PASTEURELLA AND ENVIRONMENT (FIGURE )

In humans, numerous reported cases revealed thatP. multocidas’source is domestic or wild carrier animals (e.g., pets such as dogs and cats) based on a correlation between applied antibiotics in animal farms and these airborne bacteria’s resistance to these specific antibiotics. According to an aerosol spread study, the authors concluded that a 250 to 500 m radius from source is an area of increased risk of infection mainly by dust as the bacteria carrier (Muller and Dinter, 1988). Water has been also shown to carry this pathogen.

In an outbreak in Nebraska, besides carcasses of dead waterfowls, water samples from several wetlands were found positive for the presence ofP. multocida(Price & Brand, 1984). In terms of time, Blanchong et al.(2006) suggested thatP. multocida, in spite of its presence in wetland, was not isolated after 7 weeks since the initial outbreak, indicating that wetlands are unlikely to serve as a long-term reservoir for P.

multocida. P. multocida was isolated even from dental unit waterlines, making direct contamination through open dental procedures a possible health risk (Göksayet al., 2008). Laneet al.(1992) reported an outbreak of Pasteurollosis in cattle due to sewage and effluents flood irrigation of grass pastures following

clay.P. multocidawas found to survive the longest time period of.1 year under increased protein (175 mg/ml) and NaCl (.0.5%) presence. Other parameters such as clay, sucrose and pH did not play a significant role in the bacteria’s survival. An interesting observation, supported by other studies, showed a rapid decline of this pathogen at low temperature (,3°C). Temperature dependent survival was in accordance with other reports that showed growth of this pathogen between 12 to 43°C (Wilson & Miles, 1975). In contrast,P. multocidainoculated in soil was shown to survive best at 3°C (Dimov, 1964). Winter is the main season of waterfowl infection and death, which is at odds with this pathogen’s survival data at low temperatures. Some explanations for this discrepancy were presented based on a large quantity of excreted bacteria and high density of waterfowl in close proximity. However it should be remembered that the external temperature of these avians’ skin is much higher than 3°C and the attached bacteria can survive for prolonged time periods. Another point that possibly explains this inconsistency is the divergence between soil, water and bacteria interactions. Bacteria are able to form biofilms on soil particles that increase their viability compared to the water free-state in which microorganisms are much more vulnerable (Armonet al., 1997). However, the species Pasteurella haemolyticahave been isolated from grass, water and straw bedding samples collected from two grazing fields in use by sheep, and from ewes affected with mastitis.P. haemolyticasupported by colder, wetter weather had prolonged survival time in environment, data confirmed also by laboratory experiments with distilled water, phosphate-buffered saline, Todd-Hewitt broth and ewe’s milk kept at 4°C (Burriel, 1997). Ytrehuset al.(2008) reported on a Musk ox’s fatal epizootic pneumonia outbreak (caused by P. multocida), triggered by extraordinary weather conditions, characterized by high temperatures and humidity, a pattern directly linked to global warming. According to these authors, these unusual conditions seem to modify musk ox susceptibility to infection being the decisive factors in the disease outbreak.

Figure 2.16.1. Pasteurella multocidainfection cycle and possible environmental entangled factors

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AP. multocidastrain isolated from mangrove sediment was reported to biodegrade a certain chemical, dimethyl terephthalate (DMT), commonly used in polyester production (Li & Gu, 2006). Another Pasteurella spp. isolated from activated sludge was reported to biodegrade polyaromatic hydrocarbons (PAHs) such as phenanthrene, fluoranthene and pyrene (Seˇpicˇ et al., 1997, 1998). Recently, a Pasteurella sp. was reported to be able to multiply in soils contaminated with cadmium. This particular species precipitated Cd⁺²in the form of CdCO3in these cadmium contaminated soils (Liet al., 2010).

In connection with this biochemical characteristic, Russian scientists studied large areas including the semi-desert and desert areas of Kazakhstan and Uzbekistan, as well as the steppe and forest-steppe regions of Russia and Mongolia for a relationship between infections and environmental chemistry where plague epizootics occur. In relation to Pasteurella and other microbial pathogens, they found an increased pathogenicity well correlated to several metallic elements present in pasture plants, such as Ti, V, Cr, Mn, Fe, Co, Ni, Cu, Zn, Mo, Cd and Pb. Excess of Mo in animals is known to intensify the removal of Cu from their organisms, and increased concentrations of Pb and Zn intensify the displacement of Cu (also recorded during the epizootic). Therefore it is logical that ungulates feeding on vegetation exceptionally rich in Mo, Pb, and Zn will experience a considerable shortage of Cu (observed in all the plague outbreaks studied) (Rotshild, 1996; Rotshild and Zhulidov, 2000). Based on these assumption, these authors suggested the following explanation related to plant chemistry and epizootics:

