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Abortion in cattle due to infection with Staphylococcus lugdunensis Paolo Ardigò, Mario D'Incau and Stefano Pongolini J VET Diagn Invest published online 7 October 2014 DOI: 10.1177/1040638714550182 The online version of this article can be found at: http://vdi.sagepub.com/content/early/2014/10/06/1040638714550182
Published by: http://www.sagepublications.com
On behalf of:
Official Publication of the American Association of Veterinary Laboratory Diagnosticians, Inc.
Additional services and information for Journal of Veterinary Diagnostic Investigation can be found at: Email Alerts: http://vdi.sagepub.com/cgi/alerts Subscriptions: http://vdi.sagepub.com/subscriptions Reprints: http://www.sagepub.com/journalsReprints.nav Permissions: http://www.sagepub.com/journalsPermissions.nav
>> OnlineFirst Version of Record - Oct 7, 2014 What is This?
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550182 research-article2014
VDIXXX10.1177/1040638714550182Staphylococcus lugdunensis in bovine abortionArdigò et al.
Brief Communication
Abortion in cattle due to infection with Staphylococcus lugdunensis
Journal of Veterinary Diagnostic Investigation 1–3 © 2014 The Author(s) Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/1040638714550182 jvdi.sagepub.com
Paolo Ardigò, Mario D’Incau, Stefano Pongolini1
Abstract. An aborted fetus of 7 months gestation, the associated placenta, and a single blood sample from the dam were submitted for diagnostic investigation to the diagnostic laboratory of the Lombardy and Emilia-Romagna Experimental Zooprophylactic Institute in Parma, Italy. The serum was negative for Neospora caninum, Coxiella burnetii, Chlamydophila abortus, Bovine herpesvirus 1 (BHV-1), Bovine viral diarrhea virus (BVDV), Brucella abortus, and Brucella melitensis. Fetal tissues and placental cotyledons were pooled and tested by polymerase chain reaction (PCR) for the presence of BHV-1, Bovine herpesvirus 4, BVDV, N. caninum, C. burnetii, Chlamydophila spp., Schmallemberg virus, and Leptospira interrogans. All PCR assays were negative. Bacteriological examinations performed on the fetal organs revealed a pure growth of Staphylococcus lugdunensis in all organs cultured. In human beings, S. lugdunensis is responsible for communityacquired and nosocomial infections, in both immunocompetent and immunocompromised patients. In veterinary medicine, the pathogenic potential of S. lugdunensis has not been fully investigated. The incidence of S. lugdunensis is regarded as being underreported because it could be easily misidentified as Staphylococcus aureus. The current report documents the ability of S. lugdunensis to cause abortion in cattle, indicating the need for accurate diagnostic procedures to identify this emerging and zoonotic pathogen whose incidence is likely underestimated in both human and veterinary medicine. Key words: Abortion; abortive diseases; cattle; Staphylococcus lugdunensis. Abortion in cattle is defined as loss of the fetus occurring between 42 and 260 days of gestation.7 The cause of this event is often difficult to identify, and the results of laboratory investigations reported in the literature suggest that only in approximately 35% of cases is it possible to ascertain the etiological agent.4 Most bacteria causing bovine abortion are opportunistic pathogens. Trueperella pyogenes and Bacillus spp. followed by Escherichia coli, Histophilus somni, Pasteurella spp., Listeria monocytogenes, Staphylococcus spp., Streptococcus spp., and any other bacteria that can find their way into the bloodstream can act as opportunistic pathogens and cause sporadic abortion. Such opportunists are associated with abortions at any period of gestation, even though most are associated with late second to third trimester abortions.15 In the current report, a case of abortion in cattle caused by Staphylococcus lugdunensis, an emerging pathogen in human beings10 and companion animals,22,24 is described. Sporadic abortions were reported on a farm in the Province of Parma (northern Italy). The farm was a commercial dairy, consisting of approximately 500 lactating Holstein– Friesian cows. The abortion rate had been 3.8% over the preceding 12 months, and no laboratory diagnostics had been performed on those cases. In May 2013, a fetus of 7 months’ gestation, the associated placenta, and a blood sample of the cow were submitted for routine diagnostic investigation to the diagnostic laboratory of the Lombardy and Emilia-Romagna Experimental Zooprophylactic Institute in Parma, Italy.
