scope and of low methodological quality for research purposes. Second, in most cases, evaluations had been conducted by project teams who were also responsible for promoting the uptake of the intervention by food outlet proprietors and their staff, and hence at risk of bias [ 31 ].

Interpretation of findings

The rich findings of this review provide information about the scope, specific features, and delivery of existing interventions in England. In addition, the findings provide useful information about aspects of the feasibility and process of the interventions identified. However, the findings only provide clues as to the impact of these interventions on ready-to-eat-meals sold by specific food outlets, and how this might influence the dietary intake of customers and public health.

Comparing the range of practices targeted by the interventions identified in this review with interventions from other countries [ 32 ], it is clear that the interventions operating in England are limited. Specifically, the use of price reductions, personalised receipts, telemarketing and/or mandatory legislation used in other countries, were entirely absent here. Some of these approaches may be hard for local actors to implement particularly in independently owned food outlets in areas of deprivation.

In particular, very few interventions involved working upstream with food suppliers, generating customer demand, changing competition effects, or reducing portion sizes. All of these options, at least in theory [ 33 – 35 ], could be useful practices to target. Also, few of the interventions operated at a population level. Population level interventions have the advantage that they are often more effective and equitable than more individualistic interventions, although have not been popular with governments in the UK [ 36 , 37 ].

Implications for policy and practice

The fact that there is such a diversity of schemes in operation across England makes it difficult to compare their feasibility and impact, and this must be confusing for consumers, and contribute to their general lack of awareness and understanding of the schemes.

We recommend the rich source of information presented in this paper is captured, ideally by Public Health England (PHE), who then facilitate the sharing of good practice between project teams. Given the similar context in other countries, particularly Ireland, Scotland and Wales, we suggest these findings have currency beyond England. We also suggest that PHE assesses the transferability of findings presented in this paper (for example, between chain and independent food outlets, and between areas of low and high deprivation), and translate the available evidence within a useful resource (such as a toolkit) that delivers practical and pragmatic support to project teams who are responsible for promoting the uptake of interventions to food outlet proprietors.

Implications for research

Our findings have identified two key findings for research.

First, we found few rigorous evaluations of interventions; the lack of robust evaluations of these sort of initiatives and the difficulty in conducting them (e.g. because of difficulty in undertaking nutritional analysis of food due to lack of standardised menus in independent food outlets) are particularly pertinent. More consideration should be given and efforts made to conduct rigorous evaluations of interventions to promote healthier ready-to-eat meals (to eat in, to take away, or to be delivered) sold by specific food outlets in England. We acknowledge that local authorities do not have the necessary resource for such evaluations. Researchers with specific expertise and knowledge in this area should engage and work in partnership with policy and practice staff that are developing, promoting and evaluating interventions at all levels, including the local level. Rigorous evaluations should include outcome as well as process analysis. Ideally, impacts on inequalities, and variations in effect by type of food outlet, and geographical areas should be captured.

Secondly, the feasibility of developing evidence based interventions in this area should be explored. We suggest a range of interventions should be tested, which target different behavioural change strategies at various system levels [ 38 , 39 ]. Potentially promising approaches that deserve further attention include working upstream with suppliers; and working with communities to generate greater consumer demand for healthier alternatives. Other particularly common approaches that deserve further evaluation include ‘health by stealth’ approaches, reducing portion sizes, and changing the balance of healthy to less healthy options.

This systematic mapping and evidence synthesis of interventions to promote healthier ready-to-eat-food sold by specific food outlets in England provides information to help inform the development, implementation and evaluation of interventions. The best available evidence suggests that food outlet proprietors are generally positive about implementing these interventions, particularly when they are cost neutral and use a health by stealth approach. Little robust evidence is available on the effectiveness of these approaches and further research is needed to generate this evidence. Opportunities for working upstream with suppliers, and in co-participation with consumers, when developing interventions should be explored.

Abbreviations

Healthy Catering Commitment

Public Health England

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Acknowledgements

The authors would like to thank the organisations and individuals who provided information to assist with this research.

This study was funded as part of National Institute of Health Research’s School for Public Health Research (NIHR SPHR) project: Transforming the ‘foodscape’: development and feasibility testing of interventions to promote healthier takeaway, pub or restaurant food. With additional support from Durham and Newcastle Universities, and the NIHR Collaboration for Leadership in Applied Health Research and Care of the South West Peninsula (PenCLAHRC). The School for Public Health Research (SPHR) is funded by the National Institute for Health Research (NIHR). SPHR is a partnership between the Universities of Sheffield, Bristol, Cambridge, Exeter, UCL; The London School for Hygiene and Tropical Medicine; the LiLaC collaboration between the Universities of Liverpool and Lancaster; and Fuse, UKCRC Centre for Translational Research in Public Health, a collaboration between Newcastle, Durham, Northumbria, Sunderland and Teesside Universities. Authors FHB, CDS, HJM, WLW, AA, VAS and AAL are members of Fuse. Funding for Fuse comes from the British Heart Foundation, Cancer Research UK, Economic and Social Research Council, Medical Research Council, the National Institute for Health Research, under the auspices of the UK Clinical Research Collaboration, and is gratefully acknowledged. AA is funded by the NIHR as a NIHR Research Professor. JA and MW are funded by the Centre for Diet and Activity Research (CEDAR), a UKCRC Public Health Research Centre of Excellence. Funding from the British Heart Foundation, Cancer Research UK, Economic and Social Research Council, Medical Research Council, the National Institute for Health Research, and the Wellcome Trust, under the auspices of the UK Clinical Research Collaboration, is gratefully acknowledged.

The views expressed are those of the authors and not necessarily those of the above named funders.

Availability of data and materials

All data generated during this study are included in the supplementary information files.

Authors’ contributions

AA, JA, AAL and MW devised the concept for the research, contributed to study design and development of methods, and data interpretation. AAL assisted with the searches, screening, data extraction and analysis, was responsible for the management of the study, and drafted the manuscript. FHB assisted in the study design and development of methods, conducted the searches, screening, data extraction and analysis, and contributed to drafting the manuscript. JA contributed to study design and development of methods, and data interpretation. HJM contributed to study design and the development of methods, and assisted with the searches. CDS contributed to study design and the development of methods, and assisted with the screening, data extraction and data interpretation. WLW assisted with data extraction and data interpretation. CA, VAS and MW contributed to the development of methods and data interpretation. All authors have provided critical comments on drafts of the manuscript and have read and approved the final version.

Competing interests

The authors declare that they have no competing interests.

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Obesity Related Behaviours Research Group, School of Medicine, Pharmacy & Health, Wolfson Research Institute, Durham University, Durham, UK

Frances C. Hillier-Brown, Carolyn D. Summerbell & Helen J. Moore

Fuse – UKCRC Centre for Translational Research in Public Health, Newcastle University, Newcastle-upon-Tyne, UK

Frances C. Hillier-Brown, Carolyn D. Summerbell, Helen J. Moore, Wendy L. Wrieden, Ashley Adamson, Vera Araújo-Soares & Amelia A. Lake

Human Nutrition Research Centre, Institute of Health & Society, Newcastle University, Newcastle upon Tyne, UK

Wendy L. Wrieden & Ashley Adamson

Institute of Health & Society, Newcastle University, Newcastle upon Tyne, UK

Wendy L. Wrieden, Jean Adams, Ashley Adamson, Vera Araújo-Soares & Martin White

Psychology Applied to Heath, University of Exeter Medical School, University of Exeter, Exeter, UK

Charles Abraham

Centre for Public Policy & Health, School of Medicine, Pharmacy & Health, Wolfson Research Institute, Durham University, Durham, UK

Amelia A. Lake

Present address: CEDAR – UKCRC Centre for Diet and Activity Research, MRC Epidemiology Unit, University of Cambridge School of Clinical Medicine, Cambridge, UK

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Additional files

Additional file 1:.

Process of categorisation of food outlets targeted by the interventions included in this review. (DOCX 16 kb)

Additional file 2:

List of people contacted, and method(s) of contact, asking for information about interventions to promote healthier ready-to-eat meals (to eat in, take away, or delivered) sold by specific food outlets in England. (DOCX 25 kb)

Additional file 6:

Summary of the content and delivery of interventions to promote healthier ready-to-eat meals (to eat in, take away, or delivered) sold by specifica food outlets in England (Tier 1, n = 75) (DOCX 38 kb)

Additional file 3:

List (name and location) of interventions to promote healthier ready-to-eat meals (to eat in, take away, or delivered) sold by specific1 food outlets in England and identification and data sources (Tier 1, n  = 75). (DOCX 17 kb)

Additional file 4:

List (name and location) of interventions to promote healthier ready-to-eat meals (to eat in, take away, or delivered) sold by specific1 food outlets in England identified through searches but excluded for the reason of insufficient information. (DOCX 14 kb)

Additional file 5:

Description of the content and delivery of interventions to promote healthier ready-to-eat meals (to eat in, take away, or delivered) sold by specific food outlets in England (Tier 1, n  = 75). (DOCX 81 kb)

Additional file 7:

Description of the design, methods and results of evaluations of interventions to promote healthier ready-to-eat meals (to eat in, take away, or delivered) sold by specific food outlets in England (Tier 2, n  = 30). (DOCX 63 kb)

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Hillier-Brown, F.C., Summerbell, C.D., Moore, H.J. et al. A description of interventions promoting healthier ready-to-eat meals (to eat in, to take away, or to be delivered) sold by specific food outlets in England: a systematic mapping and evidence synthesis. BMC Public Health 17 , 93 (2017). https://doi.org/10.1186/s12889-016-3980-2

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DOI : https://doi.org/10.1186/s12889-016-3980-2

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Do consumers change their perception of liking, expected satiety, and healthiness of a product if they know it is a ready-to eat meal.

