Bacterial Zoonoses
2.4.1 BRUCELLA AND ENVIRONMENT
Brucella have been isolated from a large variety of feral or domestic animals spread worldwide (Figure 2.4.1). Their association with human zoonoses is obvious and only vaccination of domestic herds can reduce the pathogen’s dispersal. Another aspect, related to brucellosis transmission seen in high density animal herds, is winter elks’feed lines in Wyoming, USA (Maichaket al., 2009). These authors concluded that:“1) reduction of elk density and time attending feed grounds, particularly on feed lines;
and 2) protection of scavengers on and adjacent to feed grounds would likely reduce intraspecific transmission risk of brucellosis”. Similar conclusions in relation to elks’ density were supported by results in the Greater Yellowstone ecosystem, revealing a significant seropositivity rise from 0–7% in 1991/2 to 8–20% in 2006/7 respectively, as complemented well by limited hunter access to private lands (Crosset al., 2010).
Table2.4.1Brucellaspp.andtheirreciprocalrelationsbetweenvariousanimalsandhumans. Brucellaspp.Biovar/SerovarYearof discovery/reportInfected animalTransmission toother animals
Humaninfection andhighriskReference B.melitensis1–31893and1920Goat,sheepCattle,dogYes,farmers,dairy workers,shepherdsWilkinson(1993) B.abortus1–6,91901and1920CattleGoat,bison,elk, squirrelYes,farmers, ranchers,dairy workers, hikers-travelers
Beja-Pereiraetal.(2009); Noletal.,(2009) B.suis1–51929Pig,feral swine,Hares,rodents, reindeer,caribouYes,workersin swine slaughterhouses, hunters
Anonymous(2009); Cvetnicetal.(2009); Munozetal.(2010); Liamkinetal.(1983);Meng etal.(2009) B.ovisnonea 1956SheepRams,reddeerNoRidleretal.(2000) B.neotomaenone1957Desertwood ratNoStoennerandLackman (1957) B.pinnipedialisnone2001and2007SealPorpoiseNoPrenger-Berninghoffetal. (2008);Fosteretal.(2007) B.microtinone2007and2008VoleNo,isolatedalso fromsoilScholtzetal.(2008b); Scholtzetal.(2008a) B.inopinatanone2008and2010Human (breast implant)
YesScholtzetal.(2010)Tiller etal.(2010) B.canisnone1968CanidsHumansYes,dogowners, veterinariansBroweretal.(2007) B.cetinone2001and2007Cetaceans (whale, dolphins, etc.)
NoNeimanisetal.(2008); Fosteretal.(2007) Serpositivityfor Brucellanot identifiedat specieslevel
Caribou,grizzly bears,wolves, foxes Zarnkeetal.(2006); Martinoetal.(2004)
Brucelloses 51
animals (including humans) and one species,B. microti, isolated primarily from a vole, was also isolated from soil samples (Scholtzet al.2008a). How this species survives in soil is still a puzzle; however these authors supplied attractive supporting explanations for their results: 1) B. microti untypically is a fast growing bacterium with increased metabolic activity, therefore organic, moist soil can support their growth and 2) whole genome comparison of B. microti and B. suis with other soil bacteria such as Agrobacterium and Rhizobium spp. exhibited fundamental similarities (Paulsen et al., 2002). Whether soil organisms such as nematodes are the reservoir of this pathogen remains to be clarified, however some proofs exist as already shown withB. anthracis’s spores fate in soil (Schuch and Fischetti, 2009).
Interconnected with the soil ecosystem, Swartzet al.(2007) reported a“spectacular”reaction ofBrucella abortusto the blue spectrum of natural light by means of a significant change in the reproduction and infectivity rate. This phenomenon was further explained byBrucellaphotosensing proteins (light-oxygen-voltage and histidine kinase proteins, “LOV-HK”) involved in gene expression, that when knocked out impaired bacterium growth rate and infectivity significantly. This behavior fits the environmental phase of the pathogen excreted cells (in soil, exposed meat, milk, secretions or expelled placenta) exposed to blue light that activate the photosensing system in order to infect a new host successfully.
Another environmental important factor that acts as aBrucellareservoir is the wild boar (Munozet al., 2010; Menget al., 2009). It should be remembered here that this feral animal, like his domestic relative, feeds also on meat (carnivorous) in addition to vegetation in contrast to cattle, sheep and other ungulates.
