Human outbreaks of emerging infectious diseases (EIDs) may be relatively rare compared to widely established diseases, but as the Ebola outbreak in West Africa has demonstrated, they can be catastrophic to societies. They can also be vastly expensive. For example, the 2003 Severe Acute Respiratory Syndrome (SARS) outbreak, which caused fewer than 900 deaths, cost the global economy an estimated US $30 billion to $50 billion.1
Ebola, SARS, and other EID outbreaks have seemingly appeared without warning. An international spread of people and goods, including wildlife trade, may be increasing their frequency and extent, or at least, detection and attention may be increasing. During the Ebola outbreak in West Africa, there was a concurrent (unrelated) outbreak in the Democratic Republic of the Congo (DRC), a case of Marburg virus in Uganda, additional deaths from Middle Eastern Respiratory Syndrome (MERS) in Saudi Arabia, and the highly pathogenic avian influenza H7N9 in China. The world was lucky that SARS was controlled and has not since reappeared in humans, although a recent study has found its causal virus in bats in China.2 The emergence of MERS in 2012 continues to yield new human cases, but the transmission pathway is still not definitively known. The difficulty of anticipating EIDs is a symptom of the public health system’s emphasis on response rather than prediction and prevention. This status quo in public health leaves us unequipped to address emerging disease threats.
Genuine changes in the public health system are needed to boost surveillance efforts and to build capacity to respond to early detection of disease risks through a ‘One Health’ approach. In doing so, innovative investments should be made to ensure environmental, financial, and capacity sustainability. Enhanced understanding of EID risks and mechanisms for detection can also provide benefit and lessons for addressing related threats, such as bioterrorism.
Where to Start: Our Current Public Health Systems
Preventing outbreaks of EIDs, such as Ebola, requires knowledge of what the risks are through routine surveillance that detects new or evolving threats in a timely and actionable way. At present, most public health systems have limited capacity for detecting diseases that are known, but have not yet been seen before in a location. For example, the precise cause of unusual encephalitis cases in humans in 1999 was only identified as West Nile virus after the first detection of its appearance in North America through the investigation of avian die-offs.3 Similarly, despite no prior outbreaks of Ebola in West Africa, a paper published during the current outbreak reported that Ebola virus antibodies had been circulating in humans in Sierra Leone from 2006 to 2008.4 There is an urgent need to collect this type of information systematically and in a timely fashion, and to convey research to government and other public health authorities.
Additionally, undiagnosed illnesses (including viral hemorrhagic fevers) in many parts of the world compromise knowledge on true incidence of disease, as well as potentially novel outbreaks.5 Imprecise or missing diagnoses are largely a result of inadequate screening capacity, taxed healthcare systems, or resource inequity. Infrastructure for detection and diagnosis are critical for identifying and initiating proactive responses to disease risks.6 Boosting screening efforts for known pathogens and identifying causes of undiagnosed illnesses in human populations can be implemented in the current system to more precisely identify current risks to populations on a local level.
At least some level of ongoing surveillance should encompass continued strain analysis to detect pathogen evolution. Research opportunities are not always salvaged during outbreaks in favor of response measures, but could provide crucial information. Public health surveillance can provide samples from infected patients to be available rapidly for whole genome sequencing that can detect specific changes in a virus,7 as well as provide genetic material for vaccine development or other therapeutics.
Future Opportunities for Public Health Systems
More challenging is the detection of zoonotic pathogens in other species before they appear in humans so that outbreak prevention or early detection may occur. Pathogen surveillance of wildlife is not currently routinely conducted as part of government activities, despite over half of known human pathogens originating from animals and approximately three-quarters of recent EIDs stemming from wildlife.8,9 Recent developments in diagnostic technology have enabled sample screening for novel pathogen discovery, and thus expanded public health horizons. However, on-the-ground capacity for the detection and prevention of EIDs has not improved significantly in decades, despite even the global burden of HIV/AIDS, which emerged from non-human primates.10 Screening of wildlife for known and yet undiscovered pathogens would complement human health and veterinary health surveillance activities. The relatively high risk of pathogen transmission from bats, rodents, and non-human primates offers a starting point.11
Efforts from the conservation community provide a platform for implementing wildlife disease surveillance, and also a testament to its potential benefits. For example, the limited knowledge available on the animal source of Ebola has been largely generated by the conservation community through wildlife health assessments and investigations of mortality in wildlife. Ebola has been recognized as causing severe declines in great ape populations—especially the critically endangered wild lowland gorillas—and thus is a threat to conservation of biodiversity, as well as to human populations.12,13 Pathogen surveillance suggests that some bat species are the natural reservoir for the virus, harboring it without signs of disease. Investigations of wild animal carcasses have detected infection and mortality in chimpanzees, gorillas, and duiker antelopes, and evidence from human outbreaks suggests that they have served as brief intermediate hosts for human infection when hunted or handled.14,15,16 The 2014 DRC outbreak and prior Ebola outbreaks elsewhere have also been linked to the hunting or handling of wild animals (with subsequent human to human transmission).
