Journal of Zoo and Wildlife Medicine 44(1): 8–14, 2013 Copyright 2013 by American Association of Zoo Veterinarians
PREVALENCE OF SALMONELLA ENTERICA SEROVAR ALBANY IN ´ N ZOO IN MEXICO CAPTIVE ZOO WILD ANIMALS IN THE CULIACA Gabriela Silva-Hidalgo, D.V.M., M.S., He´ctor Samuel Lo´pez-Moreno, Ph.D., Vianney Francisco Ortiz-Navarrete, M.S., Ph.D., Celia Alpuche-Aranda, M.D., Ph.D., Jose´ Guadalupe Rendo´nMaldonado, M.S., Ph.D., Jose´ Angel Lo´pez-Valenzuela, M.S., Ph.D., Martin Lo´pez-Valenzuela, D.V.M., M.S., and Felipe Jua´rez-Barranco, M.S., Ph.D.
Abstract: Salmonellosis is an important zoonotic disease but little is known about the role that free-living animals play as carriers of this pathogen. Moreover, the primary route of infection in the wild needs to be elucidated. The aim of this study was to determine the source and the route of transmission of Salmonella enterica serovar Albany (S. Albany) infection in captive zoo wild animals in the Culiaca´n Zoo. A total of 267 samples were analyzed including 220 fecal samples from zoo animals, 15 fecal samples from rodents, 5 pooled samples each of two insects (Musca domestica and Periplaneta americana), and 22 samples of animal feed. We detected S. Albany in 28 (10.5%) of the samples analyzed, including in samples from raw chicken meat. Characterization of isolates was performed by serotyping and pulsed-field gel electrophoresis. All isolates shared a single pulsed-field gel electrophoresis profile, indicating a possible common origin. These data suggest that the infected meat consumed by the wild felines was the primary source of infection in this zoo. It is likely that the pathogen was shed in the feces and disseminated by insects and rats to other locations in the zoo. Key words: Albany, carriers, feces, insects, Salmonella, wild animals, zoo.
and avian populations. Recent attention has turned to wildlife populations, but they are difficult to assess, making sampling for epidemiologic studies a challenge.35 For this reason, the prevalence of Salmonella in wild populations is largely unknown. Many domestic and wild animals colonized by Salmonella harbor the bacteria in their gastrointestinal tracts with no apparent signs of illness.33 Hence, Salmonella spp. may be present in feces excreted by healthy animals and can persist in the environment until they encounter conditions suitable for growth; the persistence of Salmonella spp. and serovars in the environment is an important characteristic in their epidemiology.40 In modern zoos, animals are kept in naturallooking environmental surroundings and animals, including nonpoisonous reptiles and mammals, are often allowed to roam freely in exhibits. There may be no fences so that visitors can touch the animals; this allows the possibility of contact with animal feces or contaminated surfaces. Indeed, many events at zoos are designed to allow visitors to come in close contact with the animals. In addition to direct transmission via animals to humans, Salmonella, which is relatively resistant to the environment, can be indirectly transmitted to humans through contact with a contaminated exhibit.16 Outbreaks of salmonellosis in humans have been associated with contact with animals. In 1996, an outbreak occurred among individuals who attended a lizard exhibit at the Denver Zoo (Colorado,
INTRODUCTION The genus Salmonella, which belongs to the family Enterobacteriaceae, is classified into two species, Salmonella enterica and Salmonella bongori (formerly S. enterica serotype V). More than 2,500 serovars of S. enterica are currently recognized based on O and H antigen typing.13 Salmonella enterica serovars have been isolated from numerous species of free-living and captive mammals, with many studies focusing on agricultural animals From the Programa Regional del Noroeste para el Doctorado en Biotecnologı´ a, Facultad de Ciencias Quı´ mico-Biolo´gicas, Ciudad Universitaria, Av. Americas S/ N, Universidad Auto´noma de Sinaloa, Culiaca´n, Sinaloa, 80010, Me´xico (Silva-Hidalgo, Lo´pez-Moreno, Rendo´nMaldonado, J. A. Lo´pez-Valenzuela). Present addresses (Silva-Hidalgo): Rio Mocorito 140-A ote. Col. Guadalupe, Culiaca´n, Sinaloa, 80220, Me´xico; (Ortiz-Navarrete): Departamento de Biomedicina Molecular, Centro de Investigacio´n y de Estudios Avanzados (CINVESTAV), Instituto Polite´cnico Nacional, Av. Instituto Polite´cnico Nacional No. 2508, Col. San Pedro Zacatenco, 07360 Me´xico, D.F., Me´xico; (Alpuche-Aranda): Instituto de Diagno´stico y Referencia Epidemiolo´gicos (InDRE), Carpio No. 470 Col. Santo Tomas, 11340 Me´xico, D.F., Me´xico; (Jua´rez-Barranco, Lo´pez-Valenzuela): Laboratorio de Patologı´ a, Facultad de Medicina Veterinaria y Zootecnia, Universidad Auto´noma de Sinaloa, Boulevard San Angel s/n, Fracc. San Benito, CP 80246, Culiaca´n, Sinaloa, Me´xico. Correspondence should be directed to Dr. Silva-Hidalgo (gaby@uas. uasnet.mx or
[email protected]). 8
SILVA-HIDALGO ET AL.—S. ALBANY IN ZOO WILD ANIMALS IN MEXICO
