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Objective:
Although amphibians are known Salmonella carriers, no such outbreaks have been reported. We investigated a nationwide outbreak of human Salmonella Typhimurium infections occurring predominantly among children from 2008 to 2011.
Methods:
We conducted a matched case-control study. Cases were defined as persons with Salmonella Typhimuriu...
Citations
... Although commonly transmitted through food or water, an estimated 11% of all non-typhoidal Salmonella infections are attributed to animal contact (Hale et al., 2012). Contact with reptiles and amphibians has resulted in multistate reptile-and amphibian-associated salmonellosis (RAAS) outbreaks, which disproportionately affected young children (aged <5 years) (Harris et al., 2010;Kiebler et al., 2020;Mettee Zarecki, 2013;Vora et al., 2012;Whitten et al., 2015). ...
Non‐typhoidal Salmonella cause an estimated 1.4 million human illnesses, 26,000 hospitalizations and 400 deaths annually in the United States. Approximately 11% of these infections are attributed to animal contact. Reptiles and amphibians are known sources of salmonellosis; young children (aged <5 years) are disproportionately affected by reptile‐ and amphibian‐associated salmonellosis (RAAS) outbreaks. We describe multistate RAAS outbreaks to characterize illnesses and inform prevention efforts. RAAS outbreaks were defined as ≥2 culture‐confirmed human Salmonella infections with similar pulsed‐field gel electrophoresis patterns and epidemiologic, laboratory or traceback evidence linking them to a common reptile/amphibian exposure. Data sources included the Animal Contact Outbreak Surveillance System; CDC Outbreak Response and Prevention Branch's outbreak management database; PulseNet, the national molecular subtyping network for foodborne disease surveillance in the United States; and the National Antimicrobial Resistance Monitoring System. Twenty‐six RAAS outbreaks were reported during 2009–2018, resulting in 1465 illnesses and 306 hospitalizations. The outbreaks were associated with turtles (19), lizards (5), snakes (1) and frogs (1). Sixteen (61.5%) outbreaks were linked to small turtles (<4 inches), resulting in 914 illnesses. Forty‐nine percent of outbreak‐associated patients were aged <5 years. Of 362 patients/caregivers interviewed, 111 (30.7%) were aware that reptiles/amphibians can carry Salmonella. Among 267 patient isolates with antimicrobial susceptibility information, 20 (7.5%) were non‐susceptible to ≥1 antibiotic used to treat human salmonellosis. RAAS outbreaks result in considerable morbidity, particularly among young children. Illnesses linked to small turtles are preventable through education, targeted outreach to caregivers and paediatricians, and when appropriate, enforcement. Historically, individual states and jurisdictions have enforced existing or promulgated new authorities to address outbreaks. Preventing future RAAS outbreaks requires addressing challenges related to the illegal sale/distribution of small turtles; and for legal reptile sales, providing information on RAAS risk to consumers at point of sale to support informed pet ownership decisions.
... Not washing hands after handling animals or their food,waste, habitats, or other supplies (e.g., toys, leashes) Engaging in risky forms of contact (snuggling, kissing, or holding near face) Eating or drinking around NTPs Cleaning habitats in the kitchen or in other food preparation areas that leads to cross-contamination of kitchenware used for people (e.g., baby bottles) Allowing animals to roam freely in the home or in food preparation areas Zoonotic disease transmission can also occur indirectly via contact with a surface or environment contaminated by an animal's urine, feces, blood, saliva, nasal secretions, or other body fluids; via contamination of food preparation areas and items; or less commonly through infectious droplets or aerosols (Daly et al, 2017). In multiple outbreaks of human illness linked to NTP species, contamination of food preparation surfaces by the animals themselves, contaminated items (e.g., by cleaning animal dishes or habitats in kitchen sinks), and allowing NTP species to freely roam indoors have been identified as important preventable risk factors for human infection (Gaffga et al, 2012;Loharikar et al, 2013;Loharikar et al, 2012;Zarecki et al, 2013). ...
