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<I>Staphylococcus Xylosus</I> Inoculation of Staphylococcus xylosus in SJL/J Mice to Determine Pathogenicity VENITA B. THORNTON, DVM, MPH, LCDR, VC, USPHS,1* JUDITH A. DAVIS, DVM, MS, DIPLOMATE, ACLAM,2 MARK B. ST. CLAIR, DVM, MS, DIPLOMATE, ACLAM,3 AND MARLENE N. COLE, DVM, MPH, DIPLOMATE, ACLAM, CAPT, VC, USPHS1 An experimental study was performed to investigate whether intradermal tail inoculations of Staphylococcus xylosus would result in pathologic lesions in the SJL/J strain of mice (Mus musculus). This organism historically has been classified as a nonpathogenic, commensal bacterium associated with skin and mucous membranes and rarely implicated in infections. In this study, SJL/J mice inoculated with S. xylosus developed cutaneous tail lesions post-inoculation, and the organism was recovered from those lesions. Inoculation was accomplished by surgically inserting silk suture impregnated with the concentrated suspension of bacteria. In addition, a superficial abrasion was created adjacent to the suture, and a bacterial suspension was applied. Approximately 80% of the mice in the inoculated groups developed dermatologic lesions, compared with 0% in the control group. Mice with lesions were treated with Sulfamethoxazole-Trimethoprim in the drinking water continuously for 28 days. For the mice assigned to the treat- ment group, this treatment resulted in resolution of the cutaneous tail lesions. In 1997, there was an outbreak of spontaneous necrotic tail le- Materials and Methods sions in a colony of naïve SJL/J mice housed at the National Animals. We obtained 55 specific pathogen- free SJL/J female Institute of Neurological Disorders and Stroke (NINDS), Depart- mice (Mus musculus) at 4 to 5 weeks of age from The Jackson ment of Health and Human Services (DHHS), National Institutes Laboratory (Bar Harbor, Maine). The mice were extensively of Health (NIH). Two of the coauthors of this manuscript were monitored by the supplier for the following pathogenic agents: the attending and clinical veterinarians for the SJL/J mouse colony Cilia Associated Respiratory bacillus, Ectromelia, mouse rotavirus, during the clinical outbreak. Although pure cultures of Staphylo- mouse encephalomyelitis virus, lymphocytic choriomeningitis coccus xylosus were isolated from the lesions in these mice, further virus, murine cytomegalovirus, mouse hepatitis virus, mouse studies were needed to investigate the role of this bacteria in the adenovirus, minute virus of mice, Mycoplasma pulmonis, pathogenic processes. This SJL/J mouse colony developed spon- parvovirus, polyoma virus, pneumonia virus of mice, reovirus 3, taneous tail lesions, with the most severely affected mice losing and Sendai virus. much of the tail tissue because of necrosis and sloughing. The The mice were maintained in an NIH animal facility accred- outbreak resulted in the euthanasia of the SJL/J mice, in light ited by the Association for Assessment and Accreditation of of the severity of the tail lesions. Laboratory Animal Care, International. Mice were separated by Staphylococcus xylosus (S. xylosus) is a gram-positive, coagulase- treatment groups, which were group-housed in 19.05 × 29.21 × negative, coccoid bacterium of the family Micrococcacae (1). It has 12.7-cm sterilized Micro-Isolator™ cages (Lab Products Inc., been considered a nonpathogenic skin and mucous membrane Seaford, Del.) on Harlan Tek-Fresh bedding (Madison, Wis.). commensal organism and has rarely been reported associated with All cages were changed weekly. The specific pathogen-free ani- infections. Since 1974, there have been a number of reports de- mal holding room was maintained under environmental scribing the incidence of coagulase-negative staphylococcal conditions of 20°C, 40% to 70% relative humidity, 15 air changes organisms in human clinical infections. Some of these human in- hourly, and a 12:12-h light:dark cycle. Mice were fed pelleted fections were associated with S. xylosus and resulted in rodent diet (Rodent NIH-31 Autoclavable NA, Zeigler Brothers, pyelonephritis, subacute bacterial endocarditis, pancreatic Inc., Gardners, Pa.) ad libitum and provided sterilized individual pseudocysts, and other miscellaneous infections (2-4). Coagulase- water bottles for ad libitum water sources. The mice were accli- negative staphylococci, including S. xylosus, formerly were mated a minimum of 7 days prior to being used in the described as harmless contaminants; however, these organisms experiments. Mice were identified by using numbered stainless- have assumed a more prominent role due to infections in both steel rodent ear tags (National Band and Tag Co., Newport, Ky.). immunocompromised patients and IV drug abusers (5). In vet- This study was reviewed and approved by the Institutional Ani- erinary medicine, S. xylosus has been implicated as a cause of mal Care and Use Committee. All procedures and use of animals subclinical mastitis in dairy ewes (6), mastitis in dairy cows (7), were in accordance with the Guide for the