literature review zoonotic diseases

• Open access
• Published: 16 July 2021

Identifying the research gap of zoonotic disease in displacement: a systematic review

• Dorien Hanneke Braam   ORCID: orcid.org/0000-0002-6011-2392 1 ,
• Freya Louise Jephcott 1 &
• James Lionel Norman Wood 1  

Global Health Research and Policy volume  6 , Article number:  25 ( 2021 ) Cite this article

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Outbreaks of zoonotic diseases that transmit between animals and humans, against a backdrop of increasing levels of forced migration, present a major challenge to global public health. This review provides an overview of the currently available evidence of how displacement may affect zoonotic disease and pathogen transmission, with the aim to better understand how to protect health and resilience of displaced and host populations.

A systematic review was conducted aligned with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) reporting guidelines. Between December 2019 - February 2020, PubMed, Web of Science, PLoS, ProQuest, Science Direct and JSTOR were searched for literature. Studies were included based on a focus on zoonotic disease risks in displacement and/or humanitarian emergencies, and relevance in terms of livestock dependency of the displaced populations. Evidence was synthesised in form of a table and thematic analysis.

Of all records, 78 papers were selected for inclusion. Among the included studies, the majority were based on secondary data, including literature reviews (n=43) and case studies (n=5), while the majority of papers covered wide geographical areas such as the Global South (n=17) and Africa (n=20). The review shows significant gaps in the literature, which is specifically lacking primary data on zoonotic diseases in displacement. Risk factors for the transmission of zoonoses in displacement are based on generic infectious disease risks, which include the loss of health services, increased population density, changes in environment, reduced quality of living conditions and socio-economic factors. Regardless of the presence of these disease drivers during forced migration however, there is little evidence of large-scale zoonotic disease outbreaks linked directly to livestock in displacement.

Due to the lack of primary research, the complex interlinkages of factors affecting zoonotic pathogen transmission in displacement remain unclear. While the presence of animals may increase the burden of zoonotic pathogens, maintaining access to livestock may improve livelihoods, nutrition and mental health, with the potential to reduce people’s vulnerability to disease. Further primary interdisciplinary and multi-sectoral research is urgently required to address the evidence gaps identified in this review to support policy and program development.

Research shows that most emerging infectious diseases in humans have animal origins, either originating in domestic animals or wildlife [ 1 ], while neglected and endemic zoonoses, continuously transmitted between livestock and humans, are a significant burden to public health and livelihoods [ 2 ]. The transmission of zoonotic pathogens depends on complex interactions between susceptibility, periodicity and anthropogenic activities [ 3 ], influenced by a range of ecological, political and socio-economic drivers [ 3 , 4 , 5 ]. Poverty and low socio-economic status are among the most important determinants of people’s vulnerability to disease [ 6 ], with people whose livelihoods are affected by conflict or disasters therefore considered to be at an even higher risk. Humanitarian emergencies may result in the displacement of human and livestock populations. Movement is associated with increased mixing of displaced and host populations’ and their livestock, and increased contact between domestic animals, wildlife and humans, which risks increased disease transmission between species. Where animals and humans move into new environments, they may face new pathogens and vectors prevalent among local animal and human populations – the ‘host’ population to the displaced, against which they lack immunity. Health services and staff may be affected or become displaced themselves, hampering an organized response, exacerbating zoonotic disease outbreaks [ 6 ].

The number of displaced people is consistently growing [ 7 ], increasingly caused by environmental drivers [ 8 ]. Many of these forced migrants move in regions dependent on agriculture and livestock [ 9 ]. As livestock are relatively mobile, these are often among the few assets people bring along, however currently animals are largely banned in formal relief camps, due to the hypothetical increased risk of zoonotic disease. In response, displaced people may abandon or sell their animals before or during displacement, affecting people’s nutrition, psychosocial health, and ability to rebuild livelihoods [ 10 ]. The lack of access to formal relief camps of livestock because of zoonotic disease concerns acts as a deterrent from accessing services, as households or individual family members may opt to stay behind with the herds [ 11 ]. Lacking the provision of protection, water and feed for their animals in formal humanitarian responses, owners may adapt by letting their herds graze among host communities’ livestock, or encroach on wildlife habitat, increasing the risk of introduction of zoonotic pathogens to naïve populations, further increasing the risk of zoonotic disease [ 12 ].

Due to a lack of primary research addressing zoonoses in displacement contexts, zoonotic disease dynamics and related risks in displacement are not well understood. The purpose of this literature review is to identify research gaps and analyse the current available evidence on zoonotic disease in displaced populations.

Search strategy

This literature review was conducted based on the Preferred Reporting Items for Systematic Reviews and meta-Analysis (PRISMA) statement [ 13 ]. The database search was carried out between December 2019–February 2020, using the databases of PubMed, Web of Science, PLoS, ProQuest, Science Direct and JSTOR. To capture all available publications discussing zoonoses in displacement, the search strategy used a variety and combinations of search terms related to displacement, zoonotic diseases and humanitarian emergencies. No parameters were set regarding time period.

Study selection

Papers were only considered if the full text was available in English, thereby introducing a potential publication bias. All available abstracts were screened and included based on their focus on zoonotic disease risks in displacement and/or humanitarian emergencies, and relevance in terms of livestock dependency of the displaced populations. Duplicates were excluded from the review. The most important (grey) literature references within the literature were included in screening, based on the number of times these were referenced in various literature sources.

Quality assessment

The quality of eligible studies was assessed through a full-text review, evaluating the quality of literature reviews and primary data using the Critical Appraisal Skills Programme (CASP) model. Any disagreements were resolved through discussion.

Data extraction and analysis

All included papers were subject to a full-text analysis using a thematical analysis to develop an evidence matrix, which captured relevant data from each source using the main themes emerging from the literature. Themes captured included references to animal movement, causes and type of displacement, the effect of displacement on socio-economic, environmental, and biological factors. All literature was screened with a focus on the impact of (livestock) displacement on health systems, infectious disease outbreaks, disease dynamics and references to zoonoses in particular. Eventually, 78 papers were included in the systematic literature review for qualitative analysis (Fig.  1 ).

PRISMA systematic review protocol diagram for the literature selection and narrative synthesis

In this literature review we provide an overview of the currently available evidence of 1) zoonotic diseases associated with displacement contexts, and 2) drivers during displacement affecting zoonotic pathogen transmission risks, followed by a discussion addressing 3) gaps in the literature, and 4) current risk mitigation measures, concluding with entry points for further research to increase understanding on how to protect health, livelihoods and resilience of displaced populations, host communities and livestock.

The volume of publications identified in the review increases over time, with most of the included literature published within the last five years (Fig.  2 ).

Volume of relevant publications since 1986

Our review shows that there is a lack of primary research data. Over 55% of publications are literature reviews (n=43) or case studies based on secondary data (n=5) often with a qualitative focus. Case study findings through primary research were discussed in 20 papers, while 3 were program outcome reports. The other documents included dynamic disease models and United Nations (UN) documents (Fig. 3 ).

Type of publications included in the literature review

No publication focused on the specific risk of zoonoses related to livestock movement during displacement.

Geographically, studies included in the review are primarily global reviews (n=17), or focus on the ‘Global South’, a region disproportionally affected by forced displacement. In addition to regional reviews (n=7), papers cover individual countries in Africa (n=20), South Asia (n=9) and the Middle East (n=8), all areas with high levels of displacement and livestock dependency, with a growing body of literature discussing the adverse impact of the conflict in Syria (n=5) []. Papers focusing on Pakistan primarily discuss Afghan refugee health, which remains one of the largest refugee populations in the world. Three papers focus on South America and two on Southeast Asia, but no relevant literature covered East Asia or the Pacific (Fig.  4 ).

The number of publications focusing on specific geographical regions and countries

Most publications focus on general infectious disease risks in humanitarian emergencies, which sometimes include zoonotic diseases or symptoms, which may be attributed to zoonoses. There is a gap in the literature related to livestock in displacement and the associated risk of zoonotic diseases, resulting in assumptions regarding risk factors and transmission routes.

Diseases associated with humanitarian emergencies

While disasters and conflict do not directly cause infectious diseases [ 14 , 15 ], a disaster or conflict can ‘eliminate pre-existing barriers separating hosts and agents’ through the destruction of physical structures [ 16 ], introducing pathogens to naive populations. Injuries can lead to infections where pathogens are present [ 16 , 17 ]. Watson et al [ 18 ] note that vector-borne, water and crowding-related diseases are the most common causes of epidemics after disasters, with up to 75 percent of mortality due to both zoonotic and non-zoonotic diseases. Regular occurring infectious diseases and symptoms following emergencies are diarrhea, malaria, measles, pneumonia, upper and lower respiratory tract infections, skin diseases, tetanus and anaemia, several of which may be attributed to zoonoses [ 14 , 19 , 20 ]. Diarrhea is one of the main causes of morbidity and mortality in emergencies, especially among young children [ 15 , 21 ]. In flood-related disasters eye infections, leptospirosis, hepatitis and leishmaniasis are also common (Fig.  5 ) [ 22 , 23 ].

Symptoms and diseases associated with humanitarian emergencies (as referred to in > 2 independent reviewed articles)

Among the variety of symptoms and infectious diseases identified in the literature are a number of zoonotic diseases and/or symptoms which may be caused by zoonoses, although there remains a lack of primary data. Heath et al [ 24 ] identified diseases potentially affecting livestock following disasters including parasites, respiratory infections and skin diseases, some of which zoonotic. Human disease outbreaks associated with population displacement include Ebola, Lassa fever and tuberculosis [ 17 , 25 , 26 ] (Table  1 ).

Disease drivers in displacement

Displacement as a result of disasters and conflict is considered a major risk factor for pathogen transmission, including zoonoses [ 6 , 18 , 48 , 51 , 54 , 57 ]. Mortality among refugees is reported to be as much as 60 times a population’s pre-disaster baseline [ 15 ]. Writing about the risks of displacement to Lassa fever outbreaks, Lalis et al [ 46 ] acknowledge however that other socio-economic and political factors may influence health outcomes. Rather than considering displacement as an independent risk factor, human and animal movement are more likely to exacerbate a range of other disease drivers.

Health systems

The breakdown of health systems and related infrastructure is considered a major risk factor for pathogen transmission during emergencies and displacement [ 6 , 14 , 19 , 27 , 36 , 64 ], affecting a population’s health status and immunization coverage, increasing susceptibility to disease [ 49 ]. Healthcare and veterinary services may deteriorate or get overwhelmed [ 14 ], and public expenditure into the system often decreases [ 25 , 35 , 37 ]. Medical staff become exhausted, injured or displaced themselves, while a loss of management hampers the distribution of resources, supplies and equipment [ 34 ]. An interruption in health services affects surveillance, prevention, diagnosis and treatment and control programmes including vaccinations, quarantine and vector control [ 15 , 44 , 53 , 55 ], the provision of medication and follow-up [ 19 , 64 ]. Clinics and other facilities, such as laboratories, may be destroyed or otherwise become inaccessible [ 18 , 44 ], while cold chains for vaccine and medicine storage and transfer become interrupted or unavailable [ 34 , 51 ].

Decreased immunization among displaced populations, or immunization gaps between refugees and the host population, increases the risk of vaccine preventable diseases [ 34 , 64 ], although most of these are not zoonotic. A lack of quarantine and immunization of new arrivals may cause disease outbreaks among displaced and host populations [ 65 ]. The collapse of veterinary public health systems in Syria was associated with an increase in zoonotic leishmaniasis, brucellosis and rabies cases [ 28 ], including in neighbouring countries, as shifting control of geographical locations between government and opposing forces in Syria challenged disease surveillance and control [ 64 ]. During Venezuela’s recent displacement crisis vector-borne diseases re-emerged due to the lack of control programmes, resulting in outbreaks in neighbouring countries [ 59 ]. Meanwhile, the lack of vaccinations and surveillance led to outbreaks of infectious diseases among displaced and returned populations in Pakistan after the floods in 2010, including the zoonoses Crimean-Congo haemorrhagic fever [ 62 ].

Environment

Pathogen prevalence, available vectors and suitable hosts determine the risk of infectious disease outbreaks [ 27 , 61 ]. Humanitarian emergencies may alter the natural environment, thereby affecting pathogen and vector ecology, including selection pressure, development, survival, modification and transmission rates [ 30 , 38 , 63 ]. Structural damage during conflict and disasters has shown an increase in rodent populations and associated diseases [ 36 ]. Displacement may modify the environment through deforestation, the construction of settlements and irrigation, all affecting pathogen and vector dynamics [ 19 , 38 ]. Lassa fever outbreaks for instance occurred among populations of refugee camps in West Africa due to ecological changes, impacting the size and genetic variability of the rodent and pathogen populations attributed to forest and habitat destruction, in combination with poor living and food storage conditions attracting rodents [ 36 , 46 ].

Population displacement changes the geographic distribution of susceptible populations [ 26 ] and pathogens [ 38 ], altering the rates and nature of contact between human and animal populations, increasing the risks of bites and zoonotic diseases [ 1 , 27 , 39 ]. Livestock movement further extends the range of pathogens and vectors threatening naïve host populations [ 38 , 42 , 66 ].

Displaced populations may enter new ecological zones without immunity to local pathogens [ 10 , 19 , 38 , 67 ], or introduce pathogens to naive host populations by mixing infected and susceptible herds with different levels of pre-existing immunity and immune responses [ 6 , 40 , 52 , 59 ]. Afghan refugee movements for instance are linked to the reintroduction of cutaneous leishmaniasis to Pakistan into areas where the sandfly vector is endemic [ 58 , 68 ], as well as other zoonoses [ 61 ]. Similarly, the disease resurfaced in neighbouring countries to Syria following the outbreak of conflict, associated with population movements into previously uninhabited sandfly habitats [ 28 , 56 , 57 ].

Population density

Overcrowded camps and inadequate facilities are major risks to health, including interspecies and intraspecies infection [ 18 , 19 , 25 , 27 , 31 , 34 , 36 , 39 , 42 , 50 , 62 ]. As the transmission of zoonotic pathogens is linked to the close association of humans and their livestock [ 5 , 40 , 60 ], these risks increase in areas where animals and humans share compounds in densely populated areas [ 10 , 36 , 54 , 61 ]. Sedentary conditions in relief camps and informal settlements further increases the risk of intraspecies zoonotic pathogen transmission, once the disease has become endemic among the human population [ 32 , 38 , 42 ], as population size and density affects the probability of pathogens to infect susceptible hosts [ 17 , 47 , 58 , 60 , 65 ].

Water and sanitation

Standing water amid destroyed housing and infrastructure can create new breeding sites for vectors [ 16 , 43 , 67 ], while flooding may cause sewage overflow, contaminating the water supply [ 29 ], causing favorable conditions, for instance for leptospirosis transmission [ 29 , 39 ]. Animal and human feces may contaminate water and food sources, causing disease [ 16 , 20 , 22 , 25 , 31 , 40 ], such as gastrointestinal infections and Hepatitis A and E [ 16 ]. Due to the increased sharing of water sources among domestic animals and humans zoonotic parasitic infections risk is greater during displacement [ 40 ]. In Darfur, the lack of a clean water source was an important factor in an outbreak of Hepatitis E among displaced people [ 33 ]. Shears and Lusty [ 19 ] note however that the impact of improved water supply and sanitation during displacement is minimal if overcrowding is not addressed, as pollution may still occur further down the distribution chain.