Graphical Abstract

1. Introduction

2. materials and methods, 2.1. ready-to-eat meals, 2.2. consumer tests, 2.3. data analysis, 3. results and discussion, 3.1. consumer liking, 3.2. effect of evaluation condition on the liking scores, 3.3. effect of evaluation conditions on expected satiety, 3.4. effect of evaluation conditions on healthiness perception, 4. conclusions, author contributions, acknowledgments, conflicts of interest.

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Laguna, L.; Gómez, B.; Garrido, M.D.; Fiszman, S.; Tarrega, A.; Linares, M.B. Do Consumers Change Their Perception of Liking, Expected Satiety, and Healthiness of a Product If They Know It Is a Ready-to Eat Meal? Foods 2020 , 9 , 1257. https://doi.org/10.3390/foods9091257

Laguna L, Gómez B, Garrido MD, Fiszman S, Tarrega A, Linares MB. Do Consumers Change Their Perception of Liking, Expected Satiety, and Healthiness of a Product If They Know It Is a Ready-to Eat Meal? Foods . 2020; 9(9):1257. https://doi.org/10.3390/foods9091257

Laguna, Laura, Beatriz Gómez, María D. Garrido, Susana Fiszman, Amparo Tarrega, and María B. Linares. 2020. "Do Consumers Change Their Perception of Liking, Expected Satiety, and Healthiness of a Product If They Know It Is a Ready-to Eat Meal?" Foods 9, no. 9: 1257. https://doi.org/10.3390/foods9091257

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Ready to eat shelf-stable brown rice in pouches: effect of moisture content on product’s quality and stability

• Original Paper
• Published: 15 September 2021
• Volume 247 , pages 2677–2685, ( 2021 )

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• Enrico Federici 1 , 2 ,
• Valentina Gentilucci 1 ,
• Valentina Bernini   ORCID: orcid.org/0000-0002-2255-4384 1 ,
• Elena Vittadini   ORCID: orcid.org/0000-0001-9181-0815 3 &
• Nicoletta Pellegrini   ORCID: orcid.org/0000-0002-9178-5274 4  

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Despite several nutritional benefits of brown rice (BR) its consumption remains limited compared to white rice. Two of the major barriers to its consumption are long cooking time and limited shelf life. However, those two hurdles can be overcome through the development of shelf-stable BR pouches to create new ready-to-eat (RTE) products, a food category that is gaining important market shares. Nevertheless, scarce information is available on the production and shelf-life stability of ready-to-eat BR products. The first objective of this study was the determination of the optimal moisture range to fully cook BR. The second objective was to determine the effect of moisture content and storage time on two fundamental parameters for consumer’s acceptance of rice: color and texture. Three RTE BR pouches with moisture contents of 54%, 57% and 60% were produced and texture and color were evaluated after 1 year of storage. Significant changes in hardness and stickiness were reported during long-term storage. Moisture content negatively affected hardness and positively affected stickiness. Furthermore, storage time and moisture showed a significant effect on rice color. The present results provide information that will be useful to design new RTE meals to promote brown rice consumption.

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Introduction

Ready-to-eat (RTE) meals are becoming popular among consumers due to their convenience and the change of eating habits. The busy lifestyles of young professionals and entrepreneurs have accounted for an increase in the demand for labor-saving RTE meals [ 1 ]. Availability of RTE meals has further gained importance in light of the COVID-19 pandemic, as they provide not only an easy solution to the need to minimize handling and contact-free delivery of food but also are a lunch option alternative for individuals who would have normally fed at restaurants that have been largely shut down [ 2 , 3 , 4 ].

Rice is a popular ingredient in RTE food in Europe, America and Asia [ 5 ], and it is commonly consumed and used in RTE as polished (white) rice. White rice is preferred from consumers to brown rice (BR) since the latter has a longer cooking time, chewy texture, and poor appearance [ 6 , 7 , 8 ]. Moreover, products incorporating BR also negatively impact the flavor of a product [ 9 ]. However, BR has positive nutritional features as it is rich in dietary fiber, polyphenols, and lipids which are available in good amounts in the bran layer of caryopsis [ 10 ]. Compared to BR, white rice has a poorer nutritional value as, during milling, removal of bran and germ diminishes fiber, vitamins and minerals as well as protein content [ 11 ]. Thus, the utilization of BR in RTE foods could be a good strategy to increase not only its nutritional value but also take out the burden of long cooking time [ 12 ].

A popular technology to produce RTE cereal products is sterilization in pouches. However, when this intense thermal treatment is performed on white rice grain, its integrity is lost resulting in a sticky product with a soft texture. A potential solution to produce rice-based RTE aseptic products is the utilization of BR. The long cooking time of BR is a positive feature for aseptic processing since it allows to sterilize the product with limited effects on grain structural integrity. Aseptic processing also removes the need for long cooking by the consumer, which is a barrier for BR consumption. Furthermore, the use of BR, instead of white rice, as the main ingredient in these highly processed foods, which are potentially associated with poor dietary quality and obesity [ 13 ], could greatly improve their nutritional value. Fiber, minerals and proteins present in BR are not lost during the cooking-sterilization process in an enclosed pouch, and bioactive compounds present in rice bran are more available after being thermally treated [ 14 ]. Finally, BR rice contains a higher amount of bioactive lipids and flavonoids than white rice [ 15 ] which may further support the human immune system also against COVID-19 [ 16 ]. All these characteristics make BR an optimal candidate for the design of RTE BR-based functional foods. Such RTE products could be a mean to contribute significantly to increase the consumption of BR and to help consumers in familiarizing with the consumption of whole-meal foods [ 6 ].

To the authors’ best knowledge, no information is available in the literature on the optimization of RTE BR cooking process in pouches, and on the characterization of its shelf-life stability. In this study, cooking conditions of BR have been optimized at first, and then, the effect of hydration level and storage time on main quality attributes (e.g. texture and color) of RTE BR have been evaluated.

Materials and methods

Brown rice optimal cooking time determination.

BR of Roma variety has been gently provided by a local producer (Grandi Riso S.p.A., Codigoro, Ferrara, Italy). Rice was cooked in boiling water (1:20, rice:water) in a pot for variable lengths of time (10, 15, 20, 25, 30, 35, 40 and 45 min). BR and cooking water were separated by draining rice with a colander and cooled down to room temperature for 30 min before further analysis. The minimum cooking time to consider BR cooked was calculated through the determination of the point of inflection of the rice moisture absorption curve [ 17 ]. All the experiments were carried out at the Department of Food and Drug, University of Parma (Italy).

Brown rice moisture content

The moisture content of BR at variable cooking times was evaluated by drying in an air forced oven at 105 °C to constant weight according to AACCI method 44-15.02. The analysis was performed in triplicate for each cooking time.

Brown rice texture

Texture profile analysis (TPA) was performed on rice samples using a Texture Analyzer (Stable Micro Systems, Godalming, UK) equipped with a 25 kg load cell and an aluminum cylinder probe with a diameter of 40 mm, following Boluda-Aguilar et al. [ 2 ] with some modification. A test speed of 0.1 mm/sec and a total strain of 75% were used. Three g of rice was spread in single layer grain on the instrument base. Three replicates were performed on each sample. Textural attributes considered were: hardness (N, maximum force of the first compression) and stickiness (N.cm −1 , negative area after the first compression) [ 18 ].

Brown rice grain morphology

Forty BR kernels were arranged in a thin layer on a transparent plastic sheet. A dimensional reference was added to determine pixel:mm ratio of every image. BR pictures were acquired using a scanner (HP Scanjet 8200) with a resolution of 600 pixel and analyzed with the software ImageJ [ 19 ]. Acquired images were then converted in black and white and threshold adjusted before measuring the averaged area, solidity, and circularity of rice kernels.

Brown rice cooking loss

Cooking loss, defined as the amount of solids lost into the cooking water, was determined according to the AACC official method 16–50.