The serum was negative for Neospora caninum, Coxiella burnetii, Chlamydophila abortus, Bovine herpesvirus 1 (BHV-1), Bovine viral diarrhea virus (BVDV), Brucella abortus, and Brucella melitensis. The veterinary practitioner who assisted the herd reported that no postabortion complications were observed in the dam. The fetus presented minimal autolysis, moderate cutaneous edema, increased presence of fluids in the abdominal and thoracic cavities, moderately swollen spleen and liver, and complete atelectasis of the lungs. No gross lesions were apparent on the placenta. Specimens of the brain, lung, heart, liver, spleen, kidney, abomasum content, and placental cotyledons were pooled and homogenized with sterile scissors for subsequent use in a number of polymerase chain reaction (PCR) assays. Pooling was a convenient compromise for fetal PCR diagnostics that broadened the spectrum of organs that could be tested while saving resources. Nucleic acids from the pool were extracted using commercial kits specific for DNAa and RNAb following manufacturers’ instructions. End-point PCRs were used to detect BHV-1,8 Bovine herpesvirus 4,8 BVDV,18 From the Lombardy and Emilia Romagna Experimental Zooprophylactic Institute, Parma (Ardigò, Pongolini) and Brescia (D’Incau), Italy. 1
Corresponding Author: Stefano Pongolini, Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia-Romagna, Via dei Mercati 13/A, 43126 Parma, Italy. [email protected]
Downloaded from vdi.sagepub.com at Bibliothekssystem der Universitaet Giessen on October 22, 2014
2
Ardigò et al.
N. caninum,20 C. burnetii,2 and Chlamydophila spp.23 A realtime PCR was used for Leptospira interrogans.27 Specimens of the brain, spleen, and thymus were also pool-tested for the presence of Schmallemberg virus by real-time PCR.14 All PCR assays were negative. Lung, liver, spleen, kidney, and the content of the abomasum were aseptically collected and cultured on bovine blood agar,c Gassner agar,d and Brucella agare under aerobic and increased (10%) CO2 incubation at 37°C. A pure culture appeared on the bovine blood agarc plates from all cultured organs and the abomasum content after 24 hr of incubation. After 48 hr, colonies were white, round, smooth, glistening, and 2–3 mm in diameter. A complete zone of hemolysis of approximately 1 mm was evident around the colonies. No growth was observed after 48 hr of incubation on Gassner agard and after 10 days of incubation on Brucella agar.e Gram staining revealed the organism to consist of Gram-positive cocci. The bacterial isolate was catalase positive, oxidase negative, slide-coagulase positive, and tube-coagulase negative. A commercial identification kitf gave a profile of 6312150, which corresponded to S. lugdunensis with 97.3% identity. A second commercial identification system,g which includes 43 biochemical tests, was used as a confirmatory test. The second system gave a code of 010002002623231, corresponding to S. lugdunensis with 99% probability. No unexpected test results were obtained, and no supplementary tests were required for the definitive identification of the isolate. Antimicrobial susceptibility was assessed by Kirby– Bauer disk diffusion according to the Clinical and Laboratory Standards Institute.6 The strain was resistant to sulfadiazine, but sensitive to amoxicillin–clavulanic acid, ampicillin, ceftiofur, cloxacillin, colistin, enrofloxacin, florfenicol, oxacillin, penicillin, trimethoprim–sulfamethoxazole, tetracycline, thiamphenicol, tiamulin, and tylosin. Staphylococcus lugdunensis