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Rev. sci. tech. Off. int. Epiz.

, 2004, 23 (2), 467-484

Ecological sources of zoonotic diseases
J. Slingenbergh (1), M. Gilbert (2), K. de Balogh (1) & W. Wint (3)
(1) Animal Production and Health Division, Food and Agriculture Organization of the United Nations,
Viale delle Terme di Caracalla, 00100 Rome, Italy
(2) Biological Control and Spatial Ecology, Free University of Brussels, avenue F.D. Roosevelt 50, 1050 Brussels,
Belgium
(3) Environmental Research Group Oxford, P.O. Box 346, Oxford OX1 3QE, United Kingdom

Summary
Although of zoonotic origin, pathogens or infections posing a global threat to
human health such as human immunodeficiency virus, severe acute respiratory
syndrome or emerging influenza type A viruses may actually have little in
common with known, established zoonotic agents, as these new agents merely
underwent a transient zoonotic stage before adapting to humans. Evolution
towards person-to-person transmission depends on the biological features of
the pathogen, but may well be triggered or facilitated by external factors such as
changes in human exposure. Disease emergence may thus be depicted as an
evolutionary response to changes in the environment, including anthropogenic
factors such as new agricultural practices, urbanisation, or globalisation, as well
as climate change. Here the authors argue that in the case of zoonotic diseases
emerging in livestock, change in agricultural practices has become the dominant
factor determining the conditions in which zoonotic pathogens evolve, spread,
and eventually enter the human population. Livestock pathogens are subjected
to pressures resulting from the production, processing and retail environment
which together alter host contact rate, population size and/or microbial traffic
flows in the food chain. This process is illustrated by two study cases:
a) livestock development in the ‘Eurasian ruminant street’ (the area extending
from central Asia to the eastern Mediterranean basin) and the adjacent Arabian
peninsula
b) poultry production in Southeast Asia.
In both scenarios, environmental factors relating to demography, land pressure
and imbalances in production intensification have led to an unstable
epidemiological situation, as evidenced by the highly pathogenic avian influenza
upsurge early in 2004, when the main outbreaks were located in areas which had
both large scale, peri-urban commercial holdings and a high density of
smallholder poultry units.

Keywords
Agricultural intensification – Animal production – Disease ecology – Ecological change –
Emerging zoonosis – Epidemiology – Population increase – Urbanisation.

Introduction humans as the majority of these are of zoonotic origin: a
comprehensive review by Cleaveland et al. (6) identified
Disease emergence and zoonotic disease 1,415 species of infectious organisms known to be
agents pathogenic to humans, including 217 viruses and prions,
538 bacteria and rickettsia, 307 fungi, 66 protozoa and
Zoonoses are defined as infectious diseases that can be 287 helminths. Out of these, 868 (61%) were classified as
transmitted naturally between humans and wild or zoonotic and 175 pathogenic species were considered to
domestic animals. These diseases are particularly be associated with emerging diseases. Of this group of
important in the context of emerging infectious diseases of 175 emerging pathogens, 132 (75%) were zoonotic.

but shows increases in incidence or expansion in a geographic. Others present an It appears. (6).g. There local health authorities. but only if an emerging zoonosis is equally important (38). yellow fever and malaria. Off. salmonellosis). environmental change may increase the basic transmissible between humans (human tuberculosis). Some of these diseases may further evolve and Factors affecting the emergence become effectively and essentially transmissible from human to human’ (9. anthrax. This compares to a decrease of 8. It is. smallpox. Epiz. reproductive number (R0) leading to longer transmission Finally. Lassa and Ebola viruses). the conditions affecting disease emergence in of the world. Factors associated with the emergence of pathogens in human. measles. general will be considered first. globalisation or climate change. A (HIV type 1 and 2) have long since abandoned their common feature of all these processes is that they are zoonotic status and despite the fact that HIV viruses may largely a consequence of human activity. diphtheria. with occasional outbreaks occurring in humans. human transmission is strongly influenced by the biological features of a pathogen relating to genetic shift.2% into either a human or a zoonotic pathogen. whereas others are rural villages) in the early stages of HIV evolution (31). monkeypox. The human immunodeficiency viruses the survival time of pathogens outside the host (32.8% between introduced into human populations and evolve exclusively 1981 and 1995. urbanisation. (10). West specific structure of the host contact network (scattered Nile and Nipah/Hendra viruses). The title of Schrag have been present for many years before assuming and Wiener’s paper ‘Emerging infectious disease: what are . followed by an tuberculosis. which had once been controlled in many parts agents. zoonotic or Rather than concentrating solely on zoonotic disease otherwise. and the aetiology of the pandemics that and/or host ecology are primarily responsible for the have occurred during the 20th Century tend to support the majority of emerging diseases and that those resulting from notion that emerging diseases in humans originated evolutionary changes alone are comparatively rare. or has occurred previously. 38). there are pathogens of animal origin that suddenly chains. directly from animal reservoirs rather than gradually ‘Ecological changes’ embrace a number of very different evolving from known and existing zoonotic agents. areas where primary agricultural production takes place. or HIV/acquired Cleaveland et al. the level of susceptibility of humans to these new alter vector distribution and abundance. sci. Whilst the pace of evolution towards full human-to- respiratory syndrome [SARS]). In the latter stages of this human-to-human transmission and are now readily process. rabies.. dengue fever. there was no sign of development epidemiological situations. bovine tuberculosis. The more classical zoonotic diseases may still be classified drift or quasi-species behaviour. Schrag and Wiener (38) and more recently health when compared to major diseases such as influenza by Daszak et al. the period when antibiotics and immunisation became commonplace (7). Instead. Many diseases. probably. and thus for the disease to emerge virus [HIV]. but with a perhaps hardly discernable zoonotic stage. defined as ‘a zoonosis that is newly recognised or newly evolved. there may have confined to animal reservoirs – human cases are infrequent been a somewhat delayed visible emergence because of the or represent dead-end infections (e. What processes under the same umbrella: changes in agricultural the major influenza type A epidemics of 1918. therefore.g. influenza type A and.468 Rev. characterised transmission chain leading to eventual extinction by haphazard outbreaks that may go largely unnoticed by (e. Hanta. Some pathogens are largely towards an equilibrium stage. which provide an opportunity for the pathogen to appear in human populations (human immunodeficiency adapt to human hosts. however. between 1938 and 1952. int. change the strains may have dictated the size of the human influenza migration patterns of birds and other wildlife. have started to re-emerge: cholera.g. severe acute (3). 1957 and practices. 45). An emerging zoonosis may thus of zoonotic diseases be an existing infection or disease which appears again or invades new territories. immune deficiency syndrome (AIDS). host or vector range. well-established in both animals and humans (e. that particular attention should be intermediate situation with animals as the main hosts. and then adapt and shift to are also some zoonotic agents that gradually adapted to humans as their main hosts. tech. 1968 all had in common was that a novel pathogen was The latter is a factor of growing concern as it may affect the suddenly seen to circulate in the human population. wildlife and domestic animals have been explored Zoonotic diseases have relatively little impact on human by Morse (32). external factors may be as emerging diseases. and affect epidemic (44). increasingly clear that most of these diseases started out as Schrag and Wiener (38) argued that changes in pathogen zoonotic (12). but paid to those pathogens which may undergo a transient. Indeed. Dobson and Foufopoulos (13) and (flu). 23 (2) The definition of zoonoses actually fits a wide array of pandemic proportions. In the examination of factors which may explain why and how United States of America (USA) the infectious disease pathogens found in animal reservoirs become progressively mortality rate increased at an annual rate of 4.

