Invited review
Drivers for the emergence and re-emergence of vector-borne protozoal and bacterial diseases

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Abstract

In recent years, vector-borne parasitic and bacterial diseases have emerged or re-emerged in many geographical regions causing global health and economic problems that involve humans, livestock, companion animals and wild life. The ecology and epidemiology of vector-borne diseases are affected by the interrelations between three major factors comprising the pathogen, the host (human, animal or vector) and the environment. Important drivers for the emergence and spread of vector-borne parasites include habitat changes, alterations in water storage and irrigation habits, atmospheric and climate changes, immunosuppression by HIV, pollution, development of insecticide and drug resistance, globalization and the significant increase in international trade, tourism and travel. War and civil unrest, and governmental or global management failure are also major contributors to the spread of infectious diseases. The improvement of epidemic understanding and planning together with the development of new diagnostic molecular techniques in the last few decades have allowed researchers to better diagnose and trace pathogens, their origin and routes of infection, and to develop preventive public health and intervention programs. Health care workers, physicians, veterinarians and biosecurity officers should play a key role in future prevention of vector-borne diseases. A coordinated global approach for the prevention of vector-borne diseases should be implemented by international organizations and governmental agencies in collaboration with research institutions.

Introduction

Diseases transmitted by arthropod vectors are of major importance to the health of humans and animals globally. A wide number of infectious agents, hosts and vectors are involved with these diseases and their epidemiology. Disease patterns differ from one geographic zone to another, and may change over time due to a plethora of factors. The objective of this review is to evaluate the different causes responsible for the emergence and re-emergence of vector-borne protozoal and bacterial diseases and describe how major drivers affect the patterns of their local and global distributions.

Emerging pathogens include infectious agents that have been described in other regions and imported into areas, where they were previously not known; agents that were constantly present in the affected area on a low level or in a different host and due to some change have become more widely spread in the population under concern; or organisms that were previously not recognized and have been identified and associated with a new disease or an illness with a previously unknown etiology. Accidental importation of disease vectors such as tick species or mosquitoes from one area to another could ultimately be responsible for the spread of diseases to new regions. Conversely, transmission of naive domestic or wildlife animals into an endemic region for disease such as piroplasmosis has resulted countless times in epidemic outbreaks (Caracappa, 1999, Hofle et al., 2004). The advances in molecular biology during the last two decades have led to the discovery of new vector-borne pathogenic organisms. Most of the Bartonella species were not known until 10–15 years ago. These arthropod-transmitted bacteria were associated with disease syndromes, such as cat scratch disease, bacillary angiomatosis, peliosis hepatis and endocarditis (Breitschwerdt and Kordick, 2000). Lyme disease, the most prevalent vector-borne disease in North America emerged just over 20 years ago as a new disease with a recognized borrelial causative agent (Benach et al., 1983). However, molecular detection of historical specimens indicated that this infection has been circulating in North America and Eurasia for centuries prior to the recognition of the disease as a major pathogen of humans and dogs (Marshall et al., 1994, Matuschka et al., 1996, Hubbard et al., 1998).

Newly described and older ehrlichial organisms have been recently reclassified within the family Anaplasmataceae on the basis of phylogenetic analysis of gene sequences (Dumler et al., 2001). The expansion of the Anaplamataceae family has included several zoonotic emerging ehrlichial pathogens recognized only in the last two decades. The tick-borne Ehrlichia ewingii and Ehrlichia chaffeensis were described in humans and dogs in North America (Anderson et al., 1991, Buller et al., 1999). These newly described pathogens appear to be restricted in their geographic spread by the presence of appropriate vector ticks. Anaplasma phagocytophilum (previously Ehrlichia phagocytophilum/Ehrlichia equi) has a wider known geographic spectrum and is associated with disease in several animal species including dogs, horses, ruminants, and recently also in cats (Bjoersdorff et al., 1999). It emerged in the last decade as a human pathogen in North America, Europe and some parts of Asia, and is frequently associated with the presence of rodent reservoir hosts (Chen et al., 1994, Parola, 2004).

