Enteric Disease Associated with Animal Contact, Minnesota, 1999-2004 - Minnesota Dept. of Health

Enteric Disease Associated with Animal Contact, Minnesota, 1999-2004

From the March/April 2005 Disease Control Newsletter:
March/April 2005: Volume 33, Number 2 (PDF: 167KB/8 pages)

Animals are the reservoir of several important enteric pathogens, including E. coli O157:H7, Cryptosporidium parvum, Campylobacter spp., and Salmonella enterica. Whereas foodborne (E. coli O157:H7, Campylobacter, Salmonella) or waterborne (Cryptosporidium) are considered the predominant routes of transmission, direct contact with their animal reservoirs is also an important source of these pathogens. In recent years, enteric disease associated with venues where the public has contact with farm animals (e.g., petting zoos, state or county fairs, educational farms) has been identified with increasing frequency.1-4 Minnesota is no exception to this trend. This article summarizes zoonotic enteric disease transmission from animals to humans in Minnesota in recent years, including outbreaks associated with animal contact in public and private settings, and the role of animal contact in sporadic cases of disease. Tips and prevention information for health care providers and public health professionals involving this topic are also provided.

Enteric Disease Outbreaks Due to Animal Contact in Minnesota
A list of enteric disease outbreaks linked to animal contact investigated by the Minnesota Department of Health (MDH) in recent years is provided in Table 1.

Highlights of selected outbreaks are given below.

Salmonellosis from kittens
From August 1999 through March 2000, seven cases of multidrug-resistant Salmonella enterica serotype Typhimurium phage type DT104 were associated with kittens adopted from a large Twin Cities humane society. The median age of the cases was 6 years (range, 11 months-23 years). The median duration of diarrhea was 8 days (range, 5-11 days). One case was hospitalized for 4 days. Two of the cases resulted from secondary transmission; they attended the same day-care center as an ill child who owned a kitten from the shelter. An adult case who had been treated with ciprofloxacin shed S. Typhimurium in her stool at least 214 days after illness onset (note: antimicrobial treatment does not eradicate nontyphoidal Salmonella carriage but rather can prolong it). Some of the cases’ cats had been ill with bloody diarrhea after adoption, but some were asymptomatic and still carried S. Typhimurium for prolonged periods.

Salmonellosis from chicks

In May-June 2000, four case isolates of Salmonella Montevideo that were indistinguishable by pulsed-field gel electrophoresis (PFGE) were identified at MDH through routine surveillance. Two of the cases had contact with chicks purchased at the same farm store in Chippewa County, and another case had recently consumed chicken that had been raised on a neighbor’s farm.

Multiple pathogens from calves at a farm day camp – part 1 3
During June-July 2000, an outbreak of enteric infections caused by multiple pathogens occurred at a farm day camp in the Twin Cities. Bottle-fed calves were the source of the outbreak, which affected 59 campers, predominately those in kindergarten-fourth grade. The primary pathogen identified was Cryptosporidium parvum. The median duration of illness among cases was 6 days (range, 1-25 days). One child was hospitalized for 6 days. Children worked with calves in their street clothes. Duties included feeding and grooming the calves and cleaning up calf feces from the pen. The nearest hand-washing facility was in a building adjacent to the calf barn. Taking care of an ill calf was a risk factor for illness. Washing hands before going home for the day, and always washing hands with soap after touching a calf, were protective.

E. coli O157:H7 and hemolytic uremic syndrome (HUS) from calves on a private farm
In August 2000, two cases of E. coli O157:H7 infection with the same PFGE subtype were identified among cousins (ages 3 and 11 years, respectively) who attended a family reunion at a relative’s farm in Carlton County and played with young dairy calves. Both children developed HUS; one child was hospitalized for 15 days, and one for 23 days. The outbreak PFGE subtype of E. coli O157:H7 was recovered from the feces of four of six calves tested. Campylobacter jejuni was recovered from all six calves.

Salmonellosis from owl pellets
In May 2001, outbreaks of salmonellosis at two elementary schools in Washington County resulted from dissection of owl pellets (i.e., regurgitated indigestible bones, fur and feathers from an owl’s recent meals) as part of science club. The first outbreak was identified through telephone reports from two physicians. In the first outbreak, 33 primary cases and 17 secondary cases were identified. The median duration of illness was 72 hours (range, 15-192 hours), and four cases were hospitalized. Owl pellets were dissected directly on a table in the school’s cafeteria. The students did not wear gloves and were not instructed to wash their hands. After science club, the table was used for snacks for children in the after-school care program, which also was held in the cafeteria. The table was not sanitized until after school lunch the following day. In the second outbreak, the school did have a dedicated science room for science club, but seven of the nine students who dissected pellets developed salmonellosis, along with two secondary cases among household members of students.