USA).9 In more recent years, numerous cases of reptile-associated salmonellosis have been reported in Europe, Asia, and Canada.11,26,42 Several outbreaks of multidrug-resistant Salmonella enterica serovar Typhimurium infection associated with veterinary facilities have been reported by the Centers for Disease Control and Prevention.4 Although these sources are not usually responsible for large outbreaks, they may be responsible for sporadic cases that occur in families that have contact with animals or contaminated fomites. Mammals in a zoo can be infected by Salmonella as well, and transmission among animals within an exhibit or cage has been documented.34 Furthermore, animals in an outdoor exhibit can be infected with Salmonella by contact with free-living animals such as birds and rats.19 Salmonella enterica Albany, a serovar frequently associated with meat products of avian origin, has been detected in exported frozen chickens from Thailand destined for human consumption41 and on carcasses, utensils, and work surfaces in broiler slaughterhouses in Brazil.10 In Mexico, research studies about food-borne pathogens are extremely limited. One of the few studies reported in this country was published in 1997, where Salmonella was isolated in Mexican farm animals from 1989 to 1993.2 The samples were collected from various farm animals and 122 isolates were recovered during the study. Chicken feces were the most contaminated samples (33.6% of isolates).2 Another study isolated S. Albany from chicken meat44 and another study reported that S. Albany was in the top 10 most-common serovars isolated from clinically ill humans, asymptomatic children, and retail meats.45 In Culiaca´n Valley (Mexico), 20 different S. enterica subsp. enterica serovars were recovered from domestic animals hosts. Salmonella enterica Albany was isolated from chicken farms located in the mountainsides next to the urban zone of Culiaca´n City.17 This finding suggests that chickens are important reservoirs of S. Albany in Mexico,44 where it is one of the most prevalent pathogens of poultry farms, presenting a potential risk to human and animal health.8 To establish the source of primary infection and transmission of S. Albany in captive wild animals, this investigation was conducted at the Culiaca´n Zoo.
MATERIALS AND METHODS Sample collection, culture, and screening of Salmonella Once daily during the first week of the months of October in 2007 and January and August in
9
2008, fresh feces were collected from the cages of every captive mammal, bird, and reptile species in the zoo, as well as fresh feces from rodents (Rattus spp.) and insects living in close contact with the cages. Moreover, samples of the different types of feed offered to the zoo animals were collected. Fecal samples: Fecal samples from rodents were collected indoors and within and around cages. Rodents have been reported to be reservoirs of different serotypes of Salmonella spp.14 and have been implicated in contaminating foods with the pathogen and transmitting the pathogen on livestock farms.21,22 The goal of this study was to determine the importance of free-living animals as a vector for the transmission and persistence of Salmonella within or between cages. The feces were characterized by their form and size. Freshly voided feces were collected from the animal cages or enclosures, with the exception of snake feces, which was obtained from randomly selected animals by cloacal swab. Fecal samples from cages were collected as follows. For cages housing ,5 animals, one sample was randomly collected on each sampling day while for cages containing .5 animals, two randomly selected fecal samples were collected. As a routine, the first freshly voided droppings or feces encountered in the enclosures were sampled. In cases where two samples were obtained, the second was taken from feces farthest away from the first. Insect samples: Different species of flies (Musca domestica) and cockroaches (Periplaneta americana) were collected using netting at or around cages; they were kept in plastic containers and individuals were grouped and macerated for enrichment culture. Food samples: Representative samples of food destined for omnivores, carnivores, and herbivores were collected from the zoo kitchen. In total, 267 samples were analyzed including 220 samples from zoo animals, 15 samples from rodents, 5 pooled samples of the two types of insects (M. domestica and P. americana), and 22 samples of animal feed. All samples were transported to the laboratory on ice in sterile plastic containers within 2 hr of collection and were placed in 10 ml of tetrathionate broth (Difco, Detroit, Michigan, 48201, USA), to enrich for Salmonella species, and incubated overnight at 378C. This media has been previously suggested for Salmonella isolation from clinically healthy carriers.24 The following day of incubation, the tetrathionate broth was subcultured into Rappaport-Vassiliadis broth (Difco) and incubated overnight at 428C. After incubation, the suspen-
