Environmental contamination of salmonella enterica: Where should we focus our efforts? (Proceedings)

Epidemics of healthcare-associated infections in veterinary teaching hospitals are commonly attributed to Salmonella enterica [1].  Although veterinary hospitals employ rigorous personal and environmental hygiene practices into infection control programs, large outbreaks still occur with high case fatality rates and at considerable financial cost [2].  During times of epidemic disease, there is typically widespread environmental contamination and it is not uncommon for patient and environmental isolates to be phenotypically similar (i.e., serotype and antimicrobial susceptibility pattern); a phenomenon that has also been identified during times of endemic disease, suggesting animals to be a likely source for contamination [2-5]

Managing S. enterica in equine populations should take into consideration both factors related to the occurrence of epidemic and endemic disease.  During times of epidemic disease, environmental hygiene is commonly identified as a contributing factor including ineffective infection control policies and the presence of floor surfaces which allow contamination to accumulate [2; 6; 7].  Contamination of common use equipment (e.g., buckets, nasogastric tubes, and rectal thermometers) is also a common characteristic [6-8].  During the course of an outbreak, horses with severe disease are frequently identified as shedding Salmonella and likely contribute to ongoing environmental contamination and transmission among hospitalized patients [6; 8-10].

Historically, Salmonella shedding among horses has been associated with a triad of clinical signs – diarrhea, fever and leukopenia – an observation supported in a recent case-control study [11].  However, this triad of clinical signs can occur rather infrequently, accounting for only 2.7% of shedding among a hospital population (the population attributable fraction) [12].  In addition, findings from experimental studies suggest that by the time fever and/or diarrhea are apparent, animals are frequently shedding Salmonella in their feces; emphasizing the importance of identifying commonly occurring, easily recognizable factors or groups of factors that would allow for the rapid implementation of prevention strategies [13]. 

It is generally believed that horses with more severe disease (e.g., gastrointestinal disease, abdominal surgery) and those receiving antimicrobial therapy are more likely to shed detectable quantities of Salmonella in their feces.  While this seems to make biological sense – it is important to note that over the years this has not been a consistent finding [8; 11; 14-17].  Many of these studies targeted high risk groups and extrapolating findings from studies observing limited patient populations should be done with caution. 

Studies focusing on the general patient population found that both patient and hospital factors may be important [12; 17-20].  Patients with systemic illness – regardless of body system affected – and those having any one of the classic triad of clinical signs are more likely to shed Salmonella, but shedding is not limited to these particular patients [12].  These clinical signs are specific indicators for identifying shedding, but they are not perfectly sensitive.  Additional factors that may affect the likelihood of shedding include patient management factors such as transportation distance, antimicrobial therapy, and duration of hospitalization, as well as species or rearing circumstances (intensively managed cattle being much more likely to shed than horses – an element that should not be overlooked when managing horses in a multi-species hospital) [12; 20].  In addition, reports consistently show a seasonal occurrence to shedding – highest in late summer and early fall, and lowest in the spring [12; 14; 21-23]. 

The intermittent nature of Salmonella shedding, often in the absence of clinical signs, makes it challenging to effectively manage this risk.  Patient shedding prevalence can vary from 0.5% up to 7% with horses admitted for elective procedures and those in the general equine population having a lower prevalence; as well those tested on admission typically have a lower prevalence than horses tested throughout hospitalization [18; 19; 21; 23].  A higher shedding prevalence has been reported in horses with gastrointestinal disease or colic ranging from 4.3% up to 13% [14; 16; 19].  Differential management may be warranted for patient subgroups depending upon the likelihood of Salmonella shedding on admission or throughout the duration of hospitalization.

Routine surveillance by testing fecal samples may be an effective method to detect Salmonella shedding among patients.  Consideration should be given to how this may be implemented – test all patients or target a high risk group such as horses with gastrointestinal disease.  While research does show that targeted surveillance of horses presenting for acute colic or diarrhea can be an effective method for identifying fecal shedding it also shows that many horses can be shedding Salmonella in the absence of clinical signs [3; 11; 24].  An alternative may be to use syndromic surveillance – a method that has been shown to be effective at detecting adverse events in hospitalized horses [25].  Some facilities my choose to conduct surveillance of the hospital environment rather than of patients as environmental contamination is commonly detected near where positive patients are managed [4; 17].  This could be conducted as either routine or periodic surveillance of high-traffic areas.  Yet others may choose to conduct both active surveillance of patients and the environment.  As complementary techniques, this may allow for earlier detection of endemic shedding among patients and to identify outbreaks early in their time course [3]. 