Wildlife may thus provide sentinel value. While Ebola virus outbreaks in humans are typically seemingly sporadic, information generated from recent surveillance studies in Gabon and the Republic of Congo suggest that surveillance for the Ebola virus circulating in wildlife may enable early detection or prevention of outbreaks in humans.17,18 Testing of great ape fecal samples for traces of the virus may provide a cost effective public health surveillance method, while simultaneously providing data that could benefit conservation strategies.19
Such information can yield public health action. To manage and reduce risks from Ebola virus transmission from one species to another (pathogen ‘spillover’), reporting of deceased or sick animal sightings by hunters and foresters can provide important sentinel or early warning benefits for public health and conservation monitoring.20,21 This allows for preventive actions prior to transmission of Ebola to humans. Educating people living in areas where Ebola occurs about how they can avoid the disease from both wildlife and animals can prevent deadly outbreaks. Reducing hunting and other contact with infected non-human primates may especially reduce contact opportunities that can result in human outbreaks.22
From 2009 to 2014, the United States Agency for International Development Emerging Pandemic Threats PREDICT program implemented pathogen surveillance programs in 20 developing nations that were considered ‘hotspots’ for disease emergence. It generated protocols for sampling and screening for 25 viral families at high-risk interfaces (such as hunting and wildlife markets), and worked with local partners to create a system for sharing findings across human health, agriculture, and environment or forestry ministries.23 These approaches can serve as best practices for continuation and for implementation in additional countries.
The benefits seen from the few existing pathogen surveillance programs have been encouraging. For example, the 2014 Ebola outbreak in the DRC, where there is in-country capacity for viral screening of known and novel viruses, led to early detection and containment of the outbreak through swift and thorough science-based action by the government and its partners. The ultimate aim should be to get far enough ahead of viruses to prevent their emergence in humans, but DRC’s example shows that effective surveillance systems can provide benefits for early detection and control.
Leveraging global mobile phone infrastructures can promote the efficient communication of health information.24 Mobile reporting is not only useful for tracking human cases of disease, but also for reporting disease in animals.25 For example, partners under the PREDICT program rolled out an Animal Morbidity and Mortality Monitoring Program in Uganda, with park rangers submitting reports of animal morbidity or carcasses via a mobile phone-based template. Trained responders can follow up on reports to collect specimens as needed, allowing collection of information that benefits the conservation of wild species, and potentially informs assessment of public health risks. This activity is not resource intensive, allows for targeted data collection within the workflow of park officials, and can provide rapid access to information from remote areas.
Costs and Benefits
Recent response costs for EIDs have totaled in the hundreds of billions of USD over the past two decades.26 Ebola’s persistence for more than 15 months in humans in West Africa has been massively disruptive to trade networks, tourism, and the capacity for treatment of other diseases. A preliminary assessment by the World Bank estimated short- and mid-term losses through 2015 of up to US $32 billion if Ebola spread from Guinea, Liberia, and Sierra Leone to neighboring nations.27 Ebola-related disruption could result in much higher actual long-term costs from hits to other medical condition campaigns, such as vaccination for preventable diseases and treatment of malaria and HIV, educational attainment from school closures, declining trade and travel, and perceived ongoing risks for business investments.
Implementing enhanced disease surveillance in humans and pathogen surveillance in wildlife will also have a price tag, but warrants cost-benefit considerations for investments. A study based on viral screening findings in one bat species from a surveillance program estimates that 85 percent of mammalian viral diversity could be captured through investments of approximately US $1.4 billion over 10 years, or approximately 100 percent through investments of US $6.3 billion.28 This information would potentially provide value for assessing and prioritizing zoonotic disease risks. A recent analysis suggests that implementing interventions now to mitigate emerging zoonotic disease risks, compared to response policies, would yield a cost saving of more than US $340 billion over the next century.29 The assessment was based on mitigation policies including building capacity for surveillance and diagnostics to prevent new emerging diseases, addressing the human-animal interface, and cross-disciplinary control and prevention approaches.