is a coagulase-negative staphylococcus (CNS) that was first described in 1988.11 The organism is a commensal of the human skin more frequently found on the lower part of the body and the extremities, particularly in the moist areas such as the groin, perineum, and the large toenail.3 Although CNS are generally considered nonpathogenic commensal in immunocompetent subjects, S. lugdunensis is an important exception being responsible for community-acquired and nosocomial infections,10 in both immunocompetent5,13,16,28 and immunocompromised patients.13,21 In human beings, S. lugdunensis has been described as a possible cause of skin and soft tissue infection, prosthetic and naive valves endocarditis, bone and joint infections, and bacteremia.10 The organism has rarely been isolated in peritonitis, and central nervous system, oral, ocular, and urinary tract infections.10 Staphylococcus lugdunensis has also been associated with endometritis,1 pyomyoma,26 and, in 2013, its detection in amniotic fluids collected during cesarean sec-
tions was reported, although no postoperative infection or neonatal complications were observed.19 In veterinary medicine, the pathogenic potential of S. lugdunensis has not been fully investigated. A retrospective case control study of S. lugdunensis infections in small companion animals suggested that S. lugdunensis is more often isolated from deep tissues and wounds than from superficial infections, therefore, it should be considered a potential pathogen.24 Staphylococcus lugdunensis was also isolated from a blood sample of a dog with endocarditis, but a role in the pathogenesis of the disease remains uncertain as the dog was also positive for Bartonella spp. by PCR, and possible contamination of the blood sample by S. lugdunensis through the skin could not be ruled out.22 Staphylococcus lugdunensis was also shown to cause subcutaneous abscesses, peritonitis, and osteomyelitis in mice9,17,25 and rabbits12 used in experimental studies. The incidence of S. lugdunensis is presumed to be underreported in both human and veterinary medicine as it can be easily misidentified as Staphylococcus aureus, which shares the same colony morphology, hemolytic activity, and the ability to agglutinate latex particles coated with fibrinogen.29 The current report documents the ability of S. lugdunensis to cause abortion in cattle, underlining the need for accurate diagnostic procedures to correctly identify this emerging and zoonotic pathogen whose incidence is likely underestimated. Acknowledgements The authors thank the staff of Lombardy and Emilia-Romagna Experimental Zooprophylactic Institute for technical assistance with bacterial isolation and identification procedures.
Sources and manufacturers a.
PureLink genomic DNA kits, Life Technologies Ltd., Carlsbad, CA. b. RNeasy mini kit, Qiagen Inc., Valencia, CA. c. Oxoid Ltd, Basingstoke, Hampshire, United Kingdom. d. Biolife Italiana S.r.l., Milan, Italy. e. Microbiol diagnostici, Cagliari, Italy. f. API Staph, BioMérieux, Marcy l’Etoile, France. g. VITEK 2 compact combined with VITEK 2 Gram positive identification card, BioMérieux, Marcy l’Etoile, France.
Declaration of conflicting interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and publication of this article.
Funding The author(s) received no financial support for the research, authorship, and publication of this article.
References 1. Bello C, Eskandar M, El GR, et al.: 2007, Staphylococcus lugdunensis endometritis: a case report. West Afr J Med 26:243–245.
