Disease and ecology

LOOKING at the many vector-borne diseases, particularly viral, one finds that there exists a complex host-parasite relationship among various animals, their arthropod vectors and infective organisms. The results of human entrance into the infectious chain are deleterious, since man becomes an integral part of the host-parasite relation which changes his environment. Therefore, before thinking of controlling the diseases, efforts must be made to understand vector-transmitted infections in man in relationship to his environment.

Parasitic diseases of humans and animals are obviously a part of the broad evolutionary development. The application of the theory of insect-carriers led to a better understanding of diseases such as sleeping sickness, malaria, yellow fever, bubonic plague and typhus. While the role of animals, vectors and man in the natural cycle of disease transmission was established about two centuries ago, not much importance has been given to understanding the role of the environment and the necessity of an ecological approach to study this. The lack of accurate knowledge concerning the ecology of wild reservoir hosts, vectors and the human victims in nature has been responsible for a poor understanding of the epidemiology of many diseases, particularly arthropod-borne viral diseases.

The Russian parasitologist and geographer Eugene N. Pavlovsky’s extensive researches in the middle of the last century gave us a greater understanding of the evolution of natural adaptations of infectious diseases. The concept means that wild enzootic foci of many diseases exist in nature independently of man and domestic animals. These foci present well-defined ecological peculiarities wherein pathogens and natural hosts are associated, often through an intermediate vector.

The environmental factors determining these associations are climate, soil, vegetation and topographical features (landscape epidemiology). These serve as reliable indicators of the existence of certain diseases. Areas at the edge of deserts, with burrowing rodents, may harbour Cutaneous leishmaniasis (a skin infection, as in Rajasthan); areas at the junction of mountains, forests and agricultural fields or grasslands (interfaces) may harbour many vector-borne diseases. These natural foci, which may be called “silent zones of diseases”, may remain undetected until susceptible human beings come into contact with them directly or indirectly and become infected. With accurate ecological knowledge, similar foci in other areas may be detected before human disease can be predicted.

Tenet of disease ecology One of the crucial tenets of disease ecology is that population, society, and both physical and biological environments are in dynamic equilibrium. Significant stress on this equilibrium can produce cascading effects on any of the aforementioned components. The human-environment relationship, if disturbed enough by major changes in land use, migration, population pressure or other stressors, can show significant maladaptation, as manifested by the appearance or diffusion of new diseases.

Environmental changes such as deforestation for agriculture, forestry, and human settlement/activity of various kinds have brought about changes in the ecology of vectors and the epidemiology of vector-borne diseases. Transmigration programmes, logging, agricultural activities, mining, hydropower development and fuelwood collection do bring about ecological changes in the environment. Each activity influences the prevalence, incidence and distribution of a vector-borne disease. We now know that changes in the natural ecology, or activities associated with it, provide new habitats for malaria vectors such as Anopheles dirus , An. minimus , and An. Balabacensis, and also affect their quantitative and qualitative effectiveness as vectors. Viral and parasitic infection patterns are directly or indirectly influenced by the loss of natural tropical forests, and have to be considered. The ability of zoophilic vectors to adapt to human blood as an alternative source of food and to become associated with human dwellings (peridomestic behaviour) has influenced the occurrence and distribution of diseases such as leishmaniasis in South America, and Japanese encephalitis (J.E.), Kyasanur forest disease (KFD) and a few other viral infections in India. Certain species of sandflies, which were originally zoophilic and sylvatic, have adapted to feeding on humans in peridomestic and urban surroundings.

The changes in the behaviour of reservoir hosts and the ability of pathogens to adapt to new hosts in the newly created habitats also influence the patterns of disease. As a result, a disease at one time thought to be primarily rural has acquired serious urban dimensions. The agents of a number of diseases such as kala-azar are now reappearing. This is due to changes in human habitats. Man actually intrudes into ecological cycles of disease parasites/pathogens. This has resulted in zoonotic diseases such as KFD and scrub typhus. The introduction of new ecological niches favouring the breeding of vectors results in the transmission of diseases such as malaria, J.E., dengue, chikungunya and scrub typhus.

Some have equated ecology with epidemiology. The main distinction is that while epidemiology is the study of the relationships between variations in man’s environment and his state of health (disease), ecology embraces the interrelationship of all living things and the environment. Epidemiology thus constitutes a special application of human ecology or that part of ecology relating to the state of human health. There is now an increasing recognition that the ecological environment plays a major role in vector-borne disease transmission and it is a major factor one should consider when planning control measures.

