Coming out of the jungle, infectious diseases

The devastating 2014 Ebola outbreak in West Africa can be traced back to a two-year-old boy from a small village in Guinea. Emile Ouamouno, known to the world as ‘patient zero’, who died on December 6, 2013, was the first casualty of the deadly virus. Within a month, Emile’s mother, sister and grandmother all succumbed to the virus.

Since the beginning of 2014, Ebola has killed more than 10,000 people in Guinea, Senegal and Liberia over 18 months and the epidemic is yet to be conclusively thwarted. The origin of the scourge and how Emile came to be infected is still a mystery. What is known for certain is that the disease was contracted from an animal.

Fruit bats, being natural reservoirs of the Ebola virus, have been zeroed in on as prime suspects.

The small house of Nagaratna and Suresh NS, a young farmer couple, is surrounded by the forests of the Western Ghats. They live in Bandikkoppa village in Thirthahalli taluk of Karnataka’s Shivamogga district. In January last year both of them fell ill. They thought it was flu but the fever did not subside even after five days.

“So we decided to visit the primary health centre,” says Nagaratna. At the health centre, they were referred to the taluk government hospital, which sent their blood samples to the National Institute of Virology (NIV) in Pune. Lab tests confirmed that the couple had Kyasanur forest disease (KFD), a viral haemorrhagic disease similar to Ebola and dengue.

The couple was among the 137 people who suffered from the disease in Karnataka during January- May 2014. Except eight, all were from Thirthahalli taluk. It also killed a forest guard in the area. This is the first time since 2003 that such a high number of KFD patients was reported from the state. In 2003, over 300 cases were reported.

KFD is not a new disease in the district. The first outbreak was reported in March 1957 after a number of monkeys died unnatural deaths and a mysterious fever engulfed the residents of Kyasanur, a forest village in Soraba taluk. Since then the state has seen frequent outbreaks, but the disease had been restricted to just five districts in the Western Ghats.

However, NIV director Devendra T Mourya says there was always a suspicion that KFD might be present in other states as well. He says NIV has in the past found the antibodies against this pathogen in samples collected from Gujarat, Rajasthan, Maharashtra, West Bengal, Tamil Nadu, and Andaman and Nicobar Islands.

Mourya’s fears have been proven right as cases of KFD have recently been reported in new areas. In the past couple of years a few cases have been reported from the reserved forests of Malappuram district of Kerala, Nedumgayam reserved forest range in Tamil Nadu, the Mudumalai Tiger Reserve in Tamil Nadu’s Nilgiri district and Karnataka’s Bandipur National Park.

Little is known about the reasons behind the spread of the disease because there is hardly any research on it. But it is established that deforestation could be the primary reason as it increases the contact between humans and wild animals. Shivamogga district alone lost 4,000 hectares of forest between 2001 and 2007.

There is evidence that global warming that increases population of insects like ticks that harbour the virus could also lead to the spread of the disease.

Even within a taluk, outbreaks are not reported from the same area.

“The disease keeps moving from one area to another during different epidemic seasons,” says Rajesh Surgihalli, deputy director, Virus Diagnostic Laboratory, Shivamogga, and the state’s nodal officer in-charge of monitoring the disease.

Monkeys are the primary carrier of the disease. Ticks (Hemaphysalis spinigera) that live on them harbour the pathogen and pass it among the monkey population.

“Monkeys are sure to die once infected,” says Prakash K S, health officer of Thirthahalli taluk. When infected monkeys die ticks drop from their bodies to the ground, thereby generating hot spots of infectious ticks that spread the virus.

It is transmitted to humans through the bite of a tick or when humans come in contact with an infected animal. The outbreak of the disease in humans generally occurs in the dry months, from January to May.

Once a person is infected by the virus, it takes three to eight days for symptoms to appear.

“Patients may experience abnormally low blood pressure, and low platelet, red blood cell and white blood cell count,” says Prakash. Most patients recover within a week or two. But the illness has a second phase. Only 10-20 per cent patients reach the second phase.

“The second wave of symptoms begins from the third week of the illness. These symptoms include fever and neurological disorders,” says Surgihalli. The World Health Organization and the Centres for Disease Control and Prevention have classified this virus into group-4, which means the virus can cause severe human disease and is a serious hazard to laboratory workers.

There is no effective treatment for the disease and though a vaccine is available since 1989, it is not popular. At Thirthahalli, only 30 per cent of the people are covered under the vaccination programme. While the vaccine cannot prevent the disease since its efficacy is only 65 per cent, it can completely prevent the second stage of the disease. “That means, the vaccine can prevent deaths,” says Surgihalli.

Despite vaccination drives by the government, KFD cases in the state increased between January 1999 and 2005, says a 2006 paper published in Reviews in Medical Virology.