Living conditions

Services in relief camps are often limited due to funding, logistical and sourcing constraints [ 31 ]. Inadequate shelter may increase the risk of transmission of zoonotic pathogens, as certain shelter types may not be suitable for vector control, for instance wooden huts cannot be treated with insecticide [ 19 ]. Brooker et al [ 58 ] showed that shelter materials impacted the risk of cutaneous leishmaniasis. Meanwhile, inadequate living conditions affecting human-animal interactions may pose risks to pathogen transmission pathways beyond zoonoses, as the lack of distance between animal and human hosts may cause an increase in prevalence of diseases such as malaria [ 63 ].

Broglia et al [ 69 ] identify the lack of hygiene as most problematic feature of animal husbandry in refugee camps, caused by inappropriate shelters and a change in husbandry practices. Animals may act as an additional feeding source for sandfly and other vectors [ 58 ], while the presence of dogs increases the risk of rabies [ 54 ]. Vector borne diseases in north west Pakistan have been ascribed to refugees bringing their livestock from Afghanistan into poor and dense living conditions [ 61 ], while keeping ruminants inside the compound at night for security increased people's risk of being bitten by Anopheles mosquitoes and malaria [ 70 ].

In disasters and complex emergencies, livelihoods may be lost and regular food supply disrupted due to a decline in agricultural input and output, diversion and loss [ 14 , 25 ]. Malnutrition of both animals and humans is common, and an important risk factor increasing susceptibility to, and the severity of,zoonotic disease [ 19 , 31 , 34 , 38 , 51 , 65 ].

Usually situated near roads and water sources, displacement camps and informal settlements are often established in marginalized areas lacking vegetation and agriculture, which may result in malnutrition and metabolic disorders in livestock, exacerbated by no-grazing policies in camps [ 69 ]. Compromised immunity of both animals and humans through exhaustion from displacement, untreated parasites and gastrointestinal infections further affect malnutrition [ 31 , 50 ].

Socio-economic

As socio-economic inequities and poverty are associated with poor health [ 6 , 39 , 71 ], disasters and displacement affect the availability of education, labour and livelihoods, further exacerbating poverty [ 6 ]. Displaced populations often face structural discrimination and violence, including a lack of equitable access to services [ 72 ]. Furthermore, displaced communities often live in marginalized geographical locations, with limited resources [ 73 ]. In areas where refugees move into poor host communities, disease outbreaks are more likely, for instance communities along the Afghan-Pakistan border bear the brunt of vector-borne diseases caused by displacement [ 61 ].

The literature review confirms Hammer et al [ 47 ] who noted that issues described in the literature around infectious diseases in complex emergencies have been 'poorly evidenced, not contextualised and not considered with respect to interaction effects'. While our review shows an increase in relevant literature in the past five years, which may be associated by a global increase in displaced populations, as well as renewed interest in, and emerging interdisciplinary approaches to zoonotic diseases, there remains a lack of primary, field-based evidence on zoonotic disease risks during displacement. Researchers point out the need for more research on zoonoses [ 1 ], interactions between population movement and infectious diseases [ 47 , 54 ], interspecies interactions between humans and animals, including during displacement [ 41 , 74 , 75 ], and social and epidemiological factors [ 45 ]. There is currently no data available on these complex interlinkages however, and any positive effects displaced animals may have on the epidemiology and dynamics of zoonoses [ 10 ].

Disease outbreaks depend on the presence of contagious pathogens and susceptible hosts [ 27 ], and transmission is influenced by the health and immunity status of the displaced and host human and animal populations and their mixing [ 18 ]. Most risk factors do not result in disease outbreaks in isolation. While poverty and malnutrition are associated with general ill health, the availability of quarantine and vaccinations determine the effectiveness of infectious disease control. Even where services are available, tradition and social pressure determines whether people access resources [ 10 ]. The collapse of health services and infrastructure is a major determinant for infectious disease risks in humanitarian emergencies, including zoonoses. Subsequent displacement affects vulnerability of displaced and host populations to vectors and pathogens by changing environmental conditions, increasing population density and reducing the quality of living conditions affecting hygiene [ 22 ]. Displaced populations are even more vulnerable to infectious disease due to malnutrition and long-term stress [ 36 ].

Risk mitigation

Disease prevention and preparedness, surveillance, early monitoring of risk factors and epidemiology are especially relevant in displacement [ 19 , 32 , 35 , 58 , 61 , 65 ]. To address infectious disease risks and compound hazards, the World Health Organization (WHO, 2005) recommends conducting assessments [ 17 , 18 , 47 , 56 ], followed by prevention measures, improving water supply and sanitation, preventing overcrowding, promoting hygiene [ 14 , 19 , 22 , 36 , 37 , 47 ], disease diagnoses, treatment and control, vaccination and immunization [ 14 , 19 , 34 , 47 , 62 , 65 ]. The impact of these measures is not well studied however. Data on disease incidence, epidemiology and medical geography, ecology, distribution needs to be collected [ 36 , 67 ], and include details of human behavior [ 5 , 42 , 45 , 48 , 76 ], in support of planning of camps [ 42 , 49 , 50 ].

While there is a lack of published evidence for the use of Livestock Emergency Guidelines and Standards (LEGS) or other standardized guidelines, some targeted livestock support programs are implemented in humanitarian emergencies, including vaccination campaigns and the provision of animal shelter [ 41 , 76 , 77 ]. Community based preparedness in camps and informal settlements improves animal husbandry and shelter [ 69 ], including the use of mosquito nets [ 31 , 70 ]. Feeding programs are recommended to mitigate malnutrition, improving animal health [ 14 , 21 , 24 ]. Watson and Catley [ 78 ] provide examples of an integrated livestock emergency response system, combining feed, water and health interventions, or destocking with the provision of feed.

Without proper coordination and oversight however, zoonotic disease control may have unintended consequences. In Guinea the killing, collection and burying of rats was promoted in refugee camps to prevent Lassa outbreaks; however, this may not have completely stopped the consumption of rodents, as anecdotal evidence suggests that some residents considered this as ‘wasted food’ [ 46 ]. The lack of coordination between veterinary and public health actors affects public health [ 36 ], and is therefore one of the main requirements of LEGS and WHO’s field manual ‘communicable disease control in emergencies’ [ 21 ]. To mitigate the lack of veterinary services in disaster preparedness and responses, animal health specialists should get involved in the development of legislation and response plans [ 24 ].

To address the risk of zoonotic pathogen transmission during displacement, stakeholders need to address disease control, as well as political and socio-economic factors such as poverty and access to services. Public health and policy support needs to be interdisciplinary and multi-sectoral, and consider not only veterinary and public health, but also political, social and economic realities of displacement contexts, to enable durable solutions [ 3 , 15 , 30 , 35 , 39 , 51 , 62 , 63 , 73 , 78 ].

The knowledge gap of zoonoses in displacement may be ascribed to a lack of research into the epidemiology of specific diseases, as zoonoses are often difficult to diagnose, or may indicate that the presence of livestock has not proven to be as much of a risk factor as assumed. Instead, maintaining access to livestock may improve livelihoods, nutrition and mental health, with the potential to reduce people’s vulnerability to disease, providing a strong argument for allowing animals into relief camps if inadequate living conditions and sanitation are addressed appropriately. There is a projected increase in displacement due to environmental causes, particularly affecting areas dependent on agriculture and livestock. The role of livestock in displacement, its impact on host communities, and the potential benefits of maintaining displaced communities’ access to animals, in terms of livelihoods and health, need to be actively researched to better inform policies and programs related to health, livelihoods and human movement.

Availability of data and materials

All data generated or analysed during this study are included in this published article.

Abbreviations

Livestock Emergency Guidelines and Standards

Preferred Reporting Items for Systematic Reviews and meta-Analysis

United Nations

World Health Organization

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Braam, D.H., Jephcott, F.L. & Wood, J.L.N. Identifying the research gap of zoonotic disease in displacement: a systematic review. glob health res policy 6 , 25 (2021). https://doi.org/10.1186/s41256-021-00205-3

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• Published: 21 May 2022

A generalizable one health framework for the control of zoonotic diseases

• Ria R. Ghai 1 ,
• Ryan M. Wallace 1 ,
• James C. Kile 2 ,
• Trevor R. Shoemaker 1 ,
• Antonio R. Vieira 1 ,
• Maria E. Negron 1 ,
• Sean V. Shadomy 1 , 3 ,
• Julie R. Sinclair 1 ,
• Grace W. Goryoka 1 ,
• Stephanie J. Salyer 4 &
• Casey Barton Behravesh 1  

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Effectively preventing and controlling zoonotic diseases requires a One Health approach that involves collaboration across sectors responsible for human health, animal health (both domestic and wildlife), and the environment, as well as other partners. Here we describe the Generalizable One Health Framework (GOHF), a five-step framework that provides structure for using a One Health approach in zoonotic disease programs being implemented at the local, sub-national, national, regional, or international level. Part of the framework is a toolkit that compiles existing resources and presents them following a stepwise schematic, allowing users to identify relevant resources as they are required. Coupled with recommendations for implementing a One Health approach for zoonotic disease prevention and control in technical domains including laboratory, surveillance, preparedness and response, this framework can mobilize One Health and thereby enhance and guide capacity building to combat zoonotic disease threats at the human–animal–environment interface.

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Introduction.

One Health is a collaborative, multisectoral, and transdisciplinary approach—working at the local, national, regional and global levels—with the goal of achieving optimal health outcomes that recognize the interconnection between people, animals, plants, and their shared environment. In recent decades, the One Health approach has gained traction in combatting health issues at the human–animal–environment interface. Zoonotic diseases, infectious agents shared between animals and people, are a formidable challenge in One Health. Evolving conditions at the human–animal–environment interface due to factors like climate change, land use change (e.g., deforestation and agricultural intensification) and increasing travel and trade have directly and indirectly affected the emergence and reemergence of zoonotic diseases 1 , 2 , 3 . Applying a One Health approach to optimize zoonotic disease prevention and control programs can save lives by improving efficient use of resources (finances, infrastructure and personnel) and the quality and timeliness of healthcare delivery 4 , 5 , 6 , 7 , 8 . Despite increasing awareness of the One Health approach, lack of communication and coordination between human health, animal health, and environment sectors can still hinder implementation. Internationally, the Tripartite organizations, namely the Food and Agriculture Organization of the United Nations (FAO), the World Organisation for Animal Health (OIE), and World Health Organization (WHO), have exemplified using a multisectoral, One Health approach through mandated inter-agency collaboration 9 , and endorsement of One Health to facilitate sustained collaboration for zoonotic disease control at the local, subnational, national, regional, and international level through the guide, “Taking a Multisectoral, One Health Approach: A Tripartite Guide to Addressing Zoonotic Diseases in Countries” (hereafter the Tripartite Zoonoses Guide or TZG) 10 .

A One Health approach can be applied broadly to support overarching systems that improve multisectoral, One Health coordination, or the approach can be applied to specific topics, such as antimicrobial resistance, climate change, zoonotic disease control, or food safety and security. A systems-based One Health approach (Fig.  1 ) often involves development of multisectoral, One Health coordination mechanisms (OH-MCMs) 10 . OH-MCMs can create a way to coordinate all One Health activities across all relevant sectors 10 . While One Health systems such as OH-MCMs are not necessarily specific to zoonotic diseases, they may directly oversee zoonotic disease programs, or indirectly bolster associated One Health coordination. The TZG primarily provides guidance for a systems-based One Health approach, while providing examples from specific programs. While One Health systems-based approaches are an effective method of building sustainable coordination and collaboration across sectors 10 , initiating coordination through a zoonotic disease-specific program (Fig.  1 ) that uses a One Health approach to initially focus on a few key priority diseases may be more tractable in the short term. Here, we utilize the approach established in the TZG, and apply these lessons to programs, specifically control of zoonotic pathogens.

One Health systems versus zoonotic-disease specific programs. Zoonotic disease-specific programs are generally programs with a focus on a specific pathogen, disease complex, syndrome, or subject. Zoonotic-disease specific programs often include One Health activities, but tend to be led by a specific sector (e.g., human health, animal health). In contrast, a One Health system often includes delegates from all relevant One Health sectors (e.g., human, animal and environmental health) and coordinates all One Health activities, including zoonotic-disease specific programs, across participating sectors. AMR antimicrobial resistance.

The Generalized One Health Framework (GOHF) presented here provides recommendations for how to use a One Health approach to improve multisectoral collaboration and thereby enhance the prevention and control of zoonotic diseases. The GOHF includes a visualization (Fig.  2 ) that presents a series of five steps and corresponding activities which provide structure for how countries may develop capacity to coordinate zoonotic disease programming across sectors. The objectives and outcomes intended for each step are listed in Table 1 . The GOHF was developed primarily for use by governmental officials in public health, animal health, or environment sectors working on One Health and zoonotic disease programming at the local, subnational, national, or international levels. Users of the GOHF may choose to enter this framework at any step based on their current capacity, although a numerical order is proposed for ease of use. The GOHF also includes a toolkit (see Supplementary Tables S1 – 5 ), which compiles available resources matched to each step and activity within the framework. To add context for application of the GOHF, we include zoonotic disease examples as they have been applied throughout the globe. The GOHF is not intended to be prescriptive—rather, it is meant to be broadly applicable to common zoonotic diseases in most settings, including use within both high-income and low-middle income countries, and ranging from the local to the international level.

Generalized One Health framework visualization. Dark teal circles indicate stepwise headings. Light blue boxes indicate activities under these headings that pertain to building a One Health system or zoonotic disease-specific program. Technical domains pertain to all steps within the GOHF, and often comprise essential elements of a successful One Health system or zoonotic disease-specific program to be addressed.

Finally, since effective action should involve application of the GOHF to all aspects of a zoonotic disease-specific program, we describe how the GOHF can be applied across several technical domains, specifically laboratory, surveillance, joint outbreak response, prevention and control, preparedness, communication, and government and policy (Fig.  2 ).

The GOHF was developed by subject matter experts in One Health, zoonotic diseases, public health, and animal health at U.S. Centers for Disease Control and Prevention (CDC), and FAO. This framework was developed by combining successful existing and idealized processes for implementing zoonotic disease programming globally, leveraging subject-matter experts in anthrax, brucellosis, rabies, Rift Valley fever, and zoonotic influenza to provide example. Resources included in the Supplementary Tables are not an exhaustive list of all resources available; expert opinion, accessibility of the resource, and frequency of use were used to identify the most relevant resources available.

Step 1: Engagement

Establishing one health interest by identifying and engaging stakeholders.

Whether developing a One Health systems-based or zoonotic disease-specific program (Fig.  1 ), the process begins with recognizing that a multisectoral, One Health approach can optimize resources and improve human, animal and environmental health outcomes 4 , 5 , 6 , 7 , 8 . Given these and similar advantages, an initial stage in developing One Health systems for zoonotic disease-specific programs involves exploring context-specific benefits, required modifications to current operations, and the level of interest and commitment expressed by stakeholders (Supplementary Table S1 , 1.1, 1.2).

Identifying and engaging stakeholders

Early in system or program development, stakeholders from all relevant One Health sectors (i.e., public health, agriculture/livestock health, wildlife health, environment, and others) as well as other relevant fields (e.g., social and political sciences) must be identified 9 . Identifying stakeholders that represent all interests and levels early in the process can help build trust and improve sustainability (Supplementary Table S1 , 1.3–1.5). In Kenya, for example, social network analysis not only identified relevant stakeholders involved in Rift Valley fever programs at the subnational and national level, but also identified the strength of collaboration and influence of each 11 , which helped determine the physical location to situate the OH-MCM 11 . Once appropriate stakeholders are identified, establishing roles and responsibilities (perhaps through formalized agreements such as Memorandums of Understanding or Letters of Agreement) between participating stakeholders can assist in establishing accountability and facilitating steady progress. Finally, to ensure that relevant stakeholders remain engaged as programs are expanded, combined, or re-organized, the process of identifying and including appropriate stakeholders should be routinely revisited.