A challenge remains in paying for this global good. Ideally, budgeting for wildlife disease surveillance would be implemented through national health ministries in partnership with animal health and environment ministries, to promote cross-sector sharing of results, and to demonstrate the sentinel and preventive value of this information for human health. The information generated through surveillance findings may also inform on practices that present EID risks, providing opportunities for future cost shifting.
Importantly, addressing EID risks requires sustained investments to build One Health systems, which cannot be achieved through the ‘roller coaster’ funding cycles that occur in response to each new EID threat. Donor engagement is crucial to meet this goal, since funding streams and investments themselves are often siloed. Investments must ensure a solid foundation upon which to build capacity, with realistic attention to the basic needs of a functioning system. For example, specimen storage and timely diagnostics may not be practical when a laboratory’s power is intermittent. As of the end of August 2014, a high level of Ebola treatment facilities and intervention strategies (e.g., safe burial access) in West Africa were reported as only partially functioning, and the course of upkeep of facilities post-outbreak for future outbreaks or other healthcare needs is unknown. Innovative approaches may be sought when increasing structural capacity, for example, at the 2014 UN Climate Change Summit, the WHO’s Director General, Dr. Margaret Chan, suggested developing solar power infrastructure to equip the 40 percent of hospital facilities in parts of Africa that lack access to reliable power.
A ‘One Health’ Approach
Looking to the source of new potential EIDs can help move towards a ‘One Health’ perspective that can elucidate connections between humans, animals, and ecosystem health. The One Health approach recognizes the integral health links and dependencies among different species, as well as the ecological dynamics that provide protection from or introduce risk of pathogen transmission. By taking into account information from multiple disciplines, we would gain a fuller understanding of disease ecology that would allow us to better monitor risks and intervene earlier.30
Where available, archived or prospective clinical specimens from paired human-animal surveillance can be screened to inform on pathogen spillover dynamics. One unique opportunity for paired sampling and consideration of human-animal-environment links is via One Health clinics. A One Health clinic in Bwindi, Uganda, on the border of the Bwindi Impenetrable Forest, was developed in the community hospital. Given the proximity to the forest, the community has close contact with and direct dependency on the local environment for the provisioning of resources, including food and tourism. At the same time, the introduction of domestic (e.g., pet or feral dogs or cats) or agricultural species (livestock, e.g., cattle, goats, sheep, swine) in a new location, some that may become invasive, may introduce new pathogens and transmission dynamics. Similarly, wildlife in the region, including highly threatened gorilla populations, have suffered declines from diseases, such as measles and pneumonia, acquired from humans through ecotourism and research. The direct collaboration between human, domestic animal, and wildlife health experts can have synergies in disease understanding, detection, and control for humans, livestock, and conservation not yet seen from currently siloed approaches. These collaborative approaches can also be applied to address other health concerns, such as vector-borne and ecotoxicology threats.
Development of One Health capacity for EID prevention requires understanding and addressing the underlying drivers of disease emergence. Wide-scale land use change, intensified food production, trade and travel, climate change, and other pressures on the environment to meet increasing societal demands are resulting in significant changes in ecological dynamics that place people and animals in novel contact, and facilitate pathogen transmission.31,32 Rather than viewing disease transmission as isolated random events, the impact of ecological changes on disease risks can be quantified and risks prioritized. Risk analysis infrastructure can also be developed within economic planning sectors to ensure risks are anticipated and mitigated. While development and uptake of voluntary guidelines should be encouraged directly with corporate and other development stakeholders, compliance across industries will likely require mandates from policy makers.
One Health Governance
Despite the existence of strong wildlife health and zoonotic disease expertise, current policy structures do not provide formal governance around wildlife diseases nor a mechanism for integrated human-animal-ecosystem approaches. Although the World Organisation for Animal Health (OIE) stipulates requirements for certain diseases in relation to international trade in animals, the movement of most wildlife is not covered beyond the officially listed diseases, nor is wildlife disease reporting required on non-listed diseases. OIE’s recent development of a voluntary wildlife disease reporting system (WAHIS-Wild) is a step in the right direction to help monitor wildlife diseases, but incentives are needed to encourage wildlife disease surveillance and reporting.
Similarly, the World Health Organization’s (WHO) focus has limited attention to animal diseases, despite the zoonotic origin of many priority human diseases. The WHO’s International Health Regulation (IHR) can be formally expanded to more fully incorporate animal health considerations through emphasis on the role of veterinary services and environmental authorities as allies and participants in the public health system. The IHR can also emphasize the need to move from reactive to proactive public health risk assessment and interventions, and the importance and responsibility of numerous sectors in moving this forward. For example, investment and approval policies can be enacted to require upfront health impact assessments for proposed extractive industry projects, and detection of risks can inform mitigation strategies that can be integrated into planning (such as requiring projects that place employees in forests to provide safe food sources in order to reduce demand on wildlife for nutrition).
