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Integrating research and surveillance to mitigate zoonotic disease risk in indigenous communities: Insights from an expert group meeting in Amazonas, Peru

  • Jocelyn G. Pérez ,

    Contributed equally to this work with: Jocelyn G. Pérez, Rita Ribeiro, Laura Bergner, Nardus Mollentze

    Roles Conceptualization, Formal analysis, Funding acquisition, Investigation, Project administration, Visualization, Writing – original draft, Writing – review & editing

    jocelyn.perezlazo@glasgow.ac.uk

    Affiliations School of Biodiversity, One Health and Veterinary Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, United Kingdom, Medical Research Council – University of Glasgow Centre for Virus Research, Glasgow, United Kingdom

  • Rita Ribeiro ,

    Contributed equally to this work with: Jocelyn G. Pérez, Rita Ribeiro, Laura Bergner, Nardus Mollentze

    Roles Conceptualization, Formal analysis, Funding acquisition, Investigation, Project administration, Visualization, Writing – original draft, Writing – review & editing

    Affiliations School of Biodiversity, One Health and Veterinary Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, United Kingdom, School of Veterinary Medicine & Biosciences, SRUC, Craibstone, Aberdeen, United Kingdom

  • Laura Bergner ,

    Contributed equally to this work with: Jocelyn G. Pérez, Rita Ribeiro, Laura Bergner, Nardus Mollentze

    Roles Conceptualization, Formal analysis, Funding acquisition, Investigation, Project administration, Visualization, Writing – original draft, Writing – review & editing

    Affiliations School of Biodiversity, One Health and Veterinary Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, United Kingdom, Medical Research Council – University of Glasgow Centre for Virus Research, Glasgow, United Kingdom

  • Nardus Mollentze ,

    Contributed equally to this work with: Jocelyn G. Pérez, Rita Ribeiro, Laura Bergner, Nardus Mollentze

    Roles Conceptualization, Formal analysis, Investigation, Visualization, Writing – original draft, Writing – review & editing

    Affiliations School of Biodiversity, One Health and Veterinary Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, United Kingdom, Medical Research Council – University of Glasgow Centre for Virus Research, Glasgow, United Kingdom

  • Pershing Bustamante-Chauca,

    Roles Conceptualization, Resources, Writing – review & editing

    Affiliation Dirección Regional de Salud de Amazonas, Chachapoyas, Perú

  • Lizandro Gonzales,

    Roles Conceptualization, Resources, Writing – review & editing

    Affiliation Laboratorio Referencial Regional de Salud Pública Amazonas, Dirección Regional de Salud de Amazonas, Chachapoyas, Perú

  • Roberto C. Rivera,

    Roles Conceptualization, Resources, Writing – review & editing

    Affiliation Red de Salud Condorcanqui, Santa María de Nieva, Amazonas, Perú

  • Miguel Bernal,

    Roles Conceptualization, Writing – review & editing

    Affiliation Red de Salud Condorcanqui, Santa María de Nieva, Amazonas, Perú

  • Victor L. Osorio,

    Roles Conceptualization, Writing – review & editing

    Affiliation Red de Salud Condorcanqui, Santa María de Nieva, Amazonas, Perú

  • Sergio Recuenco,

    Roles Conceptualization, Writing – review & editing

    Affiliation Departamento de Medicina Preventiva y Salud Pública, Facultad de Medicina, Universidad Nacional Mayor de San Marcos, Lima, Perú

  • Bruno M. Ghersi,

    Roles Conceptualization, Writing – review & editing

    Affiliation Tufts University, Medford, Massachusetts, United States of America

  • Paulo Colchao-Claux,

    Roles Conceptualization, Writing – review & editing

    Affiliation Wildlife Conservation Society, Lima, Perú

  • Luis Soldán-Villarreal,

    Roles Conceptualization, Writing – review & editing

    Affiliation Yunkawasi, Lima, Perú

  • William Bardales,

    Roles Conceptualization, Writing – review & editing

    Affiliation Instituto de Investigación en Ganadería y Biotecnología, Facultad de Ingeniería Zootecnista, Agronegocios y Biotecnología, Universidad Nacional Toribio Rodríguez de Mendoza de Amazonas, Chachapoyas, Perú

