Evidence was synthesised in form of a table and thematic analysis. Of all records, 78 papers were selected for inclusion. 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. 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 ]. Humanitarian emergencies may result in the displacement of human and livestock populations. 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. 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 ].
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. 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. Papers were only considered if the full text was available in English, thereby introducing a potential publication bias. 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.
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. 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. 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. Our review shows that there is a lack of primary research data. Case study findings through primary research were discussed in 20 papers, while 3 were program outcome reports. No publication focused on the specific risk of zoonoses related to livestock movement during displacement. Papers focusing on Pakistan primarily discuss Afghan refugee health, which remains one of the largest refugee populations in the world.
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. 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. 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. 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 ].
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.
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 ].
Meanwhile, the lack of vaccinations and surveillance led to outbreaks of infectious diseases among displaced and returned populations in Pakistan after the floods in , including the zoonoses Crimean-Congo haemorrhagic fever [ 62 ]. 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 ]. 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 ]. 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 ].
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.
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 ]. 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 ].
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, 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 ].
Several species of mammals—for example, deer 31 , rodents 32 , civets 33 , and fur mammals—are bred under a wide range of production systems worldwide, and provide income and protein. The legal and technical framework for these production systems is often poor 33 , 34 and published information on the biology, production and health of these non-conventional captive species is scarce, particularly in low-income countries Consequently, health-monitoring programs in wildlife farms are seldom implemented, despite intensive farming conditions and low genetic diversity 34 , These factors expose farmed wildlife species to stress and immunosuppression 13 , and predispose captive wild animal populations to disease emergence.
This is illustrated by the circulation of avian influenza strains in ostrich Struthio camelus farms in South Africa 37 , the occurrence of repeated rabies outbreaks in ranched kudu Tragelaphus strepsiceros populations in Namibia 38 , and the recent detection of SARS-CoV-2 circulation in mink Neovison vison farms in the Netherlands Although there are relatively few domesticated species, livestock and companion animals have interfaces with both wildlife and people, and therefore have an important role in the complex pathways leading to EZDs.
Intensive livestock farming is increasing worldwide, encouraged by market demands including urbanization and expanding global populations which have changed the way in which food is produced and supplied Concurrent anthropogenic factors, such as changes in land-use, provide new wildlife-domestic species interfaces by creating shared ecologies, with opportunity for spillover and amplification of new EZDs Nipah virus emergence in Malaysia in is one such example Dual—agriculture of intensive pig farming with mango plantations created a bat-pig interface that allowed spillover of Nipah virus from bats feeding on the fruit trees to pigs housed below.
Repeated spillover events from bats resulted in prolonged circulation of the virus in pigs, increasing the opportunity for spillover to people This illustrates that large, dynamic populations of a single livestock species can increase the risk of EZDs in people by enabling persistence of a potential pathogen at the livestock-human interface.
Mixing of domestic species can also give rise to EZDs; for example, avian influenza viruses circulate and re-combine in domestic poultry in live-bird markets Examples in which companion animal species have provided an interface for EZDs between wildlife and people include Hendra virus 45 and Chlamydia psittaci These examples illustrate multiple epidemiologic scenarios involving individual, mixed, or large dynamic domestic animal populations that provide an intermediate interface between wildlife and humans.
Our presentation of the different interfaces and potential sources of EZD Figure 1 , demonstrates a recurring theme of intensified anthropogenic factors driven by cultural and socioeconomic interests. The challenges for many of these interfaces include achieving a balance between sustainably managing resources required for human population growth, safeguarding species conservation and biodiversity, securing animal and human health, and respecting animal welfare, when large numbers of species are kept in confined spaces for example, farms and markets.
Such use of animals also gives rise to ethical questions related to animal husbandry. Animals' fundamental interests should not be sacrificed if it were not for weightier human interests. This means that the use of animals is, in some contexts, morally permissible for example, when there is no healthy plant-based alternative to meat , while in other contexts, it is morally problematic for example, when wild animals are traded and consumed as a symbol of wealth.
Less crowded living conditions and respect for biological and behavioral needs of species such as foraging and occupational opportunities will not only improve the animals' wellbeing, but also result in lower stress and therefore lower risk of spillover. Figure 1. Examples of zoonotic diseases that have re- emerged at the animal-human interface.
Transmission pathways include direct contact through handling of living animals wildlife trade, domestic animals , preparation of slaughtered animals for consumption of meat or for traditional medicine uses. Popular reactions to EZD emergence often target the immediate source, rather than underlying drivers.
For example, some have suggested shutting down wildlife markets However, as the drivers of wild-animal meat consumption will persist even after a global health crisis, this is likely to shift the interface elsewhere, out of sight of the regulators 48 — In our opinion, such bans could lead to the emergence of further illegal, unregulated wildlife markets and increased poaching, which would make it impossible to monitor market dynamics, develop surveillance systems, and implement risk mitigation measures.
