Knowledge and Practices of California Veterinarians Concerning the Human Health Threat of Reptile-associated Salmonellosis (1996)

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1 Knowledge and Practices of California Veterinarians Concerning the Human Health Threat of Reptile-associated Salmonellosis (1996) M. Kathleen Glynn1, DVM, MPVM, Jonathan H. Mermin2, MD, MPH; Lisa M. Durso3, MS, Frederick J. Angulo4, DVM, MPVM, PhD, Kevin F. Reilly4, DVM, MPVM 1. Division of Public Health Surveillance and Informatics, Epidemiology Program Office, Centers for Disease Control and Prevention 2. Division of HIV and Aids Prevention, National Center for HIV, STD, and AIDS Prevention, Centers for Disease Control and Prevention 3. University of Nebraska, Lincoln 4. Foodbome and Diarrheal Diseases Branch Division of Bacterial and Mycotic Diseases, National Center for Infectious Diseases, CDC, 1600 Clifton Rd NE, MS D-63, Atlanta, GA USA A bstract: The incidence of human salmonellosis resulting from direct or indirect contact with reptiles has risen markedly in the last few decades. Veterinarians who provide care for reptiles may be a primary source for information on reptile-associated salmonellosis for reptile owners. To assess knowledge and practices about reptile-associated salmonellosis, we conducted telephone interviews with 100 small-animal or exotic-animal veterinarians in California in February Knowledge: Most veterinarians (79%) mentioned salmonellosis as a reptile-associated zoonosis. Although many specifically mentioned turtles or tortoises (78%), fewer mentioned iguanas (52%), other lizards (44%), or snakes (38%). Among 33 self-identified reptile medicine practitioners, only 55% identified immunocompromised persons as having a higher risk for reptile-associated salmonellosis, with fewer mentioning children (46%), HIV-infected persons (36%), elderly persons (24%), or pregnant women (3%). Practice: Among 33 reptile practitioners, only 21 (64%) routinely discussed reptileassociated zoonoses with clients during sick reptile examinations, and only 2 (6%) discussed the same during healthy pet visits. Client education for reptile owners concerning at-risk groups was rare. While 36% of reptile practitioners warned clients that all children were at greater risk for reptile-associated salmonellosis, fewer mentioned immunocompromised persons (15%), HIV-infected persons (12%), or pregnant women (3%); none mentioned elderly persons. Veterinarians who provide care for reptiles should take the opportunity to educate themselves and reptile-owning clients about the threat to human health of reptile-associated salmonellosis Key W ords: salmonellosis, zoonosis, reptile, veterinarian, client education, California. INTRODUCTION The incidence of human salmonellosis resulting from direct or indirect contact with reptiles has markedly increased in the 1990s to an estimated 93,000 infections per year (Mermin, et al, 1998). In the early 1970s, Salmonella infection associated with ownership of small pet turtles was a large public health concern that resulted in an estimated 280,000 annual cases of human salmonellosis (Cohen, et al, 1980). After restrictions were placed on the import and sale of these turtles, the number of cases of reptile-associated salmonellosis dramatically declined (FDA, 1975, Anonymous, 1977, Cohen, et al, 1980). Other reptiles, particularly iguanas, Iguana iguana, have now replaced turtles as popular pets. In 1995, an estimated 7.3 million reptiles were owned by 3% of households in the United States (CDC, 1995). Studies have shown that most, if not all, healthy, asymptomatic reptiles carry Salmonella organism s in their intestinal tract and sporadically shed Salmonella organisms in their feces (Kaura, et al, 1972, Hall and Rowe, 1992, Monzon Moreno, et al, 1995, Burnham, et al, 1998). A study attempting to use antibiotics in reptiles for the express purpose of eliminating Salmonella carriage, although not conducted by veterinarians, was unsuccessful (D Aoust, et al, 1990). Efforts such as this have raised concerns in both human and veterinary medicine about the emergence of antimicrobial-resistant strains of Salmonella. In 1995, in response to the increased incidence of reptileassociated salmonellosis, the Centers for Disease Control and Prevention (CDC) recommended certain precautions to prevent the spread of salmonellosis from pet reptiles. These recommendations (Table 1) were updated in 1996 and again in 1999 (CDC, 1995, Mermin, et al, 1997, CDC, 1999). S im ilar recom m endations were also endorsed by the A ssociation of R eptilian and Amphibian Veterinarians (ARAV) in 1998 (Bradley, et al, 1998). One recommendation was that veterinarians should inform their clients about the Volume 11, No. 2,2001 Journal of Herpetological Medicine and Surgery 9

