Chlamydial infections
2.8.1 EHRLICHIA AND ENVIRONMENT
From the entomological point of view,Ehrlichiahas a sylvanic zoonotic cycle but is also able to spread in urban areas where domestic animals for instance dogs and cats live in close proximity to humans (Comer et al., 2001). Worldwide modern urban areas are highly populated due to migration from rural areas and foreign countries based on economic factors, increased mobility and continuous development. As a result, urban zoonoses increase due to homelessness, the decline of inner-city neighbourhoods, the increase in immonosuppressed individuals and additional complex factors (Olano and Walker, 2002).
The reasons for the increase in these urban zoonoses are multifaceted. However, urban areas, due to their focal nature, also provide a better strategic control or prevention through physician awareness and public health surveillance support, in contrast to sylvanic or agricultural rural areas, where wildlife is almost uncontrollable.
In addition, tick species that were not classified as zoonotic vectors have been recently recognized as such (e.g.,Amblyomma americanum) (Childs and Paddock, 2003) and subclinical infected companion animals
Fritzet al.(2005) reported two cases of Ehrlichosis in California during a period of two years (1997– 1999). The residence area was densely populated byIxodes pacificus ticks with over 85% of the study participants reporting tick contact in the preceding 12 months. However, the prevalence ofEhrlichiaand Anaplasmain the tick population was very low, explaining the low disease frequency among humans. In South Korea, a serological survey was conducted designed to evaluate the presence of four canine pathogens among them two Ehrlichiae genera, Anaplasma phagocytophilum and Ehrlichia canis, on rural hunting and urban shelter dogs (Lim et al., 2010). Dogs used for wild boar and pheasant hunting revealed a prevalence of 18.8% forA. phagocytophilumand 6.1% forE. caniswhile all urban stray dogs (a total of 692 dogs) were seronegative for both pathogens. This study indicates that rural hunting dogs are more exposed to vector-borne diseases.
To strengthen these results, in Brazil, dogs kept in apartments were compared with dogs with yard access for the presence of ectoparasites and hemoparasites. Not surprisingly, indoor dogs harbor ectoparasites (three tick types) at a lower prevalence than yard access dogs (2–12% compared to 14–35%
respectively). Consequently, indoor dogs did not reveal hemoparasites at all and yard access dogs tested positive forEhrlichia canis(16%) and another protozoan pathogenBabesia canis(2%) (Soareset al., 2006).
The emergence of new canine tick-transmitted diseases results from several factors: expansion of tick range into urban and semi-urban areas, movement of infected dogs into non-endemic areas and the introduction of novel molecular techniques for diagnosis and pathogen identification (Shawet al., 2001).
Mananganet al.(2007) used a logistic regression model to compare the influence of physical environment, land cover composition, and landscape heterogeneity on distributions of A. phagocytophilum and E.
chaffeensis in white-tailed deer, at multiple spatial extents in the Mississippi alluvial valley. The Figure 2.8.1. Ehrlichiaspp. distribution in various animals and tick transmission
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Mississippi alluvial valley faces frequent flooding, and though it was historically covered by bottomland forests, it is presently dominated by agriculture, while the remaining forests are highly fragmented. Using white-tailed deer seropositivity results for these two pathogens (from 1981 to 2005), deer density, elevation, land cover, normalized difference vegetation index (NDVI), hydrology, and soil moisture, they found that the best fitting model was obtained for E. chaffeensis (90.5% sensitivity) compared to A.
phagocytophilum (only 68% sensitivity). The lower fitting model for Anaplasma phagocytophilum was speculated to be a result of differences in the natural histories of tick vectors of this pathogen.