Prioritizing zoonotic diseases

Often, resources are not adequate to address all needs for zoonotic disease control, which necessitates prioritizing zoonotic diseases for resource allocation. An objective, formalized prioritization process with equal participation and input from all relevant sectors will have the added advantage of helping to establish One Health commitment and collaborations 10 , 12 , 13 . To address the prioritization needs of countries, regions and other localities, the CDC developed the One Health Zoonotic Disease Prioritization process (OHZDP; Supplementary Table S1 , 1.6). The OHZDP uses a transparent approach to prioritize zoonotic diseases of greatest concern for joint collaboration 12 , 13 . Collaborative prioritization promotes program ownership and uptake, and resource and information sharing between all participating stakeholders. Outcomes of the OHZDP and other prioritization efforts are associated with improved scores on international evaluations such as the Joint External Evaluation (JEE; Supplementary Table S2 , 2.2), development of National Action Plans for Health Security (NAPHS; Supplementary Table S4 , 4.1) and other One Health strategic plans, and enhanced zoonotic disease program capacity 14 , 15 , 16 , 17 .

Establishing sustained government support for One Health

Often, government support for zoonotic diseases may surge during outbreaks and wane in the absence of emergencies and crises-driven funding. However, several examples indicate that sustainable support entrenched in a government-led strategy to prevent and control zoonotic diseases is the cornerstone of a successful program 18 , 19 , 20 , 21 , 22 . In Thailand, an institutionalized One Health strategy was precipitated by the devastating public health and socio-economic effects of avian (H 5 N 1 ) and pandemic (H 1 N 1 ) influenza in 2004 and 2009, respectively. Growing partnerships around influenza created opportunities and demonstrated successes that promoted further collaboration, ultimately leading to a cabinet-endorsed resolution where One Health was a core principle, and formation of a Thai Coordinating Unit for One Health 21 , 22 . Published articles from Kenya 18 , 19 and Egypt 20 also chronicle the path to institutionalizing One Health within government and provide examples for establishing sustainable support. At minimum, government support for One Health systems and programs should include dedicated domestic resources (e.g., financial, infrastructure and personnel) and political will to initiate and sustain action 10 , 23 . For those advocating for increased governmental investment in One Health, one way to establish support is by demonstrating clear benefits of proposed activities at a reasonable cost, which can be accomplished through cost effectiveness analysis (Supplementary Table S1 , 1.10). More formalized measures, such as advocacy or awareness campaigns, may be useful for communicating this information to higher levels of government. Such campaigns can be conducted for little or no cost using social media platforms.

Step 2: Assessment

Mapping infrastructure.

In order to develop realistic and achievable plans for One Health systems or zoonotic disease-specific programs, the available infrastructure must be understood 10 . Infrastructure mapping can help visualize mechanisms of informal and formal communication, and collaboration and coordination occurring within and between sectors in the form of a network map. By visualizing the network, infrastructure mapping can identify redundancy, gaps and weaknesses in the system or program being assessed 4 , 10 (Supplementary Table S2 , 2.1).

Establishing a baseline

In order to develop prevention and control plans that effectively channel resources, baseline information on the status of current activities, such as the burden of the zoonotic disease and its epidemiologic situation, should be established 24 . Analyzing disease-specific data from baseline studies and existing surveillance and laboratory activities at the local, sub-national, national, and regional levels may be a first step where such data exist. In countries where adequate data are not available, primary literature and unpublished findings from academic institutions or non-governmental organizations may also provide useful information. In some instances, new investigations such as serological surveys or pilot studies may be necessary to establish the baseline epidemiologic situation, such as the primary hosts and reservoirs, circulating species or strains, and prevalence in human and animal populations.

Conducting gap analysis

Once baseline information is understood, it is possible to identify gaps in current capacity within and between sectors responsible for managing the system or program. Unlike infrastructure mapping which visually illustrates multisectoral coordination, gap analysis critically assesses technical capacity to achieve a goal. In some instances, tools for gap analysis provide stepwise guidance through the assignment of a score, allowing users to establish current and desired conditions (Supplementary Table S2 , 2.2 and 2.3). Some zoonotic diseases also have tools that are specific to the pathogen, such as the Stepwise Approach towards Rabies Elimination (SARE; Supplementary Table S3 , 3.6). In many ways, the SARE tool and paired Blueprint for Rabies Control (Supplementary Table 5 , 5.6) exemplify zoonotic disease-specific guidance that embodies a One Health approach and have therefore been widely adopted in both country-level and regional plans to eliminate human deaths from dog-mediated rabies 25 , 26 , 27 , 28 .

Completing economic assessments

Perhaps the most compelling argument for investment in zoonotic disease prevention and control is the cost-effectiveness of the proposed program. Specifically, understanding how the economic burden of “status quo” (i.e., the cost of illness) compares to various scenarios of investment in control and elimination can both only improve the probability of program success and facilitate program endorsement by stakeholders and government. For zoonotic diseases, economic evaluations or decision analyses that account for all stakeholders are necessary to establish the societal cost of the disease as well as the benefits of prevention and control 29 , 30 , 31 . Indeed, while the cost savings of zoonotic disease prevention and control may not be readily apparent to a single sector, previous research has shown economic benefits to both government (in terms of cost savings) and society (in terms of reduced morbidity and mortality in humans and animals) in the case of brucellosis 32 , rabies 33 , and salmonellosis 31 , 34 (Supplementary Tables S2 , 2.11 and S3 , 3.9).

Step 3: Planning

Developing a multisectoral, one health strategic plan.

If gaps or weaknesses are identified during the assessment phase, a formalized strategy to enhance collaboration across government can be articulated through strategic planning 10 . Strategic plans are often long-term (5–10 year), forward-looking documents that should be drafted and endorsed with equal input by all relevant sectors, and include a shared vision with achievable goals and objectives 35 . Several strategic planning resources exist to assist countries with developing One Health strategic plans, although there are also many countries that develop successful plans independently 19 , 36 , 37 , 38 . Some zoonotic diseases have specific strategic planning resources, such as the Rabies Practical Workplan, a component of the SARE which translates pending activities into actionable work plans (Supplementary Table S5 , 5.5) 39 . As applicable based on membership, governments should also consider how their One Health strategic plans and specific zoonotic disease action plans (described below) may be integrated into international initiatives, such as the NAPHS (Supplementary Table S4 , 4.1) 40 .

Developing action plans for priority zoonotic diseases

While action plans can be developed independently of a strategic plan, they can benefit from linkage. The goals and objectives developed during strategic planning can be used to develop activities in an action plan, thereby making goals and objectives implementable. Action plans can therefore serve as a roadmap for implementing the agreed upon vision of a collaborative One Health effort. Action plans typically highlight the short-term (1 year or less) activities that are required to achieve a mission. They outline the roles and responsibilities of all partners, and identify the resources needed to implement outlined activities 10 . Outcomes from prioritization exercises and disease-specific gap analysis exercises may also be used to inform the development of these action plans.

Step 4: Implementation

Soliciting, acquiring and allocating resources.

Officials that are preparing to implement developed plans should have an in-depth understanding of the tasks associated with building their One Health system or zoonotic disease-specific program. At this stage, costing the program identifies how available resources (including human, financial and physical) will be allocated. This information can assist with devising a strategy to obtain missing resources, such as launching advocacy plans, soliciting resources from private industry, or seeking non-traditional partners including the military, universities, or ministries not directly associated with health (e.g. education, finance, or tourism). Exploring whether programming fits under the mandates of international agencies or forming regional partnerships to garner international assistance may also be worthwhile depending on current or future global priorities. Ideally, sufficient resources to carry programs through to completion should be identified prior to implementation of each phase, as this can help avoid premature program terminations.

Implementing plans, protocols and procedures

Budgeted and financed plans allow One Health systems or zoonotic disease-specific programs to begin implementation. While this phase largely involves the progressive roll-out of programs resources exist to smooth or improve program implementation. Technological innovations including software and web platforms, mobile phones, tablets, and applications or “apps” are powerful resources being used to implement surveillance, prevention, control and preparedness activities. For example, in the United States, text-based monitoring has also been used to improve detection of illnesses caused by novel influenza A viruses 41 . More sophisticated smartphone technology has spurred comprehensive surveillance, data collection, and prevention applications. For example, the WVS Data Collection app (Supplementary Table S7 , 7.1) uses a One Health approach through its Integrated Bite Case Management system for rabies to collect data on mass dog vaccination campaigns, community surveys, and hospital bite case management 42 . Similarly, the Kenya Animal Biosurveillance System (KABS) smartphone app expedites detection of wildlife and livestock zoonotic diseases. In 2017, the KABS reported cattle mortalities that ultimately identified anthrax that triggered a One Health investigation that assessed people, animals and contaminated environments 43 , 44 . Smartphone technology is now also being used for laboratory diagnostics. For example, a smartphone-based system for detecting H5N1 avian influenza in clinical patient samples has a two-folder higher detectability than traditional fluorescent strip readers, making it a sensitive and portable system for field-based diagnostics 45 .

Whether implementation mechanisms are conventional or innovative, the ultimate goal at this stage is to implement an effective system that minimizes resources while reaching intended outcomes, including reductions in human and animal morbidity and mortality 46 .

Step 5: Monitoring and evaluation

Monitor and evaluate systems and/or programs.

Although monitoring and evaluation is the last step in the GOHF, monitoring and evaluation should ideally be established during the planning phase in order to track implementation outputs and systematically evaluate the successes, challenges, scope, and scale of programs. With respect to One Health systems, evidence suggests that despite a rise in One Health systems in recent years, few report the use of standardized or systematic monitoring and evaluation frameworks to demonstrate the effectiveness of the One Health approach 47 , 48 . While evaluating the multi-faceted nature of a One Health system or zoonotic disease-specific program can be complex, a framework for monitoring and evaluation of One Health systems can provide evidence to support decision-making. Recent efforts have used common frameworks for monitoring and evaluation of One Health systems, but additional work is still needed to develop a standardized approach to monitor and evaluate One Health systems (but see Supplementary Table S8 for examples).

Applying a One Health approach to specific zoonotic disease technical domains

Effective implementation of a One Health approach should involve integration into many, if not all, facets of a zoonotic disease program. In the below sections, we highlight how a One Health approach can be applied to several technical domains that are commonly a part of zoonotic disease programs: laboratory, surveillance and joint outbreak investigation, prevention and control, preparedness, communication, workforce, and government and policy.

One Health in laboratory systems

Central to any effective zoonotic disease prevention and control program is the ability to provide timely, accurate and reliable diagnostic testing to detect and characterize the pathogen within laboratory networks 24 . In many cases, however, public health, veterinary, and environment laboratories may work on the same One Health challenge without aligning methods, technologies, or analytical approaches; this can lead to duplication of effort. Implementing a multisectoral, One Health approach to laboratory systems can reduce program expenditures and improve response times through sharing of physical resources and/or data. When procedures to detect and diagnose a zoonotic pathogen are similar among human, animal and/or environmental samples, sharing resources or personnel may be beneficial. In Mongolia, for example, a program of exchanging information, experiences, and resources between veterinary and public health laboratories enabled veterinary laboratories to provide support during outbreaks of human anthrax and rabies that resulted in dramatic improvements in national diagnostic capacity 49 . Similarly in Canada, the Canadian Science Center for Human and Animal Health is the world’s first facility to have both human and animal Containment Level 4 labs together, allowing for cross-cutting laboratory research on zoonotic pathogens that have included Zika and Ebola 50 . In such instances, sector-specific laboratories may operate independently to detect and diagnose zoonotic pathogens, but laboratory protocols are aligned and standardized data are shared both within and across sectors to speed outbreak detection and identify sources of infection 51 (Fig.  3 and Supplementary Figs. S1 – S5 ). An example of success through laboratory data sharing is PulseNet, a US-based domestic and international network of food, animal, and public health laboratories where identifying enteric disease clusters of increasing incidence is estimated to have averted 270,000 foodborne illnesses and saved US $507 million each year 52 , 53 , 54 .

One Health in surveillance and joint outbreak investigation

Implementing a multisectoral, One Health approach to surveillance involves the systematic collection, coordination, and communication of data and reports between relevant sectors with the intent of providing accurate and complete information to inform decision-making 55 , 56 . In Fig.  3 , we use event-based surveillance, which is the detection and reporting of “signals”, defined as information that may represent events of health importance, to highlight how a One Health approach can be used across a more generalized surveillance system to show coordination across sectors. At the community level, zoonotic disease events at the human-animal-environment interface may trigger joint or coordinated outbreak investigations that involve relevant human, animal and environmental health officials (Fig.  3 and Supplementary Figs. S1 – S5 ) 57 . Jointly responding to outbreaks may reduce costs and foster collaboration between sectors 56 , as has been seen during investigations of monkeypox 58 , leptospirosis 59 , Rift Valley fever 60 , and anthrax and rabies 61 (Fig.  3 and Supplementary Figs. S1 – S5 ). Establishing coordinated investigation and response protocols across all participating sectors is a critical component of effective response plans 62 .

Taking a One Health approach to event-based surveillance. While each zoonotic disease requires a tailored surveillance strategy to ensure a targeted and expedient response, the One Health linkages (shown in teal) may be similar across many different event types. In this generalized zoonotic disease example, event-based surveillance begins with the detection of an “event” or verified signal in red that triggers a response. This event, detected at the community level, is reported to the sub-national (e.g., states, provinces, or jurisdictions), national and international levels from left to right. Results and recommendations are disseminated in the opposite direction (i.e., right to left), with the intention of communicating synthesized results and recommendations back to at-risk communities. See Supplementary Figs. S1 – S5 for pathogen-specific examples of event-based surveillance in anthrax, brucellosis, rabies, Rift Valley fever, and zoonotic influenza viruses.

When surveillance data are compiled and analyzed by each sector separately, coordinated surveillance (through interoperable platforms or information sharing mechanisms) can facilitate data sharing between relevant One Health sectors. Collecting common, standardized data elements ensures that data from different sectors can be linked and analyzed together (Fig.  3 and Supplementary Figs. S1 – S5 ). Coordinated surveillance can be used to identify early warning signals for emerging zoonotic disease, understand and monitor trends in the disease burden, and develop coordinated response activities 62 . A number of successful coordinated surveillance systems exist throughout the globe 56 , 63 , 64 , with the common theme being collaboration at the policy level, institutional level and operational level, as well as data and outcomes that are shared to the benefit of all participating sectors 65 .

One Health in prevention and control

While it seems evident that prevention and control programs that reduce the burden of disease in animal populations would correspondingly reduce the risk of human infection and disease (and vice versa), published records are limited to a few salient examples. For rabies, previous research has established that vaccination coverage of 70% or higher in dog populations can reduce the frequency of human dog-bite injuries, usage of post-exposure prophylaxis, and human rabies cases 66 , 67 , 68 , 69 , 70 . Further, evidence in epidemic-prone zoonotic diseases like influenza A viruses showed that animal vaccination prevented human outbreaks and perhaps also pandemics in China, where administration of a bivalent poultry vaccine eliminated human cases of H7N9 71 , 72 . Finally, for zoonotic pathogens with environmental stages, programs that reduce both animal and human exposure to contaminated environments can be more effective than single-sector disease measures 73 . While prevention and control plans may be specific to the zoonotic disease and the epidemiologic situation, these examples illustrate that taking a multisectoral, One Health approach to prevention and control can reduce the burden of disease while optimizing program resources.