All of the pellets for these science clubs originated from a single captive barred owl. The outbreak PFGE subtype was recovered from numerous pellets from this owl, the owl’s feces, and all four frozen chicks left over from a batch used to feed the owl. Our investigation documented owl pellets as a novel vehicle for salmonellosis. Dissection of owl pellets has become an increasing popular educational activity for elementary school children. We recommend using heat-treated owl pellets from commercial sources as well as appropriate hygienic practices after handling the pellets.

Multiple pathogens from calves at
a farm day camp – part 2
Despite the implementation of prevention measures (e.g., education and attempts to facilitate better hand-
washing) at the farm day camp during 2000 (see above), another outbreak due to calf contact occurred in 2001. Again, multiple pathogens were involved. Cryptosporidium parvum was the most common pathogen recovered, but several cases of infection with E. coli O157:H7 or with non-O157 Shiga toxin-producing E. coli (STEC) also were identified. Overall, 25 cases were identified among campers. No HUS cases were identified, but two children were hospitalized, each for 4 days; this included one child who had both E. coli O157:H7 and C. parvum. Getting visible manure on the hands was a risk factor. The camp was closed until more extensive interventions could be implemented. We recovered the same PFGE subtypes of non-O157 STEC from children and calves; this was the first time in the United States and only the second time in the world that cattle have been directly implicated as the source of a non-O157 STEC outbreak.

Campylobacter jejuni and Cryptosporidium parvum from dairy calves

In June 2002, three cases of Campylobacter jejuni infection and two cases of cryptosporidiosis were linked to the same local dairy farm in Kittson County. Four cases had purchased young calves from the dairy, and one was an employee of the dairy who had milked sick cows. Three of the five cases were hospitalized. Evaluation of the dairy revealed that many of the calves on the farm were ill. Of note, in 2000 this dairy was implicated in an outbreak of Campylobacteriosis associated with the consumption of malts made with unpasteurized milk.

Campylobacter coli from chickens or pigs
In June 2002, three cases of Campylobacter coli gastroenteritis occurred among employees of a Traverse County farm. Isolates from all three cases were indistinguishable by PFGE. Illness durations were 5 days, 13 days, and over 1 month, respectively; one case was hospitalized. Job duties for the three cases included handling chickens, cleaning pens, and hauling pig waste.

Campylobacter coli from turkeys
In June 2002, nine cases of Campylobacteriosis were identified among workers who volunteered to help pick up 13,000 turkey carcasses on a farm after flooding in Roseau County. Campylobacter coli was identified from one case. The median duration of illness was 96 hours (range, 48 to 168 hours). Washing hands with soap and running water (vs. in a communal bucket or a with a hose) was protective.

Cryptosporidium parvum from calves at a teaching farm

In February 2003, an outbreak of cryptosporidiosis occurred among middle and high school students in Crow Wing County who participated in an animal science class that involved caring for young calves at an educational farm. Thirty-one cases were identified. The median duration of illness was 7 days (range, 6 hours-19 days). Symptoms included diarrhea (90%), abdominal cramps (66%), vomiting (43%), and fever (17%). Of nine students who visited a health care provider, only two had stool samples submitted for enteric pathogen testing. Contact with calves was the primary risk factor; students cared for calves in street clothing and practiced poor handwashing.

Our recommendations for the program included eliminating student contact with ill calves, supervised handwashing, use of protective coveralls/boots, and eliminating food and drink at the farm. However, when the class resumed in September 2003, another outbreak of cryptosporidiosis occurred among students. This time, 37 cases were identified. Getting visible manure on one’s hands was a risk factor, as were eating/drinking on the farm campus and drying hands on one’s clothing. Interestingly, wearing coveralls and wearing boots were also risk factors. This was attributed to the fact that the closet for these items was at the exit to the calf barn; these soiled items were removed after hand-
washing occurred. And, handwashing was observed to still be poor.