RTE brown rice poches production and microbial safety assessment

RTE BR pouches were produced by a local producer. BR was washed, inserted into a pouch (250 g, composite packaging, 406,735, Goglio Packaging System, Milan, Italy) together with enough tap water to reach theoretical total moisture contents of 54, 57, and 60 g water/100 g product. Pouches were then hermetically sealed, placed vertically into baskets that were then inserted into a horizontal autoclave, which was first filled with water at 85 °C, heated to 118 °C and held for 35 min. The cooking-sterilization process was static, not allowing for pouches rotation. At the end of the thermal treatment, pouches were cooled down, unloaded, and stored at room temperature to reproduce domestic preservation conditions. One pouch was open for every point of shelf life at the following times: 0, 40, 80, 120, 160, 270, and 365 days. For every storage time, microbiological analysis was performed to assess the sterility of the product. Aliquot of samples were homogenized 1:10 (Seward Stomacher, 400 circulator, UK) with sterile Ringer solution (Oxoid, Basingstoke, UK), tenfold diluted and plated in duplicate on different culture media. Total mesophilic and spore-forming mesophilic bacteria were determined on Plate Count Agar (PCA) (Oxoid, Basingstoke, UK) after incubation at 30 °C for 48 h. Yeast and molds were grown on Yeast Extract Dextrose Chloramphenicol Agar (YEDC) (REMEL Lenexa, USA) after incubation at 25 °C for 72–120 h. Brilliance™ Bacillus cereus Agar Base supplemented with Brilliance ™ Bacillus cereus selective supplement (Oxoid, Basingstoke, UK) and incubated at 37 °C for 48 h was used to enumerate Bacillus cereus . Regarding spore-forming bacteria, first dilution of the samples was treated at 85 °C for 15 min before plate counts. Analyses were carried out in duplicate and for each sampling time average values ± standard deviations were reported as UFC/g.

Water spatial distribution in pouches

Brown rice moisture content homogeneity throughout the pouch was assessed by means of its moisture content, by extracting rice samples from 24 different locations in the pouch. Sampling locations were equally distanced to assure homogeneous distribution of sampling points through the pouch. Moisture content was then determined as described in 2.1.1. Moisture spatial distribution was measured in three pouches per each BR moisture content.

Brown rice color in pouches

Color was measured on the surface of cooked BR using a Minolta Colorimeter (CM 2600d, Minolta Co., Osaka Japan) in the 400–700 nm range using illuminant D65 and for a 2° position of the standard observer. L* (lightness), a ∗ (redness), b ∗ (yellowness) were measured for at least ten measurements at each cooking time and each shelf-life time. ΔE was calculated according to Eq.  1 , taking the color of rice cooked at time 0 as reference.

Brown rice texture in pouches

Each BR pouch was massaged to un-grain and mix their content prior to be opened to extract BR samples (80 g). Samples were transferred into a closed container and heated in a microwave for 1 min at 900 W, to replicate a standard heating procedure the product would undergo prior to consumption. Heated rice was allowed to cool down to room temperature prior to texture profile analysis (TPA) that was performed as described in “ Brown rice texture ”.

Statistical analysis

Data are presented as average ± standard deviation. At least three replicates were performed for each analysis. Significant differences ( p  ≤ 0.05) among samples were calculated by multivariate analysis of variance (MANOVA) with a Tukey-high significant difference test. SAS 9.4 (SAS institute corporation, NC, USA) was used to perform the statistical analysis.

Results and discussion

The cooking process of BR in excess water was studied with respect to water uptake and textural changes occurring in rice kernels for different lengths of time. This preliminary study was carried out to determine the amount of water needed to reach optimal cooking of BR, and therefore to design conditions to achieve optimal cooking of BR within sealed pouches. Optimal cooking time has been reported to correspond with the point at which most of the starch present in the kernel is gelatinized, condition that can be determined with the inflection point of a moisture absorption kinetic curve [ 17 ]

Appearance of BR after cooking for different times is shown in Fig.  1 . BR kernels cooked up to 20 min were characterized by a smooth surface and retained their original shape and structural integrity. At 25 min cooking, BR kernels started to break due to moisture absorption and volume expansion indicative of an important amount of gelatinized starch. The number of broken kernels increased with cooking time and their shape become progressively more irregular. After 45 min, an important amount of starch leached out from the kernels, as it was observable by the presence of a large quantity of material collecting on the plastic sheet used to arrange the sample for image acquisition. BR kernels area was measured as a function of cooking time (Table 1 ), and it was found to progressively increase from 20.9 ± 2.7 to 25.3 ± 3.7 mm 2 with cooking time increase from 10 to 25 min. Rice kernels expansion is due, primarily, to water absorption, the consequent swelling, and gelatinization of starch granules during cooking. However, after 25 min of cooking, even though rice kept absorbing water, its area increased at a slower pace, suggesting that rice starch had reached its maximum swelling ability and was not able to further expand [ 20 ]. At longer cooking times, BR kernels underwent breakage and disruption decreased their solidity, circularity and slightly, but nor significantly, increased their overall area (Table 1 ).

Appearance of brown rice kernels after cooking in a pot for different lengths of time

Water uptake in BR during cooking was monitored and it was found, as expected, to increase with increasing cooking time (Fig.  2 ). Moisture content of BR gradually increased from 38.0 ± 0.2 to 52.9 ± 0.8 g water/100 g product up to 25 min cooking. At longer cooking times, water absorption still occurred but at a slower rate, reaching a maximum of 64.9 ± 0.2 g water/100 g product at 45 min cooking. From the data reported in Fig.  2 , it is possible to observe the occurrence of an inflection after 25 min of cooking, leading to the identification of 25 min as the minimum cooking time at which the rice could be considered cooked in excess boiling water [ 17 ]. Solid loss from BR kernels increased exponentially with increasing cooking time, as measured by the increase in turbidity of the cooking water (Fig.  2 ), resulting from solids (primarily amylose and short-chain amylopectin) lost in cooking water [ 21 ]. At the initial stages of cooking, turbidity grew slowly due to the limited starch gelatinization with few broken starch granules and the presence of intact husks that protected and retained the starchy endosperm within the kernel. Increasing cooking times lead to more extensive gelatinization and an increasing number of kernels showing damaged husks, resulting in an increased release of solids.

Changes in physico-chemical attributes of brown rice (moisture content, kernel area, hardness) and cooking water (turbidity) during cooking. Gray area represents the range of acceptable cooking conditions

Textural attributes of BR significantly changed upon cooking due to water absorption and structural changes occurring in rice constituents, primarily associated with starch gelatinization. BR hardness was very high at the beginning of the cooking process, 255.1 ± 11.6 N after 10 min of cooking, and gradually decreased, as expected, to 56.4 ± 6.8 N after 45 min of cooking. Hardness decrease could be divided into two phases reflecting the trend observed for moisture uptake. A first phase, characterized by a rapid decrease in hardness, was observed until 25 min of cooking, and a slower decrease for further cooking from 25 to 45 min.

Studies on the degree of starch gelatinization at variable cooking times in pasta [ 22 ] indicated that only 80% of starch was gelatinized at the cooking time suggested by the pasta producer, while 90% starch gelatinization was reached only in an overcooked product. In this respect, a complete starch gelatinization is not required to consider a product cooked [ 23 ]. Therefore, we can expect starch to be mainly gelatinized in BR at the inflection point where water uptake is reduced, but it can be considered cooked over a larger range of moisture contents.

In this work, the extremes of BR cooking were set, for the lower limit, in correspondence of the inflection point of the moisture uptake curve (25 min, corresponding to a reduction of water uptake), and for the higher limit, at 35 min. The value of 35 min was selected because it corresponded to a condition where kernel damage was still contained. This statement was supported by limited turbidity of the cooking water (593 NTU) and BR kernel high stickiness (8.4 ± 2.1 N cm −1 ) as compared to 1082 NTU and 4.2 ± 0.8 N cm −1 , respectively, at 40 min cooking, indicating a shift of solids from BR kernel surface into the cooking water. The moisture content of rice at the lower (25 min) and higher (35 min) end of the cooking range were 52.9% ± 0.8 and 59.9% ± 1.0, respectively. Based on the results obtained, the moisture contents to cook rice in pouches were designed to be 54, 57 and 60%.

RTE brown rice in pouches: characterization and long-term shelf-life stability

Moisture content and spatial distribution in pouches.

Rice was cooked in pouches with the theoretical amount of water to reach the minimal amount of moisture necessary to cook the rice. Total mesophilic bacteria, spore-forming bacteria, yeasts and molds and B. cereus were not present above the detection limit (10 UFC/g) throughout the shelf life considered, confirming the efficacy of the treatment. At the end of aseptic processing, which was carried out in a static manner, the real moisture content of rice was determined. The average moisture content of BR in the pouches was 53.9% ± 3.8, 57.1% ± 0.7 and 60.3% ± 0.5 and well approximated the theoretical target moisture contents (54%, 57%, and 60% moisture content, respectively). The averaged moisture content of all samples remained constant for the duration of the storage time (1 year).

Water content in different locations of the pouches was measured to verify homogeneity of the cooking process inside pouches to ensure the product’s uniformity. Water distribution was not homogenous in the 54% moisture pouch, while it was evenly distributed throughout the sample in other pouches (57 and 60%), as shown in Fig.  3 . BR in the 54% moisture pouch had a higher moisture content at the top and a lower at the bottom of the pouch (Fig.  3 ). This can be explained by the dynamics of the cooking process in a confined environment (pouch); upon heating, water turns into vapor and moves towards the upper zone of the pouch, creating a dis-uniform distribution of water that is particularly relevant in the lower moisture product. An uneven water distribution causes a different degree of water penetration into rice kernel and, consequently, uneven cooking of the product. Water availability affects starch gelatinization temperature [ 24 ]. Therefore, different moisture levels can also affect starch gelatinization. BR at 54% moisture had limited available water, leaving some rice kernels, located in the lower part of the pouch, underhydrated and not able to gelatinize under the processing conditions. This resulted in uncooked rice kernels with a more vitreous aspect. Therefore, we can conclude that 54% moisture is not enough to homogeneously cook BR in pouches. On the contrary, in the pouches with 57% and 60%, the amount of moisture was enough to cook the rice evenly within the pouch ensuring homogeneous water distribution and rice grain textural attributes. These data showed that the cooking dynamic of BR in a pot and within a pouch is different and that particular care must be taken in defining the optimal moisture content of a product to ensure proper cooking of the entire pouch content and its sterilization.