2 risk of reptile-associated salmonellosis and about ways to prevent the disease. To investigate how veterinarians have responded to the original 1995 recommendations, and to identify areas of future improvement, we assessed the knowledge and practices of 100 veterinarians regarding reptile-associated salmonellosis, with emphasis on the health education of clients and the use of antibiotics to eliminate the Salmonella carrier state in reptiles. Table 1. Centers for Disease Control and Prevention recommendations for the prevention of spread of Salmonella organisms from pet reptiles to humans. Pet store owners, veterinarians and pediatricians should provide information to owners and potential purchasers of reptiles about the risk of acquiring salmonellosis from reptiles. Persons should always wash their hands thoroughly with soap and water after contact with reptiles or reptile cages. Persons at increased risk for infection or serious complications of salmonellosis (e.g., children <5 years of age and immunocompromised persons) should avoid contact with reptiles. Pet reptiles should be kept out of households in which children <1 year of age and immunocompromised persons live. Families expecting a new child should remove the pet reptile from the home before the infant arrives. Pet reptiles should not be kept in childcare centers. Pet reptiles should not be allowed to roam freely throughout the home or living area. Pet reptiles should be kept out of kitchens and food-preparation areas to prevent contamination. Kitchen sinks should not be used to bathe reptiles or to wash their dishes, cages, or aquariums. If bath- tubs are used for these purposes, they should be cleaned thoroughly and disinfected with bleach. METHODS From February 15 through 21, 1996, we conducted a telephone survey of a random sample of veterinarians listed in the 1995 Directory of the C alifornia Veterinary M edical Association. This directory includes all veterinarians licensed to practice veterinary medicine in California. Only those veterinarians with a correct business telephone number listing in the directory were included in the survey. Three interviewers attempted to contact all eligible veterinarians between 8:00 AM and 7:00 PM on the weekdays. Up to five attempts were made to contact each eligible veterinarian. Interviews were conducted only with veterinarians whose practice consisted, at least partially, of small-animal or exotic-animal medicine. The interview was conducted with a standardized questionnaire consisting of 16 open-ended and yes/no questions. The questions addressed the proportion of the veterinary practic e s caseload devoted to reptiles, the know ledge and practices regarding the potential health risks (specifically for salmonellosis) of reptile ownership, and routine antibiotic use in reptiles. Statistical analysis was performed using Epi Info version 6.04b (CDC, 1996). For the analysis, veterinarians who reported providing medical care to reptiles were categorized as reptile practitioners, and reptile practitioners who described themselves as specialists in reptile medicine were categorized as reptile experts. We used the x2 test to compare proportions and the W ilcoxon tw o-sam ple test to compare distributions between groups. We used the Yates corrected or Fisher s exact P-value to determine significance; a P-value <0.05 was considered significant. RESULTS Survey Group: Of the 5,563 California veterinarians listed in the 1995 Directory of the California Veterinary Medical Association, 327 (6%) were randomly selected, of whom 189 (58%) had a correct business telephone listing. O f these veterinarians, 137 (72% ) reportedly were sm all-anim al or exotic-animal practitioners. Interviews were conducted with 100 (73%) of these 137 veterinarians; 37 (27%) of the 137 veterinarians contacted were not interviewed because 9 (7%) were on extended leave from their practice during the study period, 25 (18%) were not available for any of our 5 telephone calls, and 3 (2%) declined to participate in the survey. Eighty-three (83%) of the 100 respondents were men. The median year of graduation from veterinary school for all respondents was 1975 (range, ). Thirty-three (33%) of the 100 interviewed veterinarians