Care and Use of Labora- lesions in gerbils (8, 9), fatalities in red progy fish (10), and fatal tory Animals. dermatitis in a colony of athymic nude mice (11). The concept of Bacterial culture and isolation. The source of the S. xylosus the existence of different substrains of S. xylosus has been reported inoculum originated from frozen aliquots of the bacteria, which in the literature (1, 12). It is conceivable that there are both patho- previously had been isolated, collected, and preserved from the genic and nonpathogenic substrains of S. xylosus. The purpose of spontaneous tail lesions observed in a naïve SJL/J mouse colony our study was to determine whether S. xylosus was a causative fac- at NIH. This stock culture was stored in T-soy broth containing tor in the tail lesions seen in SJL/J mice. 15% glycerol in a –80°C freezer. Cultures of S. xylosus were grown in 5% blood agar for 24 h at 37°C and suspended in sterile sa- Uniformed Services University of the Health Sciences (USUHS), 4301 Jones Bridge Road, line. Identification of the culture isolates was achieved by using Bethesda, Maryland 208141; National Institute of Neurologic Disorders and Stroke (NINDS), an in vitro diagnostic system with automated identification of 2 DHHS, National Institutes of Health, 9000 Rockville Pike, Bethesda, Maryland 20892 ; gram-positive bacteria (Sensititre AP90 Autoidentification Plate, National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK), DHHS, Na- tional Institutes of Health, 9000 Rockville Pike, Bethesda, Maryland 208923 Trek Diagnostic Systems Ltd., Westlake, Ohio). *Corresponding author Experimentally induced infection with S. xylosus. We obtained Volume 42, No. 4 / July 2003 CONTEMPORARY TOPICS © 2003 by the American Association for Laboratory Animal Science 49 oral cavity swab samples (Bac-T swab, Remel, Lenexa, Kans.) from Table 1. Development of tail lesions after the inoculation of SJL/J mice with all mice. These samples were cultured on blood agar plates (Tryp- Staphylococcus xylosus tic Soy Agar with 5% sheep blood, Remel, Lenexa, Kans.) to Group Inoculation Group Tail Positive S. xylosus culture detect the presence of the S. xylosus organism. The cultures were concentration sizea lesions Oral site Tail site Both sites submitted to the microbiology laboratory for diagnostic evalua- A 10 × 108 bacteria/ml 18 15 11 11 8 tion. Mice were divided into three groups: Group A (n = 18) B5 × 108 bacteria/ml 17 14 11 8 7 was inoculated with a high dose (10 × 108 bacteria/ml); Group C Negative controls 5 0 0 0 0 B (n = 17) was inoculated with a low dose (5 × 108 bacteria/ml); aGroup A, one cage death, data collected on post-mortem. and Group C (n = 5) was the negative controls. The remaining 15 mice were positive for S. xylosus and therefore were not used; cessed for histologic evaluation, and evaluated microscopically. only mice determined to be S. xylosus-negative by the swab test Statistical analysis. Fisher’s exact test (13) was used to com- were used in the inoculation groups. pare the proportion of mice with clinical effects in the S. xylosus Mice were anesthetized with isoflurane in an induction cham- inoculated groups to the control group. Fisher’s exact test was ber (Braintree Scientific Inc., Braintree, Mass.), and maintained chosen for this analysis because it is appropriate for comparing under anesthesia using a nonrebreathing system and a nosecone proportions even in the case of small sample sizes and /or rare α = facemask. The suture material was impregnated with the con- events. A one-sided significance level of 0.05 was used to test centrated suspension of bacteria for the experimental groups the hypotheses that lesions were more likely to develop in in- and in sterile water for the control group. A 27-gauge needle oculated mice than noninoculated mice and that lesions were with swaged on 4-0 silk suture (Ethicon, Piscataway, N.J.) was more likely to develop in the high-dose group than the low-dose inserted into deep tissue of the dorsal, proximal quarter of the group. The sample size was found to be sufficient to detect a tail and tied in a surgical square-knot. Adjacent to the site of difference of 0.64 between the control and inoculated groups suture placement, 0.2 × 0.3-mm superficial abrasions were cre- with 80% power. Statistical analyses were performed using SAS, ated in all animals. In Groups A and B (experimental), bacterial version 8 (SAS Institute, Inc. 1999-2001, Cary, N.C). suspension (0.1 ml) was applied to the inoculum sites, and ster- ile water (0.1 ml) was applied in Group C (control). This Results procedure was designed to enhance entry of the bacterial or- Tail lesions developed in 30 of the 35 experimentally infected ganism by the “wick effect” and thus provided a nidus for bacterial mice inoculated with S. xylosus (85.7%) in Groups A and B growth. All mice were weighed and their ear tag identification (Table 1). Lesions did not develop in Group C, which remained checked prior to placement back into the cage.
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