Moisture content of brown rice as a function of spatial distribution in pouches with different theoretical moisture contents

Texture analysis

Hardness and stickiness of BR after re-heating in a microwave oven are shown in Table 2 . Hardness and stickiness were measured as they are the most important textural attributes that affect consumer acceptability in rice [ 25 ]. As expected, water content was found to be the most important factor affecting BR hardness, with rice kernels becoming softer with increasing moisture content, as shown in Table 2 . Average values of hardness resulted comparable to BR with a similar amount of moisture cooked in a pot, as shown in Fig.  2 . The storage time had a significant effect on BR hardness up to 1-year shelf life. Indeed, BR hardness decreased with increasing storage time until 120 days in all samples, and then increased at longer storage times. This trend in hardness suggests the occurrence of different events at short and long storage times and is likely related to starch structural conformation and its interaction with water. It is well known that gelatinized starch is subjected to amylopectin retrogradation and staling during storage, resulting in increase of hardness [ 26 ]. However, as previously observed [ 27 ] heating of BR in a microwave oven prior to analysis had a partial effect on reducing amylopectin retrogradation and conferred a fresh-like consistency to the product. It is possible that at longer storage times amylopectin undergoes modification that are not reversible with the microwave treatment used to warm rice. Amylopectin modification could have limited interaction between starch and water leading to decreased chain flexibility affecting gel-like texture. Further investigation at a molecular level will be necessary to better understand changes in the hardness of rice during shelf life.

Stickiness of BR was found to increase with increasing moisture level and storage time, as shown in Table 2 . Both water ( p  < 0.0001) and time ( p  < 0.0001) had a significant effect on the stickiness of rice, however, the effect of water was predominant. Rice stickiness has been correlated with its content in amylose and protein [ 28 ]. When rice is cooked in a pot, the ratio between water to rice affects stickiness between granules, with an increase of stickiness with increasing water [ 29 ] suggesting that high leaching of starch consequent to high water content affected BR stickiness. In the native starch granules, small amylopectin molecules may entangle with large amylopectin molecules by non-covalent bonding or co-crystallize with other large amylopectin molecules, at the edges of blocklets, and are free to leach once the crystalline structure is destroyed by heating [ 30 ]. An increased degree of BR cooking can result in a higher disruption of the starch granules [ 31 ] which can lead to a larger leaching of starchy components and to a consequent increase in stickiness. Higher amount of moisture might have favored amylopectin and amylose leaching, resulting in a stickier product. H bonding between larger amylopectin and other amylopectin molecules is at the base of rice stickiness [ 30 ]. Thus, higher moisture levels might have favored greater interactions among amylopectin chains, generating a denser network of H bonds and therefore leading to higher stickiness. In this study, it was not possible to make a comparison of stickiness between BR in pouch and that in pot since a small quantity of oil was added to the pouches to reduce the adhesion among kernels during cooking.

Color of BR (L, a*, b* and Δ E , Table 3 ) was found to be significantly affected by moisture content. Increasing moisture resulted in an increased L ( p  < 0.0001), and decreasing a* ( p  = 0.0033), while b* did not change significantly. These results confirm the findings of Lamberts et al. [ 32 ] but are in contrast with a previous study on BR hydration that shows decreasing levels of L at higher levels of hydration [ 33 ].

No significant effects of time were found on L and a*. On the other hand, a significant effect was observed for the values of b* with an increase in storage time leading to a lower level of b*. Furthermore, Δ E values indicate that the difference in color during the shelf life are perceptible after 40 days of storage by an untrained eye, showing values larger than 2 [ 34 ]. Pigment migration diffused from the bran into the endosperm can potentially explain the change in color during shelf life [ 32 ], or occurrence of oxidative process into the pouch altering the color of rice might be speculated. Further research will be necessary to determine what are the changes leading to decrease in yellowness in rice.

Brown rice could be a valuable ingredient in RTE meals, but the right hydration level needs to be optimized. This information was acquired using a step-by-step decision approach. Firstly, BR physiochemical properties at different hydration levels has been assessed at lab scale. From lab-scale experiments, three different hydration levels were selected and applyed for BR cooking in pouches in a pilot plant facility. It was found that, when a low moisture content (54%) identified at lab scale, was applied in the pouch, rice was not homogeneously cooked demonstrating different cooking dynamic in different environments. Conversely, higher moisture contents resulted in uniform cooking of rice kernels without affecting its microbial safety. Significant changes in texture and color were observed in brown rice during 1-year storage time, mainly related to moisture and storage time. Samples became less hard up to 120-day storage, conversely, prolonging shelf-life led to increases in hardness that might affect the product acceptability. However, further investigation will be required to better understand the cause of the physiochemical changes during shelf life of RTE pouches. A greater understanding of the textural changes in brown rice during shelf life will potentially allow to formulate new strategies to mitigate them and to successfully employ this disregarded, but nutritionally valuable ingredient, in producing RTE meals.

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Acknowledgements

The authors would like to thank Mr. Gianni De Cecchi for producing the aseptic rice pouches.

Research was partially funded by Grandi Riso S.p.A.

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Food and Drug Department, University of Parma, Parco Area Delle Scienze, 49/A, 43124, Parma, Italy

Enrico Federici, Valentina Gentilucci & Valentina Bernini

Department of Food Science, Purdue University, West Lafayette, IN, 47907, USA

Enrico Federici

School of Biosciences and Veterinary Medicine, University of Camerino, via Gentile III da Varano 3, 62032, Camerino, MC, Italy

Elena Vittadini

Department of Agricultural, Food, Environmental and Animal Sciences, University of Udine, via Sondrio 2/A, 33100, Udine, Italy

Nicoletta Pellegrini

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Authors NP, EV, VB contributed to the study conception and design. Material preparation, data collection and analysis were performed by EF, VG. The first draft of the manuscript was written by EF and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Federici, E., Gentilucci, V., Bernini, V. et al. Ready to eat shelf-stable brown rice in pouches: effect of moisture content on product’s quality and stability. Eur Food Res Technol 247 , 2677–2685 (2021). https://doi.org/10.1007/s00217-021-03790-2

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Received : 23 February 2021

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Published : 15 September 2021

Issue Date : November 2021

DOI : https://doi.org/10.1007/s00217-021-03790-2

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Article Contents

Introduction, suggestions.

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Current situation and perspectives of ready-to-eat food/meal suppliers

Working Group 2 Members: Takashi Sakata (Leader, Ishinomaki Senshu University), Takeaki Akabane (ADEKA Corp.), Chikako Akagaki (SEVEN-ELEVEN JAPAN Co., Ltd.), Rie Akamatsu (Ochanomizu University and The Japanese Society of Nutrition and Dietetics), Toshihiko Hagiwara (NICHIREI Corp.), Naoki Hayashi (Ajinomoto Co., Inc.), Li Han (Nippon Suisan Kaisha, Ltd.), Hajime Kato (Yano Research Institute Ltd.), Kayo Kurotani and Kazuko Ishikawa-Takata (the National Institutes of Biomedical Innovation, Health and Nutrition), Shunsuke Omoto (Kirin Holdings Company, Ltd.), Takashi Tanaka (YAMAZAKI BAKING Co. Ltd.), and Yoshiko Yokomukai (International Life Science Institute JAPAN)

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Takashi Sakata, for Working Group 2 of the Healthy Diet Research Committee of International Life Sciences Institute, Japan, Current situation and perspectives of ready-to-eat food/meal suppliers, Nutrition Reviews , Volume 78, Issue Supplement_3, December 2020, Pages 27–30, https://doi.org/10.1093/nutrit/nuaa089

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Working Group 2 of the Healthy Diet Research Committee of International Life Sciences Institute Japan (WG2) assessed the concept and practice of healthy eating in the ready-to-eat food/meal industry in Japan. WG2 interviewed 14 arbitrarily selected member companies that included “health” or “nutrition” in their management policy, and sent a questionnaire to 338 member companies of the Japan Ready-Made Meal Association. Ready-to-eat food/meal suppliers mainly referred to Dietary Reference Intakes for Japanese, the Japanese Food Guide, and/or Healthy Japan 21 for their menu construction. They increased dietary fiber, variety, vegetables, whole-grain cereals, millet rice, and soy bean products; and reduced energy, carbohydrates, and salt in “healthy” food. They tended to avoid making direct appeals to health. Many companies reduced the salt content without drawing attention to the practice. They continually strive to improve flavor as the single most important factor for selling healthy food. The cycling of menus is used to increase diversity in food consumption. These industries require both academia and the government to define priorities for increasing and decreasing particular nutrients as the main targets and to establish the maximum time for balancing each nutrient.