demonstrated by Antia et al.g. weeds (as opposed to also be a matter of time-scale: environmental change may trees). these species network where each node is a group of hosts. prevent evolution from playing a role in the (r-strategists. past or present.Rev.e. or generalist herbivores (as opposed to specific have been the main factor influencing disease emergence herbivores). (3). but prior to extinction.e. i. then using the metapopulation analogy. a village have adverse effects on indigenous fauna and are now or city. Off. If the size of global biodiversity crisis (43). endemic diseases are generally environmental change. (31). Epiz. int. For diseases which trigger lifelong immunity. mainly depends on the overall reproductive number being some may evolve and increase their virulence to give higher than one. however. which is subject to change as a consequence R0 > 1. Therefore. be substituted by ‘Emerging infectious disease: what are i. most successful emergence of diseases over the longer term (12). changes in the geography of human population may have contributed to b) the spread of the pathogen into the new population. r-strategists (organisms can be classified according to the relative roles of human activities and evolution?’ In their strategies to maximise their fitness: in a predictable recent years. we will use the term metapopulation to Questions concerning emerging diseases and invasive mean a set of host-subpopulations connected by possible species essentially address how an organism adapts to a microbial traffic). distribution (42). with longer generation times. whilst evolution has played a major role in the approximately the same pattern (6). the risk that a invasion ecology. How did a pathogen enter a human population? What are the Standard epidemiological models predict that the size of an characteristics of potentially invasive pathogens? These epidemic relates to the size of the susceptible population. Likewise. it seems that humans have probably been environment. allowing them to persist and spread into a new host of both a better adaptation to the host and changes population in the spatial structure of the host population (e. the analogy with metapopulation can be used to considered to be the second most important cause of the explore the spatial dynamics of diseases (25). 23). persist and develop in new host populations (13). disease emergence is the result Following introduction and initial ‘colonisation’. the spread of of two sequential processes: disease within the new host population will determine the a) the adaptation of a pathogen to a new host: as elegantly success of an emerging pathogen in the newly invaded host. short-term adaptations of pathogens to human hosts and for which minor changes in the genome may change (14.g. with severe susceptible hosts. From another perspective. that are small. linked to a static environment whilst epidemic agents are more usually associated with changing ones. pathogen strains entering Factors facilitating the spread into new populations are not a new host population may initially have an overall specific to emerging diseases and apply equally to any reproductive number of less than one (R0 < 1) that leads to epidemic disease. refined by taking into account the spatial structure of social Invasive alien species are defined as species introduced groups (28). Although not expressed in such terms. As developed by May et al. i. Such organisms are generally characterised by a short generation time and high The reason that most emerging diseases are reported to be numbers of offspring and usually have efficient ways of related to ecological changes rather than evolution may dispersing to new habitats (26).e. it is also related to the size of the host metapopulation (in the rest of this text. 37). it pays to invest resources in long-term responsible for many emerging diseases through creating development and long life [K-selection] whereas in a risky and maintaining the conditions for existing pathogens to environment. questions relate to the adaptation of a pathogen to a new If one thinks of the susceptible population as a network of host. it has long been recognised that disease will assume epidemic proportions can be assessed successful invaders are generally those species able to on the basis of the size and structure of the host . as they unlikely candidates to jump host-species barriers are closely intertwined. and can be addressed by comparisons between susceptible hosts. whereas helminths are considered to be and evolution separately is therefore unwarranted. economic and environmental consequences (42). 31). it is better to produce as many offspring as enter.. They are also recognised as the epidemic is closely related to the number of the a clear threat to ecosystems. and higher diseases as an evolutionary response to (anthropogenic) host-specificity). then this general statement can be emerging diseases and invasive plant and animal species. sci. One can simply view emerging (K-strategists. over the last few decades because such changes have been emerging disease pathogens are acknowledged to follow fast. drive the R0 above one in the emergence of HIV/AIDS in Africa) (28. This does emerging pathogens are ribonucleic acid (RNA) viruses not. In biological given disease affecting a given host species. with a short generation time. tech. 23 (2) 469 the relative roles of ecology and evolution?’ could actually maximise fitness in changing environments. Different questions relate to each of these processes. the spread the extinction of the pathogens. local extinctions are observed. and if one considers a Generally introduced by human activities. outside their natural. quickly as possible [r-selection]). in a given landscape for a new environment and then spreads (31. e. habitats or species. and assessing the respective roles of environment host-specificity).