One Health preparedness

A great deal of activity within the realm of emergency preparedness has focused on pandemic preparedness for emerging infectious diseases. Preparedness planning using a One Health approach involves participation, engagement and readiness from all relevant sectors through all stages of preparedness planning (Supplementary Tables S1 – 5 ). Improved coordination during emergencies may reduce the size or impact of a human pandemic, as was seen in the United States where the One Health linkages created during H5N1 planning and simulation are credited for the successful response to the swine-origin influenza H1N1 pandemic 74 , 75 . More generally, preparedness efforts that strengthen One Health coordination in laboratory, surveillance, and workforce (described in other sections) can benefit both routine and emergency activities.

One Health communication

An effective communication strategy should include activities both internal and external to the government. Internally within government, a communication strategy should establish process for relevant sectors and stakeholders to communicate and share information. Communication strategies can formalize channels and methods of communication, which helps align expectations, goals and messaging, as well as build relationships among internal One Health sectors. Despite the benefits of joint communication, cross-sector communication can be challenging for several reasons, including differences in terminologies used. Some tools, such as the One Health European Joint Programme Glossary, are available to identify and overcome terminology differences 76 . Alternatively, establishing joint communication at the start of an event can ensure synchronization from the outset. For example, in the United States, the One Health Federal Interagency COVID-19 Coordination Group was established at the beginning of the COVID-19 pandemic to share information across over 20 different governmental agencies and is the primary reason for harmonized messaging on the zoonotic nature of SARS-CoV-2 across the US government. Outside of government, a communication strategy can ensure that One Health stakeholders and partners receive united, consistent messaging that is unaffected by agency or mandate. Additionally, a communication strategy should guide public awareness campaigns, education on One Health issues of importance, and risk communication to best maximize public support and promote the uptake and success of any health program 62 .

One Health workforce

A number of international training frameworks highlight the need for training and education programs that use a One Health approach to equip the labor force with the skills necessary to combat zoonotic diseases (Supplementary Table S2 , 2.2). Examples from several global programs with a focus on training health professionals using a One Health approach exist, including Field Epidemiology Training Programs (FETPs) 77 , 78 , the Global Laboratory Leadership Program (GLLP) 79 , the In-Service Applied Veterinary Epidemiology Training Programme (ISAVET) 80 , and the One Health Workforce project 81 . Through hands-on training, the cadre of health practitioners created through these and other One Health programs can amplify One Health-based training and curriculum messaging, are more likely to meet previously defined One Health Core Competencies 82 , and demonstrate improved ability to collaboratively respond to threats at the human–animal–environment interface 37 , 83 . Still needed are programs which include environmental health practitioners, incorporate curriculum on the role of climate and the environment on One Health issues, and formalize processes on when and how to engage environment sectors.

One Health in government and policy

Ensuring that the benefits of a One Health approach to zoonotic disease management are recognized by policy and decision makers can improve program success and sustainability. Institutionalizing One Health in governance is one means of establishing sustained support for programs that implement a One Health approach 74 . To this end, both the JEE and PVS Pathway (see Supplementary Table S2 , 2.2 and 2.3) have legislative sections that are geared to assist in modernizing legislation to include a One Health approach. Typically, recognizing the need to institutionalize One Health in governance and policy occurs when a lack of coordination becomes apparent while addressing zoonotic disease threats, or when a gap in coordination capacity is identified during reporting or assessments 62 . Kenya is one such country that has published on its road to One Health institutionalization, and therefore provides an example of how governments may shift from sector-specific units or task forces to overarching governance through One Health systems 11 , 18 , 19 , 83 , 84 .

Conclusions

This manuscript provides a framework for building capacity around zoonotic diseases using a One Health approach in a range of settings (Fig.  2 ). Users of the GOHF may identify their progress in developing coordinated zoonotic disease programs using the visualization and corresponding text of this manuscript, and then access resources to advance progress using the toolkit. The GOHF highlights that while developing prevention and control programs will require specialized technical expertise, the One Health approach taken is similar irrespective of the zoonotic disease. Further, rather than build independent programs for priority zoonotic diseases, this guidance is intended to deepen One Health capacity throughout the system. Therefore, ideally, a transition may occur from implementing a One Health approach for a few priority zoonotic diseases to gradually building a comprehensive One Health system that can combat a diversity of health threats, both endemic and emerging, at the human-animal-environment interface.

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Acknowledgements

PinChia Lin, Laura Murrell and Meghan Herring (visualizations and communications); Nadia Oussayef, Kate Varela, and Colleen Brouillette (policy and strategic planning feedback); Amanda Liew (toolkit tables); Tory Seffren (workforce and strategic planning).

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Conceptual design: R.R.G., R.M.W., S.J.S., C.B.B. Technical input: R.R.G., R.M.W., J.C.K., T.R.S., A.R.V., M.E.N., S.V.S., J.R.S., G.W.G., S.J.S., C.B.B. Manuscript writing: R.R.G., C.B.B. Manuscript review, feedback, approval: R.R.G., R.M.W., J.C.K., T.R.S., A.R.V., M.E.N., S.V.S., J.R.S., G.W.G., S.J.S., C.B.B.

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Ghai, R.R., Wallace, R.M., Kile, J.C. et al. A generalizable one health framework for the control of zoonotic diseases. Sci Rep 12 , 8588 (2022). https://doi.org/10.1038/s41598-022-12619-1

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Public health threat of novel zoonotic diseases: literature review

Affiliations.

• 1 Studenckie Koło Naukowe przy Katedrze i Zakładzie Medycyny i Epidemiologii Środowiskowej, Wydział Nauk Medycznych w Zabrzu, Śląski Uniwersytet Medyczny w Katowicach, opiekun koła: dr n. med. Karolina Lau., Śląski Uniwersytet Medyczny w Katowicach, Polska.
• 2 Katedra i Zakład Medycyny i Epidemiologii Środowiskowej, Wydział Nauk Medycznych w Zabrzu., Śląski Uniwersytet Medyczny w Katowicach, Polska.
• PMID: 38904313
• DOI: 10.32394/pe/188161

Abstract in English, Polish

Zoonoses, diseases transmitted from animals to humans, continue to challenge public health despite advancements in controlling infectious diseases. The intricate link between human, animal, and environmental health is emphasised by the fact that zoonoses contribute to 60% of emerging human infections. Wet markets, wildlife hunting, intensive wildlife farming, and interactions between domestic animals and humans are key transmission sources. Historical examples like the bubonic plague and English Sweats illustrate the longstanding impact of zoonotic diseases. With new transmission patterns emerging, it is necessary to use new techniques to predict disease spread. This article delves into the emergence of new zoonoses, such as the Nipah virus and the SARS-CoV-2 pandemic, emphasizing the importance of understanding zoonotic aspects for outbreak prevention. Re-emerging zoonoses, like tuberculosis and vaccine-preventable diseases, present challenges, exacerbated by factors like globalized human activities and disruptions caused by the COVID-19 pandemic. Public health implications are explored, including economic losses, antibiotic resistance, and the disruption of international trade.

Choroby odzwierzęce, choroby przenoszone ze zwierząt na ludzi, w dalszym ciągu stanowią wyzwanie dla zdrowia publicznego pomimo postępów w zwalczaniu chorób zakaźnych. Skomplikowany związek między zdrowiem ludzi, zwierząt i środowiskiem podkreśla fakt, że choroby odzwierzęce są przyczyną 60% nowo pojawiających się infekcji u ludzi. Kluczowymi źródłami przenoszenia są mokre targi, polowania na dziką zwierzynę, intensywna hodowla dzikich zwierząt oraz interakcje między zwierzętami domowymi a ludźmi. Historyczne przykłady, takie jak dżuma i poty angielskie, ilustrują długotrwały wpływ chorób odzwierzęcych. W miarę pojawiania się nowych wzorców przenoszenia konieczne jest stosowanie nowych technik przewidywania rozprzestrzeniania się choroby. W artykule omówiono pojawienie się nowych chorób odzwierzęcych, takich jak wirus Nipah i pandemia SARS-CoV-2, podkreślając znaczenie zrozumienia aspektów odzwierzęcych w zapobieganiu epidemiom. Ponowne pojawienie się chorób odzwierzęcych, takich jak gruźlica i choroby, którym można zapobiegać poprzez szczepienia, stwarza wyzwania, które dodatkowo pogłębiają takie czynniki, jak globalna działalność człowieka i zakłócenia spowodowane pandemią Covid-19. Badane są skutki dla zdrowia publicznego, w tym straty gospodarcze, oporność na antybiotyki i zakłócenia w handlu międzynarodowym.

Keywords: Choroby odzwierzęce; One Health; Public Health; Zdrowie publiczne; Zoonotic diseases.

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Rabies is a Zoonotic Disease: A Literature Review

2021, Occupational medicine and health affairs

Rabies means "to be mad". It`s a zoonotic disease which is spread by animals mostly carnivores. Rabies considers as tropic disease.

Related Papers

Rabies a mini review

GABRIEL SPOLON SILVA

Rabies is a zoonotic disease caused by infection with viruses of the genus Lyssavirus, transmitted through saliva of an infected animal, through bites and licking of mucous membranes or skin contact solutions. After its entry, viral multiplication occurs at the site of inoculation, subsequently invading the peripheral nervous system, and through centripetal migration it reaches the central nervous system where its replication occurs, causing encephalitis with neuronal degeneration of the spinal cord and brain that leads to death. In different parts of the world, dogs are an important reservoir of rabies virus, and dog bites are responsible for more than 99% of human cases. In Brazil, the main reservoir is vampire bats, and primary prevention involves the control of vampire bats combined with canine vaccination campaigns. In the event of human exposure to the rabies virus, post-exposure prophylaxis aims to prevent progression to clinical disease that involves wound care, administration of anti-rabies immunoglobulin and vaccination.

Salvador Eduardo Acevedo Monroy

Scientific Research Journal

Prof. Dr. Subha Ganguly

Mahendra Pal

SUMMARY Rabies is one of the oldest recognized diseases affecting all warm-blooded animals and remains to be the most important zoonotic disease mainly affecting the developing countries. It is an acute, progressive and almost fatal encephalomyelitis caused by the Rabies virus and other Lyssavirus species of the family Rhabdoviridae. The disease has worldwide distribution except in some countries where there is strict quarantine system, rigorous eradication program or natural barriers like mountains and rivers. Rabies occurs in more than 150 countries and territories. Of these, most deaths from rabies occur in developing countries with inadequate public health resources and limited access to preventive treatment. This category constitutes mainly the developing countries found in the Asian and African continents. This situation occurs because dog rabies is endemic with dog-to-dog transmission of the infection, which is associated with an ongoing threat to humans due to dog bite. Rabies transmission is usually from virus laden saliva of an infected animal which comes in the contact by the bite from animal to animal or animal to man. Being rabies virus is highly neurotropic; it has high affinity for the central nervous system. The lesions produced in the central nervous system and destruction of the spinal neurons results in the clinical signs manifested by the rabid patients. All rabies infected species usually exhibit typical signs of central nervous system disturbance, with minor variations among species. The direct fluorescent antibody test is the gold standard for rabies diagnosis. An important tool to optimize public and animal health and enhance domestic animal rabies control is routine or emergency implementation of low-cost or free clinics for rabies vaccination. Being rabies is a preventable disease, some possible prevention and control components include, making responsible pet ownership, routine veterinary care and vaccination, and professionals should provide public education about the disease. To facilitate the implementation of these prevention and control components, jurisdictions should work with veterinary medical licensing boards, veterinary associations, the local veterinary community, animal control officials and animal welfare organizations. 100%

Alexandra Gerlach

The Lancet Infectious Diseases

Charles Rupprecht

Journal of Animal Health and Production

Sheeba shams

The Veterinary quarterly

Karam Pal Singh

Rabies is a zoonotic, fatal and progressive neurological infection caused by rabies virus of the genus Lyssavirus and family Rhabdoviridae. It affects all warm-blooded animals and the disease is prevalent throughout the world and endemic in many countries except in Islands like Australia and Antarctica. Over 60,000 peoples die every year due to rabies, while approximately 15 million people receive rabies post-exposure prophylaxis (PEP) annually. Bite of rabid animals and saliva of infected host are mainly responsible for transmission and wildlife like raccoons, skunks, bats and foxes are main reservoirs for rabies. The incubation period is highly variable from 2 weeks to 6 years (avg. 2-3 months). Though severe neurologic signs and fatal outcome, neuropathological lesions are relatively mild. Rabies virus exploits various mechanisms to evade the host immune responses. Being a major zoonosis, precise and rapid diagnosis is important for early treatment and effective prevention and co...

Journal of Medical Case Reports

Background Rabies, caused by a lyssavirus, is a viral zoonosis that affects people in many parts of the world, especially those in low income countries. Contact with domestic animals, especially dogs, is the main source of human infections. Humans may present with the disease only after a long period of exposure. Nearly half of rabies cases occur in children <15 years old. We report on a fatal case of rabies in a Ghanaian school child 5 years after the exposure incident, and the vital role of molecular tools in the confirmation of the diagnosis. Case presentation The patient, an 11-year-old junior high school Ghanaian student from the Obuasi Municipality in Ghana, presented with aggressive behavior, which rapidly progressed to confusion and loss of consciousness within a day of onset. Her parents reported that the patient had experienced a bite from a stray dog on her right leg 5 years prior to presentation, for which no antirabies prophylaxis was given. The patient died within m...

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Research Article

Reverse Zoonotic Disease Transmission (Zooanthroponosis): A Systematic Review of Seldom-Documented Human Biological Threats to Animals

Affiliations College of Public Health and Health Professions, University of Florida, Gainesville, Florida, United States of America, Emerging Pathogens Institute, University of Florida, Gainesville, Florida, United States of America

Affiliation College of Public Health and Health Professions, University of Florida, Gainesville, Florida, United States of America

* E-mail: [email protected]

• Ali M. Messenger, 
• Amber N. Barnes, 
• Gregory C. Gray

• Published: February 28, 2014
• https://doi.org/10.1371/journal.pone.0089055
• Reader Comments

Research regarding zoonotic diseases often focuses on infectious diseases animals have given to humans. However, an increasing number of reports indicate that humans are transmitting pathogens to animals. Recent examples include methicillin-resistant Staphylococcus aureus , influenza A virus, Cryptosporidium parvum , and Ascaris lumbricoides . The aim of this review was to provide an overview of published literature regarding reverse zoonoses and highlight the need for future work in this area.

An initial broad literature review yielded 4763 titles, of which 4704 were excluded as not meeting inclusion criteria. After careful screening, 56 articles (from 56 countries over three decades) with documented human-to-animal disease transmission were included in this report.

In these publications, 21 (38%) pathogens studied were bacterial, 16 (29%) were viral, 12 (21%) were parasitic, and 7 (13%) were fungal, other, or involved multiple pathogens. Effected animals included wildlife (n = 28, 50%), livestock (n = 24, 43%), companion animals (n = 13, 23%), and various other animals or animals not explicitly mentioned (n = 2, 4%). Published reports of reverse zoonoses transmission occurred in every continent except Antarctica therefore indicating a worldwide disease threat.

Interpretation

As we see a global increase in industrial animal production, the rapid movement of humans and animals, and the habitats of humans and wild animals intertwining with great complexity, the future promises more opportunities for humans to cause reverse zoonoses. Scientific research must be conducted in this area to provide a richer understanding of emerging and reemerging disease threats. As a result, multidisciplinary approaches such as One Health will be needed to mitigate these problems.