Figure 2.4.1. Brucellaspp. cycles of infection among various animals and humans (full arrows-experimentally proved; dotted arrows- potentially unproved)
Environmental Aspects of Zoonotic Diseases 52
RB51 (vaccine) can multiply in squirrel and raven without clinical signs. A recent study of infected fish (Nile catfish) with Brucella melitensis was reported (El-Traset al.2010) suggesting that the source of infection was probably wastewater. Bogomolni et al. (2008) substantiated these results by surveying marine birds and mammals for amplicons to sequences fromBrucella spp., among other pathogens, in the Northwest Atlantic Ocean. Their findings indicated that marine mammals and birds in this geographical location are reservoirs for potentially zoonotic pathogens that may be transmitted to beachgoers, fishermen and wildlife health personnel. They also speculated that zoonotic pathogens found in marine vertebrates were possibly acquired via contamination of coastal waters by sewage, run-off and agricultural or medical waste.
Moreover, risk factors closely related toBrucellainfection were reported in many studies to be: hunting, consumption of raw meat and milk (foodborne), occupational or recreational (airborne), linked to travel and even to bioterrorism (Valderas & Roop, 2006).
2.4.2 REFERENCES
Anonymous. (2009)Brucella suisinfection associated with feral swine hunting - three states, 2007–2008.MMWR Surveill Summ58, 618–621.
Beja-Pereira, A., Bricker, B., Chen, S., Almendra, C., White, P. J. & Luikart, G. (2009) DNA genotyping suggests that recent brucellosis outbreaks in the Greater Yellowstone Area originated from elk.J. Wildl. Dis.45, 1174–1177.
Bogomolni, A.L., Gast, R.J., Ellis, J.C., Dennett, M., Pugliares, K.R.et al.(2008) Victims or vectors: a survey of marine vertebrate zoonoses from coastal waters of the Northwest Atlantic.Dis. Aquat. Org.81, 13–38.
Brower, A., Okwumabua, O., Massengill, C., Muenks, Q., Vanderloo, P., Duster, M., Homb, K. and Kurth, K. (2007) Investigation of the spread ofBrucella canisvia the U.S. interstate dog trade”.Int. J. Infect. Dis.11, 454–458.
Cross, P.C., Cole, E.K., Dobson, A.P., Edwards, W.H., Hamlin, K.L.et al.(2010) Probable causes of increasing brucellosis in free-ranging elk of the Greater Yellowstone Ecosystem.Ecol Appl20, 278–288.
Cvetnić, Z., Spicić, S., Toncić, J., Majnarić, D., Benić, M.et al.(2009)Brucella suisinfection in domestic pigs and wild boar in Croatia.Rev. - Off. Int. Epizoot.28, 1057–1067.
El-Tras, W.F., Tayel, A.A., Eltholth, M.M. & Guitian, J. (2010) Brucella infection in fresh water fish: Evidence for natural infection of Nile catfish,Clarias gariepinus, withBrucella melitensis.Vet Microbiol.141, 321–325.
Foster, G., Osterman, B.S., Godfroid, J., Jacques, I. & Cloeckaert, A. (2007)Brucella ceti sp. nov. and Brucella pinnipedialis sp. nov. for Brucella strains with cetaceans and seals as their preferred hosts. Int J Syst Evol Microbiol.57, 2688–2693.
Heymann, M.D. & David L. (2008).Control of Communicable Disease Manual. Baltimore, MD, United Book Press, Inc.
Januszewski, M.C., Olsen, S.C., McLean, R.G., Clark, L., Rhyan, J.C. (2001) Experimental infection of nontarget species of rodents and birds withBrucella abortusstrain RB51vaccine.J Wildl Dis37,532–537.
Liamkin, G.I., Taran, I.F., Safronova, V.M., Tikhenko, N.I. & Shiranovich, M.P. (1983) Taxonomic position and ecology of the causative agent of brucellosis isolated from murine rodents in regions of the northern foothills of the Greater Caucasus. II. The ecological and pathogenetic characteristics of Brucella strains isolated from murine rodents.Zh. Mikrobiol. Epidemiol. Immunobiol.7, 31–35.
Maichak, E.J., Scurlock, B.M., Rogerson, J.D., Meadows, L.L., Barbknecht, A.E.et al.(2009) Effects of management, behavior, and scavenging on risk of brucellosis transmission in elk of western Wyoming.J. Wildl. Dis. 45, 398–410.
Martino, P.E., Montenegro, J.L., Preziosi, J.A., Venturini, C., Bacigalupe, D., Stanchi, N.O. & Bautista, E.L. (2004) Serological survey of selected pathogens of free-ranging foxes in southern Argentina, 1998–2001.Rev. - Off.