In a more extensive study, covering the area of southeastern United States, Wimberly et al. (2008) compared several spatial modeling approaches to predict the geographic distribution of Ehrlichia chaffeensis and Anaplasma phagocytophilum based on extended environmental modeling, such as logistic regression combined with spatial autocorrelation (pathogen tendency to cluster in space) and heterogeneity (environmental spatial variation). The results showed that the model prediction of E.
chaffeensis based only on spatial autocorrelation had the best fit (Figure 2.8.2), while for A.
pagocytophilum with its more complex zoonotic cycle and weak spatial pattern the combined model (spatial autocorrelation and heterogeneity) had the best fit (Figure 2.8.3).
The complexity in modeling Ehrlichia chaffeensis infection risk based on its prevalence in tick population was investigated by a deterministic model (prevalence in tick populations with spatial considerations) (Gaff and Schaefer, 2010). The complex nonlinear system interactions showed that areas that would be endemic in isolation may or may not sustain the disease depending on the surrounding habitat such as: control efforts shown to be far more effective when applied in wooded habitats than in neighboring grassy habitats and that additional increase in habitat fragmentation play a major role in predicting the endemicity of an HME (human monocytic ehrlichosis) outbreak.
Sinski (1999) in a review on vector-borne diseases in Poland pointed to the environmental crucial role of changes in farming systems in the Mazury Lakes district in which a great land area had been left under grassland and pasture favoring susceptible rodent species to become competent reservoirs. This phenomenon was observed in the whole of Europe alongside intensified agriculture.
Forest workers are expected to be at risk for Ehrlichosis. Blood samples of 4,368 forestry workers in the State of Baden-Wuertternberg (B-W), southwestern Germany, were tested for seroconversion against Ehrlichia spp. (genogroup E. phagocytophila) and other tick-borne pathogens (Borrelia burgdorferi sensu lato, TBE-virus) in parallel to the collection of 12,327 ticks (Ixodes ricinus) and analysis by PCR and genotyping (RNA and DNA) for the prevalence rate of these pathogens in this geographical area (Oehmeet al., 2002). The authors stated that the 5 to 16% prevalence ofEhrlichia spp. antibodies and the 2.6 to 3.1% tick prevalence suggests “that ehrlichiosis plays a role as a tick-borne disease in Germany, but as long as no clinical data are available, this will remain unclear”.
Contact with forest parts, especially sitting and considerable contact with wood parts, results in a greater acquisition of nymphs, in spite of protective wear (hiking boots, hiking sandals, or running shoes) (Lane et al., 2004). In a study conducted in southern Scotland (during 1996–1999) in three habitats for presence of the tick Ixodes ricinusas a vector ofEhrlichia phagocytophila infection, coniferous woods provided the highest risk of attachment by ticks, possibly due to ticks concentration on the grassy rides rather than other factors for example host or climatic (Walkeret al., 2001).
Direct contact with animals is the highest risk factor to contract Ehrlichiosis. Among such predisposed groups are: veterinarians, slaughterhouse and zoo workers, farmers and hunters. Deutzet al.(2003) used seroconvertion test to evaluate human exposure to several zoonotic agents among them Ehrlichia, compared hunters vs. other high risk occupational groups in south-east Austria. High seroprevalence
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An interesting environmental aspect related to tick eradication by chemical means was outlined by Eisler et al., (2003). The authors emphasized the importance of anti-ticks and tsetse pyrethroid insecticide use to prevent cattle loss (between US$ 4–5 billions/year) in Africa. However, beside its positive effect there are several risk factors that from the environmental point of view are significant: 1. uncontrolled application of pyrethoids can lead to acaricide resistance in tick populations (Bruce and Wilson, 1998); 2. insecticides can decimate invertebrate fauna responsible for cattle dung breakdown and subsequent incorporation in soil (Dantas-Torres, 2008) and 3. reduction in ticks’numbers attaching to cattle can also lead, paradoxically, to an increase in susceptibility to tick-borne diseases (Mahoney and Ross, 1972; Norval, 1992).
