Reptile-Associated Salmonellosis—Selected States, 1996-1998 FREE

MMWR. 1999;48:1009-1012

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During 1996-1998, CDC received reports from approximately 16 state health departments of Salmonella infections in persons who had direct or indirect contact with reptiles (i.e., lizards, snakes, or turtles). Salmonella infection can result in invasive illness including sepsis and meningitis, particularly in infants. Despite educational efforts, some reptile owners remain unaware that reptiles place them and their children at risk for salmonellosis. This report summarizes clinical and epidemiologic information in four cases and provides information about state regulations to prevent transmission of Salmonella spp. from reptiles to humans.

During October 1996, a 3-week-old boy was admitted to a hospital emergency department with fever (103.6 F [40 C]), vomiting, and bloody diarrhea of 15 days' duration. Stool and blood cultures yielded Salmonella serotype IV 44:z₄,z_23-, an extremely rare serotype. The infant was hospitalized for 10 days and treated with intravenous fluids and amoxicillin. To determine the cause of the infant's illness, a stool specimen was obtained from the family's pet iguana, which also yielded Salmonella IV 44:z₄,z_23-. In an attempt to prevent reinfection, local health officials informed the parents of the importance of the infant avoiding direct and indirect contact with the reptile, and the iguana was moved to a relative's home. One month later, the infant spent 2 days in the relative's home where the iguana was housed; 48 hours after this visit, the infant was again treated at an emergency department for fever and diarrhea. A stool culture again yielded Salmonella IV 44:z₄,z_23-.

During April 1997, a 6-year-old boy had bloody diarrhea of 10 days' duration, abdominal cramps, vomiting, and fever (104.9 F [41 C]). Stool culture yielded Salmonella serotype Typhimurium. The child was treated with ceftriaxone and amoxicillin/clavulanate. Nine days after the boy started therapy, his 3-year-old brother also developed diarrhea, and a stool sample yielded S. Typhimurium. No other family members became ill. The two boys shared a room with two corn snakes that they handled regularly. Stool cultures from the corn snakes yielded S. Typhimurium. The parents reported to health department staff that they were unaware that snakes are a source of salmonellosis.

During May 1997, an 8-year-old boy with a congenital immune deficiency developed severe vomiting, abdominal cramps, bloody diarrhea, and headaches. Stool samples yielded Salmonella serotype St. Paul. The boy was ill for 14 days and received extensive supportive care at home. Three days before the boy became ill, the family had purchased two iguanas from a local pet store. The family was not informed by pet store personnel that reptiles are a source of salmonellosis; the child handled the reptiles, including putting them on his head and face. Before diagnostic testing could be performed, the reptiles were returned to the pet store. The parents informed the pet store owner of the child's illness, and the pet store owner reportedly was unaware that reptiles carry Salmonella spp.

In December 1998, a previously healthy 5-month-old girl suddenly died at home. No significant macroscopic or histologic findings were revealed during autopsy; however, culture of a heart blood sample yielded Salmonella serotype Marina. The cause of death was attributed to S. Marina septicemia. The family had a pet iguana that had not come into direct contact with the infant. Culture of a stool sample taken from the iguana yielded S. Marina. Based on an interview, the parents were unaware that the infant was at risk for salmonellosis from indirect or direct contact with the iguana.

During March 1999, CDC contacted all 50 state health departments to determine whether state regulations existed for sale of reptiles and distribution of information about salmonellosis. Of the 48 states that responded, three (California, Connecticut, and Michigan) had regulations requiring pet stores to provide information about salmonellosis to persons purchasing a turtle; two states (Kansas and Maryland) require salmonellosis information to be provided to persons purchasing any reptile. Three states (Arizona, Minnesota, and Wyoming) prohibit reptiles in day care centers and long-term-care facilities.

C Levy, MS, M Finnerty, Arizona Dept of Health Svcs. G Hansen, DVM, Kansas Dept of Health and Environment. J Cory, MPH, M McGuill, DVM, B Matyas, MD, A DeMaria, Jr, MD, State Epidemiologist, Massachusetts Dept of Public Health. G Schmunk, MD, J Grantham, MD, Brown County Medical Examiner's Office, Green Bay, Wisconsin; J Archer, MS, J Kazmierczak, DVM, J Davis, MD, State Epidemiologist for Communicable Diseases, Wisconsin Dept of Health and Family Svcs. Foodborne and Diarrheal Diseases Br, Div of Bacterial and Mycotic Diseases, National Center for Infectious Diseases, CDC.