Int. Epizoot.23, 801–806.
Meng, X.J., Lindsay, D.S. & Sriranganathan, N. (2009) Wild boars as sources for infectious diseases in livestock and humans.Philos. Trans. R. Soc. Lond., B, Biol. Sci.364, 2697–2707.
Brucelloses 53
Munoz, P.M., Boadella, M., Arnal, M., de Miguel, M.J., Revilla, M.et al.(2010) Spatial distribution and risk factors of Brucellosis in Iberian wild ungulates.BMC Infect. Dis.10:46.
Neimanis, A.S., Koopman, H.N., Westgate, A.J., Nielsen, K. & Leighton, F.A. (2008) Evidence of exposure to Brucella sp. in harbor porpoises (Phocoena phocoena) from the Bay of Fundy, Canada.J. Wildl. Dis.44, 480–485.
Nol, P., Olsen, S.C. & Rhyan, J.C. (2009) Experimental infection of Richardson’s ground squirrels (Spermophilus richardsonii) with attenuated and virulent strains ofBrucella abortus. J. Wildl. Dis.45, 189–195.
Paulsen, I.T., Seshadri, R., Nelson, K.E., Eisen, J.A., Heidelberg, J.F., Read, T.D.et al.(2002) TheBrucella suis genome reveals fundamental similarities between animal and plant pathogens and symbionts.Proc Natl Acad Sci U S A.99, 13148–13153.
Prenger-Berninghoff, E., Siebert, U., Stede, M., Koenig, A., Weiss, R. & Baljer, G. (2008) Incidence of Brucella species in marine mammals of the German North Sea.Dis. Aquat. Org.81, 65–71.
Ridler, A.L., West, D.M., Stafford, K.J., Wilson, P.R. & Fenwick, S. (2000) Transmission ofBrucella ovisfrom rams to red deer stags.N Z Vet J48, 57–59.
Scholz, H.C., Hubalek, Z., Nesvadbova, J., Tomaso, H., Vergnaud, G.et al.(2008a) Isolation ofBrucella microtifrom soil.Emerging Infect. Dis.14, 1316–1317.
Scholz, H.C., Hubalek, Z., Sedlácek, I., Vergnaud, G., Tomaso, H., Al Dahouk, S.,et al.(2008b)Brucella microtisp.
nov., isolated from the common voleMicrotus arvalis. Int J Syst Evol Microbiol.58, 375–82.
Scholz, H.C., Nöckler, K., Göllner, C., Bahn, P., Vergnaud, G.et al.(2010)Brucella inopinatasp. nov., isolated from a breast implant infection.Int J Syst Evol Microbiol.60, 801–808.
Stoenner, H.G. & Lackman, D.B. (1957) A new species of Brucella isolated from the desert wood rat,Neotoma lepida.” Am. J. Vet. Res.69, 947–951.
Tiller, R.V., Gee, J.E., Lonsway, D.R., Gribble, S., Bell, S.C.et al.(2010) Identification of an unusualBrucellastrain (BO2) from a lung biopsy in a 52 year-old patient with chronic destructive pneumonia.BMC Microbiol.27, 10:23.
Valderas, M.W. & Roop, R.M. (2006) Brucella and bioterrorism. In: Anderson, B., Friedman, H. & Bendinelli, M. (Eds.): Microorganisms and Bioterrorism. pp. 139–153. Publisher: Springer, New York.
Wilkinson, L. (1993) Brucellosis. In: Kiple, K.F. (Ed.),The Cambridge World History of Human Disease. Cambridge University Press.
Zarnke, R.L., Ver Hoef, J.M. & DeLong, R.A. (2006) Geographic pattern of serum antibody prevalence for Brucella spp.
in caribou, grizzly bears, and wolves from Alaska, 1975–1998.J. Wildl. Dis.42, 570–577.
Environmental Aspects of Zoonotic Diseases 54
Chapter 2.5
Campylobacterioses
[CAMPYLOBACTER JEJUNI]
The genusCampylobactercomprises gram-negative spirals, microaerophilic, motile, non-spore forming and oxidase-positive bacteria. The following species belong toCampylobactergenus:C. coli,C. concisus,C.
curvus,C. fetus, C. gracilis,C. helveticus,C. hominis,C. hyointestinalis,C. insulaenigrae,C. jejuni,C.
lanienae,C. lari,C. mucosalis,C. rectus,C. showae,C. sputorum and C. upsaliensis. C. jejuniandC.
coliare the main causes of bacterial foodborne disease in many developed countries.C. fetusis the main cause of spontaneous abortions in cattle and sheep, but also an opportunistic pathogen in humans.
