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<I>Corynebacterium Bovis</I>

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<I>Corynebacterium Bovis</I> Journal of the American Association for Laboratory Animal Science Vol 59, No 6 Copyright 2020 November 2020 by the American Association for Laboratory Animal Science Pages 712–718 Metaphylactic Antibiotic Treatment to Prevent the Transmission of Corynebacterium bovis to Immunocompromised Mouse Offspring Emily C Pearson,1 Umarani Pugazhenthi,2 Derek L Fong,1,3 Derek E Smith,4 Andrew G Nicklawsky,4 Lauren M Habenicht,1,3 Michael K Fink,1,3 Jori K Leszczynski,1,3 Michael J Schurr,5 and Christopher A Manuel1,3,6,* Current methods for eradicating Corynebacterium bovis, such as depopulation, embryo transfer, and cesarean rederivation followed by cross fostering, are expensive, complex, and time-consuming. We investigated a novel method to produce immunocompromised offspring free of C. bovis from infected NOD.Cg-Prkdcscid Il2rgtm1Wgl/SzJ (NSG) breeding pairs. Adult NSG mice were infected with C. bovis, paired, and randomly assigned to either a no-antibiotic control group (NAB, n = 8) or a group that received amoxicillin–clavulanic acid (0.375 mg/mL) in their drinking water for a mean duration of 7 wk (AB group, n = 7), spanning the time from pairing of breeders to weaning of litters. The AB group also underwent weekly cage changes for 3 wk after pairing to decrease intracage C. bovis contamination, whereas the NAB mice received bi-weekly cage changes. Antibiotics were withdrawn at the time of weaning. All litters (n = 7) in the AB group were culture- and qPCR-negative for C. bovis and remained negative for the duration of the study, whereas all litters in the NAB group (n = 6) remained C. bovis positive. A single adult from each breeding pair was sampled at weaning and at 5 and 10 wk after weaning to confirm the maintenance of (NAB) or to diagnose the reemergence (AB) of C. bovis infection. By the end of the study, C. bovis infection had returned in 3 of the 7 (43%) tested AB adults. Our data suggest that metaphylactic antibiotic use can decrease viable C. bovis organisms from adult breeder mice and protect offspring from infection. However, using antibiotics with frequent cage changing negatively affected breeding performance. Nevertheless, this technique can be used to produce C. bovis-free NSG offspring from infected adults and may be an option for salvaging infected immunocompromised strains of mice that are not easily replaced. Abbreviations: AB, antibiotics group; C. NAB, no antibiotics group; NSG, NOD.Cg-Prkdcscid Il2rgtm1Wgl/SzJ DOI: 10.30802/AALAS-JAALAS-20-000005 Corynebacterium bovis is a common bacterial pathogen among Rederivation methods that are likely to be effective in the immunocompromised mouse colonies. Clinical signs associated elimination of C. bovis include embryo transfer and cesarean with C. bovis infection in athymic nude mice (Foxn1, nu/nu) rederivation followed by cross fostering. These measures can be include an asymptomatic persistent carrier state and 2 to 7 d expensive and require a high degree of technical skill and con- of dermal hyperkeratosis, dehydration, lethargy, and decreased siderable time. Conversely, antibiotic administration through body condition.5,9,11,24 Haired immunocompromised mouse feed or drinking water requires minimal labor, treats multiple strains such as NOD.Cg-Prkdcscid Il2rgtm1Wgl/SzJ (NSG) mice animals concurrently, provides no additional stress to the ani- also can develop clinical C. bovis infection and present with mals, and requires no specialized surgical skills.17 rough hair coat, decreased body condition, scaly skin, alopecia, In one study, antibiotic administration prevented the detec- conjunctivitis, and erythematous pinnae.5,9,25 tion of C. bovis from infected mouse skin tested by culture during C. bovis has a negative effect on cancer research due to the treatment.5 However, after discontinuing long-term antibiotic induced changes to the immune response and some institu- administration, C. bovis can again be cultured, with definitive tions choose to exclude this pathogen from their facilities.20,29 clearance of only 13% of infected adult mice.5 We recently Depopulation, environmental and equipment sanitation, and demonstrated that prophylactic antibiotic therapy can prevent repopulation are often elected, given that the majority of suscep- the infection of immunodeficient mice after acute exposure.16 tible strains can easily be purchased from C. bovis-free vendors. As opposed to prophylaxis, metaphylaxis is the treatment of However, when unique noncommercial immunocompro- an animal population that has been infected with a microbial mised strains are infected, depopulation may not be an option. agent but is not currently experiencing any level of clinical disease.3 Metaphylaxis differs from