Citation: Messenger AM, Barnes AN, Gray GC (2014) Reverse Zoonotic Disease Transmission (Zooanthroponosis): A Systematic Review of Seldom-Documented Human Biological Threats to Animals. PLoS ONE 9(2): e89055. https://doi.org/10.1371/journal.pone.0089055

Editor: Bradley S. Schneider, Metabiota, United States of America

Received: September 24, 2013; Accepted: November 4, 2013; Published: February 28, 2014

Copyright: © 2014 Messenger et al. 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.

Funding: This work was supported by the US Armed Forces Health Surveillance Center - Global Emerging Infections Surveillance Operations (multiple grants to GCG) and a supplement from the National Institute of Allergy and Infectious Diseases (R01 AI068803 to GCG). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

Introduction

With today's rapid transport systems, modern public health problems are growing increasingly complex. A pathogen that emerges today in one country can easily be transported unnoticed in people, animals, plants, or food products to distant parts of the world in less than 24 hours [1] . This high level of mobility makes tracking and designing interventions against emerging pathogens exceedingly difficult, requiring close international and interdisciplinary collaborations. Fundamental to these efforts is an understanding of the ecology of emerging diseases. Published works often cite the large proportion of human emerging pathogens that originate in animals [2] , [3] , [4] , [5] . However, scientific reports seldom mention human contributions to the variety of emerging diseases that impact animals. The focus of this review is to examine and summarize the scientific literature regarding such zoonoses transmission. A comprehensive table of the results is included in this document.

For the purpose of this review several terms require definitions. Despite the fact that the term “zoonosis” usually refers to a disease that is transmitted from animals to humans (also called “anthropozoonosis”) [6] , in this paper, “zoonosis” was defined as any disease that is transmitted from animals to humans, or vice versa [6] , There are two related terms (“zooanthroponosis” and “reverse zoonosis”) that refer to any pathogen normally reservoired in humans that can be transmitted to other vertebrates [6] . Acknowledging that the terms “reverse zoonosis” or “zooanthroponosis” are seldom used, and that the term “zoonosis” can have several meanings, search methods were designed to include all of these terms in an effort to capture the widest possible subset of publications with documented human-to-animal transmission.

Literature search

In June 2012, we searched PubMed in addition to several databases within Web of Knowledge and ProQuest to find articles documenting reverse zoonoses transmission. Search terms included: reverse zoonosis , bidirectional zoonosis , anthroponosis , zooanthroponosis , anthropozoonosis , and human-to-animal disease transmission . Articles were limited to clinical and observational type studies and were restricted to English only. Review articles were not included as they did not demonstrate a specific account of transmission. Letters to editors or similar correspondence were also excluded. Only publications with documented human-to-animal transmission were included. No time period was stipulated.

Four search strings were used for the PubMed database: ((bidirectional OR reverse) AND (zoono* or “disease transmission”)) OR anthropono* OR “human-to-animal”), ((bidirectional OR reverse OR “human-to-animal”) AND (zoono* or “disease transmission”)) OR anthropono*), (“reverse zoonoses” OR “ bidirectional zoonoses” OR “reverse zoonosis” OR “ bidirectional zoonosis” OR “reverse zoonotic” OR “ bidirectional zoonotic” OR anthropono* OR (“human-to-animal” AND disease* AND transmi*)), and (((bidirectional OR reverse OR “human-to-animal”) AND (zoonoses[majr] OR “Disease Transmission, Infectious”[majr] OR zoonosis[tiab] OR zoonoses[tiab] OR zoonotic[tiab])) OR Anthroponos*[tiab] OR Zooanthroponos*[tiab] OR Anthropozoonos*[tiab]). In the ProQuest and Web of Knowledge databases, we only used one string: ((bidirectional OR reverse) AND (zoonosis OR zoonoses OR zoonotic)) OR anthropono* OR Zooanthropono* OR anthropozoono* OR “human-to-animal” OR “human to animal”). The lack of additional search strings for the latter databases was due to less comprehensive search capabilities. Duplicate articles were removed.

Literature analyses

Titles and abstracts were reviewed and articles were retained when there was evidence of disease transmission from humans to animals. During full text review, some citations proved straightforward in distinguishing transmission from humans to animals (e.g. via direct contact), while others were selected based on strong author suggestion or research implications toward reverse zoonotic transmission. In an effort to highlight trends in an otherwise diverse set of articles, citations were grouped by pathogen type and year of publication. To further clarify relationships, we also pictorially displayed the study locations and animal types discussed in the various articles.

This comprehensive literature review yielded 4763 titles, 2507 of which were excluded as duplicates ( Figure 1 ). During the review of abstracts, 2091 studies were excluded due to a lack of evidence of human-to-animal disease transmission. After consideration of the 165 eligible for full text review, 109 studies were excluded based on full texts being written in a language other than English, absence of human-to-animal disease transmission, or full texts being unavailable. After all exclusions, 56 articles were considered for this review ( Table 1 ).

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https://doi.org/10.1371/journal.pone.0089055.g001

https://doi.org/10.1371/journal.pone.0089055.t001

Included reports were based in 56 different countries. Although the reports spanned three decades, there seems to be an increasing number of studies published in recent years ( Figure 2 ). Twenty eight percent of the studies were conducted in the United States (n = 16), 14% in Canada (n = 8), and 13% in Uganda (n = 7) ( Figure 3 ). Within the study results, 21 publications discussed human-to-animal transmission of bacterial pathogens (38%); 16 studies discussed viral pathogens (29%); 12 studies discussed human parasites (21%); and seven studies discussed transmission of fungi, other pathogens, or diseases of multiple etiologies (13%). Bacterial pathogen reports were centered in North America and Europe. Viral studies were well-distributed globally. Parasitic disease reports were conducted chiefly in Africa. Fungal studies were conducted almost exclusively in India ( Figure 4 ).

https://doi.org/10.1371/journal.pone.0089055.g002

Note: Many reports identified several countries therefore each country in this figure does not necessarily represent a single corresponding publication.

https://doi.org/10.1371/journal.pone.0089055.g003

A. Proportion of reverse zoonoses scientific reports as illustrated by study location and pathogen type; B. Proportion of reverse zoonoses scientific reports on bacterial pathogens as illustrated by study location; C. Proportion of reverse zoonoses scientific reports on viral pathogens as illustrated by study location; D. Proportion of reverse zoonoses scientific reports on parasitic pathogens as illustrated by study location; E. Proportion of reverse zoonoses scientific reports on fungal pathogens as illustrated by study location.

https://doi.org/10.1371/journal.pone.0089055.g004

Animals with reported infection or inoculation with human diseases included wildlife (n = 28, 50%), livestock (n = 24, 43%), companion animals (n = 13, 23%), and other animals or animals not explicitly mentioned (n = 2, 4%). The majority of companion and livestock animals were studied in North America and Europe, while wildlife studies were most prevalent in Africa ( Table 1 , Figure 5 ). Typically, diagnostic specimens were collected at veterinary hospitals (n = 15, 27%), national parks (n = 8, 14%) and livestock farms (n = 8, 14%). Direct contact was the suggested transmission route 71% of the time (n = 40). Other transmission routes included fomite, oral contact, aerosols, and inoculation.

A. Proportion of reverse zoonoses scientific reports as illustrated by study location and animal(s) infected; B. Proportion of reverse zoonoses scientific reports on companion animals as illustrated by study location; C. Proportion of reverse zoonoses scientific reports on livestock as illustrated by study location; D. Proportion of reverse zoonoses scientific reports on wildlife as illustrated by study location.

https://doi.org/10.1371/journal.pone.0089055.g005

As early as 1988, zoonoses research focusing on fungal pathogens was being conducted. Initial studies implied human transmission of Microsporum (n = 2) and Trichophyton (n = 2) to various animal species, with a later article centered on Candida albicans (n = 1) ( Figure 2 ). These publications were set in India (n = 2) and the United States (n = 1).

Since 1988, research with implications of reverse zoonoses has been largely focused on infections of bacterial origin, beginning in 1995. The majority of articles in this review focused on methicillin-resistant Staphylococcus aureus (MRSA) (n = 9) and Mycobacterium tuberculosis (n = 5). Reports regarding these bacteria were primarily conducted in the United States (n = 8) among livestock (n = 10) or companion animals (n = 9).

Viruses were the second most common pathogen associated with human-to-animal transmission. Reverse zoonoses reports regarding viral pathogens began in 1998 and have since been focused primarily on influenza with great interest surrounding the 2009 H1N1 pandemic (n = 9). These studies were conducted largely in the United States (n = 6) in livestock (n = 8) and wildlife (n = 8).

Studies suggestive of transmission of human parasites to animals were first published in 2000. The most commonly reported parasitic agents to be transmitted from humans to animals were Giardia duodenalis (n = 6) and Cryptosporidium parvum (n = 4). Parasitic research has been carried out most frequently in Uganda (n = 4) and Canada (n = 2). The authors investigated human parasitic infections chiefly in wildlife (n = 10) and livestock (n = 5).

Human-to-animal transmission is plausible for a large number of diseases because the pathogens concerned are known to infect multiple species [3] . For instance, 77.3% of the pathogens infecting livestock are considered “multiple species pathogens [3] .” However, this review only found 24 reports which considered reverse zoonoses disease transmission as a potential threat to livestock, underscoring a need for further research in this area [3] . Similarly, in companion animals this review found even fewer studies (n = 13) that implied reverse zoonoses as a possible cause of infection, despite the fact that 90% of known pathogens for domestic carnivores are recognized as “multiple species pathogens [3] .” The majority of publications in this reverse zoonoses review involved studies documenting human-to-wildlife transmission (n = 28). Unfortunately, they too were severely lacking in comparison to the research need. Each type of animal- livestock, companion, or wildlife, represents a unique set of risk factors for reverse zoonoses through their specific routes of human contact.

Human and animal relationships are likely to continue to intensify worldwide over the next several decades due in part to animal husbandry practices, the growth of the companion animal market, climate change and ecosystem disruption, anthropogenic development of habitats, and global travel and commerce [2] . As the human-animal connection escalates, so does the threat for pathogen spread [1] , [63] . This review notes a number of factors that influence the risk of disease transmission from humans to animals.

For instance, human population growth and expansion encourages different species to interact in ways and at rates previously not encountered, and to do so in novel geographical areas [4] . The term “pathogen pollution” refers to the process of bringing a foreign disease into a new locality due to human involvement [64] . In the case of the endangered African painted dog, wild dogs have been infected with human strains of Giardia duodenalis , leading researchers to believe that pathogen pollution occurred through open defecation in and around national parks by tourists and local residents [53] . Anthropogenic changes in the ecosystem increase the amount of shared habitats between humans and animals thus exposing both to new pathogens. Researchers discovered the human strain of pandemic Escherichia coli strain 025:H4-ST131 CTX-M-15 in many different species of animals indicating inter-species transmission from humans to pets and livestock [23] . This particular human strain found to be infecting animals was documented across Europe.

In addition to habitat change, growth, and/or destruction, there is the ever-increasing global movement of products and travelers that extends to both humans and animals. During the pandemic of 2009 H1N1 influenza, the novel virus was able to travel across the globe and from humans to swine in less than two months [32] . One driving force behind the movement of animals and animal products is the worldwide shipment of meat. This phenomenon is a relatively new event as developing countries adjust their diets to include more meat- and dairy-based products [4] . While food and animal safety guidelines attempt to keep up with the speed of global trade, international efforts appear to be outpaced by product demand. For example, it has been estimated that five tons of illegal bushmeat pass through Paris' main Roissy-Charles de Gaulle airport each week in personal luggage [65] . However, overt retail systems of animal and animal products can also contribute to the danger of zoonoses and reverse zoonoses transmission. Many animals are sold in markets which allow humans and a myriad of animal species to interact in conditions that are known to trigger emerging diseases [66] . Specifically, this is true for live animal markets and warehouses for exotic pets [4] .

The pet industry is an enormous global business that now expands from domestic to exotic animals. A 2011–2012 national pet owners survey found that in the United States alone, 72.9 million homes or 62% of the population have a pet [67] . Of these pets, the majority of animals are dogs (78.2 million) or cats (86.4 million), but a large number of pets are birds (16.2 million), reptiles (13 million), or small animals (16 million) [67] . As pet ownership seems to be increasing worldwide and more exotic pets are being introduced to private homes, the potential for disease transmission between humans and animals will continue to increase. Veterinarians must more fervently protect animals under their care from human disease threats [68] . Adopting a One Health strategy for emerging disease surveillance and reporting will benefit both humans and animals and produce a more collaborative response plan.

Veterinarians, animal health workers, and public health professionals are not the only ones who should recognize the threat of reverse zoonoses. Increased awareness must also be communicated to the general public. Worldwide, there are 1,300 zoos and aquariums that sustain more than 700 million visitors each year [69] . The potential for pathogen spread to animals can come from a visitor with an illness, contamination of a shared environment or food, and the spread of disease through relocation of animals for captivity or educational purposes. In Tanzania, a fatal outbreak of human metapneumovirus in wild chimpanzees is believed to be the result of researchers and visitors viewing the animals in a national park that was once the great apes' territory [30] . Public education and awareness should be augmented to include the potential health threats inflicted on a susceptible animal by an unhealthy human.

This report has limitations. As demonstrated in this review paper, the trend for reporting pathogen spread of human-to-animal is increasing. However the route of human transmission to animal disease manifestation is often unknown in these reports and not well documented in this review. Also the report did not examine articles that did not document human-to-animal transmission. We acknowledge that many additional works that have recorded the existence of human pathogens in animals were not evaluated. However, this review was designed to summarize only the publications that document reverse zoonotic transmission.

Many common and dangerous pathogens have not, to the authors' knowledge, been researched as reverse zoonoses threats to animals representing a significant gap in the scientific literature. Future investigations of reverse zoonoses should take into account both transmission routes and disease prevalence. Prospective research should also include a wider variety of etiological agents and animal species. Scientific literature must document the presence and transmission of human diseases in animals such that the wealth of literature on this subject will become defined and accessible across multiple disciplines. A wider knowledge and understanding of reverse zoonoses should be sought for a successful One Health response. We recommend that future research be conducted on how human disease can, and does, affect the animals around us.

Supporting Information

PLOS PRISMA 2009 checklist.

https://doi.org/10.1371/journal.pone.0089055.s001

Acknowledgments

The authors especially thank Nancy Schaffer and Jennifer Lyon from the University of Florida Library Sciences for their research assistance.

Author Contributions

Analyzed the data: AM AB GG. Wrote the paper: AM AB GG.

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• Published: 14 September 2024

Teratoma combined with struma ovarii and sarcomatoid carcinoma: a case report and review of the literature

• Haojie Qin 1 , 2 ,
• Dan Chen 2 , 3 , 4 ,
• Shan Jin 2 , 3 , 4 ,
• Jia Liu 2 , 3 , 4 ,
• Bo Gao 2 , 3 , 4   na1 &
• Yongpeng Wang 2 , 3 , 4   na1  

BMC Women's Health volume  24 , Article number:  517 ( 2024 ) Cite this article

Metrics details

This is a rare case of struma ovarii combined with sarcomatoid carcinoma. Because struma ovarii and ovarian sarcomatoid carcinoma have an extremely low incidence, this may be the first case of a combined occurrence of both. Therefore, this report describes its clinical manifestations, diagnosis, and treatment, analyzes the pathogenesis, and summarizes the previous literature in the hope that it can be helpful to other tumor-related medical personnel and provide material support for the formation of guidelines for this disease.