  • Jesús Rodríguez-Chávez,

    Roles Conceptualization, Writing – review & editing

    Affiliation Servicio Nacional de Sanidad Agraria, Cajamarca, Perú

  • Jorge L. Maicelo Quintana,

    Roles Writing – review & editing

    Affiliation Instituto de Investigación para el Desarrollo Sustentable de Ceja de Selva, Universidad Nacional Toribio Rodríguez de Mendoza, Chachapoyas, Amazonas, Perú

  • Carlos Tello,

    Roles Writing – review & editing

    Affiliation Yunkawasi, Lima, Perú

  • Rafael Tapia-Limonchi,

    Roles Conceptualization, Writing – original draft, Writing – review & editing

    Affiliations Instituto de Investigación en Enfermedades Tropicales, Universidad Nacional Toribio Rodríguez de Mendoza de Amazonas, Chachapoyas, Perú, Facultad de Medicina, Universidad Nacional Toribio Rodríguez de Mendoza de Amazonas, Chachapoyas, Perú

  • Daniel G. Streicker ,

    Roles Conceptualization, Funding acquisition, Writing – original draft, Writing – review & editing

    ‡ DGS and SMC also contributed equally to this work.

    Affiliations School of Biodiversity, One Health and Veterinary Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, United Kingdom, Medical Research Council – University of Glasgow Centre for Virus Research, Glasgow, United Kingdom

  •  [ ... ],
  • Stella M. Chenet

    Roles Conceptualization, Project administration, Writing – original draft, Writing – review & editing

    ‡ DGS and SMC also contributed equally to this work.

    Affiliations Instituto de Investigación en Enfermedades Tropicales, Universidad Nacional Toribio Rodríguez de Mendoza de Amazonas, Chachapoyas, Perú, Facultad de Medicina, Universidad Nacional Toribio Rodríguez de Mendoza de Amazonas, Chachapoyas, Perú

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Introduction

Diseases transmitted from animals to humans disproportionately impact populations living in poverty in tropical and subtropical regions but remain overlooked in research and policy [1]. Given the complex, multi-species biology of these pathogens, neglected zoonotic diseases (NZDs) require a One Health perspective for surveillance and control [2,3]. Monitoring and managing NZDs is particularly challenging in remote indigenous communities, which often suffer regionally disproportionate health disparities [4,5]. Importantly, and in contrast to voluntary isolated or uncontacted communities, these communities are exposed to health threats from the wider society in which they live. Remote indigenous communities may also experience relatively high levels of contact with wildlife through housing practices and animal consumption, including groups that harbor zoonotic pathogens such as bats and rodents [69]. Geographical isolation and poverty further limit access to disease prevention and post-exposure healthcare [10,11]. Lack of access to safe water and sanitation may further contribute to NZD spread in these communities [10,11].

In May 2023 we held a scoping meeting at Universidad Nacional Toribio Rodríguez de Mendoza in Chachapoyas (Amazonas, Peru). Participants ranged from Peruvian governmental bodies responsible for human and animal health, academics studying human and animal health and ecology, and non-governmental organization concerned with wildlife health and conservation, and sustainable development of communities. The epidemiological situation and disease control measures were presented by health authorities, followed up by a round-table discussion to identify key challenges, and research priorities on NZDs affecting indigenous communities. We focused on the Condorcanqui province in the administrative region of Amazonas, Peru (Fig 1A), which typifies the challenges to NZD management outlined above.

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Fig 1. Location of indigenous communities in Condorcanqui and health accessibility.