were categorized as reptile practitioners. Seven (21%) of the reptile practitioners considered themselves reptile experts. A median of 9% (range, 1-20%) of the reptile experts practice was dedicated to reptile medicine. This is compared to a significantly lower median of 1% (range, 1-10%) for non-expert reptile practitioners, who were defined as those surveyed veterin arian s designated as reptile p ractitio n ers, but not additionally designated as reptile experts (P=0.0001). The seven reptile experts examined a median of 27 reptiles per month (range, 2-85%), which was significantly greater than the median of two reptiles per month examined by non-expert reptile practitioners (range, 0-26%; F=0.001). The reptile practitioners (expert and non-expert) examined a mean of one iguana (range, 0-45%), less than one turtle or tortoise (range, 0-15%), less than one other lizard (range, 0-15%), and less than one snake (range, 0-12%) per month. Reptile experts also examined significantly more reptiles from each category and saw more reptiles for healthy-pet examinations than did non-expert reptile practitioners. The median percentage of reptile visits that were for routine physical examinations was 10% (range, 0-90%) among reptile experts and <1% (range, 0-90%) among non-expert reptile practitioners. Knowledge: A high proportion (79%) of veterinarians specifically mentioned salmonellosis when asked to name a reptile-associated zoonosis (Table 2). Reptile practitioners were more likely to know about reptile-associated salmonellosis than were surveyed non-reptile practitioners (91% vs. 73%, respectively), but this difference was not significant (/M1.07). When comparing knowledge about different reptile groups, reptile practitioners were more likely than were surveyed n o n -rep tile p ra ctitio n ers to know about iguana-associated salmonellosis (70% vs. 43%, respectively; P=0.02) and other lizard-associated salmonellosis (64% vs. 34%, respectively; P=0.01). Reptile experts were not significantly more likely than non-expert reptile practitioners, however, to know about reptile-associated salmonellosis or about salmonellosis associated with a specific reptile group. Journal of Herpetological Medicine and Surgery Volume 11, No. 1,2001

3 Of the 100 veterinarians surveyed, 74 (74%) believed that healthy, asymptomatic reptiles could spread Salmonella organisms; this percentage did not vary significantly between reptile practitioners and other veterinarians, or between reptile experts and non-expert reptile practitioners. Seventy-nine (79%) veterinarians knew that some groups of humans were at greater risk than were others for contracting salmonellosis from pet reptiles. Among these veterinarians, the most frequently identified at-risk groups were immunocompromised persons or persons infected with human immunodeficiency virus (HIV) (72%), children (54%), and the elderly (27%). Additional results are shown in Table 3. Of the 54 veterinarians who identified either all children or children of specific ages as being at greater risk, only two (4%) specifically mentioned children younger than one year, and two (3%) specifically mentioned children younger than five years. Practice: Of the 33 reptile practitioners, 21 (64%) routinely discussed reptile-associated zoonoses with clients when exam ining a sick reptile, and only two (6%) discussed zoonoses when examining a healthy reptile. Although 21 reptile practitioners routinely gave clients recommendations for preventing the spread of Salmonella from pet reptiles, only 15 (71%) gave such recommendations for all species of reptiles. Of the 21 reptile practitioners who routinely gave clients recommendations, 19 (90%) gave verbal recommendations, four (19%) gave out a leaflet or brochure, and one (5%) recomm ended a book. R eptile experts were no m ore likely to Table 2. Knowledge of 100 surveyed veterinarians regarding reptile-associated zoonoses of specific reptile groups and regarding salmonellosis as a reptile-associated zoonosis, California, Reptile Group Knew of a zoonosis associated Mentioned salmonellosis as a with a specific reptile group (%) reptile-associated zoonosis (%) Turtle or tortoise Iguana Snake Other lizards Any reptile Table 3. Knowledge and practice of surveyed California smallanimal or exotic-animal veterinarians regarding specific groups at increased risk for contracting salmonellosis from pet reptiles. provide recommendations than were non-expert reptile practitioners. Among those same 21 veterinarians, 19 (90%) recommended washing hands after handling reptiles or cages; other less common recommendations included practicing good hygiene (43%), keeping reptiles away from food and food preparation areas (14%), not kissing reptiles (4%), and not letting reptiles roam around the house (4%). Although a high proportion, 27 (82%), of the reptile practitioners knew that certain groups were at higher risk for reptile-associated salmonellosis, only 15 (46%) routinely warned clients of this risk, most frequently mentioning children (87%) and immunocompromised or HIV-infected persons (40%) (Table 3). Four (12%) of the non-expert reptile practitioners routinely used antibiotics in healthy reptiles in an attempt to eliminate the presumed Salmonella carrier state. One reported using enrofloxacin, one reported using chloramphenicol, and the other two did not report the antibiotic used. DISCUSSION Among health professionals, veterinarians are perhaps the best-suited to provide accurate information about zoonotic diseases, and studies have shown that some health care providers in human medicine do not feel well informed or com fortable discussing zoonoses w ith their patients (Gorczyca, 1989, Spencer, 1992, Glaser, et al, 1994, Conti, et al, 1995). However, veterinarians have historically not consistently informed their clients about pet-associated zoonoses, including salmonellosis. For example, despite the proven association between dogs and human toxacariasis, only one third of veterinarians routinely discussed this zoonosis with their clients (Harvey, et al, 1991). Knowledge of reptile-associated salmonellosis was quite high among surveyed veterinarians. Almost 80% of all veterinarians surveyed and m ore than 90% of the reptile practitioners knew of salmonellosis as a reptile-associated zoonosis. However, only about two-thirds of the reptile practitioners routinely gave recommendations for preventing the spread of Salmonella organisms from pet reptiles. Very few took the opportunity to discuss reptile-associated zoonoses with clients during visits with healthy reptiles, and only 19% provided any written materials about the topic. This lack of client education may be because even among reptile practitioners, the risk of reptile-associated salmonellosis is not universally appreciated. For example, more than 20% did not know that healthy, asym ptom atic reptiles could spread Salmonella organisms to humans. Identified the group as being at risk Warn clients that the group is at risk Risk Group Percentage non-reptile practitioners (n=67) Percentage reptile practitioners (n=33) Percentage reptile practitioners (n=33) Immunocompromised persons HIV-infected persons All children Pregnant women Elderly persons Asplenic persons Volume 11, No. 2,2001 Journal of Herpetological Medicine and Surgery 11

4 Although studies have shown that all types of reptiles can be asymptomatic carriers of Salmonella (Cambre, et al, 1980, Chiodini and Sundberg, 1981), turtles have been associated with human salmonellosis more frequently than have other reptiles, most likely because of their previous popularity as household pets. Not surprisingly, more veterinarians m en tioned turtles than other reptile groups w hen discussing reptile-associated salmonellosis. However, only slightly more than half of the surveyed veterinarians knew that iguanas were associated with salmonellosis, and fewer than half knew that other lizards or snakes were also associated with human sal monellosis. Since the restrictions on the sale of small turtles were enacted, iguanas have become pets that are more com mon and have been frequently associated with salmonellosis (Ackm an, et al, 1995, CDC, 1995, D alton, et al, 1995). Iguanas may be more likely to spread Salmonella organisms because their owners handle them differently than they would other types o f reptiles and because inexperienced owners (who are less knowledgeable o f preventive guidelines) are more likely to purchase the herbivorous, inexpensive, and readily available iguanas. In addition, iguanas may be more likely than other reptiles to be allowed to roam around the house, leaving deposits of fecal material in which Salmonella o rganism s can live fo r up to 30 m onths (C h io d in i and Sundberg, 1981). Case reports of human salmonellosis from many states have shown that direct contact is not necessary for the spread of Salmonella organisms from reptiles to humans, and that infec tio n s can be m uch m ore sev ere in th e y o u n g and th e immunocompromised (CDC, 1995). Although