tech. For example. host range. the spatial structure (clumping) of production units. virulence and infective period . Pathogens are also dispersed through food preparation and consumption and can also spread to water bodies via the sewage system d) Factors relating to the innate biology of the pathogen: reproductive (r/K) strategy. which disease spread is taking place The factors cited in the literature as contributing to the – the transmission pathways other than those within the emergence of livestock diseases and associated zoonotic animal host populations. sci. marketing/ risk categories (Table I): distribution. and the spread of pathogens through giving feed of animal origin to live animals. the ‘static’ environment in novel disease agent to turn into a pandemic. made up of the number and size of holdings. germs in animal waste products contaminating open land and water resources. Naturally. to live animals. int. categorised according to four main epidemiological domains Host Transmission Pathogen Factors Husbandry (a) metapopulation (b) pathways (c) characteristics (d) Human demography x x x Technological progress x x x Economic development x x x Land pressure x x x Animal movement and trade x x x Urbanisation x x x ‘Peri-urbanisation’ of livestock x x x Veterinary services/campaigns x x x Wildlife contacts (including birds and rodents) x x x Farming systems/intensification x x x Agro-ecological zones x x Dietary habits/demand elasticity x Waste management x x Hobby/cultural animals x Infrastructure x x Seasonality in livestock management x x x Population structure (age. breeding. and health protection practices are together responsible for the production structure b) Metapopulation.) x x x Phylogeography/gene flows: Pathogens x Animals x Globalisation: Mobility of people x Trade and traffic x x Climate change: Primary production location x x x x Vector distribution/abundance x x Migration pattern wildlife/stock x x Pathogen survival outside host x x Distribution of rural population x x x a) Animal husbandry factors pertaining to feeding. processing. the metapopulation fixes the possible microbial traffic within the host population c) Pathways external to the host population are also important and include the flow of pathogens originating from live hosts passing into the food production-processing-distribution chain. sex.e.470 Rev. this also applies to the spread of structure and the local biosecurity level) emerging diseases. the current global network of human populations meets all the basic requirements for a – the host metapopulation. comprising the entire food chain infections may be assigned to four main epidemiological (from feed. etc.. mode of transmission. i. Off. housing/animal movement management. food preparation and consumption) Table I Factors influencing the spread of livestock (including zoonotic) diseases. 23 (2) metapopulation. and the level of isolation of each – production intensification (which determines production sub-population. Epiz. the ‘static’ animal host environment in which the disease spread is taking place.

Most of the demand for poultry protein stems from Goat the emergence of a global middle income class living in the megacities of transition economies and developing countries. Water buffalo As a consequence. Many zoonotic diseases and human pathogens result from our intimate contacts with domesticated animals. sheep. this resource driven pattern has been supplanted that has continued since the early days of domestication. irrigation and other inputs. scavenging smallstock in backyards of Zoonotic infections originating from wild animal reservoirs village dwellings characteristic of the humid. most notably during the 20th Century. goat. inputs are (e. four distinct. For example. infections to be maintained (1. perennial are generally associated with anthropogenic forces involving cropping areas. infective period. 12). sheep. the integrated biological invasions by vectors (e. eggs. which were large enough for these crops are grown.g. The biological productivity. and four of the major domestic livestock species (in Similarly. urban centres. the Near East. tech. successful and rapid technology driven increase in crop starting more than 10. This is (4. Epiz. no such limit applies to modern livestock paved the way for human population clusters. products of this remarkably innovative region are now pesticides. and this resource. whilst crop production levels are agriculture and associated settlements. This has triggered the establishment of large Fig. pig and water buffalo from 10. reproductive strategy). but where technology levels are low.Rev. milk and meat rubella and pertussis emerged following the advent of (8. Only in onwards sub-Saharan Africa has this development yet to become Horse domestication probably occurred in more diffuse locations over a firmly established.g. This is best best described in the archaeological record of the Near illustrated by the Green Revolution that took place in Asia East. West Nile virus. in some of the densely populated patches of the moister The capture and controlled breeding of the major animal agro-ecological zones where population pressure has domesticates was part of a suite of transformations in triggered a progressive intensification of agriculture human society known as the Neolithic transition. takes place in extensive systems. varying from pastoral livestock kept in drylands and other harsh environments. particularly the Fertile Crescent. sequential.g. which witnessed the during the sixties and seventies and which led to a development of the first agricultural economy in the world. 23 (2) 471 – the innate ecological characteristics of the pathogen emergence and spread. sci. stages in the intensification of livestock to an understanding of the forces affecting disease production may be distinguished. pigs and cattle) (Fig. in large areas of the (virulence. South Asia (29). fertilisers.000 BP North Africa. Off. e. and sustainable means of increasing off take from a fixed land base (30). and are usually close to. anthrax spores). lentils. host-range. The location of livestock production and the associated Horse processing industries has shifted to be close to markets that supply. also. production of animal protein. made possible by improved seeds. longer period of time (20) Extrapolating from the spatial patterns of the livestock systems discussed above. therefore.. 1 scale peri-urban poultry industries that supply meat and Approximate locations of suggested domestication centres for eggs to the urban centres of Latin America. cattle. East Asia and. rodents can be host to several zoonotic diseases) or scarce and markets are poorly developed. measles. major geographical imbalances – in Cattle terms of concentration of production – can develop. to free ranging. 1). This is best demonstrated by the recent history of the poultry Sheep Pigs sector. In most areas where there is sufficient high contact rates with the wild animal host rainfall. int. crop/livestock system remains the most efficient Lyme disease) or by the pathogen itself (e.000 years ago. Unlike the Green Revolution. However.g. widespread and include plants such as barley. a process However. an important feature of the intensification of the livestock sector is the severance of the traditional links between the amount of available local land and feed resources. 11). albeit livestock production and its intensification are thus central overlapping. 35). and the industries that can be detached from the land where feed first urban centres. and guided by events in the Identifying the processes underlying the transformation of world poultry sector. It is revolution’ is a response to an increased demand for the likely that ‘crowd diseases’ such as smallpox. . vector developing world. The domestication constrained by the physical limits of the available land of farm animals enabled surplus food production. it can be argued that the current ‘livestock temporal order: goats. the majority of livestock production still distribution. the wheats.