The lead researcher, Priyabrata Pattnaik from the Defence Research and Development Establishment in Gwalior, writes that “there is clearly a need for developing an alternative vaccine as well as a rapid diagnostic system for KFD ”. Till 2014?, state health department guidelines allowed KFD vaccination only for the six to 65 age group. The guideline was based on the assumption that children under six and adults above 65 will not visit forests for work.

The assumption is meaningless because many disease-prone areas lie within forests or in their vicinity. The authorities have now changed the guidelines to include those above 65 in the vaccination programme. But the under-six group is still not vaccinated. The reason: the vaccine has not been tested for its effects on children even though it has been in use for 25 years.

None of the government hospitals in Karnataka has laboratories that can carry out tests to diagnose KFD in patients. For conducting the required tests, laboratories need high biosafety facilities since there are possibilities of infection. Only one hospital, the private Manipal Medical College, has blood test facilities for KFD in the state.

“We are in the process of setting up facilities in the Shivamogga lab,” says Surgihally.

Experts say the government has neglected the disease because it was confined to a few areas and has a low fatality rate for humans. Pattnaik, in his paper, writes that the emergence of KFD in various states emphasises the need for nationwide surveillance among animals and humans.

Ebola, a global threat

KFD is just one of the many haemorrhagic fevers that occur across the world. The devastating 2014 Ebola outbreak in West Africa can be traced back to a two-year-old boy from a small village in Guinea.

Emile Ouamouno, known to the world as “patient zero”, who died on December 6, 2013, was the first casualty of the deadly virus. Within a month, Emile’s mother, sister and grandmother all succumbed to the virus. Since the beginning of 2014, Ebola has killed more than 11,297  people in Guinea, Senegal and Liberia over 22 months and the epidemic is yet to be conclusively thwarted. The origin of the scourge and how Emile came to be infected is still a mystery.

What is known for certain is that the disease was contracted from an animal. Fruit bats, being natural reservoirs of the Ebola virus, have been zeroed in on as prime suspects.

This is not the first time that a disease has been contracted from animals and it shall not be the last either. For millennia, humans have feared the inevitable but unpredictable devastation wrought by infectious diseases emerging from forests and transmitted through wild animals.

But there has been a stark increase in the incidence of emerging infectious diseases (EIDs) among both humans and domesticated animals in the recent past. Over the past 70 years, more than 300 zoonoses — diseases transmitted from animals to humans — have been observed. Notably, between 60 per cent of all human diseases and 75 per cent of all EIDs among humans originate in animals.

According to a 2012 study the Department for International Development, UK that mapped zoonotic diseases, zoonoses are responsible for over 2.7 million deaths and over 2.5 billion cases of human illness every year. Zoonoses are increasingly being considered a threat to the stability of human societies.

The increase in the incidence of zoonoses, to a significant extent, is a reflection of the change in our interactions with our forest ecosystems. The development of agriculture brought an end to an exclusive hunter-gatherer way of life. Despite the fact that today there are no known populations that live purely as hunter-gatherers, it is reported that in 62 developing countries, people obtain more than 20 per cent of their nutrition through wild meat and fish.

Populations living in and around forests also depend to a great extent on the forests as a source of livelihood. Nevertheless, the need for food drove the development of agriculture, which altered landscapes and populations. This changed the nature of human contact with forests.

The recent upsurge in the incidence of infectious diseases and zoonoses has often been attributed to the dramatic increase in population, mobility and the associated social and environmental changes in the past 70 years.

However, as Colin D Butler, professor of public health at the University of Canberra in Australia, says, “The harm to human health and wellbeing caused by forest clearance is often disguised by scale, time and the socioeconomic and cultural distance between the policy-makers whose decisions facilitate forest clearance and those who suffer.”

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Research has increasingly shown that changes in land use, including deforestation and forest fragmentation, urbanisation and intensification of agriculture have contributed greatly to the rise in the incidence of infectious diseases.

“Indeed the current increase coincides with accelerating rates of tropical deforestation in the past several decades. Today, both deforestation and emerging infectious diseases remain largely associated with tropical regions but have impacts that extend globally,” states a paper in Food and Agriculture Organization’s (FAO) journal of forestry and forest industries Unasylva.

As mentioned earlier, about three-fourths of all infectious diseases have, at some point, been contracted from animals. There are about 250 EIDs, about 15 per cent of which currently show a direct association with forests.

Some EIDs were originally transmitted from animals to humans but have now escaped the sylvatic cycle, where the pathogen spends some time in an animal before being transmitted, and adapted to a human-sustained cycle independent of forests.

While speaking of pathogens escaping the forests, the foremost microbe that springs to mind is HIV, which causes the devastating AIDS. Before adapting to human-to-human transmission a little over 30 years ago, HIV’s transmission cycle involved a primate.