Figure 2.8.2. Predicted endemicity probabilities forEhrlichia chaffeensisin the southeastern United States obtained from five Bayesian hierarchical models (Wimberlyet al.(2008), with permission from International Journal of Health Geographics)
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Grayet al.(2009) in a review article presented some evidences of climate impact on zoonotic tick-borne diseases affecting vector biology and disease transmission. The geographic extension of the vector tick Ixodes ricinus(and alsoDermacentor reticulates) and increased prevalence of tick-borne encephalitis in Sweden could be partially related to climate change too (Figure 2.8.4). Warmer winters and hotter summers in this region may increase the seasonal activity of these vectors. The authors suggested that Figure 2.8.3. Predicted endemicity probabilities forAnaplasma phagocytophilumin the southeastern United States obtained from five Bayesian hierarchical models (Wimberlyet al.(2008), with permission from International Journal of Health Geographics)
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2.8.2 REFERENCES
Atwill, E.R., Mohammed, H.O., Lopez, J.W., Mc Culloch, C.E. & Dubovi, E.J. (1996) Cross-sectional evaluation of environmental, host, and management factors associated with risk of seropositivity toEhrlichia risticiiin horses of New York state.Am. J. Vet. Res.57(3), 278–285.
Bjöersdorff, A., Bergström, S., Massung, R.F., Haemig, P.D. & Olsen, B. (2001)Ehrlichia-infected ticks on migrating birds.Emerg. Infect. Dis.7, 877–879.
Bruce, D. & Wilson, A. (1998) A trial to control or eradicateAmblyomma hebraeumticks and heartwater on three ranches in Zimbabwe.Ann. N. Y. Acad. Sci.849, 381–383.
Childs, J. E. & Paddock, C.D. (2003) The ascendancy ofAmblyomma Americanumas a vector of pathogens affecting humans in the United States.Annu. Rev. Entomol.48, 307–337.
Comer, J.A., Paddock C.D. & Childs, J.E. (2001) Urban zoonoses caused by Bartonella, Coxiella, Ehrlichia, and Rickettsiaspecies.J Vector Borne Dis1, 91–118.
Dantas-Torres, F. (2008) The brown dog tick,Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae): from taxonomy to control.Vet. Parasitol.152, 173–185.
Deutz, A., Fuchs, K., Nowotny, N., Auer, H. Schuller, W., Stunzner, D., Aspock, H., Kerbl, U. & Kofer, J. (2003) Sero-epidemiological studies of zoonotic infections in hunters-comparative analysis with veterinarians, farmers, and abattoir workers.Wien. Klin. Wochenschr.115, 61–67.
Dumler, J.S. & Bakken, J.S.(1995) Ehrlichial diseases of humans: emerging tick-borne infections.Clin. Infect. Dis.20, 1102–1110.
Eisler, M.C., Torr, S.J., Coleman, P.G., Machila, N. & Morton, J.F. (2003) Integrated control of vector-borne diseases of livestock–pyrethroids: panacea or poison?Trends Parasitol.19, 341–345.
Eremeeva, M.E., Karpathy, S.E., Levin, M.L., Caballero C.M., Bermudez, S.et al.(2009) Spotted fever rickettsiae, EhrlichiaandAnaplasma, in ticks from peridomestic environments in Panama.Clin. Microbiol. Infect.15,12–14.
Figure 2.8.4. Tick distribution (white squares) in northern and central Sweden during two periods: (a) before 1980 and (b) in 1994–5. Black line frame represents the area studied. [with permission from Lindgrenet al., 2000,Environ. Health Perspect.]
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Fritz, C.L., Bronson, L.R., Smith, C.R., Crawford-Miksza, L., Yeh, E. & Schnurr, D. (2005) Clinical, epidemiologic, and environmental surveillance for ehrlichiosis and anaplasmosis in an endemic area of northern California.
J. Vector Ecol.30, 4–10.
Gaff, H. & Schaefer, E. (2010) Metapopulation models in tick-borne disease transmission modelling.Adv. Exp. Med.
Biol.673, 51–65.