most veterinar ians mentioned hand washing or basic hygiene as methods to prevent the spread of Salmonella organisms from pet reptiles, very few gave other recommendations. Few gave recommen dations in written form. Although most veterinarians knew that certain groups were at greater risk than were others for getting salmonellosis from pet reptiles, the groups they men tioned varied. More than half mentioned that either children or immunocompromised persons (including persons infected with HIV) were at greater risk, but fewer veterinarians men tioned other at-risk groups. Most reptiles become colonized by Salmonella organisms. This usually occurs either by living in a contaminated envi ronment, by eating contaminated food, or through the normal development of proper hindgut fermentation (Murray, 1991, Troyer, 1982). In this survey, 12% of reptile practitioners said they routinely used antibiotics to attempt to eliminate the pre sumed Salmonella carrier state, and other studies have shown that many reptiles are treated with antibiotics at the distributor or pet store either to improve coat color and general health or to eliminate the presumed Salmonella carrier state (Dalton et al, 1995). However, prophylactically treating reptiles with antibiotics does not eliminate the Salmonella carrier state, and can cause health problems such as the disruption of necessary intestinal flora, the emergence of antibiotic-resistant strains, and a possible increase in the population of Salmonella organ isms in the carrier (D Aoust, et al, 1990, Cambre, et al, 1980, Chiodini and Sundberg, 1981, Chomel 1992). For these rea sons, veterinarians should not treat asymptomatic Salmonella carriers with antibiotics. This study is subject to the obvious limitation that veteri Journal of Herpetological Medicine and Surgery narians were surveyed in 1996, before many of the current recommendations on preventing reptile-associated salmonel losis had been released. However, it serves as a baseline assessm ent o f veterin arian s know ledge and practices in regard to reptile-associated salmonellosis at that time. A fol low-up study to survey veterinarians knowledge and practices today would be helpful in assessing whether recommenda tio n s and c o n tin u in g e d u c a tio n on re p tile -a s s o c ia te d salmonellosis since 1996 have been effective. To increase education of reptile owners concerning reptileassociated salm onellosis, all v eterinarian s who provide medical care to reptiles should take an active role in client education. The greatest public health impact would probably be achieved by first targeting veterinarians who classify them selves as reptile experts. Veterinarians recognized as reptile experts play an important role in educating non-expert veteri narians about rep tile m edicine through both form al and inform al continuing education. Specifically, veterinarians should be encouraged to provide not only verbal recommen dations for preventing reptile-associated salmonellosis but also written materials such as brochures or leaflets. These m aterials should include inform ation about the specific groups at risk for severe complications from salmonellosis, and they should be provided to all clients who own reptiles, who are considering owning reptiles, or who have contact with reptiles. Additional information on preventing reptile-associated sal m onellosis is available from other sources. In cooperation w ith the CDC, the P et Ind u stry Jo in t A dvisory Council (PIJAC) developed and distributed informational brochures and posters about reptile-associated salmonellosis and ways to prevent it. The ARAV has also drafted a position statement directed toward veterinarians and has prepared a client educa tion brochure ad d ressin g the th rea t to hum an health of reptile-associated salmonellosis (Bradley, et al, 1998). The ARAV position statement includes several guidelines for vet erinarians who treat reptiles, which are listed in Table 4. Educational materials should be provided to clients not only during visits w ith sick re p tiles but also during routine, healthy-reptile examinations. Educational brochures about Salmonella and reptiles, both for the veterinarian and the rep tile ow ner, have b ee n p re p a re d by ARAV and can be Table 4. Association of Reptile and Amphibian Veterinarians recommendations for veterinarians who treat reptiles. Veterinarians should educate their reptile-owning clients about salmonellosis and should recommend ways to prevent the trans mission of Salmonella organisms from reptiles to humans. All veterinarians, staff, and clients should follow recommended precautions to prevent reptile-associated salmonellosis. Since all reptiles should be presumed to be non-clinical carriers of Salmonella organisms, bacterial cultures intended to identify carriers are discouraged. Healthy reptiles should not be treated with antimicrobial drugs in an attempt to eliminate the Salmonella carrier state. Volume 11, No. 2,2001