Downloaded from vdi.sagepub.com at Bibliothekssystem der Universitaet Giessen on October 22, 2014
Staphylococcus lugdunensis in bovine abortion 2. Berri M, Arricau-Bouvery N, Rodolakis A: 2003, PCR-based detection of Coxiella burnetii from clinical samples. Methods Mol Biol 216:153–161. 3. Bieber L, Kahlmeter G: 2010, Staphylococcus lugdunensis in several niches of the normal skin flora. Clin Microbiol Infect 16:385–388. 4. Cabell E: 2007, Bovine abortion: aetiology and investigations. In Pract 29:455–463. 5. Casanova-Roman M, Sanchez-Porto A, Casanova-Bellido M: 2004, Urinary tract infection due to Staphylococcus lugdunensis in a healthy child. Scand J Infect Dis 36:149–150. 6. Clinical and Laboratory Standards Institute (CLSI): 2013, Performance standards for antimicrobial disk and dilution susceptibility test for bacteria isolated from animals; approved standards—fourth edition. CLSI document VET01-A4. CLSI, Wayne, PA. 7. Committee on Bovine Reproductive Nomenclature Terms: 1972, Recommendations for standardizing bovine reproductive terms. Cornell Vet 62:216–237. 8. De-Giuli L, Magnino S, Vigo PG, et al.: 2002, Development of a polymerase chain reaction and restriction typing assay for the diagnosis of bovine herpesvirus 1, bovine herpesvirus 2, and bovine herpesvirus 4 infections. J Vet Diagn Invest 14: 353–356. 9. Ferguson KP, Lambe DW Jr, Keplinger JL, Kalbfleisch JH: 1991, Comparison of the pathogenicity of three species of coagulase-negative Staphylococcus in a mouse model with and without a foreign body. Can J Microbiol 37:722–724. 10. Frank KL, Del Pozo JL, Patel R: 2008, From clinical microbiology to infection pathogenesis: how daring to be different works for Staphylococcus lugdunensis. Clin Microbiol Rev 21:111–133. 11. Freney J, Brun Y, Bes M, et al.: 1988, Staphylococcus lugdunensis sp. nov. and Staphylococcus schleiferi sp. nov., two species from human clinical specimens. Int J Syst Bacteriol 38:168–172. 12. Gahukamble AD, McDowell A, Post V, et al.: 2014, Propionibacterium acnes and Staphylococcus lugdunensis cause pyogenic osteomyelitis in an intramedullary nail model in rabbits. J Clin Microbiol 52:1595–1606. 13. Herchline TE, Ayers LW: 1991, Occurrence of Staphylococcus lugdunensis in consecutive clinical cultures and relationship of isolation to infection. J Clin Microbiol 29:419–421. 14. Hoffmann B, Scheuch M, Höper D, et al.: 2012, Novel orthobunyavirus in cattle, Europe, 2011. Emerg Infect Dis 18:469–472. 15. Holler LD: 2012, Ruminant abortion diagnostics. Vet Clin North Am Food Anim Pract 28:407–418.
3
16. Kralovic SM, Melin-Aldana H, Smith KK, Linnemann CC Jr: 1995, Staphylococcus lugdunensis endocarditis after tooth extraction. Clin Infect Dis 20:715–716. 17. Lambe DW Jr, Ferguson KP, Keplinger JL, et al.: 1990, Pathogenicity of Staphylococcus lugdunensis, Staphylococcus schleiferi, and three other coagulase-negative staphylococci in a mouse model and possible virulence factors. Can J Microbiol 36:455–463. 18. Letellier C, Kerkhofs P, Wellemans G, Vanopdenbosch E: 1999, Detection and genotyping of bovine diarrhea virus by reverse transcription-polymerase chain amplification of the 5′ untranslated region. Vet Microbiol 64:155–167. 19. Marchocki Z, Collins K, Lehane E, et al.: 2013, Staphylococcus lugdunensis cultured from the amniotic fluid at caesarean section. PloS One 8:e56373. 20. Müller N, Zimmermann V, Hentrich B, Gottstein B: 1996, Diagnosis of Neospora caninum and Toxoplasma gondii infection by PCR and DNA hybridization immunoassay. J Clin Microbiol 34:2850–2852. 21. Murdoch DR, Everts RJ, Chambers ST, Cowan IA: 1996, Vertebral osteomyelitis due to Staphylococcus lugdunensis. J Clin Microbiol 34:993–994. 