... Aquatic animals bathe, excrete, and ingest the water they live in, and these processes circulate and even amplify pathogens found in the water. Anyone can get sick from direct or indirect contact with the animals, water, or habitat substrate in a terrarium or aquarium (''Multistate Outbreak of Human Salmonella Infections,'' 2008; Lowry and Smith, 2007;Zarecki et al, 2013). Activities associated with increased risk of zoonotic disease transmission from turtles, frogs, and other aquatic animals include direct and indirect contact with the animal, tank, water, filtration equipment, or other tank contents. ...
... Ingestion of terrarium or aquarium water can transmit zoonotic pathogens to NTP owners and anyone in contact with the tank. Those who work with aquatic animals are at risk for occupational exposure (Lowry and Smith, 2007 the first known illnesses linked to African dwarf frogs in the United States (Zarecki et al, 2013). This outbreak spanned at least 3 years and caused illnesses predominantly among children (see call out box). ...
... Zoonotic and other animal-to-human infections are strongly implicated in global disease ( Krauss et al., 2003 ;Brown, 2004 ;Kruse et al., 2004 ;Karesh et al., 2005 ;Chomel et al., 2007 ;Brugere-Picoux & Chomel, 2009 ;Aiken et al., 2010 ;Hale et al., 2012 ;Karesh et al., 2012 ;Nenoff et al., 2012 ;Smith et al., 2012 ;Zarecki et al., 2013 ;Broens & van Geijlswijk, 2018 ), including the most significant pandemics, for example, Spanish flu (1918), Asian flu (1957)(1958), HIV-AIDS (1981-present), swine flu (2009), and SARS-Cov-2 (2019-present), with each of these pandemics causing approximately 50 m, 1.1 m, 30 m, 150,0 0 0-575,0 0 0, and > 2.4 m deaths, respectively ( Bean et al., 2013 ;CDC, 2020a , b ;Lau et al., 2020 ;Sharp & Hahn, 2011 ;Gibbs et al., 2009 ;WHO, 2020a , b ;Xiao et al., 2020 ), and both established and emergent human infections can be linked to wild animal species ( Brown, 2004 ;Chomel et al., 2007 ). In addition, injuries to humans are associated with both wild pet species ( Warwick & Steedman, 2012 ;Ng et al., 2018 ) and domesticated dogs and cats ( De Keuster & Overall, 2011 ;Babovic et al., 2014 ). ...
Pet trading and keeping globally involves at least 13,000 species, and at least 350 million individual non-domesticated or ‘wild pet’ animals annually. In addition, over 445 million domesticated dogs and cats are thought to occupy homes worldwide. Several major problematic concerns are associated with pet keeping, in particular linked to non-domesticated or wild pet forms, including: animal welfare; species conservation; public health and safety; antimicrobial resistance; agricultural animal health; invasive alien organism introductions; and poor information uptake by the public. Regulation of both domesticated and wild pets characteristically involves negative list systems, under which all trading and keeping problems continue to burgeon. Negative lists involve the itemization of animal types that are monitored, restricted or banned in the context of trading and keeping, with all non-listed animals essentially being unregulated. In contrast, positive lists involve the itemization of animal types that are permitted for trading and keeping, with all non-listed animals essentially being barred. Compelling rationales, as well as an important scientific evidence-base, strongly indicate replacement of historically common negative list approaches with objective positive list systems to better regulate the sale and keeping of both wild pet and domesticated pet animals. This report aims to produce a novel method for developing positive lists that meets several criteria that we considered to be fundamental to a robust decision-making protocol: operational objectivity; quantitative algorithm design; no or negligible consensus-based decision-making; binary results; independent repeatability; user-friendliness; resource efficiency; optional use alongside other methods.
... Salmonella as a pathogen Salmonella is an enteric pathogen but is also ubiquitous and can be found in a wide variety of hosts including companion animals, farm animals and wild animals, as well as plants and insects (Brooks et al. 2001;Guo et al. 2002;Natvig et al. 2002;Holt et al. 2007;Dolejska et al. 2009;Mettee Zarecki et al. 2013;Bartholomew et al. 2014;Basler et al. 2016;Bosch et al. 2016). Salmonella has been traditionally considered as a foodborne bacteria that is transmitted through contaminated meat and animal products, but Salmonella infections through other transmission routes, such as contaminated fresh produce, contact with infected animals and contaminated water and soil, are commonly reported as well (Ailes et al. 2013;Jackson et al. 2013;Marus et al. 2019). ...
