Rat bite Fever (RBF) or Sodoku
2.20.1 SALMONELLA AND ENVIRONMENT
Presently, there is an extensive literature on food- and waterborne Salmonellosis that will not be reviewed in this chapter but occasionally mentioned; however, it is important to emphasize that its transmission is in general through the oral route by consumption of contaminated food (e.g. meat, dairy products, eggs and egg products), water and direct contact (Mataragas & Drosinos, 2009; Gomez et al., 1997; Schuster et al., 2005; Woodall, 2009). There are important aspects of global infections embroiling multi-drug resistance bacteria through meat import based on international trade (Espiéet al., 2005). Other important Salmonella food borne factors are: livestock feed, animal health conditions and slaughterhouse procedures (evisceration, etc.) (Maciorowskiet al., 2007). It should be mentioned that Salmonellais a
showed that hydroponic tomato farm greenhouses were infected withSalmonellathrough runoff flood and gained entry of wild animals (opossums, mice, and sparrows), both factors introducing the pathogen in spite of a reasonable protection level.
Groundwater was found to be the main significant independent risk factor linked toS. choleraesuis transmission, following adjustments for other potential confounders in a case-control study intended to identify the possible demographic and environmental risk factors associated with S. choleraesuis infection in Taiwan (Liet al., 2009). It should be mentioned that pigs are considered as the only animal reservoir ofS. choleraesuis, and therefore it may very well be that the dwellings of clinical cases could be near pig farms or use groundwater somehow connected to these farms. The groundwater’s proximity to contaminated sources (landfill) proved to be a high risk of contamination through the leaching process (Adeyemi et al., 2007). As previously mentioned in connection with other bacteria, Salmonellae too interact with protozoa such asT. pyriformisandA. rhysodes, using their ability to survive and replicate Table 2.20.1 Salmonellagenus classification (serovars, hosts and transmission).
Salmonella
within their protozoan protective environment, increasing their environmental transmission potential (Snellinget al., 2006).
Recent publications showed that protozoa bestow protection (against low concentrations of calcium hypochlorite) and enhanced survival of the food-borne pathogen S. enterica through food vacuoles (vesicles) released by a Tetrahymena sp. isolated from moist soil (Brandl et al., 2005). Moreover, Gourabathini et al. (2008) reported the isolation of similar protozoa from fresh lettuce and spinach plants, which can internalize pathogenic bacteria such as Salmonella enterica and then release them through food vacuoles as an environmental defense mechanism against bacterial pathogens. These authors also called attention to the possible proximity of the vacuolated released pathogens to stomata cells that may possibly support further plant internalization!
Nevertheless, when various amoebae, such asAcanthamoeba,Tetramitus,NaegleriaandHartmannella, were isolated from different vertebrates it was observed that their feeding preferences on bacteria appear to reflect their environment, not their taxonomic relationships (Wildschutte and Lawrence, 2007). These authors suggested an attractive hypothesis about the survival mechanism of Salmonella spp. as human and animal pathogens against being predated by amoebae (Figure 2.20.1). They proposed that O-antigen determinant (located on bacterial outer membrane) is the main key for predation recognition by the amoebae while the prey choice is governed by their environment (host animal) and not their taxonomic relationships (genome). In a previous study, Tezcan-Merdolet al., (2004) showed that Acanthamoeba spp. can differentiate between different serovars of Salmonellae and that internalization is associated with cytotoxic effects mediated by definedSalmonellavirulence loci.
Concerning the relation between plants and bacterial pathogens, Baraket al.(2007) demonstrated thatS.
entericauses other surface polymers composing the extracellular matrix, such as cellulose and O-antigen capsule, in order to colonize plants. Schikoraet al.(2008) usedSalmonella entericaserovartyphimurium to prove that it is a real endopathogen of Arabidopsis thalianaand could successfully infect this plant.
The definitive answer came from an Israeli group that clearly showed thatSalmonella entericainduced by light can chemotactically penetrate open stomata, possibly explaining the reported high risk of Salmonellosis in connection with contaminated vegetables (Kroupitskiet al., 2009; Manaset al., 2009).