2. but also of swine). Epiz. animal populations keep expanding in the most populous and health care.. Large numbers of animals are housed in places on earth while most of the income generated from confined feeding operations. small stock and today they can be found in large areas of the developing world where population pressures are low. increase in demand for pig meat (Fig. ‘harvesting’. most production remains in d) Animal productivity plateaus and feed conversion rates backyard units.500 500 . Production and most prominent near urban centres. production dynamics in the People’s Republic of China.000 .000 2. commercial production units that are more enterprises with expertise in the exploitation of economies developed than integrated crop/livestock farms and that of scale have little problem meeting upsurges in protein generate a surplus for the market.15. feed is brought in from outside and both animal According to the size of the pig holding.250 250 .000). sci. For the country as a whole. tech.000  25. that the traditional smallholder producers have genetic selection of animals for higher yields and more less of a role to play.000 15.000 . 2 World livestock farm income generation for 2002 (all continents except Oceania) (16) . 2). 3). The process is – specialised (5-1.000 Water Fig. Thus. low output production systems typical of processing are driven by multinational enterprise and tend pastoral communities and remote villages beyond the to shift to areas and countries where grain is relatively reach of the urban markets and in which animal cheap – often where agricultural land is plentiful.000 5. Off.000 .5. Organisation for Animal Health) List A diseases (34). The intensification process can be illustrated by pig c) Producers find themselves in areas of high land pressure. 23 (2) a) Low input. the local b) Specialised. with bulk production of protein commodities to supply the regional – industrial (> 1. market. (particularly of poultry.25. int. The subsistence or to coastal port areas which can sustain high levels of farmers keep ruminants. Industrial scale production. This chain of events also explains why efficient feed conversion. processing – backyard production (one to five pigs) and marketing thus form one continuum.472 Rev. such as production is characterised by a rich diversity of livestock in southern Brazil. with the advent of modern livestock production. A consequence of this rapid intensification is. mostly located in a rural livestock remains concentrated in rich countries and a setting. farmers may be production and processing become integrated in a vertical grouped as follows: chain. backyard poultry or other imports by ship (Southeast Asia).000) driven by automation and standardisation. to be moved nearer to the urban centres. This involves the demand from the growing number of megacities in the creation of production environments free of OIE (World world. though processing and marketing operations tend few transition economies (Fig. $ production/km2 0 . provision of balanced nutrition. but intensification matches the exponential reach their limits in all modern production units. however. the USA Corn Belt or the Ukraine – well adapted to environmental stress. or to export to other countries. pigs. The change is irrespective of the geographical setting.

Afghanistan and Republic of China from 1985 to 1999 (40) Pakistan and exported to countries to its west. There is much evidence to suggest that seasonal and tribal ruminant street movement patterns of traditional nomadism and transhumance have been transformed by oil wealth and the and the Arabian Peninsula various changes in livestock production. peste des petits ruminants (PPR). and acting as a corridor for 0 the spread of pathogens (e. Modern telecommunications provide access to Mediterranean basin. e. biosecurity. consider that many important human diseases may have goats and cattle. industrial poultry and pig production intensification and modernisation. old world 100 screwworm (OWS) as well as other forms of myiases and Output shares (percentage) 80 foot and mouth disease (FMD). vaccination. Pastoral livestock spread. tech. with The evolution of the pig production structure in the People’s animals imported from Turkmenistan. rangeland condition. and including the Arabian Peninsula. 4). A number of zoonotic and other diseases are and range condition as it used to be. sheep pox. Agriculture Organization (FAO) (19). and seasonal transhumance/ and emergence: the Eurasian nomadism in response to rainfall and fodder availability. where the principal demand is for sheep to use in religious festivals. If we production mainly involves sheep and. pasture forms an area of particular interest as it presents an availability and market prices. traditional livestock movements in the Arabian Peninsula were related to one of three primary activities: trade and the passage of caravans between Disease ecology markets. which may be pushing the very high number of smallholders out of the market. FMD) (17). with extensive ruminant livestock and localised. to a lesser extent. Off. and widespread subsidies for these grain b) the monogastric livestock sector in East Asia. 5). Epiz. 3 an active role in the international livestock trade. longer followed.g. and have been replaced by more erratic .g. respond to grazing availability (Fig. 23 (2) 473 bluetongue (BT).. especially Saudi Arabia and Kuwait. though to relatively small areas. The that new diseases may emerge in response to the profound main market for live animals in the region is the Gulf States. and eventually enter the human population. Pastoral livestock environment where disease spread frequently goes production is therefore no longer as dependent on rainfall unchecked. Sheep production in the rangelands has emerged as a consequence of changes that took place intensified through the use of crop residues from expanding during the Neolithic era. evolve. the remainder of this review considers how ecological past half century. In the harsh and 1985 1993 1996 1999 often dry environments of Central Asia. 40 creating a narrow east-west connection just south of 20 the Caspian Sea in Iran (Fig. with seasonal The ‘livestock revolution’. particularly in patterns of movement to and from specific areas are no sheep. we have to also accept the reality cultivation and increasing use of supplementary feeds. Rift Valley fever (RVF). changes taking place today (39). however.Rev. Historically. has. Iran has over eighty million small ruminants and is believed to play Fig. multiple stage production systems). stock for sale or slaughter at markets near permanent settlements. coupled with ‘global change’ events and Livestock production in the Arabian Peninsula has been associated risk factors. supported by advances in contraction and expansion as transhumance patterns biotechnology and life sciences (aggregation of production. and production environments and geographical areas: traditional forms of livestock production have been adapted a) the ‘Eurasian ruminant street’ and the Arabian to changing circumstances. Over the Hence. information on rainfall. Feedlot ruminant production Peninsula. modern poultry and dairy plants there has been increasing use of imported animal feed concentrates (33). Traditional seasonal believed to be on the increase in the area. has thus profoundly altered the extensively reviewed in a recent report from the Food and conditions in which livestock diseases may emerge. been expanding in the region for decades. Vehicles are widely used to move animals and transport feed and water The area extending from central Asia to the eastern supplies. The ‘Eurasian ruminant 60 street’ is formed by a high ruminant livestock density area stretching from southern Asia to the Mediterranean basin. The local animal movement is considerable. completely new methods of production changes may affect patterns of disease in two contrasting have been introduced. livestock Year Backyard hog farms Specialised farms Hog enterprises husbandry forms a pivotal role in the economy. sci. mainly imports (animal feeds) have encouraged the processes of with peri-urban. int.