Surface water is prone to bacterial contamination as it receives wastes and pollutants from human and animal sources, and contaminated water may expose local populations to health risks. This review provides a brief overview on the prevalence and antimicrobial resistance (AR) phenotypes of Salmonella, Escherichia coli, and Enterococcus, found in natural freshwaters. These bacteria are frequently detected in surface waters, sometimes as etiological agents of waterborne infections, and AR strains are not uncommonly identified in both developed and developing countries. Data relating to Salmonella, E. coli, and Enterococcus present in environmental water are lacking, and in order to understand their development and dissemination using the One Health approach, understanding the prevalence, distribution, and characteristics of the bacteria present in surface water as well as their potential sources is important. Furthermore, AR bacteria in natural watersheds are not well investigated and their impact on human health and food safety are not well understood. As surface water is a receptacle for AR bacteria from human and animal sources and a vehicle for their dissemination, this is a crucial data‐gap in understanding AR and minimizing its spread. For this review, Salmonella, E. coli, and Enterococcus were chosen to evaluate the presence of primary pathogens and opportunistic pathogens as well as to monitor AR trends in the environmental water. Studies around the world have demonstrated the widespread distribution of pathogenic and AR bacteria in surface waters of both developing and developed countries, confirming the importance of environmental waters as a reservoir for these bacteria and the need for more attention on the environmental bacteria for emerging AR.
... Amphibians, including snails, frogs, and toads, have been associated with the transmission of Salmonella infections in human [24,85,89]. Recently, a study described that aquatic frogs, namely, African dwarf frogs, have been associated with Salmonella outbreak predominantly occurring in children during 2008 through 2011 in the United States [90]. In the same outbreak, an estimated 29% of the patients were hospitalized for one to nine days, with a median of four days. ...
... Likewise, all high-risk persons, including children below five years of age, the elderly, pregnant women, and immunocompromised persons, should not be exposed to African dwarf frogs and associated water [94]. It has been observed that public awareness regarding reptile and amphibian-associated salmonellosis is low [90]. A recent study revealed that only 38% of patients interviewed were aware of the risk of Salmonella illness from exposure to reptiles, and only 18% were familiar with the risk of Salmonella infection from amphibians [90]. ...
... It has been observed that public awareness regarding reptile and amphibian-associated salmonellosis is low [90]. A recent study revealed that only 38% of patients interviewed were aware of the risk of Salmonella illness from exposure to reptiles, and only 18% were familiar with the risk of Salmonella infection from amphibians [90]. Although, CDC's Healthy Pets Healthy People Web site (https://www.cdc.gov/healthypets/index.html) [95] published educational flyers on Salmonella infections from animal contact, public awareness of the risk illness from reptiles and amphibians has not expanded as expected. ...
Non-typhoidal Salmonella (NTS) infection is one of the major causes of diarrheal disease throughout the world. In recent years, an increase in human S. Javiana infection has been reported from the southern part of the United States. However, the sources and routes of transmission of this Salmonella serotype are not well understood. The objective of this study was to perform a systematic review of the literature to identify risk factors for human S. Javiana infection. Using PRISMA guidelines, we conducted a systematic search in Web of Science, PubMed, and the Morbidity and Mortality Weekly Report (MMWR). Searches returned 63 potential articles, of which 12 articles met all eligibility criteria and were included in this review. A review of the literature indicated that both food and non-food (such as animal contact) exposures are responsible for the transmission of S. Javiana infection to humans. Consumption of fresh produce (tomatoes and watermelons), herbs (paprika-spice), dairy products (cheese), drinking contaminated well water and animal contact were associated with human S. Javiana infections. Based on the findings of this study, control of human S. Javiana infection should include three factors, (a) consumption of drinking water after treatment, (b) safe animal contact, and (c) safe food processing and handling procedures. The risk factors of S. Javiana infections identified in the current study provide helpful insight into the major vehicles of transmission of S. Javiana. Eventually, this will help to improve the risk management of this Salmonella serotype to reduce the overall burden of NTS infection in humans.