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Introduction

Ovarian teratoma is a kind of ovarian germ cell tumor with mainly benign lesions, accounting for about 15% of the total number of primary ovarian tumors, and its malignant change rate is only 0.2% ~ 2%, and mainly squamous cell carcinoma [ 1 ]. Struma Ovarii (SO) is a special pathological type of teratoma differentiated from a single germ layer, accounting for about 2% ~ 3% of ovarian teratoma and 0.1% ~ 0.5% of all ovarian tumors [ 2 ], incorporation with sarcomatoid carcinoma is even rarer. Therefore, the clinical diagnosis, treatment plan, and prognosis evaluation of Struma Ovarii with sarcomatoid carcinoma are still unclear, and it is difficult to form a convincing expert consensus or guidelines for gynecologic oncologists. This paper reported a case of ovarian teratoma combined with struma ovarii and sarcomatoid carcinoma, summarized its clinical characteristics and treatment methods in the light of the literature, in order to improve the relevant knowledge of the disease and provide a reference for the diagnosis, treatment, and prognosis.

Case presentation

A 67-year-old woman was admitted to the hospital with "the lower abdomen was unwell for more than half a year, and the pelvic mass was found for 5 days". In May 2023, she felt abdominal discomfort and occasionally had abdominal pain. She took oral antibiotics for more than half a month (The patient self-medicated, which could only be determined to be a second-generation cephalosporin), and abdominal pain was slightly relieved. In June 2023, there was more pain in the lower abdomen than before and she went to the local hospital for treatment. Physical examination showed that vital signs were stable, generally in good condition, and no abnormal physical development. There was no palpable enlargement of superficial lymph nodes throughout the body and no abnormalities on cardiopulmonary auscultation. The abdomen was flat without tenderness and rebound pain, the liver and spleen were not palpable under the ribs, and there was negative shifting dullness. The gynecological examination revealed normal vulvar development, with notable thickening and hyperpigmentation of the left labia and perineal skin junction. The patient had a patent vagina, a smooth cervical posterior lip, and an erosion cervical inner anterior lip. The uterus was unsatisfactory on palpation, no mass was touched in the left appendage area, and the mass in the right appendage area was about 9 × 7 × 7 cm in size. The rectal mucosa was smooth and nodules were not touched in the Douglascul-de-sac.

On December 18, 2023, an ultrasound at a local hospital suggested multiple pelvic masses; Magnetic resonance imaging (MRI) of the pelvis showed a right adnexal mass (9.8 × 6.3 cm, mixed-signal) suggestive of a possible teratoma; there was also a enhancing nodule, so malignancy could not be completely excluded (Fig.  1 a and b). On December 25, 2023, she came to our hospital for further treatment. The patient had no fever recently, and her diet, sleep, urinary, and bowel function were normal. She had regular menstruation previously, with natural menopause at 51 years old, G2A0P2, VD. Past medical history and family history of tumor were denied.

a depicts a pelvic magnetic resonance T1W enhanced fat suppression image, which reveals a visible left pelvic cystic-solid interphase mass. b is a diffusion-weighted (DWI), which indicates a high signal of tumor nodules in the right posterior area of the tumor. The O-RADS MRI score is 4, indicating a high probability of malignancy. c and d show an irregular mixed mass on the right side of the pelvic cavity, with visible fat density and calcification, and enhanced soft tissue components,  indicating the presence of solid component

The routine blood test and liver and kidney function results were normal. Tumor markers were of the normal range: CA199 3.51 U / mL; AFP 4.33 ng/mL; CEA 2.08 ng/mL; CA125 26.40 U / mL; HE422.70 pmol / L. HPV: (-); TCT: NILM. ECG: Normal. Cardiac ultrasound: in the resting state, the left ventricular overall systolic function is normal. Pulmonary function test: moderately restricted ventilation dysfunction, mild ventilation dysfunction, and reduced small airway function. Computed tomography (CT) of the lung and abdomen: irregular mass on the right side of the pelvic cavity, ranging about 9.1 cm × 6.7 cm, mixed density, fat density and calcification, and enhancement of soft tissue composition; no enlarged lymph nodes in the retroperitoneal area (Fig.  1 c and d).

After a comprehensive examination, the preliminary diagnosis of pelvic mass (malignancy cannot be excluded). After the evaluation by anesthesiologists of our hospital, there were no absolute surgical contraindications, and the exploratory laparotomy was performed under general anesthesia on December 27, 2023. Intraoperative observation: no ascites, no abnormality in the upper abdomen. The right ovary was replaced by a mass, about 10 × 8 × 7 cm in size, and the right fallopian tube was attached to the mass; the appearance of the left ovary and fallopian tube was normal. No significant abnormalities were observed in the uterus and greater omentum appearance.

The peritoneum of the bladder wall layer was adhered to the right ovarian mass with an area of about 4 × 3 cm. After separation, the abnormal peritoneal membrane was completely removed and sent to intraoperative frozen pathology. The result showed that the heterogeneous cells were seen in the fiber stroma, which was considered carcinoma. The right ovarian vessels were isolated by high ligation, the right broad ligament was freed, the right utero-ovarian ligament was isolated, and the right ovary and fallopian tube were completely removed and sent for intraoperative frozen pathology. The result was (right adnexal mass) struma ovarii and the diffuse distribution of heterogeneous cells in some areas was malignant. Based on the results, the intraoperative diagnosis of ovarian cancer was stage IIB, according to the 2023 NCCN guidelines for ovarian cancer [ 3 ]. Then, the uterus and left ovary fallopian tube, greater omentum were completely resected, with peritoneal multipoint biopsy.No enlarged lymph nodes were found in the internal iliac, external iliac, common iliac, or obturator regions, so no resection was performed.

After surgery, the gross specimen was examined as follows (Fig.  2 a); upon dissection of the mass, a cystic-solid component was visible within the right ovary, with contents including oil, hair, bone structure, and thyroid components (Fig.  2 b).

a shows the gross specimen (en -bloc); b shows upon dissection of the specimen, which is a cystic-solid component, with contents including oil, hair, bone structure, and thyroid component

Postoperative pathology showed that the morphology was dominated by a teratoma component with polygonal differentiation and prominent zones of heterogeneous spindle cells, which had a clear line between the two regions (Fig.  3 ), and tumor cell infiltration could be seen under the peritoneum of the bladder wall (Fig.  4 ). The teratoma component exhibited mature thyroid follicular structures (a variable amount of eosinophilic colloids was observed within the cavity, with the follicular epithelium was a single layer of low columnar or cubic cells), and it accounted for > 50% of the tumors, and differentiated and mature squamous epithelium and skin appendages (sebaceous gland and hair follicle structures) can also be found; the spindle cell region was characterized by significant cellular heterogeneity, deeply stained nuclei, and eosinophilic cytoplasm. The immunohistochemical results were as follows CK ( +), Vimentin ( +), Ki67 (80% +), S-100 (-), Desmin (-), MyoD 1 (-), P53 ( +) / mutant, P40 (-), Sall-4 (-), Pax-8 (-), SMA minority cells ( +), the data indicated that this region had an epithelial and mesenchymal origin of biphasic differentiation and did not support differentiation into nerve, striated muscle, female germ cell tumors, and squamous cell carcinoma (Fig.  5 a-d).

HE staining shows that the morphology is mainly composed of teratoma components, with polygonal differentiation and obvious heterogeneous spindle cell regions, with clear boundaries between the two regions

HE staining shows infiltration of bladder serosa by cancer cells

a Under low magnification, epithelial derived marker CK is expressed in both the follicular of the thyroid gland and atypia spindle cell region (Envision two –step method); b Under low magnification, the mesenchymal derived marker Vimentin is not expressed in the thyroid follicular region, but in the spindle cell region (Envision two step method); c Under low magnification, the squamous epithelial marker P40 is not expressed in the spindle cell region, ruling out squamous cell carcinoma, which is the most common malignant transformation of teratoma; d Under low magnification, the proliferation index Ki67 is low expressed in the thyroid follicular region and high expressed in the spindle cell region, which means higher degree of malignancy in sarcomatoid carcinoma

TC chemotherapy is the recommended postoperative treatment. The patient is currently on chemotherapy with no adverse reactions above II°.

Ovarian teratoma was classified into mature teratoma (benign) and immature teratoma (malignant) according to their pathological nature, 95% of which were mature teratoma [ 4 ]. Early symptoms are not obvious, mainly due to the physical examination found, surgery is the main treatment currently [ 5 ]. SO is a highly specific monoembryonic teratoma, whose diagnostic criteria are microscopic thyroid tissue composition > 50%, or thyroid tissue < 50% but with significant hyperthyroidism, or visually recognizable thyroid tissue in a mature teratoma [ 6 ]. SO has predominantly unilateral, left-sided onset, with right-sided onset in slightly older patients and bilateral onset in 8% of patients [ 7 ]. The right-sided onset of the disease in this elderly patient is consistent with the literature. The clinical incidence of SO is very low and lacks typical clinical symptoms. Most of them are found by physical examination or with abdominal mass or abdominal pain. However, some studies have reported that about one-third of clinical patients have "Meigs syndrome" [ 8 ]. Based on the high incidence of pleural effusion and ascites and high level of CA125 expression in struma ovarii, some experts suggest that pleural effusion, ascites, and elevated CA125 should be included in the differential diagnosis of pelvic mass and struma ovarii [ 9 ]. However, CA125 will increase in both benign and malignant cases, and will not continue to rise even in malignant cases. It is speculated that the increase in CA125 is not a direct result of the tumor itself, but rather a side effect of ascites [ 10 ]. In a recently published case report of a papillary thyroid carcinoma within a mature cystic ovarian teratoma, CA25 was also found to be in the normal range [ 11 ]. It is worth noting that although SO is a tumor composed of thyroid tissue, only 8% of the patients have hyperthyroidism [ 12 ]. This suggests that, in the majority of cases, the thyroid tissue in the SO does not have the full function of synthesizing thyroid hormones. And some studies have shown that thyroglobulin can be used as a diagnostic reference for SO [ 13 ]. In this case, thyroid function was not tested because SO was not diagnosed preoperatively and the patient did not have symptoms of hyperthyroidism.

Because the clinical features of SO are also similar to those of ovarian malignancies, so preoperative imaging diagnosis becomes more important to distinguish ovarian cancer and avoid cancer-type surgery (eg, bilateral salpingectomy, hysterectomy). Ultrasound is the first choice for the evaluation of ovarian masses during imaging studies [ 14 ]. However, the ultrasound findings of struma ovarii are ambiguous and usually manifest as a multilocular cystic ovarian mass with solid components of various amounts, the ultrasound typically demonstrates these non-specific heterogeneous solid cystic features [ 15 ]. The SO has features overlapping with those of malignant ovarian epithelial tumors, though they both present as a unilateral complex adnexal mass often associated with ascites, or as multi-cystic mass with solid components and multiple cystic locules, usually including teratoma components. The SO contains a”struma pearl”: a rounded solid area with smooth contours corresponding to colloidal thyroid tissue [ 16 ]. Familiarity with the "doughnut sign" and the "fat layering sign" can help in the differential diagnosis, but it is possible to overestimate the malignancy of SO [ 17 ]. MRI shows a solid component with moderate to high signal intensity on T1-WI, whereas the signal intensity of the cystic portion on T2-WI depends on the viscosity of the fluid. On CT, the enhancement of the septal or solid component depends on the content of the thyroid tissue [ 18 , 19 ]. As SO is an uncommon tumor, unlike the most common types of teratoma, does not demonstrate lipid material on either CT or MRI [ 20 ], but 123I or 131I scintigraphy is useful for diagnosing a superfunction SO [ 18 ]. Because SO is difficult to make a definitive preoperative diagnosis, postoperative paraffin pathology combined with immunohistochemistry is still the ultimate basis for diagnosis. In addition to thyroid tissue, there was obvious mature teratoma tissue [ 21 ], typical presentation: multilocular, uneven wall thickness, yellow and grayish-red jelly-like contents; immunohistochemical features: TTF 1 ( +), TG ( +), PAX-8 ( +), CK7 ( +), and Muc-1 ( +). Routine gynecological examinations (especially ultrasound scans) improve the early diagnosis of SO. Due to the low incidence of SO and no clear diagnosis and treatment guidelines, surgery is still the main treatment modality. Due to its ultrasound morphology, which is quite similar to that of malignant ovarian carcinoma, most SO cases are often operated on with laparotomy, involving either ovariotomy or oophorectomy [ 22 ]. For malignant struma ovarii, radioactive iodine supplementation after surgery is effective in preventing metastasis or recurrence [ 23 ]. For people at high risk of developing cancer-causing factors, postoperative clinical and ultrasound follow-up is needed every six months or year.

In addition to teratoma and SO of the pathological components, some malignant cells also be found that have significant spindle shape changes, including both epithelial markers and sarcoma markers. At first, we thought it was carcinosarcoma. However, carcinosarcoma needs to determine the components of carcinoma, such as adenocarcinoma, and squamous carcinoma. Sarcomatoid carcinomas typically feature pleomorphic spindle cells in intertwined bundles with high-grade nuclei, expressing both epithelial (e.g, CK, EMA) and mesenchymal (e.g, Vimentin) markers. They lack tissue specificity, excluding sarcomas like liposarcoma and rhabdomyosarcoma, as well as carcinomas like ovarian plasma carcinoma and squamous cell carcinoma, thus qualifying as sarcomatoid carcinoma [ 24 ]. The specific origin of the cancerous and sarcomatous components could not be determined in this case. The protein P40, which characterizes the most common squamous carcinoma of teratoma malignancy, is negative. However, it expressed both epithelial (CK) and mesenchymal component (Vimentin) markers, so pathologists prefer to diagnose sarcomatoid carcinoma. SC is also known as spindle cell carcinoma, which the epithelial carcinoma component determines the biological behavior of metastasis, and the sarcoma component determines the prognosis. Usually, sarcomatoid tissue accounts for more than 50% of malignant tissues [ 25 ]. In addition, it is necessary to perform immunohistochemistry to confirm the presence of epithelial components or sarcomatoid tissue surrounded by epithelial tissue that has a heavy heterogeneous proliferation of carcinoma in situ. Otherwise, it should be differentiated from sarcoma, to avoid misdiagnosis when the proportion of sarcoma components in SC tissue is too large [ 26 ].

Whether it is carcinosarcoma or sarcomatoid carcinoma, for germ cell tumors, which may have the characteristics of cell stemness, there are currently three theories of its formation mechanism: collision theory, combinatorial theory, and transformation theory. "collision theory" believes that these two types of diseases have two components: epithelial cancer and sarcomatoid stroma, so it is proposed that tumor cells are biclonal, epithelial cancer components and sarcoma components are derived from two types of stem cells, evolve independently, and then collide; the "combination theory" suggests that a stem cell precursor in the early bidirectional differentiation into epithelial carcinoma components and sarcoma components; at present, the most recognized "transformation theory" proposes that the sarcoma component comes from carcinoma cells or the original stem cells is differentiated into one kind of cell and re-differentiated to form a second cell. Its essence is a special type of cancer, and the sarcomatoid component is only the transformation of the cancer component [ 27 ]. A recent study tested RNA for cancer and sarcoma components in 18 patients with ovarian carcinosarcoma (OCS) found that the cancer component in OCS was more mesenchymal compared to epithelial ovarian cancer, supporting the conjecture that the sarcoma component is transformed through epithelial-mesenchymal cancer component. In this case, CK ( +) and Vim ( +) suggested that the spindle cell area was characterized by biphasic differentiation characteristics of epithelial and mesenchymal origin, which also tended to support the "transformation theory" [ 28 ].