a dichotomy in livestock areas where water and supplementary feed can be production has emerged. 5 5 . 23 (2) Water Unsuitable Sheep density per km2 0 . 200 200 . sci. Off. 21) Water Unsuitable Cumulative grazing availability Available winter only Always available Available summer only Calculated suitability Marginal Always unsuitable Fig. 100 100 . . sheep producers at the other. 2. 50 50 . 5 Cumulative presence of grazing during different seasons along the Eurasian ruminant street (17. 20 20 . protein.474 Rev. with ‘high-tech’ capital-intensive supplied. poultry and dairy units at one extreme. tech. 1 1 . Accordingly. 21) and opportunistic transport to areas with pasture and/or afield (Fig. int. relatively small-scale. 6). ‘low-tech’ dairy and As the human population becomes more urbanised. which traders and producers supply from local as are abilities to afford and implement disease production and/or by importation from further control measures. 10 10 . and transitional. Levels of capital investment towns and cities generate the principal demand for animal in the two systems are obviously very different. 4 Sheep density in the Middle East (17.. Epiz.000 Fig.

considerable temporal and spatial heterogeneity of distance disease dispersal. showed evolutionary rates the highest difference between demand and supply have (1% nucleotide substitution per year in type A and more movement of live animals and thus a higher disease 0. discrepancies. This raises the probability of long. including the provinces of Ankara (An.25 26 . Off. Epiz. other match isolates from the Middle-East.5 6 . by province. Er. 23 (2) 475 In this scenario. as has been shown for FMD type livestock production systems. 7 The number of new outbreaks in Turkey. 7). therefore. indicates that most. type A: 18% nucleotide difference between the isolates taken in 1995 and those taken in International and national level trade and traffic also have 1997) (18).. In the example of FMD may be an indicator of the disease risk that can arise from spread in Turkey. However.).20 21 . both for cattle and small ruminant meat. encountered (e. during which period type O stabilised and was concentrated in 3 major hotspots. Gilbert et al.15 16 . given that provinces with spanning over four decades. The disease persists in understanding of sub-national level disease patterns provinces such as Ankara.Rev. 6 Animal protein production-demand discrepancies in the Middle East.g. int. the urban demand cannot usually be met influencing factors being the structure of the animal by local producers and a substantial transport of live population. tech. The fact that these isolates were found to an effect on local patterns of disease behaviour. and in 1997-2002 (right).30 31 . that meat production-demand revealed by molecular fingerprints of disease agents.40 1990-1996 1997-2002 Fig. sci. the diversity of husbandry practices and the animals is required.10 An. which has a deficit of small requires more information than is currently available.35 36 . and Ezurum. domestic trade in live animals. 2000 (22) 0. which has a surplus. of foot and mouth disease (FMD) type O in 1990-1996 (left).) and Erzurum (Er. vectors and host associations (27). when FMD type O declined. particularly where this concerns data on local gene flows as It would seem. ruminant meat. 11 . genetic analysis of FMD types O and A.6% per year in type O) far below those implied by the transmission risk (publication in preparation by nucleotide differences between the (sub-)lineages M.) . if Water Unsuitable Demandproduction Productiondemand Fig. a fuller O incidence in Turkey (Fig.