According to the World Health Organization (WHO), an estimated 39 million people have died of AIDS-related causes between 1981 and 2013. By the end of 2013, 35 million people were still infected with HIV and more than 2 million people get infected every year.

What makes HIV a striking example of EIDs is the global scale at which it proliferated. AIDS, in many ways, is the world’s first truly global epidemic with an unprecedented rate and scale of incidence. The scope and speed of HIV transmission highlights the potential of EIDs to spread beyond borders and become a significant threat to human health and wildlife.

Change in human-forests relationship 

The diseases currently associated with forests can, in several ways, be seen as a reaction to change in the relationship between humans and forests.

Changes in forest cover and land use increase human contact with pathogens that were earlier contained within forests. The impact of such pathogens is exacerbated in the case of migrant and alien populations that lack previous exposure. A rapid increase in population provides a ready pool of hosts for pathogens and enables adaptation.

The majority of the diseases currently associated with forests involve three species in their lifecycle — a pathogen, a vector that carries the pathogen and humans — and occasionally a fourth, the reservoir species, which acts as another source of infection.

In terms of association with forests, yellow fever (a viral haemorrhagic disease transmitted by infected mosquitoes) is arguably the best-studied disease. Transmission of the virus that causes yellow fever is maintained in a cycle involving arboreal monkeys and mosquitoes. Expansion of human settlements into forests has been noted as a major causal factor in yellow fever outbreaks.

The first recorded outbreak in Kenya in 1992-93 is attributed to a settlement that hunted and collected fuel wood and water from the forests. The yellow fever virus has demonstrated rapid adaptation abilities where the transmission cycle has escaped direct association with forests. A sustained transmission cycle between humans and mosquitoes in urban and semi-urban areas has been observed during large outbreaks.

Environmental changes through deforestation, forest fragmentation, intensive agricultural activities, road and canal construction and other developmental activities result in significant alteration of local ecosystems. By extension, the ecology of disease vectors and pathogens is also affected through changes in density, distribution, breeding places and incubation periods.

The observed linkages between deforestation and malaria incidence make for an interesting case study of the changes in vector ecology (see malaria’s complex forest link).

Deforestation and forest fragmentation have contributed directly and indirectly to the steep increase in the rates of extinction among wild animals in the past 50 years.

The demise and rise of species due to human activity can have a cascading effect that threatens biodiversity. Biodiversity is known to act as a buffer against the spread of pathogens because in a diverse ecosystem the concentration of reservoir species diminishes. The degradation of biodiversity, on the other hand, results in a potential flourish of the reservoir species which, in turn, implies an increase in disease risk.

Take Hantavirus, for example. The link between its outbreaks and biodiversity has been well studied. Hantavirus, named after a river in South Korea where an early outbreak was observed, has a natural reservoir in murid rodents.

The virus causes the haemorrhagic fever with renal syndrome in many parts of Asia and the Hantavirus pulmonary syndrome (HPS) in the Americas. The infection spreads through bite, scratch or faecal aerosols of rodents carrying the virus. HPS is particularly feared because of its high rate of fatality, which is around 40 per cent.

According to a 2010 research paper published in Nature, host species in which pathogens multiply rapidly to high levels, providing an important source of infection for vectors are generalist species that invest less on immunity and more on adaptability to a wide variety of habitats and food sources. By contrast, specialist species, which act as buffers against pathogen proliferation are highly adapted only to one specific habitat and food type but invest heavily in their immune system.

A loss of biodiversity due to a change in the habitat often results in a simplification of the environment through elimination of specialist species and overpopulation of generalist species.

Murid rodents that carry the Hantavirus are generalist and can adapt to varied and changing ecosystems. Habitat change due to forest fragmentation in the US and Latin America have been linked with the emergence of HPS.

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A study conducted in Panama and published in the Annals of the New York Academy of Sciences concluded that the increases in local distribution and abundance in Hantavirus reservoir species can be attributed to the changes in the environment due to deforestation in tropical areas.

In areas with compromised biodiversity, the prevalence of pathogens in the blood of the reservoir species was found to increase threefold as compared to undisturbed habitats.

Multiple studies have pointed to habitat fragmentation and biodiversity loss to explain the emergence and transmission of novel diseases, such as Lyme disease in the US and Europe, to humans.

The disease is caused by a bacterial pathogen (Borrelia burgdorferi). White footed mice and white tailed deer have been identified as natural reservoir species for the bacterium, which is transmitted by tick bites. Diminishing biodiversity and the lack of large predators have helped Lyme disease to become the most prevalent vector-borne disease in the US.

Habitat destruction can also force species to venture into urban locales in search of food. In the first outbreak of encephalitis in Malaysia in 1998 fruit bats, which act as vectors for the Nipah virus, were displaced from their natural forested habitat due to severe deforestation and fires associated with the 1998 El Niño event.