prophylaxis and therapeu- tic antimicrobial use because the expectation is to control an Received: 16 Jan 2020. Revision requested: 05 Mar 2020. Accepted: 04 May 2020. infection that is already present, rather than to prevent or cure 1Office of Laboratory Animal Resources,2 Division of Endocrinology, Metabolism, and Diabetes, School of Medicine, and Departments of 3Pathology and Immunology and infection. Using antibiotics in a metaphylactic manner requires Microbiology, Anschutz Medical Campus, University of Colorado–Denver, Aurora, a population-management mindset. Colorado; 4Biostatics Core, 5Department of Immunology and Microbiology, University of The goal of our study was to investigate the metaphylactic use Colorado Cancer Center, Aurora, Colorado; and 6University of Colorado Cancer Center, Aurora, Colorado of amoxicillin–clavulanic acid for C. bovis-infected NSG breed- *Corresponding author. Email: [email protected] ing pairs in order to prevent post-parturition transmission of 712 Metaphylaxis for C. bovis infected breeders C. bovis prior to weaning. We hypothesized that the metaphy- was removed from frozen stock, and cultured on tripticase soy lactic antibiotics would either eliminate all viable C. bovis or agar with 5% sheep blood (catalog no. 221261, Becton Dicken- decrease skin burden to undetectable levels on adult breeders. son, Franklin Lakes, NJ) at 37 °C for 72 h. At 24 hours prior to This situation would facilitate a C. bovis-free window dur- mouse inoculation, CUAMC1 was propagated in heart infusion ing which transmission to neonates and weanlings would be broth (catalog no. 238400, Becton Dickenson) containing 1% prevented, thus providing a novel and noninvasive method to Tween 80 for 24 h. Bacterial concentration was determined by eliminate C. bovis from unique immunocompromised mouse comparing the culture’s absorbance at OD600 with a standard strains that are not easily replaced. curve generated by serial dilutions. Mice were anesthetized with isoflurane, and 50 µL of culture broth containing 2× 107 Materials and Methods cfu of C. bovis was applied to the dorsal neck of each mouse. Animals and facility. Thirty male and 26 female, 7 wk old, A sterile swab (BactiSwab Dry, Remel, Lenexa, KS) was used NOD.Cg-Prkdcscid Il2rgtm1Wgl/SzJ mice (NSG) were purchased to distribute the inoculum on the skin, outer and inner pinnae, from Jackson Laboratories, Bar Harbor, ME. The mice were muzzle, lip commissures, and eyelids bilaterally. At 2 wk after documented to be free of ectromelia virus, Theiler mouse experimental inoculation, mice in each cage were swabbed, to encephalomyelitis virus, Hantaan virus, K virus, lactic dehydro- confirm infection by qPCR analysis. Cages that failed to gener- genase elevating virus, lymphocytic choriomeningitis, mouse ate an established infection were supplemented with 50 mL of adenovirus, mouse cytomegalovirus, mouse hepatitis virus, soiled bedding from an experimentally positive cage. At 2 wk mouse minute virus, mouse parvovirus, mouse thymic virus, after exposure to C. bovis-soiled bedding, all remaining cages pneumonia virus of mice, polyoma virus, reovirus 3, rotavirus, were confirmed positive by qPCR analysis. Animals were posi- Sendai virus, Bordetella spp., CAR bacillus, Citrobacter rodentium, tive via qPCR analysis for a minimum of 3 wk (21.6 ± 1.4 d) prior Clostridium piliforme, Corynebacterium kutscheri, Corynebacterium to the start of the experiment. bovis, Mycoplasma pulmonis, Salmonella spp., Streptobacillus mon- Experimental design. After qPCR confirmation of C. bovis oliformis, Encephalitozoon cuniculi, fur mites, lice, follicle mites, infection, male and female NSG mice were randomly grouped pinworms, roundworms, and tapeworms. On arrival, mice into breeding pairs, which then were assigned to receive either were tested by skin swab and confirmed negative forC. bovis treatment with antibiotic-containing drinking water (AB, n = by qPCR analysis. All animal manipulations were approved 8) or standard facility water (NAB, n = 8). Because a low birth by the IACUC of University of Colorado–Denver Anschutz rate occurred in AB, 10 additional breeding pairs were added to Medical Campus, an AAALAC-accredited institution. Personal reach a statistically significant sample size. On the day after pair- protective equipment required to enter the facility include a ing, the AB group began receiving drinking water containing hair bonnet and disposable gown worn over personal clothing; amoxicillin–clavulanic acid (amoxicillin trihydrate–clavulanate additional equipment was required in the quarantine animal potassium, 0.375 mg/mL, Zoetis, Parsippany-Troy Hills, NJ). housing room and included an additional disposable gown Medicated water was prepared by mixing 0.37 g of amoxicillin and shoe covers.15 trihydrate–clavulanate potassium,
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