... In the Netherlands, reptile-associated salmonellosis was studied during a 30-year period (1985-2014) and a significant annual increase of 19% was found in reptile-associated salmonellosis in humans [29]. Amphibians are also associated as a source of human Salmonella [30], but in our study amphibians were not assumed to be as relevant as reptiles as much lower numbers were imported. However, this number might be highly underestimated as many amphibians are imported along with, and classified as, live ornamental fish [23]. ...
The trade in live animals and animal products is considered one of the major drivers of zoonotic disease emergence. Schiphol airport in the Netherlands is one of the largest European airports and is considered a main hub for legal and illegal import of exotic animals. However, so far there is little information about what pathogens these imported animals might carry with them. Therefore, this study aimed to assess the zoonotic risks of exotic animals imported into the Netherlands through Schiphol airport in 2013 and 2014. Based on a previous list of highly prioritised emerging zoonoses for the Netherlands (EmZoo list), WAHID and Promed databases, literature and expert opinions, a list of 143 potentially relevant zoonotic pathogens was compiled. In a step-wise selection process eighteen pathogen-host combinations that may pose a public health risk by the import of exotic animals via Schiphol airport were identified and these were assessed by expert elicitation. The five pathogens with the highest combined scores were Salmonella spp., Crimean-Congo haemorrhagic fever virus, West Nile virus, Yersinia pestis and arenaviruses, but overall, the public health risk of the introduction of these exotic pathogens into the Netherlands via the legal import of exotic animals was considered low. However, the vast majority of imported exotic animals were imported by trade companies, increasing the risk for specific groups such as retail and hobbyists/pet owners. It is expected that the risk of introduction of exotic zoonotic pathogens via illegal import is substantial due to the unknown health status. Due to changing trade patterns combined with changing epidemiological situation in the world and changing epidemiological features of pathogens, this risk assessment needs regular updating. The results could give directions for further adjusting of health requirements and risk based additional testing of imported exotic animals.
... Poona, and S. enterica ser. Javiana are associated with melon related outbreaks (Zarecki et al., 2013). The investigations undertaken by the United States Food and Drug Administration (FDA) suggested that submerging warm cantaloupes in cool dump tank water may have facilitated their contamination by infusion of dump tank water contaminated with Salmonella into the cantaloupe tissue via stem scars or surface pores. ...
... Since 100% down to 25% of cantaloupe extracts yielded the same biofilm levels, the 25% extract (50 mg/ml) was chosen as the highest concentration and 1% extract (2 mg/ml) as the lowest concentration for biofilm experiments. Four outbreak strains of S. Poona were used in this study due to their incidence associated with the melon industry (Zarecki et al., 2013). In addition, one outbreak strain each of S. Stanley and S. Montevideo associated with other fruits and vegetables outbreaks were also used for biofilm formation in cantaloupe extracts. ...
Salmonella enterica is responsible for the highest number of foodborne disease outbreaks pertaining to cantaloupe industry. The objective of this study was to examine the growth and biofilm formation by outbreak strains of S. enterica ser. Poona (S. Poona), S. enterica ser. Stanley (S. Stanley) and S. enterica ser. Montevideo (S. Montevideo) on different food-contact processing surfaces in cantaloupe flesh and peel extracts at 22 °C and 10 °C. The generation time of all S. enterica strains tested was shorter in the high concentration (50 mg/ml) of cantaloupe extract and high temperature. In 50 mg/ml of cantaloupe flesh or peel extract, the populations of S. enterica were increased by 5 log CFU/ml in 24 h at 22 °C and 1 log CFU/ml in 72 h at 10 °C. In 2 mg/ml of cantaloupe flesh or peel extracts, the populations of S. enterica were increased by 3.5 log CFU/ml in 56 h at 22 °C, but there were no changes in 72 h at 10 °C. The biofilm production of S. enterica was greater at 50 mg/ml of cantaloupe extract and 22 °C, but no major differences (P ≥ 0.05) were found among the strains tested. In 50 mg/ml cantaloupe extract, S. enterica produced 5-6 log CFU/cm2 biofilm in 4-7 d at 22 °C and approximately 3.5-4 log CFU/cm2 in 7 d at 10 °C. In 2 mg/ml of cantaloupe extract, S. enterica produced 4-4.5 log CFU/cm2 biofilms in 4-7 d at 22 °C and 3 log CFU/cm2 in 7 d at 10 °C. Biofilm formation by S. Poona (01A4754) was lowest on buna-n rubber compared to stainless steel, polyethylene and polyurethane surfaces under the majority of conditions tested. Overall, these findings show that S. enterica strains can grow rapidly and form biofilms on different cantaloupe processing surfaces in the presence of low concentrations of cantaloupe flesh or peel extracts.