In the United States, pet turtles were an important source of salmonellosis until commercial distribution of pet turtles <4 inches long was banned in 1975.¹ This ban led to a 77% reduction in the frequency of turtle-associated Salmonella serotypes isolated from humans during 1970-1976.¹ The popularity of other reptiles as pets is growing and has raised concerns about their impact on public health. This and other reports² demonstrate that reptile-related salmonellosis continues to pose a substantial threat to human health. Approximately 93,000 (7%) cases per year of Salmonella spp. infections are attributable to pet reptile or amphibian contact.³ An estimated 3% of households in the United States have a reptile (CDC, unpublished data, 1999). Many reptiles are colonized with Salmonella spp. and intermittently shed the organism in their feces.⁴ Persons become infected by ingesting Salmonella after handling a reptile or objects contaminated by a reptile and then failing to wash their hands properly. Either direct or indirect contact with infected reptiles and their environment can cause human illness.^5- 6

Rare Salmonella serotypes, such as Java, Marina, Stanley, Poona, and Chameleon associated with reptiles, increasingly have been isolated from humans.⁷ For example, S. Marina isolates from humans increased from two in 1989 to 47 in 1998, and S. Poona increased from 199 in 1989 to 341 in 1998.⁸ Isolation of rare serotypes of Salmonella spp. can alert public health staff about trends in the transmission of infection from reptiles to humans.

Most persons who contract reptile-associated salmonellosis are infants and young children. In 1994, 413 (81%) of 513 S. Marina cases occurred in children aged <1 year, whereas 4301 (14%) of 30,723 reported salmonellosis cases occurred in children aged <1 year.⁶ During 1989-1998, 516 (24%) of 2150 Salmonella isolates with reptile-associated serotypes were from children aged <4 years, whereas 50,755 (19%) of 267,131 other serotypes were from this age group (CDC, unpublished data, 1999). Because infants and immunocompromised persons are more susceptible to illness, many reptile-associated Salmonella infections involve serious complications, including septicemia and meningitis.⁹

The risks for transmission of Salmonella spp. from reptiles to humans can be reduced by thoroughly washing hands with soap and water after handling reptiles or objects that have been in contact with reptiles and by preventing reptile contact with food-preparation areas. Children aged <5 years and immunocompromised persons should avoid direct and indirect contact with reptiles. Reptiles also should not be kept in homes of persons with children aged <1 year and in child care facilities (see box). All pet store personnel and reptile owners should be aware that reptiles can carry and transmit Salmonella spp. Pet stores are in a unique position to educate consumers because reptile owners obtain most of their information about their pet from pet store personnel. CDC and the Pet Industry Joint Advisory Council (PIJAC) have developed educational posters and brochures for use by veterinarians and pet stores on safe pet reptile handling.*

The effectiveness of educating the public about reptile-associated salmonellosis needs to be evaluated. To enhance efforts to educate the public in a systematic, consistent, and timely manner, the National Association of State Public Health Veterinarians and the Council of State and Territorial Epidemiologists jointly recommend "that the appropriate state and local agencies enact legislation prohibiting the sale or gift of reptiles unless there is written point-of-sale education provided to consumers on the risks for and prevention of reptile-associated salmonellosis."¹⁰ CDC will provide assistance to states interested in developing point-of-sale educational material; however, if these educational efforts should prove unsuccessful, states may wish to adopt restrictions for the sale of reptiles similar to those for turtles.

*Posters are available on request from PIJAC, telephone (800) 553-7387.

MMWR. 1999;48:1039-1042

Influenza activity was low during October 3-November 6, 1999; influenza virus isolates were reported from 30 states, and four long-term-care facility outbreaks were reported from three states. The predominant viruses isolated were influenza type A(H3N2) viruses. This report summarizes influenza activity in the United States during October 3-November 6, 1999. It also summarizes U.S. influenza surveillance methodology, including the four primary sources of surveillance data, a modification to pneumonia and influenza (P&I) mortality reporting, and discusses detection and control of institutional influenza outbreaks.