(A) Amazonas department is bordered by a dashed black line, and Condorcanqui is bordered by a continuous black line. (B) A zoomed-in view showing the districts in Amazonas, Condorcanqui, and the locations of the indigenous communities. Locations of indigenous communities derived from [12]. Biome definitions are based on data from [13,14]. Administrative boundary definitions derived from GADM (https://gadm.org/license.html) and the Peruvian National Open Data Platform (https://www.datosabiertos.gob.pe/dataset/limites-departamentales). (C) Mean travel time (hours) to each healthcare level and population size in each province, highlighting poor accessibility to almost all healthcare levels in Condorcanqui, based on [15,16]. The categories of health care centers are: Level I-1 (health posts with health workers not including physicians), Level I-2 (health posts with health workers including physicians), Level I-3 (health centers), Level I-4 (health centers that have ward beds), Level II-1/2 (hospital and clinics).

https://doi.org/10.1371/journal.pntd.0014564.g001

This high-jungle region contains many remote communities of native Amazonian ethnic groups such as Awajún or Wampis, which have distinctive native languages, cultural practices and beliefs. Condorcanqui is also a hotspot of NZDs in Latin America, with a recurring history of human rabies outbreaks transmitted by bats [7] and continuous risks of yellow fever and other infectious diseases (see below). After reviewing the epidemiological situation in the broader region, we identified current barriers to policy change and research. We next developed a set of recommendations for studying and addressing healthcare inequalities that will be relevant to improve NZD surveillance and response in remote indigenous communities more broadly.

Epidemiological situation

Condorcanqui contains 69% of the indigenous population of Amazonas (total indigenous population: 72,436) and 68% (234/344) of its indigenous communities (Fig 1B) [12]. Many communities are reachable only by river, limiting access to healthcare (Fig 1C).

Data on disease prevalence—where available—are based mostly on passive surveillance or active surveillance following perceived epidemiological shifts [17].

Research studies quantifying prevalence in this region are rare (particularly in indigenous communities), focused on single diseases, and limited to relatively short time periods [18,19]. Meeting participants identified nine infectious and non-infectious diseases of major concern to the region, most of which were neglected tropical diseases (NTDs) (Fig 2). Three of these (rabies, leishmaniasis, leptospirosis) are primarily zoonotic, and two are primarily human-transmitted but also occur in zoonotic/sylvatic cycles (yellow fever, dengue). Two additional infectious diseases (HIV and malaria) are not NTDs but exert considerable direct health burden and have indirect effects on the detection and clinical outcomes of rarer zoonoses [2022].

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Fig 2. Prevalence of NTDs and other major infectious diseases per district in Amazonas, Peru, from 2000 to 2023.

Diseases were grouped by prevalence levels: high (A), medium (B) and low (C). Prevalence is expressed as a percentage of cases per total population in 2017, per district [23]. Condorcanqui is bordered in black. Surveillance data supplied by the Centro Nacional de Epidemiología Prevención y Control de Enfermedades - Ministerio de Salud (CDC-MINSA), Peru. Administrative boundary definitions derived from the Peruvian National Open Data Platform (https://www.datosabiertos.gob.pe/dataset/limites-departamentales).

https://doi.org/10.1371/journal.pntd.0014564.g002

Compared to other areas of Amazonas, most of these diseases are more common in Condorcanqui (Fig 2). Furthermore, it is notable that all NTDs highlighted are relatively well-known; other NTDs or NZDs might be present but not subjected to similar diagnostic efforts.

Among the focal NTDs, dengue, snakebite envenoming and leishmaniasis showed constant incidence over time while rabies and yellow fever were sporadic threats (Fig 3).

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Fig 3. Incidence of NTDs and other major infectious diseases in Amazonas, Peru, from 2000 to 2023.