Ready-to-eat food or meals in Japan is defined as “food or a meal that can be eaten without cooking or heating at home, workplace, school, etc., such as lunch boxes and daily dishes with a short shelf life.” 1 The sales of ready-to-eat food/meals is growing and, in 2017, they exceeded JPY 10 trillion. 1 The expected increase in the number of elderly people and the results of women’s empowerment in Japan should favor this sector of the food industry.

The main products of these ready-to-eat food/meal suppliers are cooked rice (50%) and daily dishes (34%), namely lunch boxes, rice balls, sandwiches, croquettes, and vegetable salads in the Tokyo metropolitan area. 1 These products are sold mainly via convenience stores (32%), specialty stores (29%), and food supermarkets (26%). 1

We conducted a survey to evaluate the concept of “healthy eating” among ready-to-eat food companies that are expected to grow in Japan, and we summarized the findings for academic research and governmental policy and regulation needed to achieve healthy eating.

Working Group 2 of the Healthy Diet Research Committee of International Life Sciences Institute (ILSI) Japan (WG2) conducted a round-table discussion with the Japan Ready-Made Meal Association (JRMA) to clarify the general business structure, and then performed semistructured interviews to arbitrarily select 14 (of 24 approached) JRMA member companies stating “health” or “nutrition” in their management policy. We administered a nationwide online questionnaire via Google forms to only the 14 selected JRMA member companies via the JRMA. JRMA is a national association comprising 338 regular member companies, 216 supporting member companies, and 40 cooperating companies.

Findings from interviews

Of 24 member companies of JRMA that publish statements on healthy or nutritious food in their policies and were selected for visits by WG2, 14 companies accepted the visit. Annual sales of these 14 companies exceeded JPY 40 billion; the average annual sales of JRMA regular member companies in 2019 totaled JPY 12.6 billion ( Table 1 ).

Characteristics of interviewed companies

Abbreviations: Dept., department; JPY, Japanese yen.

Interviewed companies generally based their meals and menus on Dietary Reference Intakes for Japanese, 2 the Japanese Food Guide, 3 or Healthy Japan 21. 4 These companies intended to increase or improve ingredient variety (n = 5 companies), vegetables (n = 4), dietary fiber (n = 3), lactic acid bacteria (n = 2), green and yellow vegetables, millet rice, organic ingredients, quinoa, ω3-fatty acids, iron, lycopene, calcium, protein, and nutrient balance. They intended to reduce or omit salt (n = 8 companies), energy (n = 5), additives (n = 4), chemical seasoning (n = 3), carbohydrates (n = 2), and lipids.

It was a general tendency of all interviewed companies to avoid direct health appeals such as “reduced salt,” although many of them actually reduced the salt content in their products gradually but continuously. These companies considered direct health appeals to be unpopular and to reduce sales. They emphasized a healthy atmosphere as a whole. It was also noted that some positive wording such as “rice bowl with lots of vegetables” increased sales.

All companies considered good flavor to be the single most important sales factor. Therefore, they regularly worked to improve the flavor of their products and tested the customers’ opinions of the improvements often via face-to-face tastings as points of sale, which resulted in an increase or recovery of the sales.

One company selling warm lunchboxes developed 2 series of cycling menus for 1 week, one with large portions and another relatively fit with respect to energy and salt content. The main customers of the company are busy people who do not pay much attention to nutrition or health. The company intended to increase the variety of ingredients and tried to balance the nutrient intake if the customer purchases the same cycling menu, even without considering the contents of the lunch box. Interestingly, most of these customers purchased the large-portion meals and the fit meals alternately, that is, there was approximately a 50% improvement. This can be an important tactic for improving the nutritional status of laymen without pressing them to behave healthily.

Findings from nationwide questionnaire

JRMA distributed the questionnaire to 338 member companies online in July 2019. In total, 88 companies responded the questionnaire (response rate, 26.0%). Just 50 of the 88 responding companies had annual sales of more than JPY 1 billion. Considering the average annual sales of JRMA regular member companies of JPY 12.6 billion, response rate should have been higher in smaller companies than in large companies. The proportion of responding companies selling via supermarket was approximately twice that of the JRMA regular member companies. Therefore, the results may have sampling bias and, accordingly, may not represent the overall tendency of JRMA members.

Distributions of their main product and route of sales indicated that the composition of these companies approximately, but not entirely, reflected the composition of the JRMA ( Figure 1 ). Therefore, the results may not represent the status quo of all JRMA member companies.

Main products and routes of sales of responding Japan Ready-Made Meal Association member companies (multiple answers, n = 88). Abbreviation: EC, electronic commerce.

Approximately 60% of the responding companies had health- or nutrition-oriented wording in their management policies or on their homepage. Approximately 75% of the responding companies produced health- or nutrition-oriented products ( Figure 2 ). The responding companies most often cited Dietary Reference Intakes for Japanese 2 and Japanese Food Guide Spinning Top as the resources on which they based their the menu design ( Figure 3 ).

Health or nutrient orientation of responding companies (n = 88).

Governmental guidelines or policies on which responding companies based their menu construction (multiple answers, n = 88). *Ministry of Health, Labour and Welfare; **Ministry of Health, Labour and Welfare, and Ministry of Agriculture, Forestry and Fisheries; ***Ministry of Health, Labour and Welfare, Ministry of Agriculture, Forestry and Fisheries, and Ministry of Education, Culture, Sports, Science and Technology.

Nutrients focused on in successful health- or nutrition-oriented products were energy, carbohydrate, dietary fiber, sodium, protein, and lipid. Ingredients in successful health- or nutrition-oriented products were vegetables, whole-grain cereals, soy products, miscellaneous grains, seasoning, animal meat, seafood, fermented products, and oil ( Figure 4 ). There was no marked tendency with regard to focused nutrient or ingredient in failed health- or nutrition-oriented products.

Nutrients and ingredients focused in successful health or nutrition-oriented products (multiple answers, n = 88). Abbreviation: Na, sodium.

The challenges for responding companies in the development and sales of health- or nutrition-oriented products were to produce good-tasting products at a low cost that appeal to the consumer via an efficient production process with stabilization of the food content.

On the basis of the surveys findings, WG2 wants to highlight the importance of developing and disseminating simple and easily understandable guidelines and labeling policies for the production of healthy and nutritious ready-to-eat food/meals. In this regard, WG2 proposes to define priorities for which nutrients to increase or decrease, to prioritize target population (eg, those who are establishing food habits or those who eat without consideration of what they eat), and to indicate the maximum time to balance each nutrient.

Acknowledgments

The WG2 members sincerely express their gratitude for the generous cooperation of Japan Ready-Made Meal Association and its member companies, which was essential for conducting this study. The study plan of the survey was reviewed by the Ethics Committee for Human Studies of Ishinomaki Senshu University (application no. 2018–001) and determined to be a study not requiring the permission of the committee. Although, many authors belong to private companies, all authors wrote a pledge stating that all information gathered during this survey belongs to ILSI Japan and will not be used otherwise without the consent of ILSI Japan.

Author contributions . T.S. supervised the study. All authors equally contributed to develop the research design, conduct the survey, analyze the data, and prepare the manuscript, and all approved the final manuscript.

Funding . This research was conducted as a part of the activities of the International Life Sciences Institute Japan Research Committee, which are not compensated except for travel expenses for academia members, as required.

Declaration of interest . T.S. is a vice president and a member of the Board of Trustees for International Life Sciences Institute (ILSI) Japan. He is also a member of the organizing committee and the program committee for the 8th International Conference on Nutrition and Aging held October 1-2, 2019. R.A. is a member of the program committee for the 8th International Conference on Nutrition and Aging. Companies to which authors belong are members of ILSI Japan and support the organization’s activities.

White Paper of Japan Ready-Made Meal Association (2018) (Digest on-line edition). Japan Ready-Made Meal Association.   http://www.nsouzai-kyoukai.or.jp/wp-content/uploads/hpb-media/hakusho2018_digest1.pdf .

Ministry of Health, Labour and Welfare. Overview of Dietary Reference Intakes for Japanese (2015). Available at: https://www.mhlw.go.jp/file/06-Seisakujouhou-10900000-Kenkoukyoku/Overview.pdf . Accessed April 18, 2020.

Ministry of Health, Labour and Welfare; Ministry of Agriculture, Forestry, and Fisheries. Japanese Food Guide Spinning Top. Do you have a well-balanced diet? https://www.maff.go.jp/j/balance_guide/b_use/pdf/eng_reiari.pdf . Accessed April 18, 2020.

Ministry of Health, Labour and Welfare. A basic direction for comprehensive implementation of national health promotion. Ministerial Notification No. 430 of the Ministry of Health, Labour and Welfare. Available at: https://www.mhlw.go.jp/file/06-Seisakujouhou-10900000-Kenkoukyoku/0000047330.pdf . Accessed April 28, 2020.

Author notes

• dietary fiber
• carbohydrates
• biological sciences
• science of nutrition
• whole grains
• healthy diet
• academia (organization)

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Assessment of the Microbiological Quality of Ready-to-Eat Salads—Are There Any Reasons for Concern about Public Health?