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sion was plated on xylose lysine tergitol (XLT4) agar (Difco) and incubated at 378C overnight. Colonies with black centers were selected and isolated. The media used are all selective media for Salmonella. The recovery process included a primary enrichment with tetrathionate broth and Rappaport-Vassiliadis broth. Pre-enrichment is usually suggested when samples with low numbers of Salmonella are expected. All of the samples used in the current study originated from animals not clinically ill. The selectivity of tetrathionate broth is accomplished by the combination of sodium thiosulfate and tetrathionate, which suppresses commensal intestinal organisms. Tetrathionate is formed in the medium upon addition of the iodine and potassium iodide solution. Organisms containing the enzyme tetrathionate reductase will proliferate in the medium. In the case of Rappaport-Vassiliadis broth, Salmonella spp. are enriched because the bacteria are better able to survive the high osmotic pressure in the medium and because they can multiply at a relatively lower pH and higher temperatures compared with other enteric bacteria.29 The importance of suppressing Salmonella-competing bacteria in the original sample is to allow Salmonella to grow to the level of detection by the plating media applied, in this case XLT4, a highly selective plating medium.32,37 Differentiation of Salmonella from other organisms that also grow on this medium is based on fermentation of xylose, lactose, and sucrose, decarboxylation of lysine, and the production of hydrogen sulfide. Typical Salmonella colonies (H2S-positive) appear black or black-centered with a yellow periphery. Characterization of Salmonella isolates Confirmation of the isolates as Salmonella and standard serological typing was performed at the Epidemiology Reference Institute (InDRE; D.F., 11340, Me´xico), the national reference center for salmonellosis. Pulsed-field gel electrophoresis (PFGE) was used to establish relatedness and diversity among Salmonella isolates. PFGE was performed in accordance with the PulseNetEurope protocol.30 Genomic DNA was digested with XbaI (Roche Diagnostics GmbH, Mannheim, Baden-Wuerttemberg, 68305, Germany) and analyzed in 1% agarose gels (Bio-Rad, Hemel Hempstead, Hertfordshire, HP2 7TD, United Kingdom) in 0.53 TBE buffer at 148C using the CHEF Mappert system (Bio-Rad). The runtime was 18 hr at 6 V/cm, with initial and final switch times of 2.16 and 54.17 sec, respectively. XbaI-
digested genomic DNA from Salmonella enterica serovar Braenderup H9812 was used as a molecular size marker. Thiourea (50 ll) was added to the running buffer to prevent DNA degradation.31 Images were analyzed with the InfoQuestFP software (Bio-Rad). Isolates were allocated a different PFGE type when a genetic difference could be detected. Cluster analysis was performed using the Jaccard coefficient and the unweighted pair group method with arithmetic averages.
RESULTS Salmonella enterica Albany was detected in 28 (10.5%) of the samples analyzed. Table 1 reports the distribution of the Salmonella isolates by animal type and Table 2 documents the culturepositive animal feed. These results indicate a relatively high prevalence rate of Salmonella isolation at this zoo when compared with other studies reporting prevalence rates of approximately 5–7%.11 PFGE analysis of XbaI DNA fragments of these isolates displayed identical patterns (Fig. 1), indicating that these isolates are either clonal types from different sources or had a common origin.
DISCUSSION The relatively high prevalence of Salmonella infection found in this study may have resulted from either contaminated food, contaminated fomites, or by contamination of the environment by infected insects or rodents. The isolation of clonal strains from different sources may possibly be explained by insects or rodents acting as vehicles for Salmonella transmission between cages.25 Another possible transmission route could have been the food or serving utensils; nevertheless, in this investigation Salmonella was only isolated from the raw chicken meat and the insect samples. Many insects are thought to be carriers of pathogens, and cockroaches are known to carry diverse pathogenic bacteria and may possibly contribute to disease transmission. Insects and cockroaches may acquire Salmonella naturally from the animal and human-polluted environment.7 Cockroaches carrying Salmonella are the natural prey of a variety of animals and birds and may contribute to the spread of bacteria within the zoo via that route.20 Other animals that may contribute to the dissemination of S. Albany in the zoo are the flies and rodents. Some investigators have found Salmonella in the intestines and feces of these insects and rodents.15,27,43 In this study, all the Salmonella isolates obtained were
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SILVA-HIDALGO ET AL.—S. ALBANY IN ZOO WILD ANIMALS IN MEXICO
Salmonella enterica serovar Albany-positive cages or enclosures.
Table 1.