Environmental contamination cannot be completely eliminated, therefore the goal is to reduce contamination of the environment to a level that becomes biologically irrelevant.  Veterinary hospitals can be frequently contaminated near where positive patients are managed with floors, floor drains, cracks and crevices being common sights for contamination [4; 24; 26; 27].  To gain meaningful information, environmental testing should be performed regularly to establish a baseline level of environmental contamination to which future findings can be compared.  In this way potential environmental reservoirs of Salmonella can be detected and cleaning effectiveness can be continually monitored.

References

Benedict, K.M., Morley, P.S. and Van Metre, D.C. (2008) Characteristics of biosecurity and infection control programs at veterinary teaching hospitals. J Am Vet Med Assoc 233, 767-773.

Dallap Schaer, B.L., Aceto, H. and Rankin, S.C. (2010) Outbreak of salmonellosis caused by Salmonella enterica serovar Newport MDR-AmpC in a large animal veterinary teaching hospital. J Vet Intern Med 24, 1138-1146.

Steneroden, K.K., Van Metre, D.C., Jackson, C. and Morley, P.S. (2010) Detection and control of a nosocomial outbreak caused by Salmonella newport at a large animal hospital. J Vet Intern Med 24, 606-616.

Burgess, B.A., Morley, P.S. and Hyatt, D.R. (2004) Environmental surveillance for Salmonella enterica in a veterinary teaching hospital. J Am Vet Med Assoc 225, 1344-1348.

Castor, M.L., Wooley, R.E., Shotts, E.B., Brown, J. and Payeur, J.B. (1989) Characteristics of Salmonella isolated from an outbreak of equine salmonellosis in a veterinary teaching hospital. Journal of Equine Veterinary Science 9, 236-241.

Tillotson, K., Savage, C.J., Salman, M.D., Gentry-Weeks, C.R., Rice, D., Fedorka-Cray, P.J., Hendrickson, D.A., Jones, R.L., Nelson, W. and Traub-Dargatz, J.L. (1997) Outbreak of Salmonella infantis infection in a large animal veterinary teaching hospital. J Am Vet Med Assoc 211, 1554-1557.

Schott, H.C., 2nd, Ewart, S.L., Walker, R.D., Dwyer, R.M., Dietrich, S., Eberhart, S.W., Kusey, J., Stick, J.A. and Derksen, F.J. (2001) An outbreak of salmonellosis among horses at a veterinary teaching hospital. J Am Vet Med Assoc 218, 1152-1159, 1100.

Hird, D.W., Pappaioanou, M. and Smith, B.P. (1984) Case-control study of risk factors associated with isolation of Salmonella saintpaul in hospitalized horses. Am J Epidemiol 120, 852-864.

House, J.K., Mainar-Jaime, R.C., Smith, B.P., House, A.M. and Kamiya, D.Y. (1999) Risk factors for nosocomial Salmonella infection among hospitalized horses. J Am Vet Med Assoc 214, 1511-1516.

Ekiri, A.B., MacKay, R.J., Gaskin, J.M., Freeman, D.E., House, A.M., Giguere, S., Troedsson, M.R., Schuman, C.D., von Chamier, M.M., Henry, K.M. and Hernandez, J.A. (2009) Epidemiologic analysis of nosocomial Salmonella infections in hospitalized horses. J Am Vet Med Assoc 234, 108-119.

Dallap Schaer, B.L., Aceto, H., Caruso, M.A., 3rd and Brace, M.A. (2012) Identification of predictors of Salmonella shedding in adult horses presented for acute colic. J Vet Intern Med 26, 1177-1185.

Burgess, B.A. (2014) Epidemiology and prevention of Salmonella in veterinary hospitals, Colorado State University, Libraries.