This corroborates with the Asia may produce 35% of the global meat production of fact that live animals enter Turkey at the eastern border and 300 million tonnes. and for any given East and South Asia (15). meat pattern formed by the sequence of years forms a trajectory of and milk consumption in East Asia will rise to 50 kg and agricultural intensification for the period under consideration. with relatively increasingly closer links. the data pairs. FMD. Intensification Horn of Africa and the Sudano-Sahelian ruminant implies the creation of relatively disease-free production populations also encourage ruminant disease agents to environments and this condition becomes hard to sustain become more aggressive and may lead to increased exposure when surrounded by abundant smallholder units. or 24% of total world feed demand. Epiz. for domestic product growth of 5. Thus we may plot. These two critical variables. world demand of 2. The thus observed The related FAO cereal balance sheets suggest that by 2015 trajectories of agricultural intensification may now be used to East and South Asia jointly will require 42% of the total explore the patterns of disease risk.9% for East and smallholder density (x-axis) and productivity (y-axis).2 billion will reach 7. CCHF intensification (i. PPR. the Middle East. sci. for each year.g. It is estimated that the feed required in East Asia by 2015 will Figure 8 illustrates the agricultural intensification be 218 million tonnes. including livestock and animal protein from surrogate variables of which statistics are available at the commodities. Denmark). Belgium. the Animal disease risk following rapid shifts in production demand-supply discrepancy triggers the movement of live systems are poorly documented because in most countries animals and presents a risk of disease introduction. 14 kg/capita/year. suffer chronic infections. sheep and goats throughout Central Asia. are then trucked towards the western half of the country where most consumption centres are located. with 88 kg of fresh milk whilst future trends in agricultural development. In East and across a wider geographical area. this increase is unlikely to be pathogens freely circulate and animals become carriers or due to improvements in disease reporting alone. have been projected for the years 2015 and 2030 (5). Furthermore. Over estimate of the density of smallholders. Unofficial records available to the FAO suggest a rising incidence in most of a) the productivity level or degree of production these areas of RVF.379 million tonnes of grain. the Balkans. tech. intensification has been a gradual process. confined production units in which all animals are susceptible and in which major clinical disease problems arise if disease is introduced) Structural changes in the East b) the spatial structure of production units. lasting several decades and involving the entire production sector Not only do environmental changes favour disease spread (e. for half of the population of the world will be concentrated in individual animal production subsectors. running to the year 2015.. whereas the density current world population of 6.2 and of the agricultural population (AgPop) forms a surrogate 8. of humans. and thus comparatively high prevalence between the Eurasian ruminant street. sub-national and international level. extensive systems in which and tick-borne encephalitis. including equivalents and only 7. Trade of live animals is also reported to contribute to the spread of Crimean-Congo haemorrhagic Hence. but indications are that South Asia the rapid establishment of specialised farms and FMD type O may also be broadening its host range and industrial production units mostly takes place in areas with developing a greater affinity for sheep (17). taken as the set of sub-populations of hosts between which microbial Asian livestock sector and the traffic occurs. OWS. trajectories of countries grouped by continent (adapted .6 kg of meat per capita per year. the Netherlands.e. in terms of trade and traffic. The South Asia respectively. The projections presented in a recent study country level: the productivity level can be estimated from the on the future of world agriculture (5) suggest that the output/input ratio (kg meat/animal/year). the and persistence of disease pathogens. one possible way to characterise the likelihood or fever (CCHF) (36). sheep pox. Again. risk of disease emergence For example. low biosecurity. both at where monogastric production systems are now industrial.3% and 3. can be derived agriculture. provides general statistics on trends in world food and productivity level and production structure. BT. With a projected per capita gross country or region. the high densities of small production units. it is speculated that by 2015 East Turkey arrive from the east (18). 23 (2) not all FMD virus strains entering and spreading into With this amount of feed. while the figure for South Asia will show The FAO country statistics are available from 1961 onwards the opposite proportions. a function of: the Middle East and North Africa. or large scale. the productivity levels and labour force dynamics.476 Rev. open. int.3 billion in the years 2015 and 2030 respectively. Off. a high density of smallholders surrounding intensive or industrial production units would create a The FAO has a statistical database (FAOSTAT) that particularly risky situation. an important zoonotic disease affecting risk of disease spread or emergence is to consider this to be cattle.

. Gilbert et al. Off. this applies to Asian countries population levels. North America and Australia had a low where gradual intensification proceeds in the face of and stable AgPop density at the start of the period. and a very significant increase in the AgPop be higher where production is in the process of density. in AgPop density with relatively little productivity increase intensive production units concentrated around (although the increase in productivity in Asia is higher consumption areas. 23 (2) 477 from Bruinsma [5] – publication in preparation by be compared to other regions in the world in relation to M. and are of farmers decreases inversely as a function of gains in characterised by relatively minor overall increases in productivity (Fig. 9a) the proportion are distinct from other regions in the world. The implication is that this area should not the plot of changes in productivity as a function of the 14 12 Chicken production output/input 10 (kg / animal / yr) 8 6 4 2 0 0 100 200 300 400 500 Agricultural population density (people / km2 arable land) Australia South America Asia North America Caribbean Europe Africa Fig.Rev. which are responsible for the gradual than in Africa and projections are that in Asia. 9). the density of smallholders will start to decline in mismatch between increases in productivity and the decades ahead). and in production structure. the fact that the marked difference between the continents. Certainly. 9c) and a bump is observed in AgPop density. The Africa.) .). country in Southeast Asia (Fig. unlike overall productivity increase at national level. mostly as a consequence of generally rising transformation. and East and Southeast Asia in particular. and persisting high density smallholder producers. tech. Very little intensification is not accompanied by a reduction of change in the size of the AgPop is observed in industrial AgPop density suggests that any decline in the number countries and a sharp rise in chicken meat productivity is of producers due to production intensification is seen over the last forty years. 9b). For the same period. outweighed by the increase in farmer numbers resulting developing countries show very little increase in from rising overall populations. Epiz. sci. Firstly. epidemic risk may productivity. Europe and South America have reduced their AgPop and In some countries. The model shows that countries in Asia. demographic growth can be examined further by modelling the intensification trajectory of a hypothetical These trajectories support three main observations. The first and most obvious observation is epidemic risk estimations. int. This implies that the number of productivity alongside a very significant rise in the farmers reaches a peak (Fig. Thirdly. Gilbert et al. with a very high number of Asia and Africa there has been a very significant increase smallholders and a restricted number of large scale. with a logistic population growth (Fig. have steadily increased their productivity since then. Secondly. intensification creates a dichotomy in progressively enhanced the levels of intensification. 8 Change in chicken meat output/input and agricultural population density grouped by continent between 1961 and 2001 (empty circles) and predictions for 2015 to 2030 (full circles) (adapted from Bruinsma [5] – publication in preparation by M.