Another epidimeliogical study, performed in Oregon and British Columbia, showed that Salmonella transmission through plants can occur by consumption of alfalfa (Medicago sativa) sprouts originating from contaminated seeds (133 reported cases of Salmonella enterica serotype Newport-SN) (Van Beneden et al., 1999). Alfalfa sprouts are excellent means for transmission of Salmonella and other enteric bacteria, as seeds are stored for extended time periods (even years) in dry environment. The sprouting process which takes 3 to 5 days, favorsSalmonellagrowth to 3 to 4 orders of magnitude and further refrigeration does not reduce their number significantly and final consumption occurs without washing or cooking, therefore leaving the consumer completely unprotected.
There is an extensive literature on environmental factors impactingSalmonellapresence in the coastal area, mainly due to the recreational and marine food role of these sites. Settiet al.(2009) surveyed 122 km of the coastline of Agadir (southern Morocco) for Salmonella spp., related to environmental parameters. They sampled seawater, marine sediment and mussels and found an overallSalmonellaspp.
prevalence of 7.1% (at the following ratios: mussels-10%, sediment-6.8% and seawater-4.1%). Amongst observed environmental variables, rainfall was the only parameter directly related to Salmonella occurrence, showing a linear positive effect well supported by other studies (Collin et al., 2008).
Salmonella highest numbers in shellfish is obviously related to these bivalve mollusks high filtration potential ability to concentrate various contaminants with high efficiency. A similar trend was found in
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on the food chain scale, California’s sea otters feeding on mollusks were found to harbor different Salmonella serovars beside other enteric pathogens (Miller et al., 2010). Otters from more urbanized coastlines and areas with high freshwater runoff mainly in the rainy season (near outflows of rivers or streams) were more likely to test positive for bacterial pathogens. Otters exposure to fecally-associated protozoan pathogens such as Toxoplasma gondii and Sarcocystis neurona and enteric pathogenic bacteria, is suspected of impairing sick otters recovery in these geographical areas.
In all these cases, presence ofSalmonellaspp. in coastal areas was merely confined to rainy periods, stream discharges and runoff, all factors involved in the transport of this pathogen via streams from source points to sea (Martinez-Urtazaet al., 2004).
In another geographical edge (Australia), comprising both tropical and sub-tropical climates, researchers found that temperature and rainfall were the only significant parameters, suggesting that a potential 1°C rise in maximum or minimum temperature may cause a very similar increase in the number of Salmonelloses cases in both climatic regions (Zhanget al., 2010).
Canadian researchers studied the survival ofSalmonella salamaein estuarine waters of the St. Lawrence River (Monfortet al., 1994).Salmonalla salamaecells exposed to starvation, increasing salinity and solar irradiation showed a rapid decline in viability; however, when bacteria were kept in darkness while Figure 2.20.1. Predators prey choice and phytopathogenesis based on surface antigens ofSalmonellaspp.
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exposed to increasing salinity, their die-off rate was even higher than of those exposed to sunlight. Hence S. salamaecells exposed to sunlight seemed to be more resistant to gradual salinity stress than cells that were not subjected to sunlight. Bacteria exposed to sunlight irradiation are damaged by the UV short wave spectra causing DNA damage, however bacteria are able to cope with this germicidal activity. Bacterial sunlight damage repair (reactivation) has two well known enzymatic mechanisms: photoreactivation and dark repair. The photoreactivation mechanism, which requires light is much more effective than the dark mechanism. Zaafraneet al.(2004), studingSalmonella thyphimuriumsurvival in sea water, found results similar to those of the Canadian researchers and furthermore emphasized that “bacteria grown in media with high salinity or osmolarity and transferred to sea water in stationary phase were more resistant to irradiation than those grown in media with low salinity”.