22. Nakamura RK, Zimmerman SA, Lange AJ, Lesser MB: 2012, Isolation of methicillin-resistant Staphylococcus lugdunensis in a dog with endocarditis. J Vet Cardiol 14:531–536. 23. Ossewaarde JM, Meijer A: 1999, Molecular evidence for the existence of additional members of the order Chlamydiales. Microbiology 145:411–417. 24. Rook KA, Brown DC, Rankin SC, Morris DO: 2012, Case– control study of Staphylococcus lugdunensis infection isolates from small companion animals. Vet Dermatol 23:476–e90. 25. Rozalska B, Ljungh A: 1995, Biomaterial-associated staphylococcal peritoneal infections in a neutropaenic mouse model. FEMS Immunol Med Microbiol 11:307–319. 26. Shaaban HS, Choo HF, Sensakovic JW: 2011, A case of Staphylococcus lugdunensis related pyomyoma occurring after cesarean section. J Glob Infect Dis 3:101–102. 27. Stoddard RA, Gee JE, Wilkins PP, et al.: 2009, Detection of pathogenic Leptospira spp. through TaqMan polymerase chain reaction targeting the LipL32 gene. Diagn Microbiol Infect Dis 64:247–255. 28. Wasserman E, Lombard L, Walzl G: 1999, Staphylococcus lugdunensis endocarditis in a young, previously healthy female. Eur J Clin Microbiol Infect Dis 18:289–291. 29. Zbinden R, Müller F, Brun F, von Graevenitz A: 1997, Detection of clumping factor-positive Staphylococcus lugdunensis by Staphaurex Plus®. J Microbiol Methods 31:95–98.
Downloaded from vdi.sagepub.com at Bibliothekssystem der Universitaet Giessen on October 22, 2014
Abortion in cattle due to infection with Staphylococcus lugdunensis Paolo Ardigò, Mario D'Incau and Stefano Pongolini J VET Diagn Invest published online 7 October 2014 DOI: 10.1177/1040638714550182 The online version of this article can be found at: http://vdi.sagepub.com/content/early/2014/10/06/1040638714550182
Published by: http://www.sagepublications.com
On behalf of:
Official Publication of the American Association of Veterinary Laboratory Diagnosticians, Inc.
Additional services and information for Journal of Veterinary Diagnostic Investigation can be found at: Email Alerts: http://vdi.sagepub.com/cgi/alerts Subscriptions: http://vdi.sagepub.com/subscriptions Reprints: http://www.sagepub.com/journalsReprints.nav Permissions: http://www.sagepub.com/journalsPermissions.nav
>> OnlineFirst Version of Record - Oct 7, 2014 What is This?
Downloaded from vdi.sagepub.com at Bibliothekssystem der Universitaet Giessen on October 22, 2014
550182 research-article2014
VDIXXX10.1177/1040638714550182Staphylococcus lugdunensis in bovine abortionArdigò et al.
Brief Communication
Abortion in cattle due to infection with Staphylococcus lugdunensis
Journal of Veterinary Diagnostic Investigation 1–3 © 2014 The Author(s) Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/1040638714550182 jvdi.sagepub.com
Paolo Ardigò, Mario D’Incau, Stefano Pongolini1
Abstract. An aborted fetus of 7 months gestation, the associated placenta, and a single blood sample from the dam were submitted for diagnostic investigation to the diagnostic laboratory of the Lombardy and Emilia-Romagna Experimental Zooprophylactic Institute in Parma, Italy. The serum was negative for Neospora caninum, Coxiella burnetii, Chlamydophila abortus, Bovine herpesvirus 1 (BHV-1), Bovine viral diarrhea virus (BVDV), Brucella abortus, and Brucella melitensis. Fetal tissues and placental cotyledons were pooled and tested by polymerase chain reaction (PCR) for the presence of BHV-1, Bovine herpesvirus 4, BVDV, N. caninum, C. burnetii, Chlamydophila spp., Schmallemberg virus, and Leptospira interrogans. All PCR assays were negative. Bacteriological examinations performed on the fetal organs revealed a pure growth of Staphylococcus lugdunensis in all organs cultured. In human beings, S. lugdunensis is responsible for communityacquired and nosocomial infections, in both immunocompetent and immunocompromised