In addition, the interconnectedness of the different interfaces discussed here is illustrated when wildlife hunting is replaced by livestock farming.
Some farming practices result in deforestation of large areas 51 , and this in turn provides a livestock-wildlife interface and therefore, the potential risk for pathogen spillover from wildlife to livestock.
The interconnectedness and complexity of these ecologies demonstrates the need for that holistic approaches according to the One Health and Planetary Health concepts. Both concepts follow the principle that human, animal, and environmental health cannot be separated, and therefore, to solve health problems, all three health fields and the sustainable use of natural resources have to be considered The focus has been on early detection and rapid response to EZDs in our efforts to control their impacts.
Epidemiologists have many tools that can be integrated—for example, horizon scanning, prioritization, and disease modeling—to provide a greater awareness of the EZDs, as well as provide insights for their control Whilst many improvements using integrated tools can still be made across systems for disease preparedness 54 , we now also call for actions to reduce the rate of EZDs at the human—animal interfaces.
Such actions could include improving hygiene, animal welfare, disease surveillance and safeguarding species conservation through comprehensive and culturally tailored regulations. This will require, in many circumstances, a greater understanding of the sociocultural drivers. For example, the application of social and ethnographic sciences could provide insights about the sociocultural context of wildlife exploitation and trade, and identify potential solutions to promote healthier bushmeat consumption and trade, particularly in tropical forest regions in which livestock farming is poorly developed In addition, wildlife production systems should be supervised and monitored by international bodies in a comparable way as international certification agencies already control forestry exploitation activities to ensure sustainable wood exploitation Similarly, we need regulation of wildlife farms in the same way that mainstream agriculture is regulated to control welfare and biosecurity conditions.
Although wildlife farms represent a minor contribution to national economies, they can have important implications in terms of public health and we have now seen how that affects economies.
Also, alternative protein sources such as aquaculture should be explored; the large diversity of farmed species in aquaculture provides a wide range of opportunities for many countries, while the risk of zoonotic disease emergence is negligible when compared with terrestrial species. Due to the anthropogenic nature of drivers of EZDs increased human population, globalization, climate change changes require government-level strategies that are integrated globally, as well as raising awareness through targeted education of stakeholders including consumers and farmers to improve pathogen surveillance, animal welfare, and reduce environmental impacts of livestock and wildlife farming.
With massive human population growth, globalization of trade and travel, and unsustainable use of natural resources, humanity is in a critical phase in which we head toward irreversible global crises. The more we focus on our short-term anthropocentric model of development, the more our coexistence becomes disconnected from nature.
This has been proven to have serious and devastating consequences for humankind, such as the impact of EZDs, and for the planet As demonstrated here, the challenges associated with risk mitigation and control of EZDs are tightly interlinked with global sustainability. We therefore appeal for more sustainable animal harvesting and production practices, with a stronger focus on health, and not solely productivity. This will not only reduced the risk for EZDs, but also improve environmental balance and animal welfare.
IM and SD conceptualized the manuscript. IM wrote the introduction, the part about wet markets and other live animal markets and designed the figure. VB wrote the part about domestic animals-livestock and pets. FJ wrote the part about intensive wildlife farming. AM provided input on animal ethics. DP provided input on all topics and the discussion. SD wrote the part about wildlife hunting and consumption and the main body of the discussion. All the authors contributed in the discussion and editing of the manuscript.
All the authors have read and approved the manuscript. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Risk factors for human disease emergence. Wildlife trade and global disease emergence. Emerg Infect Dis. The persistent competitive advantage of traditional food retailers in Asia: wet markets' continued dominance in Hong Kong. J Macromarketing. The increased use and exploitation of wildlife can bring humans in closer contact with wild animals, thus increasing the risk of zoonotic disease emergence.
This includes activities such as harvesting of wild animals for meat, hunting and consumption of wildlife for recreation, trading of live animals for recreational use or research, or use of animal parts for decorative, medical or commercial purposes. Utilisation of natural resources owing to urbanisation, changes in land-use pattern and growing industrialisation can also cause destruction and fragmentation of wildlife habitats and increase contact between humans and wildlife.
The report made ten recommendations based on the One Health approach that could aid a coordinated multi-sectoral response to future pandemics. These included:. The document is one of the first to focus on the environmental side of the zoonotic dimension of disease outbreaks during the COVID pandemic.
It underlined the need for strengthening the environmental dimensions of the One Health approach, since this was key to zoonoses risk reduction and control. This is also a crucial element of AMR containment efforts since waste from intensive farms using antimicrobials paves way for AMR determinants for instance, antibiotic residues, resistant bacteria in the environment.
There is an immediate need to invest in in-depth understanding of environmental linkages with zoonotic diseases, monitoring of such diseases in human-dominated environments, investigating how environmental change or degradation is impacting zoonotic disease emergence. We must also begin to re-think our relationship with food, how it is grown and what impacts in can have on us and our environment.
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