pathogens that survive in environment through soil saprophytic cycle, water and their host bodies (asymptomatic) having enough nutrients including trace elements for their survival and multiplication however, when deprived of some elements (e.g., Fe) they compete with their host through activation of some hidden pathogenic attributes expressing their virulence and initiating disease. This theory sounds plausible; however, there are additional questions to be verified before its acceptance, such as: a) Does excess metals impair host immunology therefore favoring already opportunistic pathogens to prevail?; b) Do certain metals have an effect on pathogens virulence genes’ expression? c) Do excess metals in plants impact their biochemistry in such a way that plants as food in turn impact animals immune system? Botzler (1991) in a review on epizootiology of P. multocidain wildfowl (infecting more than 100 species of free-living birds), described the disproportionate mortality and year-round disease periodicity. The survival of P. multocida seems to be significantly linked to the presence of animal organic matter in soil and water. Another important factor involved in the persistence of this pathogen in enzootic areas, as pointed out by this author, is the availability of carrier animals. Daane et al.(1996) showed that selected terrestrial earthworm species enhance gene transfer between different bacteria present in soil. UsingPseudomonas fluorescens harboring the plasmid pJP4 [Pseudomonas fluorescens C5t (pJP4)], the authors showed that among a large variety of successful transconjugant indigenous soil microorganisms were alsoPasteurellaspp.. This important study strongly supports an already published report on earthworms’ role in soil pathogenic bacteria spread and possible enhancement of virulence transfer through their burrowing, casting, and feeding behaviors (Schuch and Fischetti, 2009). There is increasing evidences of a large variety of microbial pathogens interaction with free-living amoebae ubiquitous in water and soil environments. Hundt and Ruffolo (2005) showed experimental amoebae infection using a particular P. multocida sp. harboring green fluorescent protein (GFP) expression. In vitro, their results showed that thisP. multocida sp. can invade and survive, replicate, and lyse in the amoebal host with a possible related occurrencein vivo.

2.16.2 REFERENCES

Environmental Aspects of Zoonotic Diseases 104

Blanchong, J.A., Samuel, M.D., Goldberg, D.R., Shadduck, D.J. & Lehr, M.A. (2006) Persistence ofPasteurella multocidain wetlands following avian cholera outbreaks.J. Wildl. Dis.42, 33–39.

Botzler, R.G. (1991) Epizootiology of avian cholera in wildfowl.J. Wildl. Dis.27, 367–395.

Bredy, J.P. & Botzler, R.G. (1989) The effects of six environmental variables onPasteurella multocidapopulations in water.J. Wildl. Dis.25, 232–239.

Burriel, A.R. (1997) Isolation ofPasteurella haemolyticafrom grass, drinking water, and straw bedding used by sheep.

Curr. Microbiol.35, 316–318.

Carter, G.R. (1955) Studies onPasteurella multocidaI. A haemagglutination test for the identification of serological types.Am J Vet Res16, 481–484.

Daane, L.L., Molina, J. A. E., Berry, E. C. & Sadowsky, M. J. (1996) Influence of earthworm activity on gene transfer fromPseudomonas fluorescensto indigenous soil bacteria.Appl. Environ. Microbiol.62, 515–521..

Dimov, I. (1964) Survival of avianPasteurella multocidain soils at different acidity, humidity and temperature.Nauchni Tr Vissh Veterinarnorgo-Med. Inst Sofia12, 339–345.

Garcia, V.F. (1997) Animal bites andPasturellainfections.Pediatr. Rev.18, 127–130..

Göksay, D., Çotuk, A & Zeybek, Z. (2008) Microbial contamination of dental unit waterlines in Istanbul, Turkey.

Environ Monit Assess147, 265–269.

Harper, M., Boyce, J.D. & Adler, B. (2006)Pasteurella multocida pathogenesis: 125 years after Pasteur.FEMS Microbiol Lett265, 1–10.

Heddleston, K.L., Gallagher, J.E. & Rebers, P.A. (1972) Fowl cholera: gel diffusion precipitin test for serotyping Pasteurella multocidafrom avian species.Avian Dis16, 925–936.

Hundt, M.J. & Ruffolo, C.G. (2005) Interaction ofPasteurella multocidawith free-living amoebae.Appl. Environ.

Microbiol.71, 5458–5464.

Jiaxi Li, J. & Gu, J-D. (2006) Biodegradation of dimethyl terephthalate by Pasteurella multocidaSa follows an alternative biochemical pathway.Ecotoxicology15, 391–397.