Salmonella Ealing from reptiles in a private home
Two cases of Salmonella Ealing infection were linked to the private home of a herpetologist (one who studies reptiles). The first case, in February 2003, was a friend who visited the herpetologist’s home for several hours and consumed some food and drink. Two days later she became ill with Salmonella gastroenteritis; she was subsequently hospitalized for 2 days. The second case, in April 2003, was the 3-month-old grandchild of the herpetologist; the infant and the infant’s mother were living at the herpetologist’s home at the time. The herpetologist kept approximately 50 reptiles and amphibians in her home. Salmonella was isolated from 16 (76%) of 21 reptile fecal/cage samples and four (29%) of 14 environmental samples. Salmonella Ealing was isolated from a pooled fecal sample from a gecko and frog terrarium in the front room; this terrarium was only a few feet away from the infant’s playpen. Salmonella Ealing was also isolated from the edge of the kitchen sink and a bathroom countertop.

Cryptosporidium parvum among employees at a veterinary clinic
In June 2003, two teen-age employees of a veterinary clinic in Kandiyohi County acquired cryptosporidiosis after cleaning a pen that had been occupied by a calf that was sick with diarrhea. The cases did not wear gloves while cleaning the pen. Durations of illness were 6 days and 13 days, respectively.

E. coli O157:H7 from a county fair
In August 2003, an outbreak of E. coli O157:H7 infections occurred at the Scott County Fair. Two of the five cases were hospitalized, including one who developed hemolytic uremic syndrome. The fair held a petting zoo that included calves, sheep, and goats, but no specific source of the outbreak could be confirmed.

Multidrug-resistant Salmonella Typhimurium from pet rodents

In 2004, MDH led an investigation of a multi-state outbreak of S. Typhimurium infections associated with commercially distributed pet rodents. The investigation is still in process, but at least 15 confirmed infections in 10 states (including one Minnesota case) have been identified. Rodent exposures included pet hamsters, pet mice/rats, and mice/rats purchased to feed snakes. The median case age was 16 years (range, 0-43 years); seven cases (47%) were <7 years of age. Six cases were hospitalized. In Minnesota, the outbreak strain of S. Typhimurium was cultured from a 5-year-old case’s pet “fancy” mouse, and from several ill hamsters from a group submitted by a Minnesota pet distributor.

The Role of Animal Contact in Sporadic Infections with Enteric Pathogens in Minnesota: Results of Case-Control Studies

The majority of cases of infection with the enteric bacterial and protozoal pathogens reported to MDH are not associated with recognized outbreaks. Thus, to better understand the epidemiology of these pathogens it is necessary to understand sources for sporadic infections. Since 1995, MDH has been part of the Centers for Disease Control and Prevention Centers Emerging Infections Program. Part of this program, termed the Foodborne Diseases Active Surveillance Network (FoodNet), incorporates a multi-faceted approach to study bacterial and parasitic foodborne pathogens, including active laboratory-based surveillance to ensure ascertainment of all confirmed cases of infections with these pathogens. MDH also has conducted case-control studies of sporadic infections with select pathogens. Although, the studies have identified numerous food and water-related risk factors, animal contact has also been identified as an important risk factor for infection with several of our prominent enteric pathogens (Table 2). Highlights of recent FoodNet case-control studies concerning animal contact-related risk factors follow.

Cryptosporidiosis 7
This case-control study, carried out from 1999 to 2001, involved 282 cases and 490 age- and residence-matched well controls in seven states. Minnesota contributed 145 cases and 239 controls. In the overall analysis, contact with calves or cows was a risk factor. Other risk factors included international travel, contact with children with diarrhea, and freshwater swimming. In Minnesota specifically, well water consumption also was a risk factor. The largest proportion of cases in the study population was attributable to contact with cattle (population attributable risk [PAR]=16%).

E. coli O157:H7 8
This case-control study, carried out from 1996 to 1997, involved 196 cases and 372 age- and residence-matched well controls in five states. Minnesota contributed 112 cases and 212 controls. For children <6 years of age, living on or visiting a farm was a risk factor. For persons >6 years of age, visiting (but not living on) a farm with cattle was a risk factor. Overall, 18% of cases in Minnesota had visited a farm with cattle during the week before their illness onset. Other risk factors (all ages) included eating at a table service restaurant (PAR=20%), eating a pink hamburger at home (PAR=8%), and eating a pink hamburger away from home (PAR=7%). Among those who consumed ground beef or hamburgers at home, obtaining beef through a private slaughter arrangement was a risk factor. For persons >6 years of age, using an immunosuppressive medication was a risk factor (PAR=5%).

Salmonella enterica 9
This case-control study evaluated nontyphoidal Salmonella enterica serogroup B and D cases from five states from 1996 to 1997; 463 cases and 7,618 well controls were included. Risk factors included any reptile or amphibian contact, having a reptile or amphibian in the home, and touching a reptile. Other risk factors included international travel, eating eggs in a restaurant, and having a chronic, non-diarrheal illness. Among persons <21 years of age, the PAR for any reptile or amphibian contact increased to 9.5%; 16% of cases and 9% of controls in this age group reported this exposure.

