Rare zoonotic bacteria
2.26.2 MISCELLANEOUS ZOONOTIC BACTERIA AND ENVIRONMENT (FIGURE 2.26.1)
Actinobacillus lignieresii,equuliandsuisspecies are a common component of oropharingeal microbiota of animals such as cattle, horses, sheep and pigs. TheseActinobacillusspp. are also the main human zoonotic pathogens of this genus, even if rare (Ashhuurst et al., 1988). A. lignieresii andA. suis were detected following horse and pig bites (Dibbet al., 1981; Escandeet al., 1996), in a farmer (A. lignieresii) (Orda and Wiznitzer, 1980) and also directly recovered from horses, the majority exhibiting some kind of illness, in New Zealand (Carman and Hodges, 1982). In Japan they have been isolated more frequently from respiratory infections and endocarditis cases (Sakazakiet al., 1984).
Andrade et al.(1997) studied the effects of roots and of arbuscular-mycorrhizal (AM) fungi on the composition of soil bacterial colonies and their combined effects. Roots were experimentally colonized by three arbuscular-mycorrhizal (AM) fungi:G. etunicatum,G. intraradicesor G. mosseae. Among the large variety of bacteria isolated from the rhizosphere and hyposphere (the soil area not directly influenced by roots), Actinobacillus lignieresiiwas only isolated from the hyposhere of the AM-fungi G. mosseae.
Actinobacillus suishas been shown to cause diseases in pigs, horses, geese, cats, rodents, sheep (Maddux et al., 1987; Daignaultet al., 1999; Lentsch and Wagner, 1980; Peelet al., 1991) with elevated serological heterogeneity in horses (Badaet al., 1996).
Carvalhoet al.(1999) tested different soil bacteria strains for their emulsification activity on water-diesel oil combinations. Actinobacillus lignieresii was among the high biosurfactant producers with high emulsification potential. This feature seems to be related to its susceptibility to hydrophobic compounds such as the antibiotic novobiocin (Hart and Champlain, 1988).
2.26.1Potentialzoonoticbacteriathathavebeenrarelyisolatedfrominfectedandillhumans. SpeciesGram StainingGrowth conditionsTransmissionDiseaseOccurrence luslignieresii−Facultative aerobicAnimalbiteAbscess, septicemiaDomestic animals equuli− suis− teriumpyogenes+AnaerobicAnimals,fliesSepticemia, endocarditis, meningitis, arthritis, pneumonia, empyema, pharyngitis, abscess
Domestic animals bronchiseptica−ObligateaerobicAerosols,close contactwith animals
Paroxysmal cough, respiratory whoop Horses,Pigs, dogs,cats, rabbits teriumpseudotuberculosis+Aerobicor facultatively anaerobic
Closecontactwith animals,rawmilkInguinalnodes, granulomatous necrotizing lymphadenitis Domestic animals philuscongolensis+Facultative anaerobicAnimals,fliesDiphteria-like pharyngitis, pneumonitis
Soil,domestic andwild animals cterpylori−MicroaerophilicOralChronicgastritis, ulcerHumansand animals heilmannii− canis− felis− fennelliae− suis− usequi+Facultative aerobic, intracellular
Sapronosis?Necrotizing pulmonary infections Foalsand domestic animals
Environmental Aspects of Zoonotic Diseases 166
Arcanobacterium pyogenesis another commensal of mucous membranes of domestic animals (cattle, sheep and pigs) that may cause disease in other animals and humans (Linet al., 2010; Levyet al., 2009;
Kavithaet al., 2010). In humans, infection withArcanobacterium pyogenescan result in severe diseases with infrequent fatality (Gomez-Mateoset al., 2009; Hermidaet al.2004; Plamondon et al.2007). The transmission path is not clear, but direct contact with carrier or sick animals and their mucous membranes, exudates or aerosols can infect humans (Jost et al., 2002). Beside the regular domestic animals mentioned above as carrying this bacterium, cats and dogs were found also to be infected with A. pyogenes suggesting them also as a possible human infection source (Billington et al., 2002). In animals, especially ungulates, the bacterium becomes pathogenic when the animal is stressed by captivity or something else (Palmer and Whipple, 1999; Nettles et al., 2002). Lavin et al. (2004) described a foot infection in three adult male free-living fallow deer in Asturia, Spain. The authors described the area, showing some weather and geographical conditions that were possibly related to animals infection, such as mild temperature, high humidity, mixed pasture and rock land, domestic and wild herds living side by side and hunting activity (that may stress wild animals).
