**3.** *Salmonella* **spp. in wild animals**

The increased demand for wild animals raised as domestic animals has become a public health and environmental concern due to the spreading of pathogens [21].



*NI: not informed.*

*\*4-day-old neonate developed Salmonella meningitis.*

*\*\*3-month-old child with microcephaly.*

*\*\*\*3-week-old baby developed Salmonella meningitis and died.*

*\*\*\*\*Used to feed pet reptiles.*

#### **Table 2.**

*Salmonellosis outbreaks in humans associated with wild animals (2000–2021).*

Cases of salmonellosis in humans caused by contact with wild animals kept away from their natural habitat have been reported (**Table 2**). These animals are often the carriers of not only *Salmonella* strains, but of other pathogens, for which there are not always effective control measures [44].

As shown in **Table 2**, among wild animals in captivity, reptiles cause most outbreaks of salmonellosis in humans [45, 46]. Salmonellosis in reptiles usually occurs asymptomatically [47]. The animals shed the bacterium intermittently and the elimination of the pathogen may increase due to stress factors [48]. Moreover, it is difficult to diagnose even in the presence of clinical signs [47]. However, human infections arising from human-reptile interaction can lead to clinical conditions ranging from mild to severe enteric infections, hospitalizations, and even deaths, especially in children, the elderly, and people with comorbidities [45].

Human contamination by *Salmonella* spp. from reptiles can be direct or indirect through secretions and excretions [49]. In a study conducted in southwest England between 2010 and 2013, 27.4% (48/175) of children under the age of five who had some contact with reptiles tested positive for *Salmonella* spp. and hospital admission rates totaled 50% for children under 1 year of age [50]. In another study conducted between 2008 and 2009 in New Zealand with 378 cloacal swabs of 24 different exotic reptile species kept as pets, 11.4% tested positive for *Salmonella enterica* subsb. Enterica, with emphasis on the serovars Onderstepoort (30.2%), Thompson (20.9%), Potsdam (14%), Wangata (14%), Infantis (11.6%), and Eastbourne (2.3%), which can also cause infectious conditions in humans [51].

The participation of free-living wild reptiles in the epidemiology of *Salmonella* should also be stressed. In a park in Poland, 16 free-living road-killed snakes were analyzed and 87.5% were positive for *Salmonella* spp. [52]. Briones et al. [53] analyzed free-living wild reptiles in preserved areas in Spain and found that 41.4% tested positive for *Salmonella enterica*, with 27 serotypes identified, 37.5% of which were associated with salmonellosis in humans. Regarding the group of affected animals, snakes and lizards are more prevalent than chelonians [51, 54].

A high prevalence of *Salmonella* spp. with serotype diversity is also found in amphibians. In a study conducted in Indiana County, Pennsylvania (USA), Chambers and Hulse [55] collected 92 free-living amphibians and found that 39.1% tested positive (23 salamanders and 13 frogs), with isolated serotypes Muenchen, Enteritidis, Typhimurium, Senftenberg, and Montevideo. The prevalence of *Salmonella* in amphibians was also examined in 58 Bufo marinus of the West Indies and 41% tested positive to five serotypes, especially *Salmonella enterica* subsp. Enterica serovar Javiana (33%) and *S.* Rubislaw (33%) [56]. In Thailand, eight serotypes of *Salmonella* spp. were identified (Hvittingfoss, Newport, Thompson, Stanley, Wandsworth, Panama, Muenchen, and subsp. diarizonae ser. 50:k:z) in 69.07% of the amphibians sampled in three different habitats - rural areas, protected areas, and urban areas. Of these serotypes, the first six have already been isolated in people in Thailand. Surprisingly, the animals coming from urban areas were negative [57]. The prevalence of *Salmonella* in amphibians regarding habitat remains unclear, although a possible cause is an environmental contamination by sewage [58]. This scenario is a public health concern because these amphibians can spread *Salmonella* spp. from the aquatic environment.

Outbreaks of salmonellosis in humans associated with contact with wild birds have been reported [59–61]. In 2000, an outbreak was reported in New Zealand caused by *S*. Typhimurium DT160, which led to the death of wild birds in rural areas, mainly sparrows, and enteric infections in humans [62]. In 2001, New Zealand reported an outbreak of human salmonellosis by *S*. Typhimurium DT160 related to contact with dead wild birds [63]. In 2001, two outbreaks were reported in the United States with at least 40 people contaminated with *S*. Typhimurium from the dissection of owls in two primary schools [43].

Between 1995 and 2003, Pennycott et al. [64] sampled 779 free-living wild birds in Great Britain and identified that the most prevalent serotype was *S*. Typhimurium. In Norway, *S.* Typhimurium variant O: 4,12 was identified in 96% of the isolates in a sample of 470 wild birds of 26 different species [44]. Despite the acute and chronic infection caused by *Salmonella*, in wild birds, it is asymptomatic [65]. During migration, the immune system can be affected by stress, as in the case of hunger, which may lead to a greater release of the pathogen by feces, contributing to even greater environmental contamination.

Regarding wild mammals, some species such as African pygmy, ferrets, hedgehogs, prairie dogs, primates, and sugar gliders are raised as pets [66], which can cause salmonellosis infections and outbreaks from direct human contact with carrier animals or indirectly due to access to or living in the same contaminated environments

as these animals [49]. Two human outbreaks in Norway, caused by *S*. Typhimurium 4.5, 12:i: 1.2 associated with hedgehogs, were reported from August to October 1996 and from July to November 2000, with 28 confirmed cases and 37 confirmed cases, respectively. In both cases, hedgehogs were the only common source, with positivity rates of 39% and 41%, respectively for the outbreaks of 1996 and 2000 [42].

Free-living wild mammals can also be asymptomatic carriers of *Salmonella* spp.; however, the prevalence is usually lower than when these animals are bred in captivity. From 2002 to 2010, 2713 animals were sampled in Italy, a total of 1612 mammals (1222 canids, 221 mustelids, 100 rodents, 69 ungulates), resulting in 7.25% animals positive for *Salmonella* spp. (63 canids, 25 mustelids, 5 ungulates, 24 birds), with emphasis on the Typhimurium serotype [67].

Notably, urbanization causes the spread of zoonotic agents due to new ecological interactions [68], from changes in eating habits to changes in migration routes [69]. When wild animals have access to urban spaces or modified environmental areas, they also come into contact with waste produced by humans, such as garbage and sewage. Moreover, these spaces are a food source for these animals [70]. Due to ineffective waste management, contaminated environments can be the source of numerous pathogens and favor the spread of antimicrobial resistance genes [71].