Aceto, H., Miller, S.A. and Smith, G. (2011) Onset of diarrhea and pyrexia and time to detection of Salmonella enterica subsp enterica in feces in experimental studies of cattle, horses, goats, and sheep after infection per os. J Am Vet Med Assoc 238, 1333-1339.

Ernst, N.S., Hernandez, J.A., MacKay, R.J., Brown, M.P., Gaskin, J.M., Nguyen, A.D., Giguere, S., Colahan, P.T., Troedsson, M.R., Haines, G.R., Addison, I.R. and Miller, B.J. (2004) Risk factors associated with fecal Salmonella shedding among hospitalized horses with signs of gastrointestinal tract disease. J Am Vet Med Assoc 225, 275-281.

Hird, D.W., Casebolt, D.B., Carter, J.D., Pappaioanou, M. and Hjerpe, C.A. (1986) Risk factors for salmonellosis in hospitalized horses. J Am Vet Med Assoc 188, 173-177.

Kim, L.M., Morley, P.S., Traub-Dargatz, J.L., Salman, M.D. and Gentry-Weeks, C. (2001) Factors associated with Salmonella shedding among equine colic patients at a veterinary teaching hospital. J Am Vet Med Assoc 218, 740-748.

Dunowska, M., Patterson, G., Traub-Dargatz, J.L., Hyatt, D.R. and Morley, P.S. (2004) Recent progress in controlling Salmonella in Veterinry Hospitals. In: 50th Annual Convention of the American Association of Equine Practitioners, Lexington, KY. p 1461.

Traub-Dargatz, J.L., Salman, M.D. and Jones, R.L. (1990) Epidemiologic study of salmonellae shedding in the feces of horses and potential risk factors for development of the infection in hospitalized horses. J Am Vet Med Assoc 196, 1617-1622.

Alinovi, C.A., Ward, M.P., Couetil, L.L. and Wu, C.C. (2003) Risk factors for fecal shedding of Salmonella from horses in a veterinary teaching hospital. Prev Vet Med 60, 307-317.

Burgess, B.A. and Morley, P.S. (2013) Factors associated with large animal inpatient shedding of Salmonella enterica in a veterinary teaching hospital. In: 94th Annual Conference of Research Workers in Animal Diseases, Chicago, IL.

Smith, B.P., Reina-Guerra, M. and Hardy, A.J. (1978) Prevalence and epizootiology of equine salmonellosis. J Am Vet Med Assoc 172, 353-356.

Carter, J.D., Hird, D.W., Farver, T.B. and Hjerpe, C.A. (1986) Salmonellosis in hospitalized horses: seasonality and case fatality rates. J Am Vet Med Assoc 188, 163-167.

Traub-Dargatz, J.L., Garber, L.P., Fedorka-Cray, P.J., Ladely, S. and Ferris, K.E. (2000) Fecal shedding of Salmonella spp by horses in the United States during 1998 and 1999 and detection of Salmonella spp in grain and concentrate sources on equine operations. J Am Vet Med Assoc 217, 226-230.

Ewart, S.L., Schott, H.C., 2nd, Robison, R.L., Dwyer, R.M., Eberhart, S.W. and Walker, R.D. (2001) Identification of sources of Salmonella organisms in a veterinary teaching hospital and evaluation of the effects of disinfectants on detection of Salmonella organisms on surface materials. J Am Vet Med Assoc 218, 1145-1151.

Ruple-Czerniak, A.A., Aceto, H.W., Bender, J.B., Paradis, M.R., Shaw, S.P., Van Metre, D.C., Weese, J.S., Wilson, D.A., Wilson, J. and Morley, P.S. (2013) Syndromic surveillance for evaluating the occurrence of healthcare-associated infections in equine hospitals. Equine Vet J.

Pandya, M., Wittum, T., Tadesse, D.A., Gebreyes, W. and Hoet, A. (2009) Environmental Salmonella surveillance in the Ohio State University Veterinary Teaching Hospital. Vector Borne Zoonotic Dis 9, 649-654.

Alinovi, C.A., Ward, M.P., Couetil, L.L. and Wu, C.C. (2003) Detection of Salmonella organisms and assessment of a protocol for removal of contamination in horse stalls at a veterinary teaching hospital. J Am Vet Med Assoc 223, 1640-1644.