Although sarcomatoid carcinoma has been found in several organs, including the breast, bladder, and kidney [ 29 , 30 , 31 ], there are few clinical reports and studies on ovarian sarcomatoid carcinoma (OSC) and only a few documents on PubMed, and most of them are case reports [ 32 , 33 ]. There are no standard guidelines for their diagnosis and treatment currently. Combined with the existing literature and our clinical experience, the early symptoms of OSC are not obvious, and they are usually found in physical examination or abdominal pain, abdominal distension, and other manifestations. Tumor markers generally increase in CA125, and then the pelvic mass is found by imaging examination. Preoperative imaging does not allow for differential diagnosis. However, the extent and staging of the disease can be assessed. Ultrasound cannot differentiate ovarian sarcomatoid carcinoma from other poorly differentiated ovarian cancers. CT can provide the condition around the lesion and the presence of peritoneal and lymph node metastasis, providing an important basis for clinical staging. MRI shows mixed images of hemorrhage, cyst, or necrosis [ 34 ]. Due to the difficulty of preoperative diagnosis of OSC, it is finally determined by postoperative pathological examination, as a result, the condition has often progressed to advanced stages when identified. In this case, the diagnosis of teratoma was initially confirmed by preoperative imaging, which prompted the patient to seek further treatment at our hospital. Although the preoperative imaging could not further confirm the diagnosis, it still plays an important role. This suggests that with the existing medical technology, although we cannot accurately diagnose teratoma combined with ovarian struma and sarcomatoid carcinoma, we can make good preoperative preparations for malignant tumor during the patient's operation if teratoma is diagnosed, which is very meaningful. There is no direct relevant literature for the evaluation of prognosis, which can refer to the latest literature report on ovarian carcinosarcoma, whose 5-year survival rate is 29.8%, and the median survival period is 16 to 24 months [ 35 ]. Median survival was reported to be 11 months for patients with sarcomatoid carcinoma of the bladder and 3.5 months for patients with sarcomatoid carcinoma of the rectum [ 36 , 37 ].

Currently, the treatment of OSC is based on cytoreductive surgery combined with platinum-based chemotherapy, similar to ovarian carcinosarcoma or epithelial carcinoma [ 38 ]. Among other treatments, radiotherapy is not recommended, and the efficacy of targeted therapy and immune checkpoint inhibitors for OSC is still controversial and needs more studies [ 39 , 40 ]. Aoki M et al found that the loss of expression of the ARID1A gene and the same PIK3CA mutation in different tissues, proving the monoclonality of sarcomatoid carcinoma and also providing evidence to support the transformation theory [ 41 ]. According to the monoclonality of the disease, individual treatment options can be selected for the mutation gene to improve the survival rate and improve the quality of life for patients.

We report a rare case of ovarian tumor in which preoperative investigations showed a high likelihood of benignity, but malignancy could not be completely excluded. Intraoperative frozen section pathology revealed a malignant component. According to FIGO staging, the diagnosis was stage IIB, and total hysterectomy + double adnexa + greater omentum was performed. Postoperative pathology diagnosed teratoma combined with struma ovarii and sarcomatoid carcinoma. According to our case and published literature, in patients with teratomas of old age and large local foci, attention should be paid to the possibility of sarcomatoid carcinoma in addition to the possibility of malignant teratoma. It is important to achieve complete excision of the tumor and avoid rupture during surgical treatment to prevent metastasis or spread.

Limitations

(1) Although the patient was initially diagnosed with teratoma by color ultrasound and MRI, the patient had no history of thyroid disease or hyperthyroidism symptoms. Therefore, the relevant test was not carried out, and the struma ovarii was not diagnosed before surgery; (2) Up to now, the observation time is short, and the final survival and outcome still need to wait; (3) Genetic testing should be helpful to the diagnosis and treatment of this disease, but because its consumption is not covered by the Chinese medical insurance, so not be given to patients. In the future, we plan to seek funding for genetic testing to uncover more insights into the pathogenesis at the genetic level.

Availability of data and materials

Not applicable.

Data availability

No datasets were generated or analysed during the current study.

Abbreviations

Struma Ovarii

Magnetic resonance imaging

Computed tomography

Vaginal delivery

Sarcomatoid carcinoma

Ovarian carcinosarcoma

• Ovarian sarcomatoid carcinoma

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Yongpeng Wang and Bo Gao contributed equally to this work.

Authors and Affiliations

Liaoning University of Traditional Chinese Medicine, Shenyang, 110847, China

Liaoning Cancer Hospital & Institute, Shenyang, 110042, China

Haojie Qin, Dan Chen, Shan Jin, Jia Liu, Bo Gao & Yongpeng Wang

Cancer Hospital of China Medical University, Shenyang, 110042, China

Dan Chen, Shan Jin, Jia Liu, Bo Gao & Yongpeng Wang

Cancer Hospital of Dalian University of Technology, Shenyang, 110042, China

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H wrote the main manuscript text and was a surgical participant; D and S are surgical participants; J Managed the patient; B provide pathological diagnosis and specimen pictures; Y revised manuscript, the main participant in the surgery. 

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Correspondence to Bo Gao or Yongpeng Wang .

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Qin, H., Chen, D., Jin, S. et al. Teratoma combined with struma ovarii and sarcomatoid carcinoma: a case report and review of the literature. BMC Women's Health 24 , 517 (2024). https://doi.org/10.1186/s12905-024-03354-y

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DOI : https://doi.org/10.1186/s12905-024-03354-y

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A systematic review of vision transformers and convolutional neural networks for Alzheimer’s disease classification using 3D MRI images

• Published: 17 September 2024

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• Mario Alejandro Bravo-Ortiz 1 , 2 , 7   na1 ,
• Sergio Alejandro Holguin-Garcia 1 , 2 , 7   na1 ,
• Sebastián Quiñones-Arredondo 1 ,
• Alejandro Mora-Rubio 6 ,
• Ernesto Guevara-Navarro 1 , 2 ,
• Harold Brayan Arteaga-Arteaga 1 ,
• Gonzalo A. Ruz 3 , 4 , 5 &
• Reinel Tabares-Soto 1 , 2 , 3  

Alzheimer’s disease (AD) is a progressive neurodegenerative disorder that mainly affects memory and other cognitive functions, such as thinking, reasoning, and the ability to carry out daily activities. It is considered the most common form of dementia in older adults, but it can appear as early as the age of 25. Although the disease has no cure, treatment can be more effective if diagnosed early. In diagnosing AD, changes in the brain’s morphology are identified macroscopically, which is why deep learning models, such as convolutional neural networks (CNN) or vision transformers (ViT), excel in this task. We followed the Systematic Literature Review process, applying stages of the review protocol from it, which aims to detect the need for a review. Then, search equations were formulated and executed in several literature databases. Relevant publications were scanned and used to extract evidence to answer research questions. Several CNN and ViT approaches have already been tested on problems related to brain image analysis for disease detection. A total of 722 articles were found in the selected databases. Still, a series of filters were performed to decrease the number to 44 articles, focusing specifically on brain image analysis with CNN and ViT methods. Deep learning methods are effective for disease diagnosis, and the surge in research activity underscores its importance. However, the lack of access to repositories may introduce bias into the information. Full access demonstrates transparency and facilitates collaborative work in research.

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Acknowledgements

Mario Alejandro Bravo-Ortiz is supported by a Ph.D. grant Convocatoria 22 OCAD de Ciencia, Tecnología e Innovación del Sistema General de Regalías de Colombia y Ministerio de Ciencia, Tecnología e Innovación de Colombia. We would like to thank Universidad Autónoma de Manizales for making this paper as part of the “Clasificación de los estadios del Alzheimer utilizando Imágenes de Resonancia Magnética Nuclear y datos clínicos a partir de técnicas de Deep Learning” with code 873-139 and "Aplicación de Vision Transformer para clasificar estadios del Alzheimer utilizando imágenes de resonancia magnética nuclear y datos clínicos" project with code 847-2023 TD. Additionally, we acknowledge the support from the projects ANID PIA/BASAL FB0002 and ANID/PIA/ANILLO ACT210096. We also extend our gratitude to Universidad de Caldas for their support, as this paper is part of the project “Plataforma tecnológica para la clasificación de los estadios de la enfermedad de alzheimer utilizando imágenes de resonancia magnética nuclear, datos clínicos y técnicas de deep learning.” with code PRY-89. We also thank the National Agency for Research and Development (ANID); Applied Research Subdirection (SIA); through the instrument IDeA I+D 2023, code ID23I10357, and ORIGEN 0011323, Sistema General de Regalías (SGR) - Asignación para la Ciencia, Tecnología e Innovación, project BPIN 2021000100368, and PRY-121 - Interactive Virtual Didactic Strategy for the Promotion of ICT Skills and their Relationship with Computational Thinking.

This work was funded by Universidad Autonoma de Manizales as part of the project “Clasificación de los estadios del Alzheimer utilizando Imágenes de Resonancia Magnética Nuclear y datos clínicos a partir de técnicas de Deep Learning” with code 873-139, and also by the projects “CH-T1246: Oportunidades de Mercado para las Empresas de Tecnología-Compras Públicas de Algoritmos Responsables, Éticos y Transparentes,” ANID PIA/BASAL FB0002, and ANID/PIA/ANILLOS ACT210096.

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Mario Alejandro Bravo-Ortiz and Sergio Alejandro Holguin-Garcia have contributed equally to this work.

Authors and Affiliations

Departamento de Electrónica y Automatización, Universidad Autónoma de Manizales, Manizales, 170001, Caldas, Colombia

Mario Alejandro Bravo-Ortiz, Sergio Alejandro Holguin-Garcia, Sebastián Quiñones-Arredondo, Ernesto Guevara-Navarro, Harold Brayan Arteaga-Arteaga & Reinel Tabares-Soto

Departamento de Sistemas e Informática, Universidad de Caldas, Manizales, 170004, Caldas, Colombia

Mario Alejandro Bravo-Ortiz, Sergio Alejandro Holguin-Garcia, Ernesto Guevara-Navarro & Reinel Tabares-Soto

Facultad de Ingeniería y Ciencias, Universidad Adolfo Ibáñez, 7941169, Santiago, Chile

Gonzalo A. Ruz & Reinel Tabares-Soto

Center of Applied Ecology and Sustainability (CAPES), 8331150, Santiago, Chile

Gonzalo A. Ruz

Data Observatory Foundation, 7941169, Santiago, Chile

Unidad Mixta de Imagen Biomédica FISABIO-CIPF, Fundación para el Fomento de la Investigación Sanitario y Biomédica de la Comunidad Valenciana, 46020, Valencia, Spain

Alejandro Mora-Rubio

Centro de Bioinformática y Biología Computacional (BIOS), 170001, Manizales, Colombia

Mario Alejandro Bravo-Ortiz & Sergio Alejandro Holguin-Garcia

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Contributions

MABO contributed to Conceptualization, Methodology, Investigation, Writing—original draft, Writing—review and editing. SAHG contributed to Conceptualization, Methodology, Investigation, Writing—original draft, Writing—review and editing. SQA contributed to Writing—review and editing. EGN contributed to Writing—review and editing. AMR: Writing—review and editing. HBAA contributed to Writing—review and editing. GAR: Writing—review and editing, acquired the funding and provided the resources. RTS contributed to Writing—review and editing, acquired the funding and provided the resources.

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Bravo-Ortiz, M.A., Holguin-Garcia, S.A., Quiñones-Arredondo, S. et al. A systematic review of vision transformers and convolutional neural networks for Alzheimer’s disease classification using 3D MRI images. Neural Comput & Applic (2024). https://doi.org/10.1007/s00521-024-10420-x

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Received : 26 April 2024

Accepted : 20 August 2024

Published : 17 September 2024

DOI : https://doi.org/10.1007/s00521-024-10420-x

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• v.14; 2022 Jun

Zoonotic pathogens and diseases detected in Vietnam, 2020–2021

Long pham-thanh.

a Department of Animal Health, Ministry of Agriculture and Rural Development, Hanoi, Vietnam

Thu Van Nhu

b Food and Agriculture Organization of the United Nations (FAO), Country Office for Vietnam, Hanoi, Vietnam

Trung Vinh Nguyen

c Oxford University Clinical Research Unit, Ho Chi Minh City, Vietnam

g Department Veterinary Medicine, College of Agriculture, Can Tho University, Can Tho, Vietnam

Khang Vuong Tran

Khanh cong nguyen.

d National Institute of Hygiene and Epidemiology, Ministry of Health, Hanoi, Vietnam

Huong Thi Nguyen

e General Department of Preventive Medicine, Ministry of Health, Hanoi, Vietnam

Ngo Thi Hoa

f Pham Ngoc Thach University of Medicine, Ho Chi Minh City, Vietnam

h Nuffield Department of Clinical Medicine, Oxford University, Oxford, UK

Pawin Padungtod

Vietnam has been identified as a country at high-risk for emergence and re-emergence of zoonotic diseases. The government of Vietnam recognized five priority zoonoses, including highly pathogenic avian influenza, rabies, leptospirosis, anthrax, and Streptococcus suis , and established a framework for One Health investigation and response to these diseases. From July 2020 to February 2021, quantitative data of zoonoses were collected from an online survey in 61 of 63 provinces based on either clinical diagnosis or laboratory confirmation. The responses were followed up by using in-depth interviews, and scientific literatures on zoonoses in Vietnam during 2010 to 2020 were reviewed. A total of 234 human health professionals and 95 animal health professionals responded to the survey. The proportion of clinical-based respondents was higher than laboratory-based respondents in both human health (130/234, 55.6%) and animal health (65/95, 68.4%) sectors. There were differences in the reported frequency of zoonoses between human and animal health professionals, and between clinical-based and laboratory-based respondents. Rabies was the most serious zoonotic disease based on the number of human cases and the geographic distribution. No human cases of avian influenza infection have been reported since 2015, although the H5 subtype viruses have been found in poultry. Besides, some bacterial, fungal, and parasitic zoonoses were detected in both humans and animals. Out of the 75 zoonoses identified, we recommend that the original five prioritized zoonoses, plus 24 additional zoonoses, should be targeted for future prevention, detection, and control under One Health approach in Vietnam.

1. Introduction

In recent years, global public health security has been threatened by the emergence and re-emergence of zoonotic diseases, as exemplified by outbreaks of Ebola virus, avian influenza viruses, severe acute respiratory syndrome (SARS) coronavirus, and the Middle East respiratory syndrome (MERS) coronavirus [ 1 ]. The 2019 outbreaks of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), likely caused by animal species crossing to infect humans, have become a serious public and global health threat [ 1 ].

The increase of emergence and re-emergence of zoonotic diseases has been driven by increasing human and animal populations, infringement of wildlife habitats, the growing demand for wildlife and wildlife products, changing farming practices, climate change, and ease and speed of global travel [ 2 ]. Vietnam is a country at risk for emergence and re-emergence of zoonotic diseases due to high human and livestock densities, increasing urbanization, large volume of domestic as well as cross-border trades for animals and animal products, prevailing small-scale livestock production, poor biosecurity practices, and mixed farming systems [ 3 ].