Campylobacter spp. 10
This case-control study, carried out from 1998 to 1999, involved 1,316 cases and 1,316 age- and residence-matched well controls in seven states. Minnesota contributed 242 cases and 242 controls. Risk factors included having contact with animal stool, having a pet puppy, having contact with farm animals, and drinking raw milk. Many other risk factors, most involving poultry and other foods of animal origin, also were identified.

Synopsis: Salient Points for the Health Care Provider

The pathogens discussed in this article are common enteric pathogens in Minnesota11 and thus should always be considered in patients presenting with gastroenteritis. Animal contact is an important route of transmission for these pathogens, so potential animal exposures should be included in the patient history. Table 3 provides a quick reference guide for health care providers for the most frequent or important animal reservoir-pathogen associations observed in Minnesota.

The combination of the patient history and the clinical features of the
illness12-14 can be extremely helpful in the timely diagnosis and management of gastrointestinal illnesses. For example, E. coli O157:H7 is typically characterized by prominent abdominal cramping and a day of watery diarrhea, followed by the development of bloody diarrhea. The primary clinical feature of cryptosporidiosis is watery diarrhea of several days duration; vomiting also commonly occurs, particularly in pediatric patients. Recent exposure to cattle in patients with these clinical histories should elicit a high index of suspicion for these etiologies. Cattle are the primary reservoir for E. coli O157:H7 and Cryptosporidium parvum; both of these pathogens are present in the vast majority of cattle herds in Minnesota. Sheep and goats also may carry these pathogens; recent E. coli O157:H7 outbreaks in other states attributed to sheep/goat barns or petting zoos at fairs4 demonstrate the potential of disease transmission from these species as well.

A high index of suspicion for E. coli O157:H7 is important for a number of reasons. First and foremost, this pathogen is the most common cause of post-diarrheal HUS. Acute gastroenteritis possibly due to E. coli O157 needs to be managed carefully; antimicrobial treatment should be avoided as it may contribute to the development of HUS. Confirmation of all E. coli O157:H7 infections is highly desirable, as submission of isolates to the MDH Public Health Laboratory is critical to the timely detection and control of outbreaks. Finally, since E. coli O157:H7 can spread readily from person-to-person, particularly in child care settings, confirmation allows for exclusion of children from child care until they are culture-negative.

Testing for Cryptosporidium is typically not done when health care providers order an ova and parasite exam on a stool sample. Therefore, providers should ask specifically for a Cryptosporidium test if this agent is suspected.

Salmonella and Campylobacter are characterized by fever and fecal leukocytes; vomiting and bloody stools can occur. Recent exposure to reptiles or baby chicks should cause you to think about Salmonella; these creatures are widely documented sources of Salmonella for humans.15-17 Reptiles in particular are important sources of Salmonella, because they are popular pets and 90% of reptiles carry Salmonella in their normal flora.

Puppies and kittens may also be the source of enteric pathogens (usually Campylobacter). They frequently have had diarrhea recently themselves.

Of course, there are many sources for these pathogens other than animal contact. Foodborne, waterborne, and person-to-person transmission occur to varying degrees, depending on the pathogen. Therefore, absence of recent animal contact should not be used to rule out any of the pathogens discussed here.


Prevention of Enteric Disease Associated with Animal Contact
(see also>> Preventing Illness Associated with Animal Contact)

All animals, animal environments, or animal products are potentially contaminated with pathogens and should be treated as such. The backbone of prevention of enteric disease associated with animal contact is thorough handwashing with soap and water after exposure to these entities. For young children, hand washing should be supervised. In addition, food, drink, and items that promote hand-to-mouth contact (e.g., pacifiers) should not be permitted in animal contact areas. The food and drink prohibition is critical. Accumulating evidence from recent outbreaks at fairs indicates that E. coli O157:H7 can be aerosolized on dried sawdust bedding, causing widespread contamination of environmental surfaces in an animal barn, and possibly also food and clothing of patrons viewing the animals (even in the absence of direct animal contact).

Specific national prevention recommendations have been developed for specific species or settings.18 The National Association of State Public Health Veterinarians has developed an extensive set of recommendations for the prevention of disease associated with animals in public settings;4 these recommendations are updated annually. As demonstrated by the outbreaks associated with educational programs in Minnesota, it is extremely difficult to prevent infections in children who have close, prolonged contact with young calves. A detailed and comprehensive prevention plan should be created before such a program is undertaken.