To improve readability, diseases were grouped by overall temporal trend. Incidence is expressed as the number of cases per 100,000 people in 2017.

https://doi.org/10.1371/journal.pntd.0014564.g003

The incidence of malaria, HIV, leptospirosis and loxoscelism increased over time, with malaria and HIV exhibiting particularly large increases. It is unclear whether increased incidence reflects improvements in awareness and detection of these diseases or changes in epidemiology (e.g., malaria driven by climate factors [18]).

Condorcanqui is a high-risk area for the emergence and spread of NTDs considering the different factors (e.g., limited accessibility of healthcare, impacts of climate and land use change, poor quality housing and sanitation, cultural beliefs, human activities) that contribute to the observed prevalence of NTDs.

Challenges and strategies

The challenges to research, diagnostics and treatment of NZDs within indigenous communities identified by our expert panel, along with strategies to resolve them, span both broad-scale policy issues and challenges specific to the research required to inform policy (Table 1). We use Amazonas as an example, but many concepts will be relevant beyond this region.

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Table 1. Policy and research challenges identified and solutions proposed.

https://doi.org/10.1371/journal.pntd.0014564.t001

Policy challenges

There are strategic lines of actions from PAHO and WHO that provide valuable guidance for national health authorities to establish policies to address the health threats at the human-animal-environment interface [2]. However, the following policy challenges are currently faced by the indigenous communities in Peru. Novel zoonotic outbreaks are increasing globally. As occurred during the COVID-19 pandemic, mitigating actions are commonly taken after disease has emerged and spread in humans. To minimize the impact of future pandemics, the implementation of both primary prevention actions (e.g., pathogen discovery and monitoring) and preparedness actions seeking to arrest early transmission chains (e.g., vaccine development) are necessary.

Surveillance underpins both primary prevention and preparedness, enabling actions aiming to prevent spillover (e.g., managing wildlife trade and land use change), rapidly identify the identity and origins of novel human pathogens, and develop diagnostics, therapeutics and vaccines. However, zoonotic surveillance systems—and the primary healthcare systems required to respond to zoonotic threats at the point of emergence—face structural challenges related to sustainability and allocation of funding. A timely and effective zoonotic disease surveillance system can help public health decision makers to set priorities and plan interventions. However, a policy challenge in Peru and elsewhere is the compartmentalization of diagnostic systems for veterinary and human cases of the same diseases. We suggest integrating data across monitoring agencies in a unified resource. Digital platforms of zoonotic disease monitoring at the regional or national level would be valuable for response and preparedness plans if the ethical and legal constraints of data sharing are adequately addressed. Ideally, this approach should integrate human, animal and environmental health data (i.e., a One Health approach). Data sharing in an open platform is also needed to address concerns around the introduction of zoonoses across international borders. Current efforts in Peru such as the avian influenza surveillance system launched in 2023, which integrates data from agencies responsible for agricultural health, agrarian development, wildlife and forestry, and protected areas (Servicio Nacional de Sanidad Agraria [SENASA], Programa de Desarrollo Productivo Agrario Rural [AGRO RURAL], Servicio Nacional Forestal y de Fauna Silvestre [SERFOR], and Servicio Nacional de Áreas Naturales Protegidas por el Estado [SERNANP]) demonstrates the feasibility and value of such an approach [24].

An important challenge in controlling NZDs in remote communities is the lack of access to high-quality health services. For instance, hospital services are concentrated in urban areas of Amazonas (Fig 1C), while people in rural areas lack timely access to healthcare, resulting in limited availability of diagnosis, treatment options, and patient follow-up. Such disparities are further exacerbated by the fragmented Peruvian healthcare system since access to health services depends on the insurance scheme [27]. The lack of adequate and opportune health care in Condorcanqui communities was evident during the COVID-19 pandemic, with a higher incidence rate in indigenous communities compared to other areas in the region [5]. Strengthening primary health care (infrastructure, internet, multidisciplinary teams) is therefore urgently needed. Similarly, there is limited access to veterinary services; more veterinarians are needed locally to improve animal health and to monitor disease emergence.