The bats relocated to nearby pig farms where they fed on fruit trees. Persons who contracted the disease were closely associated with pigs, which were infected through contact with bats and bat faeces. The outbreak killed more than 100 people and caused an estimated loss of $500 million through its impact on the Malaysian pig industry.

The Nipah virus outbreaks observed so far in South and Southeast Asia have been relatively short- lived and contained in scale. Migratory impacts on proliferation and adaptation of pathogens can be much more severe. Take avian influenza, commonly known as bird flu. It is caused by diverse variants of the avian influenza virus.

The primary mode of transmission is bird to bird, although bird flu has adapted to humans with increased human-bird contact since the advent of large-scale poultry farming.

Since birds do not obey geographic borders, the virus has caused flu globally.

In the past year alone, bird flu outbreaks have been recorded in over 35 countries. The virus is notoriously difficult to track owing to its adept adaption. Different strains of the virus can interact with each other and exchange chromosomes to create new stable variants that can be fatal to humans. One such strain, H5N1, has caused over 143 cases and 42 deaths in 2015.

In total, there have been at least 844 confirmed cases and 449 deaths among humans due to the H5N1 strain of avian influenza since 2003 when the disease was first identified in human beings.

Greater mobility

As much as the pathogen and vector ecology is responsible for zoonotic diseases, changes in human ecology are responsible for the speed of transmission and the global scope many diseases have recently acquired.

Construction of roads and dams in recently cleared forested areas and rapid urbanisation often bring people, especially migrant populations that are immunologically naïve, in close contact with pathogens.

The spread and persistence of chikungunya serves as a classic example of how immunologically naïve populations can sustain an infectious disease. The fever is transmitted by Aedes mosquito. Chikungunya is thought to have originated in Africa, where the chikungunya virus is maintained in a sylvatic cycle between forest-dwelling mosquitoes and non-human primates.

Outbreaks among humans have been observed to be sporadic and short-lived. In urban centres across Africa and Asia, though, the virus is sustained by immunologically naïve human hosts.

The most recent outbreak of chikungunya happened in Kenya in 2004 and spread to several Indian Ocean islands, India and Southeast Asia. The outbreak in India started in 2006 and has affected several million people since then.

In India large populations of immunologically naïve humans have helped sustain the virus cycle between mosquitoes and humans.

In 2015, there were 16,235 cases of clinically suspected chikungunya cases in Karnataka. In Telangana, there have been nearly 1,500 cases. This is in contrast to outbreaks in other affected countries and islands with a limited pool of human hosts.

These areas did not report cases once the epidemic was over. During the epidemic in India, the virus spread from India to Italy through a traveller and was introduced into the local species of Aedes mosquitoes. It was then sustained in a mosquito-human-mosquito transmission cycle in the Mediterranean country.

Increased speed and scope of mobility due to globalisation has amplified the extent of zoonoses. Proximity to forests or close contact with animal vectors or reservoirs is no longer a limiting constraint on the reach of a pathogen. The case of severe acute respiratory syndrome (SARS) exemplifies the modern situation.

The virus that causes SARS originated in wild animals in southern China. The corona virus mutated to adapt to nearby human settlements and jumped to humans in a few closely located towns and villages and then spread to the urban area Guangzhou.

The crowded region facilitated the development of the disease into an epidemic in late 2002. Early next year, the virus spread to Hong Kong through a doctor from Guangzhou. The island city served as the hub for what would become a global pandemic.

The SARS pandemic started in February 2003 and within a few months it had spread to more than 20 countries across the Americas, Europe and Asia. By the time it was contained more than 8,000 cases and 774 deaths had been reported. The total losses related to the global outbreak were estimated to run into billions of dollars.

Despite the potency of the virus and the extent of the spread, SARS was curtailed much sooner than expected.

It has been argued that the SARS pandemic was a milestone in disease management because it moved disease response beyond national sovereignty. It took close coordination between several state and non-state actors under the guidance of WHO to get the disease under control.

The case of the global pandemic is a stark reminder of how global mobility for travel and trade has rapidly increased the extent to which humans can act as carriers of deadly infections. Diseases born in forests are no longer restricted to forests. As humans have altered forests to suit their needs, many organisms in forests have also adapted to humans.

Human mobility provides these organisms gateways to unchartered territories.

Coping with the unprecedented rise in the risk of global pandemics and epidemics requires a holistic approach to medicine that treats human health as part of environmental health. Suppression of SARS was possible only through coordinated, multidisciplinary and multi-institutional efforts.

Similarly, if we are to address zoonotic outbreaks and emerging infectious diseases, there must be a proactive approach to restore wildlife health. It will also require close monitoring of how the increasing ecological footprint of humans is affecting health and disease dynamics.

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