Each week from October through May, volunteer physicians in 47 states and the District of Columbia report the number of patient visits and the number of those visits for influenza-like illness (ILI). ILI is defined as cough or sore throat and a temperature of ≥100 F (37.8 C). Baseline levels of total patient visits for ILI range from 0 to 3%. Levels >3% usually correlate with increased influenza activity.

Each week during October-May, state and territorial epidemiologists report statewide estimates of influenza activity to CDC. Activity levels are defined as: (1) no activity, (2) sporadic—sporadically occurring ILI or culture-confirmed influenza with no outbreaks detected, (3) regional—outbreaks of ILI or culture-confirmed influenza in counties with a combined population of <50% of the state's population, and (4) widespread—outbreaks of ILI or culture-confirmed influenza in counties with a combined population of ≥50% of the state's population.

Each week throughout the year, the vital statistics offices for 122 U.S. cities report the total number of death certificates received and the number of death certificates on which influenza or pneumonia is listed on Part I (immediate, intermediate, or underlying cause of death) or Part II (contributing cause of death). These data are used to calculate a P&I mortality curve. A periodic regression model incorporating a robust regression procedure is used to estimate a seasonal baseline for P&I deaths. An increase of 1.645 standard deviations above the seasonal baseline for P&I deaths is considered the epidemic threshold.

Each week from October through May, approximately 115 WHO and NREVSS collaborating laboratories in the United States report the total number of specimens received for respiratory virus testing and the number testing positive for influenza A(H1N1), A(H3N2), A (not subtyped) and influenza B. A subset of isolates are submitted for complete antigenic characterization to CDC.

From October 3 through November 6, 1999, 1% of patient visits to sentinel physicians were for ILI. Among the nine surveillance regions, patient visits for ILI ranged from 0 to 3% during the week ending November 6, except in the West South Central region, which reported 5% of patient visits for ILI. For the week ending November 6, state and territorial epidemiologists in New York, Indiana, and Puerto Rico reported regional activity, and 35 states reported sporadic activity. No state reported widespread activity. A long-term-care facility outbreak was identified in New York on September 30, in New York City on October 14, in California on October 17, and in Illinois on November 3. During the week ending November 6, 621 (7.4%) of 8414 total deaths in 122 U.S. cities were attributed to P&I; this proportion was above the epidemic threshold of 6.5%. The proportion of P&I deaths has remained above the threshold for 7 consecutive weeks.

From October 3 through November 6, WHO collaborating laboratories and NREVSS laboratories in the United States reported 117 influenza A and four influenza type B laboratory-confirmed infections out of 5198 specimens submitted for respiratory virus tests. All 49 subtyped influenza A viruses were H3N2 viruses. Three influenza B viruses were isolated from persons returning to Tennessee from a trip to Ireland. Another influenza B virus was confirmed by CDC in addition to those reported by WHO and NREVSS laboratories. All 51 U.S. influenza A(H3N2) isolates collected from September 6 through November 6 and antigenically or genetically characterized at CDC were influenza A/Sydney/5/97-like (H3N2) viruses, and all four influenza B isolates were characterized as B/Yamanashi/166/98-like viruses. Both of these strains are contained in the 1999-2000 influenza vaccine.

C Waters, P Smith, MD, State Epidemiologist, New York State Dept of Health. R Taylor, DVM, W Reimels, A Craig, MD, W Moore, MD, State Epidemiologist, Tennessee Dept of Health. R Murray, DrPH, DJ Vugia, MD, Acting State Epidemiologist, California Dept of Health Svcs. CE Jennings, SL Bornstein, MD, Illinois Dept of Public Health. Participating state and territorial epidemiologists and state public health laboratory directors. World Health Organization collaborating laboratories. Sentinel Physicians Influenza Surveillance System. National Respiratory and Enteric Virus Surveillance System Laboratories. Surveillance Systems Br, Div of Public Health Surveillance and Informatics, Epidemiology Program Office; Mortality Statistics Br, Div of Vital Statistics, National Center for Health Statistics; Respiratory and Enterovirus Br and Influenza Br and WHO Collaborating Center for Reference and Research on Influenza, Div of Viral and Rickettsial Diseases, National Center for Infectious Diseases; and an EIS Officer, CDC.