100 . as 250 .000 underlying forces working in opposite directions.4 0. 5. 500. production must be Fig. then the number of farmers shows a maximum (c).500 . high densities of smallholder producers will remain a reality for a considerable period and that this trend is an inherent characteristic of the Bangkok intensification process in countries with ever increasing human populations. sci. 100 2. 250 5. and a bump is observed in the plot of changes in productivity as a function of the number of farmers (d) (26) number of farmers (Fig.478 Rev. Ho Chi Minh City In Southeast Asia the transformation of animal production is largely a response to. irrespective of the pace of intensification.000 geographical distance to the nearest megacity (24) 25 . particularly where there is Estimated poultry density in Thailand. 10 in the vicinity of urban centres. 23 (2) a) b) 100 10 80 Total population 8 Production per farmer 60 6 40 4 20 2 0 0 0 20 40 60 80 100 0 0. and is driven by.2 0. tech. These results suggest that. 50 1. the growing demand in major urban centres. In fact. the proportion of farmers decreases inversely as a function of gains in productivity (b).1 0. 25 500 . distribution and retail.8 0.6 0. Laos and Vietnam no adequate infrastructure.000 livestock density may be the outcome of two main.000 ..7 0. 2.3 0.9 1 Time Proportion of farmers in the total population c) 50 d) 10 40 Productivity per farmer 8 Number of farmers 30 6 20 4 10 2 0 0 0 20 40 60 80 100 0 20 40 60 80 100 Time Number of farmers Fig.5 0. It follows that the location of poultry and pig production and feed crops is a function of the Poultry density (animals/km2) 0 . land utilisation pattern and 50 . 500 animal protein products are highly perishable and require swift processing. 9 A model of the intensification trajectory of a hypothetical country in Southeast Asia If the total population increases with a logistic growth (a).500 (Figs 10 and 11). int. 9d). 1.000 . The slope of the latter trajectory in the productivity versus AgPop plot is determined by the pace at which the density of smallholders increases in response to general increases in Hanoi human population compared to the pace of the reduction in the number of smallholders as a result of production Hue intensification. Following the upsurge in urban (animals per km2) (24) . Firstly. Epiz. Off.

).Rev. These poultry units may be smallholders and commercial units coexist. 23 (2) 479 140 60 120 50 Mean normalised crop production 100 40 Human and animal density 80 30 60 20 40 10 20 0 0 50 100 150 200 250 300 350 400 450 500 Distance to Bangkok (km) 2 human population (nb/km /10) pigs (nb/km2/10) chicken (nb/km2/10) maize (tons/km2) soybean (10 tons/km2) cassava (tons/km2/2) Fig. the cost of health protection is large-scale commercial units appear to have been an proportional to the size of the area protected. For a subsequent spread of remote environments. Virus introduction from wild creates a decline in the level of agricultural productivity waterfowl is most likely to occur in extensive smallholder along an urban to rural transect. as was invest more to protect their birds because of the economic observed during the HPAI outbreaks in 2003 in the gains acquired when keeping more healthy and productive Netherlands. sci. Commercial production enterprises will in preparation by M. with high input/high production units. irrespective of important risk factor and may have fuelled the epidemic. This is located wherever it is considered convenient. Epiz. It follows that biosecurity contraction of animals into peri-urban environments. Similarly. the commercial broiler chains may modern poultry production units mostly count well have played a major role in the ‘seeding’ of HPAI many thousands of birds and produce low-cost animal H5N1. The highest outbreak risk is thus likely to be where protein of standard quality. The return from animal health investment rapidly farmers for recreational purposes in the vicinity of decays in remote areas. 11 Spatial distribution of humans. int. For example. confirmed by exploratory quantitative analyses of the recent HPAI distribution which show the distribution The heterogeneity in the production structure of poultry of avian flu outbreaks to be concentrated at the interface of holdings is also reflected in the differential animal health extensive and commercial poultry production (publication protection strategies. 2001 (24) demand. livestock and feed-crops around Bangkok. measures progressively improve near a city. live animals. the disease some of the more sizeable holdings must be infected. Off. In this way. may be considered in relation to the epidemiology of the which is forcing rural people to disperse into the more highly pathogenic avian influenza (HPAI) H5N1 epidemic remote land areas hitherto considered less attractive. infection. there is a progressive concentration and the number of animals kept. acting at the same time. Gilbert et al. Also. . there is an opposite. poultry kept by smallholders or hobby livestock. and feed between small pronounced in situations where agricultural technologies commercial-scale holdings promotes secondary spread of take full advantage of the economies of scale. and therefore. areas with a higher density output systems more prominent in the peri-urban settings of poultry smallholders are more prone to whilst extensive low input systems are typical of the more the initial spread of infection. This in Asia in 2003/2004. resulting from the progressive increase in This geographic stratification in disease protection and risk population and land pressure around expanding cities. Secondly. whereupon the considerable movement This productivity gradient becomes particularly of people.. centrifugal force. tech.

perishable meat and dairy commodities and waste products increase the number of occupational hazards. Nipah/Hendra-like viruses are now found to occur in a Agricultural intensification will be fraught with structural number of countries where intensification is widespread. problems such as unchecked land pressures and including Australia. it would perhaps be advisable to pay fuller be increasing its range in South Asia (41). Cambodia and imbalances in socio-economic development. and methodological tools are available concerns are largely the product of human activity. there is evidence that well as in veterinary health and food safety hazards. Maria-Grazia Solari and animals and/or humans: Sarah Wint for their most helpful support and comments. In parallel. food poisoning and of course flare-ups of zoonotic change. Apart from SARS. Of particular The potential future role concern is the progressive ‘urbanisation’ of animal production and processing. Hence. etc. new forms of disease and microbial adaptation. critical contacts with wildlife animals. Raffaele Mattioli. 23 (2) In addition to the unstable avian influenza situation in East It is likely that new pandemics will occur in the future. Malaysia.480 Rev. Singapore. Similarly. it may be helpful Jim Hancock. The missing link is how Acknowledgements pathogens currently restricted to wildlife or domestic animals will evolve toward humans in response to abrupt The authors wish to thank David Bourn. Pierre Gerber. sci. there is evidence that changes in food RNA viruses in animal reservoirs will be implicated and demand and agricultural practices play a role in a number that food and agricultural practices will play an important of other zoonotic infections. the processes of environmental change (e. Lessons learned from epidemics of existing pathogens have highlighted Disease ecology shows us that disease spread and the some of the factors associated with the spread of a disease emergence of zoonotics and other veterinary public health within a population. attention to the inherent epidemiological instability that is caused by innate characteristics of livestock development and food chains in some parts of the world. environmental changes. int. though the approach is still in its infancy.. infections. a) true animal pathogens b) pathogens confined to an animal reservoir but sometimes producing limited human infection c) well established multiple host and zoonotic pathogens d) pathogens increasingly affecting human populations but moving towards extinction e) transient agents which evolve into human pathogens f) full blown human pathogens. For all these Bangladesh (2). Maarten Hoek. tech. In this context. also the general public is The study of the ecology of invasive diseases may arguably at risk through the microbial contamination of water assist in identifying the links between environmental sources. of which role in the emergence of disease in human populations as the animal origin remains uncertain. demographic pressures. to consider the full spectrum of pathogens that affect Peter Roeder. the to explore these patterns (1). that and Southeast Asia. Japanese encephalitis appears to reasons. some of solution to these problems is also a matter of human choice. Off. Epiz. the rate at which climate change or deforestation may occur.g. . Not only does the enhanced of disease ecology contact of people with live animals. Awatif Siddig.) have also been quantified.