Clinical symptoms of Campylobacteriosis or as once called“cholera infantum”or “summer complaint” (Condran and Murphy, 2008; Samie et al., 2007) are inflammatory diarrhea or dysentery syndrome, cramps, fever, and pain (occasionally with blood). The disease is usually self-limiting and in most cases, symptomatic treatment by reposition of liquid and electrolyte replacement is sufficient in human infections. The common routes of transmission are fecal-oral, ingestion of contaminated food or water and consumption of raw meat.
As already mentioned, Campylobacter is a pathogen related to animal food origin, especially poultry and other birds (e.g., seagulls excrete C. lari) (Figure 2.5.1). During the past decades Campylobacter has been shown to be responsible for enteritis in humans and animals. The natural habitats of most Campylobacter species are the intestines of birds and other warm-blooded animals such as: cattle, calves, sheep, dogs, cats, hamsters, guinea pigs, mice and different zoo animals.
Farm pigs are the main carriers excreting C. coli (Levin, 2007). These organisms may enter the environment, including drinking water, through the feces of different mammals, birds or infected humans (Table 2.5.1). Campylobacter had been shown to survive in aqueous environment for several weeks (at∼4°C) and possibly enter the human food chain through the animal slaughtering process. Campylobacter is sensitive to heat, acidic pH, food preservatives, some heavy metals and irradiation but has increasing resistance to antibiotics due to extensive exposure following farmers over utilization (Baserilashi et al., 2006). Milk, mushrooms, hamburger, pork, shellfish and eggs are vehicles of Campylobacter, however most Campylobacter enteritis is acquired by the handling and consumption of poultry. Although, many methods and media have been developed for the
detection of the Campylobacterfrom various samples, universally accepted methods and media are not yet available.
J F M A M J J A S O N D 0
2000 4000 6000
(a) 8000
(b)
No. of Cases
Month
E.coli Salmonella Campylobacter
81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 0
10000 20000 30000 40000 50000 60000
No. of Confirmed Cases
Year
Salmonella Campylobacter
Figure 2.5.2. Number of confirmed cases ofCampylobacter,Salmonellaand enteropathogenicE. coliin UK –
Figure 2.5.1. Campylobacterspp. infection cycles
Environmental Aspects of Zoonotic Diseases 56
Table2.5.1Campylobacterspp.isolationfromdifferentenvironments. IsolationsiteCountryMethodLowestHighestStrainsSeasonaltrendReference Ribble,Calder andHodderriversUKGlassmicrofibre filtrationmethod andamost probablenumber (MPN)method ,10CFU/100ml.10–230 CFU/100mlC.jejuni,C.coli, C.laridisHigh-late autumnand winterLow- springand summer
Boltonetal. Urban Wastewater treatmentand composting
FranceQuantitative real-timePCR andculture method
10–200target genes/ml(October)106 targetgenes/ml (April)C.jejuniDryweatherWéryetal., (2008) Cattle,sheep, birdsandother wildlifefecesand water
Cheshire,UKCulturemethod andsingle reactionPCR
%ofsamplestesting positive 11(C.jejuniincattle feces) 21(C.coliincattleand birdsfeces),0(C.lari insheepfeces),7(C. hyointestinalisin water,sheepand wildlifefeces)
%ofsamples testingpositive 36(C.jejuniincattle feces) 21(C.coliinsheep feces),7(C.lariin birdsfeces),7(C. hyointestinalisin cattlefeces) C.jejuni,C.coli, C.lari,andC. hyointestinalis
Lowernumbers duringrainy weather
Brown etal.,2004 Contaminated urbanfloodwaterUtrecht,The Hague TheNetherlands
MPN2.3×103 2.4×104 Campylobacter sp.Heavyrainten Veldhuis etal.,2010 Soil,poultry manure,irrigation water,andfreshly harvested vegetables
MalaysiaMPN-PCR0MPN/g1100MPN/gCampylobacter spp.DryweatherChaietal., 2009 BeachsandUKCulturemethod andserotyping31%prevalence66%prevalenceC.jejuni,C.coli andC.lariRainyweatherBolton etal.,1999 Organicpigs, paddock environmentand crow-birdsand rats University researchfarmin Taastrup, Denmark
Culturemethod, colony-blot hybridization, real-timePCR, serotypingand pulse-fieldgel electrophorsis (PFGE) 103 CFU/g107 CFU/gC.jejuniandC. coliDryweatherJensen etal.,2006
Campylobacterioses 57