... 14 Enteric disease outbreaks among visitors to fairs, farms, petting zoos, and other public settings are well documented. Cattle, sheep, or goats 15,17,20,21,[26][27][28]30,31,34,36,38,40 have typically been identified as sources for infection; however, live poultry, 16,[41][42][43][44][45][46][47][48] rodents, [49][50][51][52][53] reptiles, 33,54-60 amphibians, 61 and other domestic 4,62,63 and wild 4 animals also are established sources. Animals that appear healthy can carry pathogens that cause illness in people. ...
... Animals that present a high risk for human Salmonella spp infections and have been implicated as sources of outbreaks of human illness include poultry (eg, chicks, chickens, and ducklings) 16,[41][42][43][44][45][46][47][48][69][70][71][72] ; reptiles (eg, turtles, snakes, or lizards) 33,[54][55][56][57][58][59][60][73][74][75][76][77][78][79][80] ; and amphibians, especially frogs. 61,[81][82][83] From 1990 through 2014, 53 disease outbreaks linked to live poultry in the United States have been documented. 16,43,69,84 Some of the ill persons in those outbreaks reported contact with live poultry at feed stores, 16,43,69 schools or daycare facilities, 16,41,69 fairs, 69 petting zoos, 69 and nursing homes (CDC, unpublished data, 2010). ...
... Ill people included those who reported acquiring frogs at carnivals, pet stores, and other retail stores. 61,82 Activities associated with increased risk of zoonotic disease transmission from turtles, frogs, and other aquatic animals include direct and indirect contact with the animal, tank, water, filtration equipment, or other tank contents. These findings have implications for risk of infection from aquatic exhibits (eg, aquariums and aquatic touch tanks). ...
... Veterinarians can reinforce these messages by recommending reptiles as pets only for households with children >5 years of age and by providing detailed instruction to clients on proper reptile care and practices to prevent zoonoses. Healthcare providers for humans and animals can make educational literature available in waiting rooms and provide information on websites and in newsletters (36,37). Suitable educational materials are available in multiple formats and languages on the CDC Zoonotic Diseases (Diseases from Animals) website (http://www.cdc.gov/zoonotic/gi). ...
During 2006-2014, a total of 15 multistate outbreaks of turtle-associated salmonellosis in humans were reported in the United States. Exposure to small pet turtles has long been recognized as a source of human salmonellosis. The risk to public health has persisted and may be increasing. Turtles are a popular reptilian pet among children, and numerous risky behaviors for the zoonotic transmission of Salmonella bacteria to children have been reported in recent outbreaks. Despite a long-standing federal ban against the sale and distribution of turtles <4 in (<10.16 cm) long, these small reptiles can be readily acquired through multiple venues and continue to be the main source of turtle-associated salmonellosis in children. Enhanced efforts are needed to minimize the disease risk associated with small turtle exposure. Prevention will require novel partnerships and a comprehensive One Health approach involving human, animal, and environmental health.
... Protocols should be established for aquarium management, including measures to reduce contamination of the environment with aquarium water. Because of the increased risks associated with reptiles (eg, aquatic turtles) 62 and amphibians (eg, African dwarf frogs), 63 aquatic reptiles should not be kept in aquariums in healthcare facilities. III. ...
Animals in Healthcare Facilities: Recommendations to Minimize Potential Risks - Volume 36 Issue 5 - Rekha Murthy, Gonzalo Bearman, Sherrill Brown, Kristina Bryant, Raymond Chinn, Angela Hewlett, B. Glenn George, Ellie J.C. Goldstein, Galit Holzmann-Pazgal, Mark E. Rupp, Timothy Wiemken, J. Scott Weese, David J. Weber