Three of four influenza surveillance systems indicated that influenza activity was low from October through early November in the United States; however, 30 states reported laboratory-confirmed cases of influenza, and four long-term-care-facility outbreaks were reported. The 122 cities mortality reporting system data indicated that P&I mortality was above epidemic thresholds for 7 consecutive weeks; however, these results must be viewed with caution because recent changes have been made to the reporting system.

In 1993, the WHO International Classification of Diseases, Ninth Revision (ICD-9) coding guidelines were updated to International Statistical Classification of Diseases and Related Public Health Problems, 10th Revision (ICD-10), and were implemented by CDC's National Center for Health Statistics (NCHS) in 1999.¹ For ICD-10, the application of a coding rule was broadened such that when pneumonia is listed by a certifying physician on a death certificate as the underlying cause of death, nosologoists should give preference to coding the cause of death to an alternative condition that might have led to the pnuemonia. Preliminary results from an NCHS comparability study have shown that the ICD-10 coding rule change will result in a substantial decrease in the number of reported pneumonia-related deaths (CDC, unpublished data, 1999).

In response to ICD-10, CDC requested that the 122 cities report pneumonia deaths to the surveillance system if pneumonia is listed anywhere on the death certificate. This may partially account for the observed increase in reported P&I deaths above threshold levels; baseline and threshold levels of P&I mortality are estimated using the previous 5 years' mortality data. CDC continues to evaluate the impact of these changes in reporting criteria on P&I mortality estimates.

Influenza introduced into hospitals and long-term-care facilities by patients, visitors, or staff can cause nosocomial outbreaks that can occur year-round, but tend to occur during periods of increased influenza activity, usually December-March. Institutional outbreaks can result in high attack rates among staff and patients and increased patient mortality, particularly among elderly and other vulnerable populations, such as bone marrow transplant patients.^2- 5 In a survey of Emerging Infections Network (EIN) physicians,* conducted during the spring of 1999, 344 (74%) of 462 reported diagnosing influenza in hospitalized patients, and 65 (14%) recognized one or more nosocomial influenza cases during the preceding influenza season. Despite the frequent diagnosis of influenza among hospitalized patients, only 163 (35%) of 458 of the EIN physicians reported that their hospitals had a written policy for the control of nosocomial influenza outbreaks.⁶

When influenza outbreaks occur in health-care institutions, early recognition and initiation of control measures are important because influenza can spread rapidly in these settings.^2,7- 10 The use of rapid diagnostic tests to confirm an influenza outbreak can facilitate the immediate activation of control measures such as cohorting ill patients, initiating droplet precautions, and using antiviral medications for influenza prophylaxis and treatment. Four influenza antiviral medications are available. Amantadine and rimantadine are approved for both treatment and prophylaxis of influenza type A but not influenza type B. Zanamivir and oseltamivir are active against influenza A and B viruses and are approved for the treatment but not the prophylaxis of influenza.^7- 8,10† Although antiviral medications are an important adjunct for the prevention and control of influenza, they are not a substitute for vaccination. Vaccination is the primary means of preventing influenza and is recommended for persons at high risk for influenza-related complications and persons who may transmit influenza to those at high risk, including health-care workers.⁷

Influenza surveillance data collected by CDC are updated weekly during October-May and are available by telephone, (888) 232-3228, or fax, (888) 232-3299 and requesting document number 361100, or through CDC's National Center for Infectious Diseases, Division of Viral and Rickettsial Diseases, Influenza Branch World-Wide Web site, http://www.cdc.gov/ncidod/diseases/flu/weekly.htm.

*A group of infectious-disease physicians from the Infectious Diseases Society of America.

†Further information is available from the Food and Drug Administration, Center for Drug Evaluation and Research on the World-Wide Web, http://www.fda.gov/cder/drug.htm. (References to sites of non-CDC organizations on the World-Wide Web are provided as a service to MMWR readers and do not constitute or imply endorsement of these organizations or their programs by CDC. CDC is not responsible for the content of pages found at these sites.)