Highly pathogenic avian influenza, rabies, anthrax, leptospirosis and Streptococcus suis ( S. suis ) have been commonly reported in Vietnam [ 4 ]. In 2015, a study was conducted to establish strategic priorities for zoonotic disease control in Vietnam, and 5 out of 12 diseases were selected for prioritization including avian influenza, rabies, S. suis , pandemic influenza and foodborne bacterial diseases [ 5 ].

To mitigate the risk of emergence and re-emergence of zoonotic diseases, the government of Vietnam issued a joint circular number 16 in 2013 [ 6 ] providing the guidelines for a multisectoral coordinated investigation and response to zoonotic diseases and specified Vietnam priority zoonoses using the One Health approach [ 7 ]. In subsequent years, both the Ministry of Health [ 8 ] and Ministry of Agriculture and Rural Development [ 9 ] issued regulations to support surveillance and reporting of these prioritized zoonoses and to strengthen coordination, information sharing, and collaboration between human health and animal health sectors.

Identifying zoonotic pathogens/diseases commonly detected in Vietnam can provide critical evidence to support further investment in the One Health coordinated zoonotic diseases surveillance and effective prevention and control measures in both humans and animals. Specifically, we identified what zoonoses have been detected, and estimated their frequency of detection in Vietnam.

2. Methodology

2.1. study design.

A retrospective mixed method study was conducted from July 2020 to February 2021, in which quantitative data were gathered from an online survey, the responses were followed up using in-depth interviews, and a literature review of zoonotic pathogens/diseases in Vietnam was analyzed.

The online survey was implemented from July to September 2020. For human health sector, at the central level, all general hospitals, specialized hospitals, medical research institutes, and laboratories related to zoonotic diseases were invited to respond to our questionnaires. At the regional level, we included the National Institute of Hygiene and Epidemiology (NIHE), the Pasteur Institute of Nha Trang, the Pasteur Institute of Ho Chi Minh city (PI– HCMC), and Tay Nguyen Institute of Hygiene and Epidemiology. At the local level, we surveyed provincial general hospitals and all provincial Centres for Disease Control.

For animal health, at the central level, all veterinary research institutes, universities, companies related to animal health and national veterinary laboratories were selected. Seven Regional Animal Health Offices (RAHOs) were included as the regional level. At the local level, the provincial Sub-Departments of Animal Health, local veterinary laboratories, zoos and safari, wildlife rescue centres, and livestock production companies having laboratory diagnostic capacity were also recruited in the survey.

2.2. Selection of respondents

Individuals working for the human health or animal health sectors, either as physicians or medical, laboratory or technical staff in the selected entities were eligible for their participation in the survey. We assumed receiving at least two respondents from all the shortlisted entities either clinical-based or laboratory-based staff to fill in the questionnaires, plus departments involved in research on parasitic pathogens/diseases in animals or humans.

2.3. Questionnaire design

To select the survey items, we initially reviewed a list of potential global zoonotic pathogens/diseases from the MSD manual [ 10 ], the book ‘Diseases That Can Spread Between Animals and People’ [ 11 ], and information from Public Health England [ 12 ]. The inclusion criteria were zoonotic pathogens/diseases and their potential hosts and reservoirs previously identified either globally, in Asia, in Southeast Asia region or in Vietnam, and neglected zoonoses transmitted between humans and vertebrate animals.

Three types of questionnaires were developed for three different groups of respondents. Clinical-based respondents in animal health and human health (Survey BM01) were asked for: (1) any suspected or treated case(s) of zoonotic diseases during last five years; (2) an estimation of the average number of cases for one year; (3) indication of laboratory confirmation or suspected cases. If a laboratory confirmation was verified, the number of cases of each specific zoonotic disease in the last five years was investigated. Laboratory-based respondents in animal health and human health (Survey BM02) were asked about the number of cases/samples for zoonosis testing, the number of positive cases in every year during the last five years. Respondents who conducted research on parasitic pathogens/diseases in animal health and human health (Survey BM03) were interviewed on the number of cases/samples and the number of positives recorded in the last five-year period. The pre-tested questionnaires were then designed as a web-based online survey, using Kobo-toolbox [ 13 ].

2.4. Survey follow-up activities

The initial data analysis was undertaken between October and November 2020. A team consisting of a specialist in qualitative research from Oxford University Clinical Research Unit (OUCRU) in Ho Chi Minh city and other members from the Food and Agriculture Organization (FAO), Department of Animal Health (DAH), NIHE, PI–HCMC, and USAID followed up in-depth interviews to the participants who provided information on the frequency of detection and identification of zoonotic pathogens/diseases in the questionnaires (BM01, BM02, or BM03). Other respondents not participating in the online survey received a shorter version of the survey asking for the number of times of detection of any zoonosis.

2.5. Literature review

A literature review was implemented from December 2020 to February 2021 by searching for publications related to zoonotic diseases in Vietnam from 2010 to 2020 through PubMed.

2.6. Data management and analysis

The Kobo-toolbox application automatically recorded the online response data. Besides, the answers of the respondents from the follow-up activities and those who completed the short form of the survey were also entered in the application. The data were downloaded into MS-Excel, then were transferred to MS-Access. The frequency of pathogens/diseases was estimated from the total number of responses. The literature review information was summarized in MS-Excel tables. We assigned a score for each pathogen/disease according to the number of cases reported in the literatures as: 0 = no report; + = 1–3 cases; ++ = 4–10 cases; and +++≥10 cases. To select pathogens/diseases for prioritization, we determined the relative significance of those identified by combining information from the online survey and the literature review into an index based on history of detection (frequency, host, identification methods) weighted by the expected public health impact of the outbreaks. The weighted index ranged from 0, +, ++ and +++. Diseases/pathogens with weighted index ++ and +++ were considered as a significance for future detection, prevention, and control in addition to the current prioritized zoonotic diseases by the government.

2.7. Ethical considerations

To protect the confidentiality of the respondents in the on-line survey, and those who took part in follow-up activities, it was stated that no information linked to respondents would be publicized without their consent and that participation in the survey was voluntary.

We shortlisted 397 entities to participate in the online survey. Of these, 36 were unable to connect to internet, or did not receive a letter of invitation. An additional 153 did not participate, citing their busy schedules or no information to share.

A total of 209 entities responded to our questionnaires, of which 61 were from animal health sector and 148 were from human health sector ( Fig. 1 ). The response rate by organisations was 57.9% (209/361). The total respondents in this survey were 332. The proportion of clinical-based respondents was higher than laboratory-based respondents in both human health (138/237, 58.2%) and animal health (66/95, 69.4%) professionals ( Table 1 ).

Number of respondents to the online survey by province, July–November 2020, Vietnam.

Online survey by sector, entity and response, linked to animal or human health and clinical or laboratory/research respondents, July–November 2020, Vietnam.

The location of the 209 entities responded was disaggregated by provinces. Of 63 provinces, 61 were represented, with only Kon Tum and Bac Lieu provinces abstaining. The location of responses was summarized based on the four epidemiological regions of human health sector, linked to the seven regional animal health offices ( Table 2 ).

Responses to the online survey by epidemiological regions, regional animal health offices and provinces, July–November 2020, Vietnam.

Regarding the current five prioritized zoonotic diseases, for highly pathogenic avian influenza (HPAI), there were 127 human cases of H5N1 virus infection during 2003–2014, of which 63 were fatal. However, there has been not any case reported since 2015, although the H5 subtype viruses have been frequently detected in domestic bird population. According to a report of DAH, 84 communes in 28 provinces notified outbreaks of HPAI and 255,209 poultry were culled in 2020. Two subtypes of HPAI strains, including H5N1 and H5N6, were confirmed in these outbreaks.

Rabies was the most dangerous disease in Vietnam causing the highest number of deaths compared to other infectious diseases in humans. There was an average of 88 human cases and 398,545 dog-bite victims per year during 2012–2016, and fewer 76 fatal cases but higher 510,913 dog-bite cases per year in the period from 2017 to 2021. More human cases were found in the northern, central, and highland regions. Between 2017 and 2021, 2068 dog head samples taken from 35 provinces were tested, of which 227 (10.98%) provided positive results for rabies.

Annual incidence rate of Leptospira was estimated at 0.05–0.25 per 100,000 during 2002–2011, including 369 laboratory confirmed cases with no deaths. Of the 25 serogroups circulating in Vietnam, serogroups Hebdomadis, Pomona, Saxkoebing, and Panama were the most common. From 2014 to 2016, 5 provinces reported a thousand pigs getting leptospirosis. However, Leptospira has not been detected in humans as well as in animals since 2017.

From 2006 to 2011, there were 413 patients of anthrax including 3 fatal cases. During 2012–2022, a total of 266 human cases were confirmed in six mountainous provinces in the northwest region, with no deaths. Between 2020 and 2021, 7 livestock were infected by anthrax in the northwest region.

About 55 to 173 people were hospitalized per year because of S. suis type 2 during the period from 2011 to 2018. The morbidity rate was highest in 2017 with 0.19 cases per 100,000. In domestic pigs, the infection rate varied from 0% to 85.19% during 2011–2019.

The online survey results indicated that six bacteria were detected in both humans and animals, which are Campylobacter, Clostridium, E. coli , Methicillin-resistant Staphylococcus aureus (MRSA), Salmonella, and Vibrio parahemoliticus . However, cat-scratch disease, erysipelas, and pasteurellosis were found only in animals. In contrast, melioidosis and V. cholera were diagnosed only in humans. There were very few reports of brucellosis, Mycobacterium avium , listeriosis, and rat-bite fever. In addition, reports of cases of Acrobacter, Lyme disease, chlamydiosis, glanders, M. bovis and plague were not confirmed by the laboratory testing. Furthermore, Q-fever was reported by 8 laboratory-based respondents, but only three cases had laboratory confirmation.

Four fungi and rickettsia diseases were recorded in both humans and animals, which are aspergillosis, ringworm, typhus, and ehrlichiosis. Five fungal diseases were detected only in humans including cryptococcosis, histoplasmosis, Malassezia infection, penicilliosis, and sporotrichosis.

Twelve zoonoses caused by protozoa and helminths were found in both humans (as larva migrans) and in animals (as adult worms), which are balantidiasis, cryptosporidiosis, giardiasis, toxoplasmosis, fascioliasis, clonorchiasis, dicrocoeliasis, paragonimiasis, cysticercosis, Asian taeniasis, trichostrongyliasis, and trichuriasis. Whereas six diseases were detected only in animals including diphyllobothriasis, raillietiniasis, beef tapeworm disease, ascariasis, ancylostomiasis, and oesophagostomiasis. Both dracunculiasis and dirofilariasis were detected only in humans.

Four viruses were reported in both humans and animals including HPAI, rabies, Japanese encephalitis B, and hepatitis E. However, diseases caused by the H1N1 subtype virus and zika virus were reported in humans only. Additionally, the online survey respondents reported human cases of herpes B and SARS. In contrast, there were no reports of Newcastle disease or foot and mouth disease in humans, even they are the diseases transmissible to humans. Some reports of chikungunya, Nipah virus in bats, hantavirus, and coronaviruses were also recorded in this online survey.

In total, we reviewed 107 publications for zoonoses in Vietnam during 2010–2020 ( Table 3 ). Of the original 112 zoonotic pathogens/diseases from the literature review, we identified 75 to be recorded from the online survey, including 22 bacterial, 2 rickettsia, 4 fungal, 38 parasitic, and 9 viral zoonoses. Furthermore, our study illustrated that 26 zoonoses achieved 1 to 3 publications, 19 had 4 to 10 publications, and 11 were found with more than 10 publications.

Research published between 2010 and February 2020 linked to zoonoses reported in the online survey, December 2020–February 2021, Vietnam.

In addition to the original five priority zoonoses, this study identified 24 additional zoonoses commonly detected in Vietnam during last 10 years ( Table 4 ). These findings can benefit from investigation and response based on their relative significance in terms of One Health application ( Table 5 ).

Frequency of common zoonoses reported by online survey and literature review, Vietnam, 2020–2021.

Proposed targeted 24 zoonoses from online survey and literature review, July 2020–January 2021, Vietnam.

4. Discussion and conclusions

The objective of this online survey was to assess the frequency of circulating zoonotic pathogens/diseases in Vietnam that could be targeted for multisectoral collaboration and cooperation following One Health approach. A previous attempt to prioritize zoonoses in Vietnam conducted in 2015 provided a list of 12 zoonotic diseases (5). In this study, of the 75 reported zoonotic diseases, we identified 24 additional zoonoses commonly detected in Vietnam during last decade in addition to the five current prioritized zoonoses.

Several other countries have conducted similar studies. We used a common methodology of generating lists of pathogens/diseases to be prioritized based on expert consultation and review of literature and then determining their significance based on disease frequencies in the population [ [14] , [15] , [16] , [17] , [18] , [19] , [20] ]. Prioritization criteria commonly include measures of disease burden or frequency such as prevalence or incidence [ 19 , 20 ]. However, if incidence or prevalence data are not readily available, especially in low-income countries, other proxy measures have been used such as epidemic scales [ 14 ]. Our study generated a measure of frequency that was used as one criterion for prioritization. The list of common zoonotic diseases in Vietnam was similar to other countries. For instance, rabies, influenza, and brucellosis were commonly included in the list of priority zoonoses in Asia [ 14 , 17 ], and Africa [ 16 , 18 , 20 ].

Our analysis of the online survey identified a difference between the responses of the clinical and the laboratory groups. While the laboratory analysis confirmed the prevalence of a pathogen/disease with fewer positive cases, the clinical diagnosis provided broader data on suspected cases that can support a basis for laboratory diagnosis. To maximize the probability of identifying the presence of zoonotic pathogens/diseases in this study, we combined both laboratory and clinical examination results into the level of cases observed.

The survey was conducted during COVID-19 pandemic in Vietnam which may resulted in limited number of responses. However, the online survey data received responses from provincial agencies in every region. We could estimate frequency of zoonoses based on the number of responses, but we were unable to estimate the total number of populations to calculate the incidence. We circulated the invitation and the surveys to the entities with no control over the responders who may not be aware of the disease situation or only aware of some pathogens. A review of hospital and laboratory records for zoonoses can help validate our findings.

Additional surveillance efforts on the 24 identified zoonotic diseases in this study can shed lights on the roles of animal reservoir and their public health impact. A One Health multisectoral response to the detection of these zoonoses can also reduce the burden of the zoonotic diseases in Vietnam.

This work was conducted with financial support from the United States Agency for International Development (USAID) grant number GHA-G-00-06-00001 through the Emergency Centre for Transboundary Animal Diseases (ECTAD), Food and Agriculture Organization of the United Nations (FAO), Country Office for Vietnam.

CRediT authorship contribution statement

Long Pham-Thanh: Conceptualization, Methodology, Data curation, Validation, Writing – original draft. Thu Van Nhu: Conceptualization, Methodology, Investigation, Data curation, Validation, Writing – review & editing. Trung Vinh Nguyen: Methodology, Software, Data curation, Visualization. Khang Vuong Tran: Data curation, Investigation, Validation. Khanh Cong Nguyen: Conceptualization, Methodology, Data curation, Investigation. Huong Thi Nguyen: Conceptualization, Methodology. Hoa Thi Ngo: Conceptualization, Methodology, Investigation, Validation. Pawin Padungtod: Conceptualization, Methodology, Supervision, Writing – review & editing.

Declaration of Competing Interest

The authors declare no Conflicts of Interests.

Acknowledgements

We appreciate the strong commitment and support from DAH, GDPM, NIHE and OUCRU staff members for supporting the development of the questionnaire and collecting and analysing data. We thank Dorothy L Southern, the Manuscript and Publication Editor of FAO, for his critical review of this manuscript.