Anna Łepecka.

1 Department of Meat and Fat Technology, Prof. Waclaw Dabrowski Institute of Agriculture and Food Biotechnology—State Research Institute, 02-532 Warsaw, Poland; [email protected]

Dorota Zielińska

2 Department of Food Gastronomy and Food Hygiene, Institute of Human Nutrition Sciences, Warsaw University of Life Sciences-SGGW, 02-776 Warsaw, Poland; lp.ude.wggs@aksnileiz_atorod (D.Z.); moc.liamg@49sarubalebazi (I.B.); lp.ude.wggs@akswejark_nyzolok_atunad (D.K.-K.)

Piotr Szymański

Izabela buras, danuta kołożyn-krajewska.

Ready-to-eat food products can be readily consumed without further preparation and are convenient for busy on-the-go consumers. The objective of the study was to assess the microbiological quality of ready-to-eat salads. Thirty RTE salads were tested for the presence of bacteria, yeasts, and molds using the TEMPO and agar plate method. The study demonstrated that most of the tested products were characterized by varying microbiological quality. The total number of mesophilic microbiotas was about 6 log CFU g −1 . The high number of microorganisms was due to yeast and molds or Enterobacteriaceae . Half of the salads were contaminated with E. coli and three salads were contaminated with S. aureus . LAB were also found, which can be explained mainly by a dairy ingredient. In some salads, Salmonella spp. and L. monocytogenes were detected (26.7% and 33.3% of the samples, respectively). Based on the conducted tests, it was found that the microbiological quality was not satisfactory. The results presented in this study indicate that there is a significant problem of the presence of pathogens. Manufacturers should strive to reduce the possibility of microbial contamination through the use of widely understood hygiene of the production process, using hurdle technology, including the modified atmosphere and refrigerated storage.

1. Introduction

Convenience food has become an alternative to traditionally prepared food. Convenience food can be defined as: food, typically a complete meal, that has been pre-prepared commercially and so requires minimum further preparation by the consumer. The market offers more and more new high-quality food products, produced using new recipes, modern production and packaging technologies [ 1 , 2 ].

Currently, the demand for ready-to-eat (RTE) products, including salads, is increasing. RTE salads are minimally processed products. By definition, minimally processed food has the appearance of fresh food, is characterized by the least changed characteristics, and is safe to eat. RTE food products can be readily consumed without further preparation and are convenient for busy consumers. The production of ready-to-eat salads is constantly growing and they are currently produced on an industrial scale [ 3 ]. The availability of both RTE fruit and vegetables on the market may contribute to increasing the consumption of fruit and vegetables in the general population and thus contribute to efforts to achieve a daily consumption of 400 g of vegetables and fruit per capita, as recommended by the World Health Organization [ 4 ]. It was estimated that in Europe in 2021, the average amount of ready-to-eat meals consumed per person was about 15 kg [ 5 ].

In addition to providing the necessary ingredients, food items should be characterized by health quality, including appropriate microbiological quality, guaranteeing safety to health. Healthy food quality depends on the conditions and ways of obtaining the raw materials, pre-treatment and thermal processing, storage, transport, and conditions of sale [ 3 ]. All these operations can result in damage to the natural barrier of the epidermis and disrupt the internal compartmentalization, which in turn separates enzymes from substrates, thus, promoting microbial proliferation and inducing increased respiration in the plant. This, in turn, results in an increase in metabolism and the aging of tissues [ 4 ]. Due to numerous cases of food poisoning caused by microorganisms and toxins found in food, research and the control of food products are important. There are legal regulations regarding food, defining microbiological criteria and limits for the occurrence of microorganisms in food. These criteria, however, apply to selected food groups and regulate the selected acceptable limits of microorganisms [ 6 , 7 ].

According to the WHO [ 8 ], 550 million people suffer from Salmonella poisoning every year, and about 220 million of them are children under 5 years of age. Salmonella is one of the four key global causes of diarrheal diseases. Currently, in the European Union, salmonellosis is the second most deadly disease, after campylobacteriosis, causing food poisoning [ 9 ] with a notification rate of 20.0 cases per 100,000 population [ 10 ]. The trend towards human salmonellosis has been stable over the past five years after a long period of a downward trend. Additionally, Salmonella Enteritidis caused the vast majority (72.4%) of food-borne salmonellosis outbreaks [ 10 ].

Subsequently, 1 million people suffer from listeriosis per year [ 11 ]. Unfortunately, most cases require hospitalization. According to EFSA and ECDC [ 9 ], the number of poisonings by Listeria monocytogenes in the European Union is constantly increasing. The listeriosis notification rate is 0.47 cases per 100,000 people [ 12 ]. One of the reasons for this increase is the interest in ready-to-eat products. Based on the EFSA and ECDC study [ 9 ], L. monocytogenes was found in RTE foods in the largest number of samples of fish and fish products (6.0% of samples), salads (4.2% of samples), meat and meat products (1.8% of samples), soft and semi-soft cheeses (0.9% of samples), fruit and vegetables (0.6% of samples), and hard cheeses (0.1% of samples). According to the EFSA BIOHAZ Report [ 13 ] ready-to-eat salads were found to be the main source of poisoning by L. monocytogenes . In 2013, in Germany, three human cases of listeriosis were found after eating ready-to-eat vegetables, juices, and mixed salads (one death was reported). In the same country, in 2014, two cases were observed after eating mixed food (iceberg lettuce with yogurt dressing, and gouda cheese). In Switzerland, thirty-one human listeriosis cases were found in 2014 (four deaths were reported). L. monocytogenes were found in ready-to-eat vegetables, juices and pre-cut salads.

Ready-to-eat salads could show the presence of various microbial pathogens including Escherichia coli , Staphylococcus aureus , Salmonella spp., Listeria monocytogenes , Campylobacter jejuni , Clostridium perfringens , total aerobic and spoilage bacteria, yeasts, and molds, which are concerned with serious threats [ 14 , 15 ]. In addition, a high number of microorganisms are also becoming a reservoir of antibiotic resistance genes, which has now become a global problem [ 16 , 17 ].

Although the European Commission Regulation No. 852/2004 [ 18 ] on the hygiene of foodstuffs requires businesses to implement Good Hygiene Practice and a food safety management system based on hazard analysis and critical control point (HACCP) principles, many authors indicated that RTE food causes high microbiological risk [ 19 ]. However, the knowledge of factors affecting the quality of RTE foods is still inconclusive.

The main objective of this study was to assess the microbiological quality of ready-to-eat salads from the Polish market and to evaluate whether the composition, time, and method of packaging had an impact on the shelf life of these salads.

2. Materials and Methods

2.1. materials.

Thirty salads were purchased in autumn at several discount stores from the Polish market (Warsaw) and retail chains. The products were fresh, before the expiry date, transported in thermal bags, and then refrigerated (4–8 °C) until the beginning of the study. The samples were tested on the day of purchase. All of the products were tightly packed in plastic boxes like ‘lunch boxes’. Three salads of each type were purchased from the same production batch and tested. Table 1 and Table 2 present information about the tested salads according to the manufacturers’ declarations.

Ingredients of the tested salads according to the producer’s declaration.

Nutritional value and other information about the salads.

Explanatory: (+)—modified atmosphere/preservatives presence; (−)—modified atmosphere/preservatives absence.

The mixed ingredients of the ready-to-eat salads included raw and cooked ingredients, e.g., vegetables (leafy vegetables, cherry tomatoes, and carrots), meat (ham, smoked chicken, and grilled chicken), fish (salmon and tuna), cheeses, and carbohydrate sources (pasta, and buckwheat). The tested salads differed in composition, shelf-life, the way they were packed and storage temperature. The recommended maximum storage temperature as indicated on the label was 10 °C. The shelf life was 1–7 days. Some of the salads had dressings/sauces in sachets and some of the salads were mixed and ready to eat. In most cases, the producers did not give the composition of the dressings/sauces. Some of the dressings/sauces in the salads were with the addition of preservatives.

2.2. Methods

2.2.1. samples preparation.

Three salads were prepared from each production batch. First, 25 g of the salad product was weighed by taking different ingredients to obtain a representative sample. Then, 225 mL of peptone water (BioMaxima, Lublin, Poland) was added and homogenized in a stomacher (Stomacher 80 Biomaster, Seward Limited, London, UK) for 5 min. Filtered stomacher bags (BagFilter ® 400 P, Interscience, Paris, France) were used to eliminate any solid particles. Decimal dilutions were made, and the prepared samples were used for further testing.

2.2.2. Microbiological Analysis

Microbiological tests (count of aerobic mesophilic total flora, Staphylococcus aureus , Enterobacteriaceae , Escherichia coli , lactic acid bacteria, yeasts, and molds) were carried out using the TEMPO ® system (bioMérieux, Marcy-l’Étoile, France). The dehydrated culture media in the bottles were prepared by adding 3.9 mL of sterile distilled water. Then, 0.1 mL of the sample solution was added to them in a suitable dilution and vortexed (5–10 s; Heidolph, Schwabach, Germany). The samples were incubated in INE 400 Incubator (Memmert GmbH + Co.KG, Buechenbach, Germany) according to the manufacturer’s manual. The results are presented on a logarithmic scale (log CFU g −1 ) and standard deviation.