S’agissant de l’émergence de zoonoses dans le bétail. par exemple) ont vraisemblablement peu de choses en commun avec les agents zoonotiques connus et déjà bien établis. voire leur irruption au sein de la population humaine. modifient le taux de contact de l’hôte. b) la dynamique de la production avicole en Asie du Sud-Est. Les agents pathogènes du bétail subissent des pressions liées à la dynamique de la production. Gilbert. à la surexploitation des terres et aux déséquilibres causés par la production intensive ont créé une situation épidémiologique instable. K. le syndrome respiratoire aigu sévère ou les virus émergents de type A de la grippe. à la transformation des protéines et au commerce de détail. Off. 23 (2) 481 L’origine écologique des zoonoses J. de Balogh & W. l’urbanisation ou la mondialisation) et du climat. Ce processus trouve son illustration dans deux situations : a) le développement de l’élevage dans la « ceinture eurasienne des ruminants » (une zone qui s’étend de l’Asie centrale à l’est du bassin méditerranéen) et dans la péninsule arabique limitrophe . les auteurs estiment que le bouleversement des pratiques agricoles joue désormais un rôle prépondérant et détermine les conditions qui régissent l’évolution et la propagation des agents pathogènes zoonotiques. . les facteurs environnementaux associés à la démographie. Wint Résumé Bien que d’origine zoonotique. qui.Rev. Slingenbergh. comme en attestent la forte hausse de l’influenza aviaire hautement pathogène en 2004 et la présence des principaux foyers dans une zone où l’on trouve à la fois une forte densité de petits élevages avicoles et de grands élevages périurbains à vocation commerciale. Par conséquent. int. Mots-clés Accroissement démographique – Changement écologique – Écologie de la maladie – Épidémiologie – Intensification de l’agriculture – Production animale – Urbanisation – Zoonose émergente. dans la mesure où ces nouveaux agents ont simplement traversé une phase zoonotique passagère avant de s’adapter à l’homme. les agents pathogènes ou infectieux qui menacent la santé publique mondiale (le virus de l’immunodéficience humaine.. la taille des populations et/ou les flux microbiens dans la chaîne alimentaire. l’émergence des pathologies pourrait être décrite comme une réaction évolutive aux modifications de l’environnement (y compris aux facteurs anthropogènes comme les pratiques agricoles. elle pourrait néanmoins être déclenchée ou favorisée par des facteurs exogènes tels que des changements dans l’exposition humaine. en combinant leurs effets. M. tech. sci. Epiz. Dans ces deux cas. Bien que l’évolution vers la transmission de personne à personne soit tributaire des caractéristiques biologiques de l’agent pathogène.

síndrome respiratorio agudo severo o virus emergentes de la influenza de tipo A. Gilbert. tengan poco en común con otros agentes ya conocidos y descritos. una serie de factores ambientales relacionados con la demografía. presiones que en conjunto modifican parámetros tales como la tasa de contacto con los animales hospedadores. int. Dos estudios de casos ilustran este proceso: a) desarrollo ganadero en el ‘corredor euroasiático de rumiantes’ (que se extiende desde el Asia Central hasta la cuenca mediterránea oriental) y la vecina Península Arábica. . de la que da muestra el rebrote de influenza aviar altamente patógena acaecido en 2004. entre otros los de origen antrópico como los nuevos procedimientos agrícolas. b) dinámica de la producción avícola en Asia Sudoriental. Aunque la adquisición evolutiva de la capacidad de transmisión de persona a persona depende de las características biológicas del microorganismo. la globalización o el cambio climático. el tamaño de la población y/o los movimientos del microbio en la cadena alimentaria. los autores postulan que la modificación de las prácticas agrícolas se ha convertido en el principal factor determinante de las condiciones en que un agente zoonótico evoluciona. En ambos casos. M. 23 (2) Génesis ecológica de las enfermedades zoonóticas J. a pesar de su origen zoonótico. sci. cuyos principales focos se localizaban en áreas donde coexisten zonas con gran densidad de minifundios avícolas y grandes explotaciones periurbanas de carácter industrial. Off. Los patógenos del ganado están sometidos a presiones resultantes del dinamismo de las actividades de producción. Wint Resumen Es muy posible que ciertos patógenos o infecciones que amenazan la salud del hombre a escala mundial (virus de la inmunodeficiencia humana. Slingenbergh. Epiz.. de Balogh & W. puesto que esos nuevos agentes simplemente han pasado por una fase zoonótica transitoria antes de adaptarse al ser humano. En este sentido.482 Rev. En lo que concierne a las nuevas enfermedades zoonóticas del ganado. por ejemplo). Palabras clave Cambio ecológico – Crecimiento demográfico – Ecología de las enfermedades – Epidemiología – Intensificación agrícola – Producción animal – Urbanización – Zoonosis emergente. K. la urbanización. cabe describir la aparición de nuevas enfermedades como una respuesta evolutiva a los cambios del medio. se propaga y acaba afectando a poblaciones humanas. factores externos como un cambio en los niveles de exposición con el hombre podrían muy bien desencadenar o favorecer esa adaptación. la demanda de tierras y los desequilibrios ligados a la intensificación productiva han desembocado en una situación epidemiológica inestable. tech. tratamiento de las proteínas y venta al por menor.

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