A proper emphasis must, therefore, be built into the planning process to prevent degradation of the ecosystem. Prevention of diseases through ecological or environmental manipulation or intervention is a safer, cheaper and more effective and rational approach than all other methodologies. In the case of malaria and filariasis, control through naturalistic and environmental methods were demonstrated clearly and there are many well-known examples, such as the control of A. quadrimaculatus in the Tennessee Valley Authority, control of A. maculatus and A. minimus in Malaysia by naturalistic methods, and the drastic reduction of C. quinquefasciatus, the urban filariasis vector, in Puducherry and Mansonia vectors of Brugian filariasis in Cherthala, Kerala. But the point is, in recent years, firefighting operations are undertaken to control vector-borne viral diseases such as J.E., dengue and chikungunya whenever sporadic outbreaks take place in different parts of India, without understanding why these are occurring. Recently, insecticidal sprays were suggested to control diseases such as scrub typhus and KSD, without knowing fully the dynamics of their transmission.

Silent enzootic Ecological investigations on Western equine encephalitis (WEE) showed that birds served as natural hosts and mosquitoes as vectors, and humans and horses were terminal hosts. In J.E., man is a dead-end host and there is no man-to-man transmission. Small animals and birds were suggested as potential (over-wintering) reservoirs. Some mammals may be amplifiers of the virus (such as pigs or even ducks in some places in West Bengal) in J.E. while cattle may help in the multiplication of the vector population without involvement in the natural cycle. It was clearly shown that in the case of KFD, cattle increased the tick population exponentially. One should consider the similarity in ecology among WEE, Murray Valley encephalitis (MVE), the West Nile (W.N.) virus, and J.E., where mosquito transmission and birds as natural hosts have been established. Ecological studies on other arbo-viruses such as yellow fever (Y.F.) and KFD have led to a clearer understanding of their epidemiology, and in both these cases monkeys play a significant role as amplifying hosts. KFD is now reported to have broken out in new territories, though not in epidemic proportions. But with rapid changes taking place in the ecosystem, one will not be surprised if the disease reaches epidemic proportions in the not-too-distant future. Most of the salient features in the epidemiology of KFD are already described by Jorge Boshell. There are still some areas that need to be studied, particularly the nature of the virus in the silent areas. Is there a silent enzootic going on in nature? Are there any epizootics due to KFD? There are many questions such as this that remain to be answered. The first serological survey for arbo-viruses in India (1949) had given many indications that KFD could appear in several areas with ecological conditions similar to that of Shimoga district in Karnataka. The reported appearance of the new foci in recent years confirms this. Long-term painstaking research with adequate manpower has to be initiated in several areas to really understand the natural cycle of this fascinating virus.

In the case of dengue, the existence of a cycle apart from man has yet to be demonstrated, though it was suggested as far back as 1931 that there might be a sylvatic cycle with Aedes albopictus as the vector and monkeys as sylvatic hosts. Unfortunately, no research seems to be in the offing to study this. Dengue occurs throughout the tropical region and spreads into subtropical and warm temperate zones where the vector Aedes aegypti is present. It has been suggested that the urbanisation of new strains of dengue viruses, which had previously existed in some sylvatic reservoir, had taken place, transmitted by Aedes aegypti and with hemorrhagic manifestations (in some countries). When one starts investigating the inter-epidemic cycle, the existence of a sylvatic cycle has to be kept in mind. In the presence of Aedes aegypti , dengue always occurred in an endemic form. Whether vector density and extrinsic incubation governed the occurrence of the epidemic is not understood clearly. In Malaysia, Aedes aegypti is a vector in the coastal region and Aedes albopictus in the interior. Can you predict a similar situation with dengue and chikungunya in Kerala? A high proportion of monkey sera was found with antibodies with dengue type I in Malaysia. It was shown that the monkeys tested came from an urban area where dengue was epidemic, with Aedes aegypti as vector. In Australia, it was shown sera from two species of fruit-eating bats ( Pteropus sp .) were found with antibodies to dengue type I. There is also strong evidence that dengue is endemic in areas in many countries where monkeys are not present. It has been suggested that the main sylvatic hosts are bats and rodents. (Not unlikely, since such a cycle has been suggested in KFD, where a silent cycle of infection between bats and Ornithodoros (a kind of tick), independent of man, is suspected. It is, therefore, possible that different groups of mammals are important in different parts of the world in the epidemiology of many diseases and they need to be studied on a case-by-case basis. Has anyone looked into these aspects in India?

Chikungunya Chikungunya causes severe fever with polyarthritis. This is at present an urban disease in some parts of India. Both Aedes aegypti and Aedes albopictus have been incriminated as vectors. There is only one piece of evidence to suggest a sylvan cycle of this virus as the virus was isolated from Aedes africanus caught in the Zika forest in Uganda. So there is also the possibility of a sylvan cycle for this virus, other than man, an Aedes aegypti/Aedes albopictus cycle. In short, the forms of haemorrhagic dengue and chikungunya are essentially urban diseases with a cycle between man and mosquito. There may be sylvatic cycles of this virus also, and they are not involved in an epidemic phase. The occurrence of chikungunya cases in typically rural areas in Tamil Nadu was recently reported, but this needs confirmation. It is also possible that there is an enzootic cycle involving small rodents and shrews. These mammals have large population turnovers and can be ideal participants in an enzootic cycle. (This was demonstrated in the case of KFD.) The possibility of non-mosquito vectors such as gamasid and laelaptid mites to maintain a rodent-mite-rodent chain cannot be ruled out. Intensive long-term research has to be undertaken into all these aspects, as chikungunya can pose serious public health problems in the future.