patients. In veterinary medicine, the pathogenic potential of S. lugdunensis has not been fully investigated. The incidence of S. lugdunensis is regarded as being underreported because it could be easily misidentified as Staphylococcus aureus. The current report documents the ability of S. lugdunensis to cause abortion in cattle, indicating the need for accurate diagnostic procedures to identify this emerging and zoonotic pathogen whose incidence is likely underestimated in both human and veterinary medicine. Key words: Abortion; abortive diseases; cattle; Staphylococcus lugdunensis. Abortion in cattle is defined as loss of the fetus occurring between 42 and 260 days of gestation.7 The cause of this event is often difficult to identify, and the results of laboratory investigations reported in the literature suggest that only in approximately 35% of cases is it possible to ascertain the etiological agent.4 Most bacteria causing bovine abortion are opportunistic pathogens. Trueperella pyogenes and Bacillus spp. followed by Escherichia coli, Histophilus somni, Pasteurella spp., Listeria monocytogenes, Staphylococcus spp., Streptococcus spp., and any other bacteria that can find their way into the bloodstream can act as opportunistic pathogens and cause sporadic abortion. Such opportunists are associated with abortions at any period of gestation, even though most are associated with late second to third trimester abortions.15 In the current report, a case of abortion in cattle caused by Staphylococcus lugdunensis, an emerging pathogen in human beings10 and companion animals,22,24 is described. Sporadic abortions were reported on a farm in the Province of Parma (northern Italy). The farm was a commercial dairy, consisting of approximately 500 lactating Holstein– Friesian cows. The abortion rate had been 3.8% over the preceding 12 months, and no laboratory diagnostics had been performed on those cases. In May 2013, a fetus of 7 months’ gestation, the associated placenta, and a blood sample of the cow were submitted for routine diagnostic investigation to the diagnostic laboratory of the Lombardy and Emilia-Romagna Experimental Zooprophylactic Institute in Parma, Italy.
The serum was negative for Neospora caninum, Coxiella burnetii, Chlamydophila abortus, Bovine herpesvirus 1 (BHV-1), Bovine viral diarrhea virus (BVDV), Brucella abortus, and Brucella melitensis. The veterinary practitioner who assisted the herd reported that no postabortion complications were observed in the dam. The fetus presented minimal autolysis, moderate cutaneous edema, increased presence of fluids in the abdominal and thoracic cavities, moderately swollen spleen and liver, and complete atelectasis of the lungs. No gross lesions were apparent on the placenta. Specimens of the brain, lung, heart, liver, spleen, kidney, abomasum content, and placental cotyledons were pooled and homogenized with sterile scissors for subsequent use in a number of polymerase chain reaction (PCR) assays. Pooling was a convenient compromise for fetal PCR diagnostics that broadened the spectrum of organs that could be tested while saving resources. Nucleic acids from the pool were extracted using commercial kits specific for DNAa and RNAb following manufacturers’ instructions. End-point PCRs were used to detect BHV-1,8 Bovine herpesvirus 4,8 BVDV,18 From the Lombardy and Emilia Romagna Experimental Zooprophylactic Institute, Parma (Ardigò, Pongolini) and Brescia (D’Incau), Italy. 1
Corresponding Author: Stefano Pongolini, Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia-Romagna, Via dei Mercati 13/A, 43126 Parma, Italy. [email protected]
Downloaded from vdi.sagepub.com at Bibliothekssystem der Universitaet Giessen on October 22, 2014
2
Ardigò et al.