Specific recommendations for the prevention of reptile-associated salmonellosis have been developed by the Centers for Disease Control and Prevention (see inset below). Please note that reptiles (lizards, snakes, turtles) should not be allowed in childcare centers or households that include children <5 years of age or immunocompromised persons. The same recommendation has been made for chicks, ducklings, and other young fowl.16

The MDH Foodborne, Vectorborne, and Zoonotic Diseases Unit (FVZDU) has available two 11 x 17 inch posters that animal exhibit operators can use for the prevention of enteric diseases at public venues (see facing page).

The FVZDU is happy to consult on prevention plans for educational programs.

We also are happy to consult with health care providers on case-patients with specific animal exposures; we can be reached at 612-676-5414 or 1-877-676-5414 (outstate).


  1. Bender JB, Shulman SA, et al. Reports of zoonotic disease outbreaks associated with animal exhibits and availability of recommendations for preventing zoonotic disease transmission from animals to people in such settings. J Am Vet Med Assoc. 2004;224:1105-9.
  2. LeJeune JT, Davis MA. Outbreaks of zoonotic enteric disease associated with animal exhibits. J Am Vet Med Assoc. 2004;224:1440-5.
  3. Smith KE, Stenzel SA, Bender JB, et al. Outbreaks of enteric infections with multiple pathogens associated with calves at a farm day camp: Public health implications. Ped Infect Dis J. 2004;23:1098-1104.
  4. National Association of State Public Health Veterinarians, Inc. Compendium of Measures to Prevent Disease and Injury Associated with Animals in Public Settings, 2004. Available at s94745432.onlinehome.us/AnimalsIn
    Public2004.pdf Accessed February 2005.
  5. Ezell H, Tramontin B, Hudson R, et al. Outbreaks of multidrug-resistant Salmonella Typhimurium associated with veterinary facilities—Idaho, Minnesota, and Washington, 1999. MMWR. 2001;50:701-4.
  6. Smith KE, Medus C, Leano F, et al. Outbreaks of salmonellosis at elementary schools associated with dissections of owl pellets. J Vectorborne and Zoonotic Dis. In Press.
  7. Roy SL, DeLong SM, Stenzel SA, et al. Risk factors for sporadic cryptosporidiosis among immunocompetent persons in the United States from 1999 to 2001. J Clin Microbiol. 2004;42:2944-51.
  8. Kassenborg HD, Hedberg CW, Hoekstra M, et al. Farm visits and undercooked hamburgers as major risk factors for sporadic Escherichia coli O157:H7 infection: Data from a case-control study in 5 FoodNet sites. Clin Infect Dis. 2004;38 Suppl 3:S271-8.
  9. Mermin J, Hutwagner L, Vugia D, et al. Reptiles, amphibians, and human Salmonella infection: A population- based, case-control study. Clin Infect Dis. 2004;38 Suppl 3:S253-61.
  10. Friedman CR, Hoekstra RM, Samuel M, et al. Risk factors for sporadic Campylobacter infection in the United States: A case-control study in FoodNet sites. Clin Infect Dis. 2004;38 Suppl 3:S285-96.
  11. Annual Summary of Communicable Diseases Reported to the Minnesota Department of Health, 2003. Disease Control Newsletter July/August, 2004; 32:33-52.
  12. CDC. Diagnosis and management of foodborne illnesses: a primer for physicians. MMWR 2001;50:RR-2.
  13. Guerrant RL, Van Gilder T, Steiner TS, et al. Practice guidelines for the management of infectious diarrhea. Clin Infect Dis. 2001;32:331- 51.
  14. Thielman NM, Guerrant RL. Acute
    infectious diarrhea. NEJM. 2004;350:38-47.
  15. CDC. Reptile-associated salmonellosis-selected states, 1998-2002. MMWR 2003;52:120-09.
  16. CDC. Salmonellosis associated with chicks and ducklings-Michigan and Missouri, 1999. MMWR 2000;49:297-9.
  17. Oregon Department of Human Services. Chick associated salmonellosis. CD Summary. Apr 6, 2004;53:1- 2. Available at: www.oshd.org/ cdsummary/2004/ohd5307.pdf
    Accessed February 2005.
  18. National Center for Infectious Disease
    Healthy Pets, Healthy People;
    Available at: www.cdc.gov/healthypets/ Accessed February 2005.

Updated Wednesday, 15-Nov-2017 08:36:56 CST