Scrub typhus Another disease which is now drawing increasing attention, is scrub typhus. Many cases were reported in Tamil Nadu and undivided Andhra Pradesh in the recent past. Assuming that the cases are diagnosed correctly, this can be attributed to increased construction activities in recent years and the conversion of rural and fallow lands into real estate. The vectors are trombiculid mites. The adults are about one millimetre long. The parasitic hexapod larvae feed on animals for a few days only and then return to the soil and moult twice. The octopod adults are non-parasitic but are predators of soil arthropods. The whole life cycle is completed in two to three months. Engorged larvae detach from the host in batches, so that a small patch of soil becomes “seeded” with trombiculid mites. This is the “mite colony” of J. Ralph Audy. Such a colony will perish unless a proportion of the larvae return to the same place after a second engorgement on the “maintaining host”, usually field rats and mice. There are few possibilities for this. Other incidental hosts are birds such as warblers, pheasants, quails and fowls. These are important as they distribute the mites over a longer range. Man is only a casual host and is of no importance in the life cycle of the vector. The vectors are Trombiculid mites. These facts are not clearly understood by some of the present-day investigators.

Rickettsial infection in man is caused by several species of Leptotrombidium mites (many of the scientific names have undergone revision) and their natural hosts are limited to small ground-living mammals. Two species are the most important— L. akamushi and L. deliensis —and these are widespread. According to Audy, the geographical range of scrub typhus contains the centre of evolution of the mite and of the small rodent hosts. Ecological characteristics of the vector habitats are of extraordinary interest. A “mite colony” as mentioned above is the infested site which usually comprises several mite colonies, and the entire area is called a mite island. The mite colony is usually seeded from a single warm-blooded host, while the “mite island” may be maintained with help from several hosts of the same or different species. Where suitable population of hosts is present in patches but mite islands are absent, the site is called a “receptive focus”.

The vector completes its life cycle in the soil if it has the required moisture content. When the soil becomes dry, the larvae disappear, while the adults tend to disperse more widely and stop laying eggs. This explains the relationship of the epidemiological units of infection called “typhus islands” to vegetation and ground features. A typhus island is a small area infected by R. tsutsugamushi either an infected mite or a host from the neighbouring typhus island.

Transfer of rickettsiae from rodent host to uninfected larvae maintains the epidemiological chain. It has been reported that in the course of successive passages, the virulence of the infective agent increases. Trombiculid mites are generally found feeding together in clusters in the ears of rats and this facilitates the transfer of the infective agent. Rickettsiae can be transmitted transovarially from adult mites to larvae. “Typhus islands” are usually found in man-made wasteland (overgrown clearings, back gardens and abandoned villages) on forest fringes, or in rows of bushes. An optimum temperature of 20-35°Celsius, humidity and soil moisture are important. When the weather is dry, the mite islands are restricted to places kept moist by groundwater.

The influence of man on the spread of this infection is considerable. The destruction of forests and shifting cultivation encourage the growth of specific vegetation and of the accompanying small rodents. This brought the genus Rattus and the mite together and increased the spread of endemic foci of infection. Rat control alone may temporarily do more harm than good; removing the rodent may increase the chances of infected larvae feeding on man. This is a good example of the importance of a sound ecological approach to problems of control of any vector. But there is very little understanding of the complexity of the infective chain.

There are also diseases grouped under emerging or neglected tropical diseases, but these are not yet in the public domain and in any case no one has taken these seriously. In recent years, many research schemes have been formulated for the control of viral and rickettsial infections without understanding their natural cycle, particularly in the non-epidemic season. Many of these infections occur in nature in slow, silent, lurking enzootic cycles. Only when there is a combination of several factors in the environment, as demonstrated in KFD, does an epidemic occur. Now, more and more research schemes are formulated for eradication and elimination, which seems to be a utopian idea. Look at what happened to the National Malaria Eradication Project (NMEP) in 1958. It is more than 55 years now; did we succeed in eradicating malaria?

It is abundantly clear from the above that many of the parasitic diseases occur as a result of changes in the ecosystem and human behaviour. We have to base our science on solid ecological grounds to properly understand the disease process and before trying to control vector-borne diseases. We should also focus our efforts on disease management strategies rather than total disease eradication approaches, as favoured by some. The latter approach is expensive to administer and is doomed to fail in the long run.

Nature is constantly evolving. With changes being made to the environment, it is adapting to the new situation. There are no short-cut or quick-fix remedies. Only a sound ecological approach will help in the understanding of the complexities in the natural cycle of the disease entity and enable effective control measures.

Dr Payyalore Krishnaier Rajagopalan is a former Director of the Vector Control Research Centre in Puducherry.