Bordetella bronchisepticais another commensal of respiratory tract of horses, pigs, dogs, cats, rabbits and guinea pigs (Baetzet al., 1974). The transmission seems to be through aerosols or close contact with infected animals (Tamionet al., 1996; Stehmannet al., 1991; Hermannet al., 2008). Aerosol transmission has been shown to be supported by its enduring nature at lower and humid temperatures, especially in intensive Figure 2.26.1. Actinobacillus,Arcanobacterium,Bordatella,Corynebacterium,Dermatophilus,Helicobacter andRhodococcusspp. as miscellaneous zoonotic diseases and their suspected transmission
Rare zoonotic bacteria 167
husbandry (Stehmannet al., 1992).B. bronchisepticahas the potential to survive and grow in the natural environment through expression of two virulence determinants (controlled by its genomic bvgand ris loci) modulated by different environmental signals (e.g., low temperature). Experimental evidence indicated that, for B. bronchiseptica, bvg locus controlled determinants expressed under modulating conditions (e.g., motility) facilitate adaptation and survival in environments outside the host (Coote, 2001).
Corynebacterium ulceransandpseudotuberculosiswere also described as zoonoses, though much less frequent than their classical relatives (Kraevaet al., 2007).C. pseudotuberculosisfound its natural hosts in many domestic animals such as: cattle, sheep, goats, horses and even camel (Cetinkaya et al., 2002;
Tejedor-Junco et al., 2009; Doherr et al., 1998; Stefanska et al., 2007), while C. ulcerans is mainly found in cattle although cats were also implicated (De Zoysa et al., 2005; DeWinter et al., 2005).
Wagneret al. (2010) reviewedC. ulceranscases in United Kingdom for the period from 1986 to 2008 and found that the major risk factor of infection is contact with companion animals. In relation to C.
pseudotuberculosis, people in direct contact with domestic animals are also at high risk (shepherds, children and animal workers) (Bartolomeet al., 1995; Join-Lambertet al., 2006; Dorellaet al., 2006).
Another bacterial pathogen suspected of infecting humans isDermatophilus congolensisfound mostly in tropical and subtropical and much less in temperate areas (Matheron et al., 1989; Towersey et al., 1993; Zaria, 1993; Kaminski and Sutter, 1976; Oduye, 1975; Pal, 1995; Pospisilet al., 1992). Wild and domestic animals are affected by this bacterium present in contaminated soil (Martinez and Prior, 1991).
Soil type and water content were the main components impacting survival of D. congolensis in environment. Martinez and Prior (1991) also reported that organic matter content protectsD. congolensis in oxisol soil as a temporary reservoir, but not in vertisol, though it retains its pathogenicity. Their conclusion was that ponds and dipping tanks may constitute sources of cattle infection as a result of soil and water environmental mix. Direct close contact with infected animals (domestic and wild) was also reported to cause infection in humans (Amor et al., 2011). Interestingly, flies were also suggested as vectors, possibly through their direct contact with soil or domestic animals urine, feces and gut mucus.
Morris et al., (1997) tested the odors originating from these excretion including those produced by growth of different bacteria, among themD. congolensis, as attractants for the Australian sheep blowfly (Lucila cuprina), revealing significant movement of this insect towardsD. congolensiscultures.
Rhodococcus equi (a soil actinomycete) was also suggested as a human zoonotic pathogen (Martens et al., 2000). In humans the disease represents itself as pulmonary infections (Silva et al., 2010).