Class
Birds (feces samples) Aquatic birds (water, feces, and soil samples)
Mammals (feces samples)
Fishes (water sample) Rodentsc (feces samples) Insects (group)d Food Total
Common name
Scientific name
Scarlet macaw White pelican Swan goose Greylag goose Mallard duck Mandarin duck Black-bellied whistling-duck Yellow-bellied fiddler duck Bobcat Ocelot Cougar African lion Sumatran tiger American black bear Hippopotamus Nile tilapia Goldfish Black rat Flies Cockroaches Raw chicken meat
Ara macao Pelicanus erythrorhynchos Anser cygnoides Anser cygnoides Anas platyrhynchos Aix galericulata Dendrocygna autumnalis Dendrocygna bicolor Lynx rufus Leopardis pardalis Felis concolor Panthera leo Panthera tigris sumatrae Ursus americanus Hippopotamus amphibius Oreochromis niloticus Carassius auratus Rattus spp. Musca domestica Periplaneta americana
No. of isolatesa
1 5b
2 2 1 1 2 1 1 1 3 3 3 2 28
Salmonella colonies isolated from enrichment culture and serotyping as S. Albany. Samples correspond to a conglomerate of feces of all the birds that coexist in the same cage. c Characteristics of the feces considered for this item; rat droppings area about one-half inch to three-quarters inch in length. d Each group was composed of two to five insects. a
b
Table 2. Salmonella enterica serovar Albany-positive animal food. Groups based eating habits
Herbivores
Omnivores
Carnivores Total
Food
Samples
No. of isolates
Green alfalfa Ground corn Grain concentrate (Purinat) Alfalfa meal Bird seeds Sunflower seeds Peanuts Linseed Rabbit chow (Purina) Dog chow (Purina) Carrots Cucumber Pear Papaw Grapes Apple Banana Sliced bread Lettuce Granola Raw chicken meat
1 1 1
0 0 0
1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 2 22
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 2
epidemiologically related to each other, supporting the hypothesis that transmission occurred via the mobile insects, cockroaches, and rats. Regarding the finding of S. Albany in the raw chicken meat destined as food for the felines, this indicates that poultry and poultry products constitute a significant proportion of the sources implicated in food-borne Salmonella outbreaks.28,38,39 The contamination indicates a potential breakdown of hygiene at various stages of the food processing and distribution chain, a lack of refrigeration of meat, or both. Tropical climates may be more prone to Salmonella outbreaks. Culiaca´n City is tropical, with an annual average temperature of approximately 268C, which may promote replication of Salmonella spp.12 Salmonella spp. have been isolated from feces of exotic felines fed raw meat diets5 and, interestingly, diet modification could diminish the excretion of Salmonella.23 All the strains isolated in this investigation came from clinically healthy animals; that is, no animal was presenting with diarrhea or any sign of a digestive system disorder. Nevertheless, subclinical fecal shedding of S. Albany by exotic felines fed raw diets creates the possibility of zoonotic transmission of disease via direct contact or
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Salmonella spp. in 0.6% of zoos’ animal fecal samples was reported, 20 times more than in domestic farm animals, demonstrating that management practices can limit the spread and prevalence of microbial pathogens.18 In this case, the environment was not sampled; therefore, the transmission could also have taken place through fomites and animal caretakers (i.e., boots and hands) as well as via water run-off. Understanding the factors that contribute to the spread and persistence of Salmonella in animal populations is useful for the development of effective intervention strategies to reduce human or animal exposure to Salmonella. Future study should include attempts to detect Salmonella in the environment or on potential fomites in order to document transmission routes. These findings indicate that the risk of exposure to pathogens via direct or indirect contact with animal feces, or via contact with raw diets, must be considered, particularly with Salmonella. Bacterial contamination of surfaces is also a potential source of infection for humans that visit zoos and animal parks, particularly high-risk individuals such as infants, elderly persons, and immunocompromised individuals.
Figure 1. All strain isolates from zoo wild animals, insects, and raw chicken meat were indistinguishable by PFGE analysis following digestion with restriction endonuclease XbaI.
through environmental contamination. Once in the environment, Salmonella is able to survive long periods of time outside the host, for example in soil or water,3 promoting a cyclic lifestyle with transferences between the host and the environment.40 Salmonella can be spread extensively in the soil and sediment and is frequently isolated from environmental samples of agricultural origin.1 Previous evidence indicates that this bacteria can survive and multiply for at least 1 yr in this ecosystem.6 Furthermore, the bacteria can alter its cell membrane to favor adhesion of Salmonella to the particles of the soil and sediment.36 The limited number of studies in relation to the presence of Salmonella in the environment makes it difficult to understand the prevalence and survival capabilities of these bacteria in natural habitats. In a previous study, the presence of
Acknowledgment: This project was financially supported by the Programa de Fomento y Apoyo a Proyectos de Investigacio´n (PROFAPI-2009/ 172), Direccio´n General de Investigacio´n y Posgrado, Universidad Auto´noma de Sinaloa.
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