5 dow nloaded from the W orld Wide Web (at no charge). Ultim ately, the veterinarian may be the average reptile owner s only source of information about reptile-associated salmonellosis; veterinarians must therefore make all efforts to educate their clients. ACKNOWLEDGEMENTS The authors gratefully acknowledge Adam Langer for his assistance in preparing this manuscript for publication. REFERENCES Ackman DM, Drabkin P, Birkhead G, Cieslak P Reptileassociated salmonellosis in New York State. Pediatr Infect Dis J, 14: Anonymous Turtle Salmonellosis. California Code of Regulations, Bradley T, Angulo FJ, Raid P Association of Reptilian and Amphibian Veterinarians guidelines for reducing risk of transmission of Salmonella spp. from reptiles to humans. JAVMA, 213(l): Burnham BR, Atchley DH, DeFusco RP, Ferris KE, Zicarelli JC, Lee JH, Angulo FJ Prevalence of fecal shedding of Salmonella organisms among captive green iguanas and potential public health implications. JAVMA, 213: Cambre RC, Green DE, Smith EE, Montali RJ, Bush M Salmonellosis and Arizonosis in the reptile collection at the National Zoological Park. JAVMA, 177: Centers for Disease Control and Prevention Reptileassociated salmonellosis selected states, MMWR, 44: Centers for Disease Control and Prevention Epi Info version 6.04b. Centers for Disease Control and Prevention Reptileassociated salm onellosis selected States, MMWR, 48: Chiodini RJ, Sundberg JP Salmonellosis in reptiles: a review. Am J Epidemiol, 113: Chomel B Zoonoses of house pets other than dogs, cats, and birds. Pediatr Infect Dis J, 11: Cohen ML, Potter M, Pollard R, Feldman RA Turtleassociated salmonellosis in the United States: Effect of public health action, 1970 to JAMA, 243: Conti L, Lieb S, Liberti T, Wiley-Bayless M, Hepbum K, Diaz T Pet ownership among persons with AIDS in three Florida counties. Am J Public Health, 85: Dalton C, Hoffman R, Pape J Iguana-associated salmonellosis in children. Pediatr Infect Dis J, 14: D Aoust JY, Daley E, Crozier M, Sewell AM Pet turtles: a continuing international threat to public health. Am J Epidemiol, 32(2): Food and Drug Administration Part Control of communicable diseases: Ban on the sale and distribution of small turtles. Federal Register, 40:6. Glaser CA, Angulo FJ, Rooney JA Animal-associated opportunistic infections among persons infected with the human immunodeficiency virus. Clin Infect Dis, 18: Gorczyca K, Abrams D, Carmack B Pets and HIV disease: a survey of providers knowledge and attitudes [Abstract], Proc Fifth International Conference on AIDS, Abstract 181. Hall MLM, Rowe B Salmonella arizoniae in the United Kingdom from 1966 to Epidemiol Infect, 108: Harvey JB, Roberts JM, Schantz PM Survey of veterinarians recommendations for treatment and control of intestinal parasites in dogs: Public health implications. JAVMA, 199: KauraYK, Sharma VK, Singh IP, Sakazaki R, Rohde R Snakes as reservoirs of Arizona and Salmonella. Zbl Bakt Hyg, I Abt A, 219: Mermin J, Hoar B, Angulo FJ Iguanas and Salmonella Marina infections in children: A reflection of the increasing incidence of reptile-associated salmonellosis in the United States. Pediatrics, 99: Mermin J, Hutwagner L, Vugia D, Kirley P, Bender J, Koehler J, McGivern T, M arcus R, Angulo FJ and The FoodNet Group Salmonella infections from reptiles in FoodNet sites: the resurgence of a preventable illness [Poster]. Proc Infectious Diseases Society of America. Monzon Moreno C, Ojeda Vargas MM, Echeita A, Usera MA Occurrence of Salmonella in cold-blooded animals in Gran Canaria, Canary Islands, Spain. Antonie van Leeuwenhoek, 68: Murray CJ. Salmonellae in the environment Revue Scientifique et Technique, 10: Shane SM, Gilbert R, Harrington KS Salmonella colonization in commercial pet turtles (Pseudemys scripta elegans). Epidemiol Infect, 105: Spencer L Study explores health risks and the human/animal bond. JAVMA, 201: Troyer K Transfer of fermentative microbes between generations in a herbivorous lizard. Science, 216: Volume 11, No. 2,2001 Journal of Herpetological Medicine and Surgery 13