Vector-borne infections transmitted from wildlife reservoir species to domestic animals or humans are of major concern. New pathogens that may jump the species barrier and be transmitted from one host to another are a constant threat to human and animal welfare. Borrelia burgdorferi, Babesia microti and A. phagocytophilum are zoonotic pathogens which are clearly associated with sylvatic cycles of infection involving wild rodents and ticks. These pathogens may be found concomitantly in mammalian hosts or ticks (Krause et al., 2002, Adelson et al., 2004). A less well known tick-transmitted organism which emerged as a pathogen of cats during the 1970s is the piroplasm Cytauxzoon felis. It infects bobcats (Lynx rufus) asymptomatically in North America, while causing a violent and frequently fatal hemolytic disease when infecting domestic cats (Wagner, 1975, Glenn et al., 1983, Meinkoth et al., 2000).

Re-emerging pathogens are those organisms that have re-appeared in locations from which they have previously disappeared or radically decreased in prevalence. The re-emergence of vector-borne pathogens is often related to changes in the environment, the pathogen, or the host. For instance, the phenomenon of malaria re-emergence is frequently related to changes that affect the spread of the mosquito vectors (Tyagi, 2004), the development of drug-resistant parasites (Sharma, 1996), or human migration (Marques, 1987). The epidemiology of vector-borne diseases is often associated with other events affecting the populations that are exposed to the infectious organisms. Visceral leishmaniasis caused by Leishmania infantum in the Mediterranean basin was traditionally predominantly a disease of young children. The name of the causative agent of this disease reflects the predilection to infants. However, immunosuppressed adults are apparently highly susceptible to the development of clinical visceral leishmaniasis. With the spread of HIV into Europe during the last 25 years, a current major risk group for visceral leishmaniasis in southern Europe is HIV-positive people (Desjeux and Alvar, 2003).

Some outbreaks of protozoal vector-borne diseases appear mysterious at this time and require further research for elucidation and basic understanding of their transmission mechanisms, epidemiology and environmental drivers responsible for their emergence. The recent detection of cutaneous leishmaniasis in red kangaroos in Australia's Northern territory is posing a potential threat to humans and animals (Rose et al., 2004). Australia has previously been considered free of endemic Leishmania species and also of suitable sand fly vectors for the transmission of leishmaniasis (Stein and Dyce, 2002, Rose et al., 2004). A somewhat comparable puzzling situation is present in the eastern USA, where kennel dogs infected with zoonotic L. infantum have been found in several states without known vectors or autochthonous human cases, which are usually present, where active transmission of visceral leishmaniasis occurs (Gaskin et al., 2002, Rosypal et al., 2003). The vector-competence of a local sand fly species is currently being investigated (Ostfeld et al., 2004).

The following sections will discuss the major impacts of vector-borne zoonotic, human and veterinary diseases and the drivers for their emergence and re-emergence. A cause and effect approach will be utilized to analyze the impact of the different drivers on the occurrence and spread of infections responsible for some of the world's most common causes of mortality, such as malaria, or economic losses with diseases leading to human disability or severe livestock production losses (Fig. 1).

Section snippets

Major impacts of vector-borne diseases

The costs incurred due to bacterial and protozoal vector-borne infectious diseases are numerous and diverse. They range from economic losses related to production of farm animals to disability and loss of work years and most severely to the loss of human lives. The drivers influencing vector-borne diseases, can therefore, have devastating effects upon the lives of people of every nationality or socioeconomic class.

Major drivers for the emergence and re-emergence of vector-borne protozoal and bacterial organisms

The ecology and epidemiology of vector-borne diseases are affected by the ‘disease triangle’ comprising three major factors. These include the pathogen, the host (human, animal or vector) and the environment consisting of physical, biological and socioeconomic aspects. The interrelations between these three factors depend on the sensitivity of each factor and the rate of exposure to the other two factors (Sutherst, 2004). In this section, a simplistic approach was carried out to describe the

Scientific advances, conclusions and future prospects

The complex association between disease drivers such as changes in weather, pollution or global travel, and their health and financial impacts is gradually being elucidated by research. Epidemiologic tools and techniques for the research of infectious diseases have improved significantly in the last few decades. The use of risk analyses, geographic information systems (GIS), remote-sensing technologies and climate models in research has provided tools for the expansion of epidemic knowledge,

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