The samples were analyzed for the presence of microorganisms commonly isolated from RTE vegetables, i.e., Salmonella spp. and L. monocytogenes . The plate method was used according to ISO standards [ 20 , 21 ].

The samples of the salads (25 g) were mixed with peptone water (BioMaxima, Lublin, Poland) and incubated at 37 °C for 24 h to pre-incubation. For selective propagation, nutrient broth (BioMaxima, Lublin, Poland) was used. An aliquot of 1 mL was withdrawn and transferred to 9 mL of broth and incubated again at 37 °C for 24 h. Sterile Petri dishes were poured into 15–20 mL of BGA (Brilliant Green Agar; Oxoid, Waltham, MA, USA) and, after setting with an automatic pipette, surface culture was performed. Subsequently, 0.1 mL of the sample was applied to the surface of the substrate and spread over the substrate with a sterile paddle. The cultures were incubated at 35 °C for 24 h. In the case of a positive result on the BGA, a confirmation on the XLD agar was made (Xylose Lysine Deoxycholate agar; LabM, Heywood, UK). Agar was poured onto a sterile plate and the surface was set after solidification. Subsequently, 1 mL of the inoculated nutrient broth was applied to the surface of the medium and spread over the substrate. The plates were incubated at 37 °C for 24 h. The results are presented as the presence (+) or absence (−) of Salmonella spp.

Samples of the salads (25 g) were mixed with half-Fraser broth (Oxoid, Waltham, MA, USA) and incubated at 37 °C for 24 h. Then, 1 mL was removed and transferred to the Fraser broth (Oxoid, Waltham, MA, USA) and incubated for 24–48 h. In sequence, 15–20 mL of ALOA (Agar Listeria according to Ottaviani and Agosti; LabM, UK) was poured onto sterile plates and the surface was set after setting. Using an automated pipette, a 1 mL test sample was applied to the surface of the substrate and spread evenly over the substrate using a sterile paddle. The cultures were incubated at 37 °C for 24 h. In the case of a positive result on the ALOA, a confirmation on the PALCAM agar was made (LabM, Heywood, UK). Agar was poured onto a sterile plate and the surface was set after solidification. Subsequently, 1 mL of the inoculated Fraser broth was applied to the surface of the medium and spread evenly over the substrate. The plates were incubated at 37 °C for 24 h. The results are presented as the presence (+) or absence (−) of Listeria monocytogenes .

2.2.3. Statistical Analysis

Microbiological tests were performed in three replications (three repetitions with three different products from the same batch). All of the data were analyzed using the Statistica 13 (TIBCO Software Inc., Palo Alto, CA, USA). Correlation coefficients were calculated and a principal components analysis (PCA) using a correlation matrix and a cluster analysis was performed

3. Results and Discussion

The tested salads were characterized by different microbiological quality. Table 3 below shows the results of the number of selected microorganisms and the results of the presence of Salmonella spp. and L. monocytogenes .

Microbiological quality of the tested RTE salads.

Explanatory: AC—aerobic mesophilic total flora, STA— S. aureus , EB— Enterobacteriaceae family, EC— E. coli , LAB—lactic acid bacteria, YM—yeasts and molds; SAL— Salmonella spp., LM— L. monocytogenes ; <1.00—below the detection level. The results are shown as log CFU g −1 ; means ± standard deviation; (+) presence of bacteria in 25 g of the product, (−) absence of bacteria in 25 g of the product; n = 3.

There are not many studies on microbiological tests on salads with dressings/sauces. Typically, the studies apply only to raw vegetables or salad blends [ 22 , 23 , 24 , 25 , 26 , 27 , 28 ], only dressings/sauces and pesto [ 29 ], or RTE products in general [ 30 ]. These mixtures are the least processed and form a large part of the product, but they are not the only factors that determine the quality of the final product. When ingredients are mixed together with green leaves, cross-contamination may occur at any point in the production chain to consumption. Cross-contamination can occur during processing when the equipment in contact with potentially contaminated products is not regularly sanitized and cleaned [ 31 ].

Although there are no established microbiological criteria for ready-to-eat foods in the European Union, the only applicable regulation is Commission Regulation 1441/2007 (formerly Commission Regulation 2073/2005) [ 6 , 7 ]. However, it does not include this category of food, but only their individual components. For fruit and vegetables, the limit is established for bacteria E. coli (1000 CFU g −1 of product) and precut ready-to-eat fruit and vegetables are limited in Salmonella (absence in 25 g of product). Ready-to-eat meat products are limited in L. monocytogenes (100 CFU g −1 of a product or absence in 25 g of a product) [ 7 , 32 ].

Although the total viable count is not a legislation criterion for RTE salads, it is an important hygienic and sensory quality indicator, which may inform about the total microbiological status of the food. In the present study the total number of aerobic mesophilic microorganisms found in the tested salads were on a different level and, on average, about 6 log CFU g −1 (ranged from 2.36 log CFU g −1 to 9.30 log CFU g −1 ) ( Table 3 ). The lowest total viable count of microorganisms was evaluated in salad S4. Salads S8, S9, S10, S11, S16, S19, and S23 were characterized by a high number of total viable counts. The high numbers of organisms in S16 and S23 salads were due to the high number of yeast and molds (7.00 log CFU g −1 and 6.60 log CFU g −1 , respectively) or Enterobacteriaceae family bacteria (6.84 log CFU g −1 ). In salads S16, S19, and S23, high numbers of lactic acid bacteria were found. The count of total microbiota in the salads in this study was similar to those observed in Polish studies by Berthold-Pluta et al. [ 33 ] who reported that the count of aerobic mesophilic total microbiota in leafy vegetables and their mixes ranged from 5.6 log CFU g −1 to 7.6 log CFU g −1 . Similarly, Jeddi et al. [ 34 ] reported that the total mesophilic microbiota observed in vegetables from Iran ranged from 5.3 log CFU g −1 to 8.5 log CFU g −1 . Importantly, the count of aerobic mesophilic microbiota is an indicator of only the overall microbiological quality of a food product and that there are no binding standards for the quality of products of this type [ 33 ]. In general, aerophilic microbiota is capable of growing, even at low temperatures; hence, its high number even when products are stored in a refrigerator. The high number of packed ready-to-eat salads of all types of vegetables in Portugal was classified as unsatisfactory due to the presence of more than 6 log CFU g −1 aerobic mesophilic microorganisms, even if Salmonella and L. monocytogenes were not detected in any ready-to-eat salad samples [ 35 ]. Adopting only this criterion in our research, we should classify 18 out of 30 of the tested salads as being unsatisfactory.

In three of tested salads (S7, S17, and S18) the S. aureus bacteria (2.00 log CFU g −1 , 3.54 log CFU g −1 , and 2.9 log CFU g −1 , respectively) ( Table 3 ) was revealed. In seven samples of salads (S7, S9, S10, S13, S14, S15, and S23), bacteria of the Enterobacteriaceae family in a number higher than 6 log CFU g −1 were found, which indicates a high degree of microbiological contamination. Leff and Fierer [ 36 ] reported that vegetables, e.g., spinach and lettuce, were mainly affected by the Enterobacteriaceae family and half of the salads were contaminated with E. coli . Salads S6, S8, S14, and S23 showed high contamination levels with E. coli (more than 1000 CFU g −1 limited according to the Commission Regulation 1441/2007). In the study of Faour-Klingbeil et al. [ 37 ], in vegetable salads, a high number of bacteria Staphylococcus spp. (1.83–7.76 log CFU g −1 ) and bacteria from the E. coli group (0.33–7.15 log CFU g −1 ) were found, which indicates the possibility of the large contamination of vegetable salads with these bacteria. De Oliveira et al. [ 38 ] reported high contamination vegetable salads with E. coli (53.1% of tested samples). As the authors emphasize, the determination of E. coli is a good indicator for fecal infections, referring to fresh, cut leafy vegetables. Other authors have reported that almost all of the salad samples in Ghana were contaminated with E. coli and Bacillus cereus bacteria (96.7% and 93.3%, respectively) [ 39 ].

Lactic acid bacteria (LAB) were also found in the tested salads, which can be explained mainly by the presence of dairy additives as a salad ingredient, e.g., yogurt, cheese, blue cheese, and mozzarella (salads S1, S3, S5, S6, S7, S8, S9, S14, S19, S23, and S25), or pickled products like pickled cucumber (salads S16 and S18) ( Table 3 ). LAB are a natural vegetable microbiota [ 40 ], but may also contaminate a product [ 41 , 42 ]. Some LAB were found in fresh-cut vegetables (like iceberg, lettuce, or endive). A high number of LAB also affects the total number of bacteria, greatly overstating them. In the majority of the samples tested, a significant of yeast and mold was found (1.00–7.00 log CFU g −1 ). Significant yeast and mold contamination of food products of this type was also determined by Abadias et al. [ 43 ]. The observed numbers of yeasts and molds were lower than bacteria. Furthermore, the ranges in fresh-cut vegetables were from 2.0 log CFU g −1 to 7.8 log CFU g −1 .