To date, much of the push for an ecosystem perspective to promote health has come from the conservation world. This is remarkable, given the relatively limited investments in conservation versus veterinary and human medicine, and shows the potential of investments that effectively span the three sectors. At the UN Convention on Biological Diversity’s (CBD) Twelfth Conference of the Parties in October 2014, CBD parties officially agreed to recognize the value of a One Health approach, acknowledging the shared drivers of biodiversity loss and disease emergence, and the urgent need for the world to address EIDs in light of the Ebola outbreak. The CBD can lead meaningful engagement with the public health sector by identifying priority areas for collaboration, and by driving a research agenda through the CBD-WHO Joint Work Program on Biodiversity and Human health, and engaging experts to establish best practice guidance for CBD Parties. Implementation opportunities also abound at the national level for CBD Parties. CBD delegates, who are often based out of the environment ministry, can form inter-ministry One Health networks and task forces to promote discussion about zoonotic disease risks, and to identify a country context-specific roadmap for zoonoses prevention. These long-term plans can inform investment requests and reduce duplication of efforts by working in a cross-disciplinary and synergistic way.
The integrated policy approaches needed for EID prevention could be prioritized through the pending UN Sustainable Development Goals (SDGs). The current iteration of the SDGs does not sufficiently capture the complementarity and efficiencies that can be leveraged to maximize resources and outcomes. The nature of ecology-health connections and dynamics lends itself to a holistic, broader, and integrated approach for cross-disciplinary collaboration, co-investments, and co-benefits. For example, conducting paired environment, health, and social risk assessments before approval of development projects and ensuring that results inform preventive or mitigative actions, may more effectively promote environmental sustainability, reduce disease threats, and protect vulnerable populations from worsening inequities.
Lastly, while international policy and donor engagement are crucial for priority setting and resource allocation to support EID prevention, involvement in a local context is also essential. Given the role of cultural practices in the spread of Ebola (e.g., close contact with deceased relatives through burial practices or hunting and butchering practices linked to prior outbreaks), on-the-ground community-engaging interventions can serve an important long-term role in reducing risky practices. There is great benefit in expanding the construct of what constitutes public health. Local community leaders and other trusted members with strong cultural awareness must be seen as vital partners in public health efforts to find realistic solutions.
Conclusion: Lessons from a Current Challenge
The ongoing Ebola crisis in West Africa is the worst Ebola outbreak recorded in history, with approximately 24,000 known cases and over 9,800 deaths as of early March 2015. Most transmission has been focused in Guinea, Liberia and Sierra Leone, but cases have spread thousands of miles via international travel. Ending the current outbreak has seen signs of progress in Guinea and Liberia through successful control measures to reduce transmission and perhaps through natural development of protective immunity.
Response efforts have involved healthcare and public health providers, military forces, and financial investments from around the world. Despite global concern, the situation has demonstrated major challenges in detection, reporting, and resource mobilization, and widespread deficits in capacity and baseline knowledge of Ebola virology. Its trajectory provides insight on solutions to help prevent, and more effectively respond to emerging diseases in the future.
The first known human case in the current outbreak was traced back to December 2013 in Guinea, but national health authorities did not receive reports until March 2014, and the scale of the outbreak was not realized until summer 2014.33 The delayed timeframe for response resulted in months of missed opportunities for equipping countries with the support and materials they needed to fight new infections. Emphasis has been placed on control measures, including vaccination and treatment research. Yet minimal attention has been paid to learning about the dynamics that caused this outbreak and enabled such a devastating crisis, and to preventing future outbreaks.
The current outbreak especially articulates the need for more rapid detection and reporting mechanisms, integrated surveillance systems, and governance for One Health capacity. Public health systems can take immediate steps to better detect current human disease risks, and to move toward future approaches that assess risks to enable prevention. Ebola is one of many zoonotic EIDs that present a risk to humanity, and their impact may increase as we continue to fundamentally change our planet’s ecology and transmission dynamics. Getting ahead of EIDs requires urgent upstream and systematic solutions that realize the potential of our connected society, recognize integral human-animal-environmental links, and promote sustainable and healthy development.
Acknowledgments
The authors thank Marc Levy, Isabelle-Anne Bisson, and Naomi Stewart for their constructive reviews, which improved this paper. We are also grateful for the generous support of the DIVERSITAS-Future Earth ecoHEALTH project. This paper benefited from intellectual developments from the PREDICT project of the United States Agency for International Development (USAID) Emerging Pandemic Threats program.