Localized capacity was deemed critical to address recurring issues of delayed diagnosis and underreporting. Although diagnostic tests for some viral pathogens (e.g., Dengue, COVID-19, Monkeypox, Influenza A and B, Chikungunya, Zika) are currently carried out by local reference laboratories, these laboratories are located in larger cities in Amazonas (Chachapoyas, Bagua). Alternatively, samples may be shipped to the National Institute of Health (Instituto Nacional de Salud; INS) in Lima for confirmatory testing, delaying diagnosis. This could be addressed through strengthening capacity in local reference and research laboratories—for instance, cooperation between these entities improved understanding of risk factors for infection and outcome during the COVID-19 pandemic in Amazonas [19].

Both detection and treatment of NZDs could be improved by re-evaluating investment priorities, ensuring that surveillance and healthcare spending match the risk of high-impact zoonoses and the exposure risk of communities (Figs 1 and 2). The current health system prioritizes a few high-burden diseases (e.g., malaria, dengue). While it is undoubtedly important to direct resources towards these diseases, investment in sustained surveillance, diagnostics and treatment of NZDs could help alleviate the burden of known pathogens (e.g., rabies) and allow identification of as yet unknown pathogens before they become widespread threats [28].

Research challenges

Determining community needs is necessary to plan research activities that could meet their health agenda. Community health workers identified under-reporting of infectious diseases as a key regional challenge. In Peru more generally, it is necessary that all facilities access the internet and have electronic medical records to ensure up-to-date consensus metadata for monitoring health changes in indigenous populations [27]. The disease prevalence data presented here were collected passively, providing relatively limited insight into the true disease burden on indigenous populations. Enhanced active surveillance, integrating animal and human data including syndromic cases, could help the early detection of spillover events or disease reemergence for developing control strategies. This is particularly important in light of the presence of febrile illnesses such as malaria and chronic immunosuppressive diseases such as HIV in geographically isolated regions of Amazonas (Fig 2), which may mask or exacerbate the impact of NZDs, respectively. Relatively common diseases in the region that initially present with nonspecific febrile illness (malaria, dengue, leptospirosis, yellow fever; Fig 2) may mask the occurrence of other zoonoses given limited diagnostic capacity in the region. The high prevalence of HIV in this region, combined with a lack of specialized care required to prevent progression to AIDS, may further exacerbate the burden of zoonotic NTDs [20].

The remoteness of indigenous communities creates challenges for research attempting to measure the true burden of NTDs and their underlying causes (Table 1, Box 1). We suggest better coordination between academia, external partner institutions and governmental surveillance efforts, to build local capacity and reduce the high costs associated with reaching affected communities. While the importance of research coordination and expanding local capacity as part of global health research programmes is increasingly recognized [29], sustained support at the governmental level is also required. This could be accomplished via networking events and meetings between researchers and the government officials and developing joint training or education programmes to obtain a higher degree or specialize in specific public health topics.

A recurring theme in our discussions was the reluctance of communities to engage with research. Some of these challenges stem from cultural beliefs around the causes of zoonotic diseases or suspicions of outsiders (Table 1). In addition to coordinating visits as suggested above, wider sharing of already collected samples—subject to obtaining informed consent for future use of samples—could help minimize participation fatigue. Further, community engagement throughout the lifespan of a project and beyond, promoting the direct involvement of community members in research activities, and clear communication of results would help to build trust. Crucially, such activities would need explicit support from research funders, and—given the clear ethical and sustainability implications—should be viewed as an integral requirement of research activities involving historically neglected communities.