Koch, C.A., Mabee, C.L., Robyn, J.A., Koletar, S.L. & Metz, E.N. (1996) Exposure to domestic cats: risk factor for Pasteurella multocidaperitonitis in liver cirrhosis?Am. J. Gastroenterol.91, 1447–1449.

Lane, E.P., Kock, N.D., Hill, F.W.G. & Mohan, K. (1992) An outbreak of haemorrhagic septicemia (septicaemic Pasteurellosis) in cattle in Zimbabwe.Trop. Anim. Hlth Prod.24, 97–102.

Li, L., Qian, C., Cheng, L. & Wang, R. (2010) A laboratory investigation of microbe-inducing CdCO₃precipitate treatment in Cd²⁺contaminated soil.J. Soils Sediments10, 248–254.

Mezentsev, V.M., Rotshild, E.V., Medzykhovsky, G.A. & Grazhdanov, A.K. (2000) Experimental study of the influence of trace elements on the infectious process in plague.Zh. Mikrobiol. Epidemiol. Immunobiol.1, 41–45.

Muller, W. & Dinter, P.S. (1988) The survival ability of pasteurella in the environment with special reference to the airborne situation.Tierarztl Prax Suppl3, 16–20.

Price, J.I. & Brand, C.J. (1984) Persistance ofPasteurella multocidain Nebraska wetlands under epizootic conditions.

J. Wildl. Dis.20, 90–94.

Rotshild, E.V. & Zhulidov, A.V. (2000) Changes in the concentrations of trace elements in plants as a factor of a plague epizootic in gerbils. (In Russian).Biull Mosk Ova Ispyt Prir (Biol)105, 10–20.

Rotshild, E.V. (1996) Disease and environment. Correlations between trace metals in plants and infectious diseases in wild animals.Science Spectra6, 48–54.

Seˇpicˇ, E., Bricelj, M. & H. Leskovseˇk, H. (1997) Biodegradation studies of polyaromatic hydrocarbons in aqueous media.J. Appl. Microbiol.83, 561–568.

Seˇpicˇ, E., Bricelj, M. & Leskovseˇk, H. (1998) Degradation of fluoranthene byPasteurellasp. IFA andMycobacterium sp. PYR-1: isolation and identification of metabolites.J. Appl. Microbiol85, 746–754.

Snipes, K. P., Biberstein, E.L. & Fowler, M.E. (1980) APasteurellasp. associated with respiratory disease in captive desert tortoises.J. Am. Vet. Med. Assoc.177, 804–807.

Wilson, G.S. & Miles, A. (1975) Pasteurella septic. In: Topley and Wilson’s principles of bacteriology, virology and immunity, Vol.1, Edward Arnold Ltd., London, England, pp. 950–951.

Ytrehus, B. Bretten, T., Bergsjø, B. & Isaksen, K. (2008) Fatal pneumonia epizootic in Musk Ox (Ovibos moschatus) in a period of extraordinary weather conditions.EcoHealth5, 213–223.

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Chapter 2.17 Plague

[YERSINIA PESTIS]

Yersinia pestis(formerlyPasteurella pestis) is a gram-negative rod, non-motile, facultative anaerobe of the Enterobacteriaceaefamily. Microbiologists devideY. pestisinto three biovars: Antiqua, Medievalis, and Orientalis that can be distinguished depending on their abilities to ferment glycerol and reduce nitrate (Devignat, 1951). This pathogen is highly virulent with lethal effects, infecting humans and a large variety of animals (cat, dog, coyote, rabbit, camel, bobcat, raccoon, and bear but mainly free-living rodents that are also reinfection reservoirs) (von Reyn et al., 1976, 1976a; Gage et al., 2000; Gould et al., 2008; Cloveret al., 1989; Wong et al., 2009). Transmission to humans occurs mainly by rat flea as well by other ectoparasite vector bites (Wimsatt and Biggins, 2009) however, direct transmission through cat bite was also reported (Thornton et al., 1975). Y. pestisinfection has three clinical forms:

pneumonic, septicemic, and the infamous bubonic plagues (connected to human demographic history).

The disease expresses itself according to entry portal as follows: a) bubonic plague - fever, chills, headache, myalgias, malaise, lymphoadenopathy, septicemia, tachycardia, renal failure, gangrene, chest pain and death; b) primary pneumonic–fever, headache, myalgias, pulmonary signs (chest pain, cough, dyspnea, hypotension) and cardiac failure with∼20% death rate in spite of early antibiotic treatment; c) septicemic–gastrointestinal symptoms (abdominal pain, diarrhea, vomiting, nausea), hypotension, acute respiratory distress syndrome (ARDS), intravascular coagulation, organ failure with 50% death rate (without treatment) and,5% (with early antibiotic treatment).