N. caninum,20 C. burnetii,2 and Chlamydophila spp.23 A realtime PCR was used for Leptospira interrogans.27 Specimens of the brain, spleen, and thymus were also pool-tested for the presence of Schmallemberg virus by real-time PCR.14 All PCR assays were negative. Lung, liver, spleen, kidney, and the content of the abomasum were aseptically collected and cultured on bovine blood agar,c Gassner agar,d and Brucella agare under aerobic and increased (10%) CO2 incubation at 37°C. A pure culture appeared on the bovine blood agarc plates from all cultured organs and the abomasum content after 24 hr of incubation. After 48 hr, colonies were white, round, smooth, glistening, and 2–3 mm in diameter. A complete zone of hemolysis of approximately 1 mm was evident around the colonies. No growth was observed after 48 hr of incubation on Gassner agard and after 10 days of incubation on Brucella agar.e Gram staining revealed the organism to consist of Gram-positive cocci. The bacterial isolate was catalase positive, oxidase negative, slide-coagulase positive, and tube-coagulase negative. A commercial identification kitf gave a profile of 6312150, which corresponded to S. lugdunensis with 97.3% identity. A second commercial identification system,g which includes 43 biochemical tests, was used as a confirmatory test. The second system gave a code of 010002002623231, corresponding to S. lugdunensis with 99% probability. No unexpected test results were obtained, and no supplementary tests were required for the definitive identification of the isolate. Antimicrobial susceptibility was assessed by Kirby– Bauer disk diffusion according to the Clinical and Laboratory Standards Institute.6 The strain was resistant to sulfadiazine, but sensitive to amoxicillin–clavulanic acid, ampicillin, ceftiofur, cloxacillin, colistin, enrofloxacin, florfenicol, oxacillin, penicillin, trimethoprim–sulfamethoxazole, tetracycline, thiamphenicol, tiamulin, and tylosin. Staphylococcus lugdunensis is a coagulase-negative staphylococcus (CNS) that was first described in 1988.11 The organism is a commensal of the human skin more frequently found on the lower part of the body and the extremities, particularly in the moist areas such as the groin, perineum, and the large toenail.3 Although CNS are generally considered nonpathogenic commensal in immunocompetent subjects, S. lugdunensis is an important exception being responsible for community-acquired and nosocomial infections,10 in both immunocompetent5,13,16,28 and immunocompromised patients.13,21 In human beings, S. lugdunensis has been described as a possible cause of skin and soft tissue infection, prosthetic and naive valves endocarditis, bone and joint infections, and bacteremia.10 The organism has rarely been isolated in peritonitis, and central nervous system, oral, ocular, and urinary tract infections.10 Staphylococcus lugdunensis has also been associated with endometritis,1 pyomyoma,26 and, in 2013, its detection in amniotic fluids collected during cesarean sec-
tions was reported, although no postoperative infection or neonatal complications were observed.19 In veterinary medicine, the pathogenic potential of S. lugdunensis has not been fully investigated. A retrospective case control study of S. lugdunensis infections in small companion animals suggested that S. lugdunensis is more often isolated from deep tissues and wounds than from superficial infections, therefore, it should be considered a potential pathogen.24 Staphylococcus lugdunensis was also isolated from a blood sample of a dog with endocarditis, but a role in the pathogenesis of the disease remains uncertain as the dog was also positive for Bartonella spp. by PCR, and possible contamination of the blood sample by S. lugdunensis through the skin could not be ruled out.22 Staphylococcus lugdunensis was also shown to cause subcutaneous abscesses, peritonitis, and osteomyelitis in mice9,17,25 and rabbits12 used in experimental studies. The incidence of S. lugdunensis is presumed to be underreported in both human and veterinary medicine as it can be easily misidentified as Staphylococcus aureus, which shares the same colony morphology, hemolytic activity, and the ability to agglutinate latex particles coated with fibrinogen.29 The current report documents the ability of S. lugdunensis to cause abortion in cattle, underlining the need for accurate diagnostic procedures to correctly identify this emerging and zoonotic pathogen whose incidence is likely underestimated. Acknowledgements The authors thank the staff of Lombardy and Emilia-Romagna Experimental Zooprophylactic Institute for technical assistance with bacterial isolation and identification procedures.