Fresh plant-origin products may be a vehicle for the transmission of bacterial pathogens, e.g., E. coli , S. aureus, L. monocytogenes , and Salmonella spp. Food contaminated by fecal microorganisms may be a source of antibiotic resistant organisms that can cause infections in people. Raw vegetables that are particularly vulnerable to contamination with bacteria are: lettuce, spinach, cabbage, cauliflower, celery, broccoli, and all salads packaged in a modified atmosphere [ 44 ]. Among animal products, poultry, meat, and eggs are the main infection sources of Salmonella [ 45 , 46 ].

The microbiological criterion for Salmonella spp. and L. monocytogenes in freshly-cut vegetables is an absence in 25 g of food [ 7 ]. In the salad samples S2, S5, S11, S14, S18, S19, S20, S21, S23, S25, S26, S27, S29, and S30, no pathogenic Salmonella and L. monocytogenes were found (46.7% of samples). Salmonella spp. were found in eight of the tested salads (salads S1, S3, S4, S6, S8, S16, S17, and S24). The L. monocytogenes species were detected in salads S7, S9, S10, S12, S13, S15, S16, S17, S22, and S28 ( Table 3 ). The presence of these indicates high microbiological contamination and may be the cause of being affected by one of the diseases, such as salmonellosis or listeriosis. In the study of Abadias et al. [ 43 ] Salmonella strains were detected in corn salad, lettuce, spinach, and mixed salads (1.7% of samples were contaminated). In other studies, the occurrence of Salmonella in RTE vegetables varies, but usually does not exceed more than a few percent [ 38 ].

Bacteria in the Listeria genus are found in a variety of products, and they are clearly evident in minimal processed food. Listeria is a bacterium with a broad spectrum of development, capable of growing in harsh environmental conditions, and has the ability to create biofilms which may be the cause of cross-contamination [ 47 , 48 , 49 ]. According to the meta-analysis provided by Churchill et al. [ 50 ], the summary estimate of the prevalence of L. monocytogenes was 2.0% in packaged salads. In the study of Söderqvist et al. [ 26 ], L. monocytogenes was isolated from 1.4% of all RTE tested salads. This is a much lower percentage of contamination compared to our own research, as well as the EFSA and ECDC results (13.8%) [ 9 ]. According to the Scientific Report of EFSA [ 51 ], in 2010–2011, ready-to-eat samples were contaminated with L. monocytogenes (1.7%, 0.43%, and 0.06% for fish, meat, and cheese samples, respectively). Gurler et al. [ 52 ] found L. monocytogenes and Salmonella spp. Contamination in RTE foods commercialized in Turkey (6% and 8%, respectively). RTE meat products can be contaminated during or after processing by L. monocytogenes and Salmonella spp. [ 32 ]. Moreover, all of the Salmonella spp. And L. monocytogenes isolates exhibited resistance to one or more of the antimicrobial agents used. The results indicate the need to improve hygiene standards and implement regulations in the RTE food chain in order to ensure microbiological safety. On the other hand, Koseki et al. [ 53 ] presented data about iceberg lettuce in Japan. No pathogenic bacteria, i.e., Salmonella , E. coli O157:H7 and L. monocytogenes , were found. The results of the study could be used to develop risk management policies. In similar results, no pathogenic Salmonella in 233 vegetables, freshly-cut fruits and sprout samples, were detected by Althaus et al. [ 54 ]. Xylia et al. [ 19 ] reported that RTE salads from the Cypriot market are free from S. enterica and L. monocytogenes .

The principal components analysis (PCA) was used to analyze data obtained in the present study and revealed 20 factors that determine the quality of salads, where the first two explain 37.37% of variable variances. A dispersion of the first two factors (PC1 and PC2) on the surface is shown below in Figure 1 and Figure 2 .

Dispersion of quality factors on a surface for the first two principal components (PC). Explanatory: AC—aerobic mesophilic total flora, STA— S. aureus , EB— Enterobacteriaceae family, EC— E. coli , LAB—lactic acid bacteria, and YM—yeasts and molds.

Projection of samples on a surface for the first two principal components (PC).

It was found that the modified atmosphere of package (samples S1, S2, S3, S4, S5, and S6) and preservatives (samples S2, S4, S5, and S14) used in the tested salads were negatively correlated with total aerobic microbiota (−0.46 and −0.42, respectively), as well as with L. monocytogenes presence (−0.35 and −0.28 respectively). Milk ingredients used in salads were correlated with lactic acid bacteria occurrence (0.53), whereas meat (S17) and eggs (S18) were correlated with S. aureus presence (0.31 and 0.37, respectively). On the other hand, salt added to salads was important to prevent Salmonella and yeast and molds developing (−0.45 and −0.33, respectively).

The number of bacterial cells may indicate the contamination of a product, its degree of deterioration, but also may be part of the natural microbiota of the food product. According to FAO/WHO [ 55 ], leafy vegetables (spinach, cabbage, lettuce, and watercress) and fresh herbs (cilantro, basil, chicory, and parsley) are a group with a very high microbiological risk. The threat is mainly E. coli , S. enterica , Campylobacter , Shigella spp., Hepatitis A virus, Noroviruses, Cyclospora cayetanensis , Cryptosporidium , Yersinia pseudotuberculosis , and L. monocytogenes . Leafy vegetables, as a rule, cannot be subjected to thermal treatment, which prevents the deactivation of microorganisms. The cleaning of leaves is a crucial stage in the production process. Moreover, other factors can extend the shelf-life of a product, especially used as hurdle technology.

Increased hygiene at every stage of the production process, application of GHP, GMP, and HACCP principles in the production plant, as well as maintenance of the refrigeration sequence in product storage, can increase the microbiological safety of RTE products [ 3 , 56 , 57 ]. Furthermore, packaging is a key element in the production of ready-to-eat salads, which was found in our study. Samples in which a modified atmosphere was used had lower total aerobic bacteria, as well as the L. monocytogenes count; however the presence of Salmonella spp. was higher. These results being somehow inconsistent, may be a basis for further in-depth research, including more research samples. Packing in a modified atmosphere, which involves the use of a composition of non-atmospheric gases inside the package and the use of appropriate packaging made from permeable materials, was found as an effective method [ 24 , 58 , 59 , 60 ]. The shelf-life of pre-packed salads is determined by microbial and chemical changes. According to Mir et al. [ 61 ] commonly used techniques for the shelf-life prolongation of RTE foods are sanitizers, modified atmosphere packaging, refrigeration, irradiation, high pressure processing, and essential oils.

In ensuring the microbiological safety of products, it is also essential to maintain an appropriate storage temperature [ 28 ]. A low temperature, usually kept at 0–4 °C, inhibits the biochemical and chemical processes of microorganisms, which inhibits their growth in the food product [ 61 ]. Söderqvist et al. [ 26 ] recommended a temperature lower than 4 °C, while the salads tested in this study had the recommended temperature by the manufacturer even up to 10 °C. A low temperature is necessary to prevent the growth of psychrotrophs (like L. monocytogenes ) [ 62 ]. Ziegler et al. [ 63 ] recommended a temperature lower than 5 °C, which could help minimize the risk of L. monocytogenes in RTE salads. Xylia et al. [ 19 ] suggest that shelf-life testing is essential to understanding and developing novel techniques to monitor the safety and quality of ready-to-eat products.

4. Conclusions

Based on the conducted tests, it was found that the microbiological quality of the evaluated ready-to-eat salads was not satisfactory from the safety point of view. Due to the increased interest of consumers in vegetable salad mixes with meat, fish, or cheese, carbohydrate additives (e.g., pasta and toast), and the dressings/sauces available on the market as ready-to-eat products, it is very important to study their microbiological quality. These products are minimally processed; the risk of contamination with microorganisms, including pathogenic ones, is high.

The results presented in this study indicate that there is a significant problem of the presence of pathogenic microorganisms, mainly L. monocytogenes and Salmonella sp. in ready-to-eat salads. Although no negative visual changes of the products were observed, there were a high number of bacteria, yeast, and molds in the products. It is noteworthy that although the products appear edible according to visual inspection, they often contain microorganisms that cause product spoilage, because the first signs of product spoilage may not be visible. Taking into account the limitation of the study, which was the number of samples, future investigation should include more research samples, differentiated in terms of the packaging method and season. Such data would provide valuable information and are in the great interest both of legislators and producers of food products.

It can be summarized that RTE food manufacturers should strive to reduce the possibility of microbial contamination, through the use of widely understood hygiene production guidelines, using hurdle technology, which includes the modified atmosphere and storage of products, especially with a temperature below 5 °C. Where possible, the heat treatment of raw ingredients should be carried out, and raw products, i.e., leafy vegetables, should be thoroughly subjected to washing and drying processes.

Author Contributions

Conceptualization, A.Ł.; methodology, A.Ł. and D.Z.; formal analysis, A.Ł. and P.S.; investigation, A.Ł. and I.B.; resources, A.Ł.; writing—original draft preparation, A.Ł. and D.Z.; writing—review and editing, P.S. and D.K.-K.; visualization, A.Ł. and D.Z.; supervision, D.K.-K. All authors have read and agreed to the published version of the manuscript.

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Conflicts of interest.

The authors declare no conflict of interest.

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