Gray, J.S., Dautel, H., Estrada-Peña, A., Kahl, O. & Lindgren, E. (2009) Effects of climate change on ticks and tick-borne diseases in Europe.Interdiscip Perspect Infect Dis2009, 12 pp doi:10.1155/2009/593232.
Lane, R.S., Steinlein, D.B. & Mun J. (2004) Human behaviors elevating exposure toIxodes pacificus(Acari: Ixodidae) nymphs and their associated bacterial zoonotic agents in a hardwood forest.J. Med. Entomol.41, 239–248.
Lim, S., Irwin, P.J., Lee, S., Oh, M., Ahn, K.et al.(2010) Comparison of selected canine vector-borne diseases between urban animal shelter and rural hunting dogs in Korea.Parasit Vectors3, 32.
Lindgren, E., Tälleklint, L. & Polfeldt, T. (2000) Impact of climatic change on the northern latitude limit and population density of the disease-transmitting European tickIxodes ricinus. Environ. Health Perspect.108, 119–123.
Mahoney, D.A. & Ross, D.R. (1972) Epizootiological factors in the control of bovine babesiosis.Aust. Vet. J.48, 292– 298.
Manangan, J.S., Schweitzer, S.H., Nibbelink, N., Yabsley, M.J., Gibbs, S.E.J. & Wimberly, M.C. (2007) Habitat factors influencing distributions ofAnaplasma phagocytophilum andEhrlichia chaffeensisin the Mississippi Alluvial Valley.Vector Borne Zoonotic Dis.7, 563–573.
Norval, R.A.I.et al.(1992) The epidemiology of Theileriosis in Africa, Academic Press.
Oehme, R., Hartelt, K., Backe, H., Brockmann, S. & Kimmig, P. (2002) Foci of tick-borne diseases in Southwest Germany.Int. J.Med. Microbiol.291, 22–29.
Olano, J.P. & Walker, D.H. (2002) Human ehrlichioses.Med. Clin. North Am.86, 375–392.
Parola, P. & Raoult, D. (2001) Ticks and tickborne bacterial diseases in humans: an emerging infectious threat.Clin.
Infect. Dis.32, 897–928.
Shaw, S.E., Day, M.J., Birtles, R.J. & Breitschwerdt, E.B. (2001) Tick-borne infectious diseases of dogs.Trends Parasitol.17, 74–80.
Sinski, E. Enzootic reservoir for newIxodes ricinus-transmitted infections. (1999)Wiad Parazytol45, 135–42.
Soares, A.O., Souza, A.D., Feliciano, E.A., Rodrigues, A.F.S. F., D’Agosto, M. & Daemon, E. (2006) Evaluation of ectoparasites and hemoparasites in dogs kept in apartments and houses with yards in the city of Juiz de Fora, Minas Gerais, Brazil.Rev Bras Parasitol Vet15, 13–16.
Vale, G.A. & Grant, I.F. (2002) Modelled impact of insecticide contaminated dung on the abundance and distribution of dung fauna.Bull. Entomol. Res.92, 251–263.
Walker, A.R., Alberdi, M.P., Urquhart, K.A. & Rose, H. (2001) Risk factors in habitats of the tickIxodes ricinus infuencing human exposure toEhrlichia phagocytophilabacteria.Med. Vet. Entomol.15, 40–49.
Wen, B., Rikihisa, Y., Yamamoto, S., Kawabata N. & Fuerst, P.A. (1996) Characterization of the SF Agent, anEhrlichia sp. isolated from the flukeStellantchasmus falcatus, by 16s rRNA base sequence, serological, and morphological analyses.Intern. J. System. Bacteriol.46,149–154.
Wimberly, M.C., Baer, A.D. & Yabsley, M.J. (2008) Enhanced spatial models for predicting the geographic distributions of tick-borne pathogens.Int J Health Geogr7, 1–15. doi:10.1186/1476-072X-7-15.
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