Jones (1971) already reported that the death of sewage bacteria in seawater is mainly due to starvation and to natural heavy metal toxicity. In his study, other factors were found to be effective in controlling bacterial survival such as sunlight, temperature, salinity, antibiotics, bacteriophages, adsorption and sedimentation, parasitism, lysis, and protozoan predation. Enterobacteriaceae includingSalmonellapossess theσSsubunit, encoded by rpoS gene of RNA polymerase, which functions as a master regulator of general stress responses (cessation of growth, acid resistance, thermotolerance and adaptation to growth in a medium of high osmolarity). TheσSlevel increases in response to environmental stresses in cell; hence sunlight irradiation damage of the gene rpoS, lacking an effective repair, will decrease cellσSlevel leading to cell death under extreme environmental conditions.
When dealing with bodies of water it should be remembered that fish are also involved in transmission of Salmonellae. Miruka et al. (2009) studied Nile tilapia fish for contamination with members of Enterobacterioceae. Among the fish batch examined, 52.5% were positive for Enterobacteriaceae among which 11.1% with S. typhimurium and 25.4% with S. enteridis compared to an open-air fish market where S. typhimurium was present in 20% of fish. The authors concluded that the high level of Salmonella pathogens in fish indicates that beaches in this area are contaminated with untreated municipal sewage, runoff and storm-water.
Soil is also highly related toSalmonellaecology, mainly through utilization of organic fertilizers such as manure for different soils. Castro-Del Campoet al.(2010) studied the regrowth potential ofSalmonella enterica subsp. enterica in three soil types: vermicompost, Class A biosolids and amended. At 30%
moisture, the longest survival persistence of this pathogen (up to 20 days) was obtained for amended soil. Additional studies showed even more extended survival periods of time of Salmonellain soil and swine manure environments (for ∼45 days, temperature dependent) (Guan and Holley, 2003). On bacterial soil endurance aspect, it should be pointed out that a Salmonella typhimurium strain has been shown to survive in soil for up to 54 days with decline in colony numbers (measured by direct plate culture) but constant viable cells when measured with 5-cyano-2,3-ditolyl tetrazolium chloride (CTC), as respiration-sensitive dye. A close look at these results revealed that direct CTC soil counts of S.
typhimuriumconfirmed that intact cells were still present in an intact metabolic state after 54 days in the non-sterile soil, indicating a significant proportion of unculturable but active cells (Marshet al., 1998).
In an extra framework, soil was also reported as a possibleSalmonellacarrier state in amphibians and reptiles kept in terraria (private or zoological parks) (Hasslet al., 2003). In Austria, where this study was carried out, there are∼90,000 households that keep a large variety of these“kind of pets”. The authors detected a strong association between Salmonellasubspecies (I and III) among captive reptiles and free living lizards accordingly. Kourany and Telford (1981) surveyed lizard species in Panama for Salmonellapresence. Among these species, 29.4% were positive for Salmonella(with a range from 5.6
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Lizard soil contact reveals the possible contamination through excreta-contaminated ground. The infected lizards’distribution varied from remote rural and forested regions to urban developments, revealing their potential reservoir role. In the same geographical area (Panama) other animals such as opossums and rodents were also positive for Salmonella(∼10 to 20%) especially throughout the dry season (Kourany et al., 1976).
Interaction between algae andSalmonella has been shown in Lake Michigan (USA) related to algal bloom.Chladophora glomeratais a filamentous, green alga that grows in nearshore water, on rocks and other hard surfaces. After their peak bloom, these algae detach and accumulate on the shore, creating an environmental problem through aesthetic, malodorous conditions and growth enhancement of pathogens suchSalmonella(Byappanahalliet al., 2009; Verhougstraeteet al., 2010).
As a final point, a group of ungulate veterinarians reported on pathogens and climate influence on the fecundity of ungulates in natural conditions. Beside animal density, they identified two other major confounding effects on the reproductive success of an alpine chamois ungulate (Rupicapra rupicapra):
1) prevalence of antibodies against pathogenic bacteria (among them, Salmonella enterica serovar abortusovis (36%), and 2) weather conditions (31%). Bad weather conditions that may act either as a direct stress or through food availability, were linked to increased infection with pathogens including Salmonellaspp. (Piozet al., 2008).
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