Box 1. Challenges to mitigate the risk of a widespread zoonosis in indigenous communities—Rabies as a case study

In Peru, 26.1% of human rabies cases transmitted by vampire bats from 2000 to June 2024 have been reported in Amazonas and 100% of these outbreaks occurred in indigenous communities (Fig 4). During this period, there were 3576 reported bat bite cases in this region, disproportionately affecting children 0–11 years old (Fig 4). Challenges to prevent human rabies in remote Amazonian communities include:

  • Chronic exposure to bats due to open-air dwellings, infrequent use of mosquito netting to prevent bat bites, and shifting of bat blood feeding behavior from wildlife to humans or livestock [7].
  • Diagnostic results can be delayed due to the long transportation route of samples to the reference laboratory in Bagua and later confirmation at INS-Lima.
  • Pre-exposure vaccination campaigns have been implemented in high risk areas [17], but both coverage and duration of immunity is uncertain due to the lack of follow-up antibody titration.
  • Reluctance to vaccination due to local beliefs regarding the vaccine or disease etiology is also challenging for health workers, who sometimes face hostility [7]. Educational campaigns would be beneficial in explaining the value of preventing exposure to bat bites and building trust in vaccination.

The Regional Directorate of Health (DIRESA) in Amazonas included human bat-bites as a reportable incident in their surveillance system in 2000, the notification improved progressively and more recent data shows that a considerable problem was missed entirely because there was not a system in place to detect it. This data could help to know the frequency of communities that experience bat bites and identify ecological factors that drive bite and subsequently rabies risk, information that could ultimately guide the distribution of resources, including human vaccines. Joint efforts between health authorities and researchers may aid to fill the gaps of the knowledge of rabies in humans and animals contributing to estimate human local risk [30], and the development of strategies to control rabies outbreaks in livestock and bat populations (e.g., through vaccination [31]).

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Fig 4. Challenges and strategies to control rabies in indigenous communities in Amazonas.

Figures show the bat bite incidence from 2000 to June 2024 in Amazonas, the number of cases by age group, and a population pyramid of the five provinces with reported bat bites (Bagua, Bongara, Condorcanqui, Rodriguez de Mendoza and Utcubamba). Map shows the confirmed human rabies cases in Peru per district from 2000 to June 2024, Amazonas is bordered in black. Surveillance data supplied by the CDC-MINSA and DIRESA-Amazonas. Population data derived from [32]. Administrative boundary definitions derived from GADM (https://gadm.org/license.html).

https://doi.org/10.1371/journal.pntd.0014564.g004

Conclusions

Remote indigenous communities are particularly vulnerable to NZDs due to both high human-wildlife contact and lack of access to healthcare. Many communities also face compounding challenges including climate change, incursion by non-indigenous people onto indigenous lands, and development policies that prioritize resource extraction [33]. While development might lead to some positive outcomes (e.g., increased access to healthcare), extractive development models involving land degradation can facilitate disease spread, resulting in higher local disease burdens [33].

In addition to the key policy and research strategies outlined in Table 1, we stress the importance of a One Health approach in both research studies and proposed solutions [3,7]. This would have mutual benefits for researchers, healthcare officials and affected communities. For instance, a One Health approach to managing NZDs might include (1) determining potential pathways of wildlife-human contact, (2) coordinated surveillance in animals and humans, (3) community campaigns to enhance awareness of potential routes of exposure, (4) developing strategies to minimize exposure risks, and (5) building local research capacity to ensure research continuity. Across all stages, seeking the input of communities themselves (i.e., co-development) is critical to ensure proposed research agendas and solutions are embraced.

In summary, our meeting has brought together experts from diverse fields to establish a new network aiming to coordinate research into NZDs in remote indigenous communities in the Amazonas region. Here, we provide guidance to researchers to engage in meaningful collaborations with indigenous communities. Forming research networks to work collaboratively on topics such as NZDs can benefit both individual participants and the wider research community. Developments since this meeting include joint research grant applications, establishing collaborative projects, international online seminars for government officials, and initial planning towards a follow-up meeting in 2026.

Acknowledgments

We thank Llunely and Evely Güimac for their administrative support in the organization of the meeting.

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