Domestic animals such as cattle, horses, sheep and pigs are also infected (Martens et al., 2000; von Bargen and Haas, 2009; Muscatello et al., 2007). The main reservoir seems to be contaminated soil where domestic animals graze (Martenset al., 2000; Barton and Hughes, 1982, 1984); however a study performed in Japan on the presence of R. equi in soil and sand from parks and yards, revealed a significant presence (73.9%) but only of non-virulent strains (Takaiet al., 1996). When horse farms’soil was surveyed for the presence of R. equi, only 18.8% of soils contained virulent strains and no correlation was found between bacterial presence and diseased horses (Takaiet al., 2001). Additionally, Barton and Hughes (1984) showed thatR. equi was isolated from gut contents, rectal feces and dung of all grazing herbivorous but not from penned animals, indicating soil as the main source of this bacterium. It is very much possible that soil containing virulent strains can be dispersed as dust and directly infects humans through respiratory system, primarily in immunocompromised individuals.
Finally, Helicobacter a genus of gram-negative bacteria, microaerophilic, helical shape, living in stomach was also incriminated as being of zoonotic origin.Helicobacter pylori is well established as a human pathogen in association with gastritis, peptic ulcer disease, gastric adenocarcinoma, and mucosa
Environmental Aspects of Zoonotic Diseases 168
and already reported to be infectious in humans (Marshall and Warren, 1984; De Groote et al., 2000;
Haesebrouck et al., 2009). Potential transmission patterns are: person–to-person (oral-oral, fecal-oral, iatrogenic and familial), waterborne and zoonotic (vector-borne) (Brown, 2000; Svecet al., 2000; Sasaki et al., 1999; Haesebroucket al., 2009). De Grooteet al.(2000), based on experimental data, advocated Helicobacter human infection via zoonotic path as evidential proof of transmission. Helicobacter canadensis(from avian reservoirs such as geese) was also linked to human disease (Waldenströmet al., 2003; Fox et al., 2000). Some authors also pointed out that, besides direct contact with infected or carrier animals, transmission through carrier arthropods able to excreteHelicobacterin their feces is also feasible in connection with water and food (Imamuraet al., 2003; Shineng and Stutzenberger, 2000).
Table 2.26.2 Helicobacterspp. natural colonizers of animals’stomach and human association.
Helicobacter spp. Natural host Human
H. bizzozeronii Dog, cat Yes Finnish patient with
severe dyspeptic symptoms
H. salomonis Dog, cat, rabbit Yes Dams and puppies
“Candidatus
H. mustelae Ferret No Stoats and ferrets from
New Zealand
∼47–48
H. aurati Syrian Hamster No Hamster
H. nemestrinae Macaque No Pigtailed macaque
H. acinonychis Cheetah, tiger No Stray dogs ?
H. cetorum Whales, dolphins No Human upper digestive
tract, gastric mucosa of
H. canadensis Geese Yes Geese, shorebirds, ∼48
Rare zoonotic bacteria 169
Water seems to be one of the major environmental potential carriers of Helicobacter based on this pathogen’s survival potential for many hours (Table 2.26.2), grown in mixed bacteria biofilms and on different abiotic materials (Azevedo et al., 2008; Percival and Thomas, 2009; Azevedo et al., 2006;
Dube et al., 2009). Liet al.(2001) reported a significantly higher prevalence ofH. pylori infection in immigrant population from a flooded area and inversely related to flood stages, indicating floods and living conditions as a source of high prevalence. Fujimura et al. (2004) reported the correlation of H. pylori prevalence in children andH. pylori DNA presence in water of an adjacent river in Japan.
H. pyloriprevalence in children living near the middle reaches was 9.8% and 23.8% for children nearby downstream reaches, both values being greater than in an area distant from this river (0%) (p,0.01) used as control.
Soil polluted by human and animals excreta was shown also to harbor the pathogen (9% prevalence in soil tested) providing a possible source of infection for children in contact with playgrounds (Perezet al., 2010). As a final point associated to water and soil survival,H. pyloriwas reported to be competent to infect and internalize free-living amoebae, as a result enhancing this pathogen’s environmental endurance (Winiecka-Krusnellet al., 2002).
It should be pointed out that, due to actual confusion onHelicobacter spp. classification and newly emerging species isolated from a variety of animals, an unambiguous transmission route is still not available and more research is required to clarify this important issue.
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