Sources and manufacturers a.
PureLink genomic DNA kits, Life Technologies Ltd., Carlsbad, CA. b. RNeasy mini kit, Qiagen Inc., Valencia, CA. c. Oxoid Ltd, Basingstoke, Hampshire, United Kingdom. d. Biolife Italiana S.r.l., Milan, Italy. e. Microbiol diagnostici, Cagliari, Italy. f. API Staph, BioMérieux, Marcy l’Etoile, France. g. VITEK 2 compact combined with VITEK 2 Gram positive identification card, BioMérieux, Marcy l’Etoile, France.
Declaration of conflicting interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and publication of this article.
Funding The author(s) received no financial support for the research, authorship, and publication of this article.
References 1. Bello C, Eskandar M, El GR, et al.: 2007, Staphylococcus lugdunensis endometritis: a case report. West Afr J Med 26:243–245.
Downloaded from vdi.sagepub.com at Bibliothekssystem der Universitaet Giessen on October 22, 2014
Staphylococcus lugdunensis in bovine abortion 2. Berri M, Arricau-Bouvery N, Rodolakis A: 2003, PCR-based detection of Coxiella burnetii from clinical samples. Methods Mol Biol 216:153–161. 3. Bieber L, Kahlmeter G: 2010, Staphylococcus lugdunensis in several niches of the normal skin flora. Clin Microbiol Infect 16:385–388. 4. Cabell E: 2007, Bovine abortion: aetiology and investigations. In Pract 29:455–463. 5. Casanova-Roman M, Sanchez-Porto A, Casanova-Bellido M: 2004, Urinary tract infection due to Staphylococcus lugdunensis in a healthy child. Scand J Infect Dis 36:149–150. 6. Clinical and Laboratory Standards Institute (CLSI): 2013, Performance standards for antimicrobial disk and dilution susceptibility test for bacteria isolated from animals; approved standards—fourth edition. CLSI document VET01-A4. CLSI, Wayne, PA. 7. Committee on Bovine Reproductive Nomenclature Terms: 1972, Recommendations for standardizing bovine reproductive terms. Cornell Vet 62:216–237. 8. De-Giuli L, Magnino S, Vigo PG, et al.: 2002, Development of a polymerase chain reaction and restriction typing assay for the diagnosis of bovine herpesvirus 1, bovine herpesvirus 2, and bovine herpesvirus 4 infections. J Vet Diagn Invest 14: 353–356. 9. Ferguson KP, Lambe DW Jr, Keplinger JL, Kalbfleisch JH: 1991, Comparison of the pathogenicity of three species of coagulase-negative Staphylococcus in a mouse model with and without a foreign body. Can J Microbiol 37:722–724. 10. Frank KL, Del Pozo JL, Patel R: 2008, From clinical microbiology to infection pathogenesis: how daring to be different works for Staphylococcus lugdunensis. Clin Microbiol Rev 21:111–133. 11. Freney J, Brun Y, Bes M, et al.: 1988, Staphylococcus lugdunensis sp. nov. and Staphylococcus schleiferi sp. nov., two species from human clinical specimens. Int J Syst Bacteriol 38:168–172. 12. Gahukamble AD, McDowell A, Post V, et al.: 2014, Propionibacterium acnes and Staphylococcus lugdunensis cause pyogenic osteomyelitis in an intramedullary nail model in rabbits. J Clin Microbiol 52:1595–1606. 13. Herchline TE, Ayers LW: 1991, Occurrence of Staphylococcus lugdunensis in consecutive clinical cultures and relationship of isolation to infection. J Clin Microbiol 29:419–421. 14. Hoffmann B, Scheuch M, Höper D, et al.: 2012, Novel orthobunyavirus in cattle, Europe, 2011. Emerg Infect Dis 18:469–472. 15. Holler LD: 2012, Ruminant abortion diagnostics. Vet Clin North Am Food Anim Pract 28:407–418.
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