APMIS 123: 726–729
© 2015 APMIS. Published by John Wiley & Sons Ltd. DOI 10.1111/apm.12396
Case Report
Staphylococcus lugdunensis endocarditis following vasectomy – report of a case history and review of the literature HOSSEIN SCHANDIZ,1 NILS OLAV HERMANSEN,2 TROND JØRGENSEN3 and BORGHILD ROALD1,4 1
Departments of Pathology; 2 Microbiology, Oslo University Hospital, Oslo; 3Volvat Medical Centre; and 4 Faculty of Medicine, Institute of Clinical Medicine, University of Oslo, Oslo, Norway
Schandiz H, Olav Hermansen N, Jørgensen T, Roald B. Staphylococcus lugdunensis endocarditis following vasectomy – report of a case history and review of the literature. APMIS 2015; 123: 726–729 Staphylococcus lugdunensis is a coagulase-negative Staphylococcus (CoNS), and part of the normal skin flora. The bacterium is an emerging pathogen that, unlike other CoNS, resembles coagulase-positive Staphylococcus aureus infections in virulence, tissue destruction, and clinical course. We report a fatal case following minor surgery. The frequency of S. lugdunensis infections has probably been underestimated and under-reported in the past as few clinical laboratories routinely identify coagulase-negative Staphylococci. Key words: Staphylococcus lugdunensis; Staphylococcus aureus; coagulase-negative staphylococcus; valve endocarditis; vasectomy; surgery. Hossein Schandiz, Department of Pathology, Oslo University Hospital, P. O. Box 4950 Nydalen, N-0424 Oslo, Norway. e-mail: [email protected]
We report a serious complication after a simple vasectomy procedure in a healthy male. Postoperative infections, regardless of the extent of the surgical procedure, are important, sometime fatal complications that must be addressed swiftly and accurately. The bacteria found in this case, Staphylococcus lugdunensis, is an emerging pathogen that, in some instances, has attributed to death. We discuss the case and review the literature.
CASE HISTORY 56-year-old married male, self-employed with two children. The patient’s prior medical history revealed hypertension, otherwise unremarkable. In Autumn 2012, the patient underwent bilateral vasectomy (sterilization) at a private medical clinic. Few days following the procedure, he complained of a painful swelling in his scrotum. He contacted the surgeon after 2 weeks due to persisting sympReceived 8 January 2015. Accepted 8 March 2015
726
toms. The surgeon adviced him to contact him again if the problems persisted. The patient never did. Some days later he experienced flu-like symptoms with chills, high fever, asthenia, and headache. His wife noticed cognitive alterations and amnesia. The symptoms escalated and the patient’s general condition started to deteriorate. Six weeks following the vasectomy procedure, the patient visited his family practitioner (GP) due to general malaise. Creactive protein (CRP) was 200 mg/L in capillary blood. Oral penicillin treatment was prescribed under the clinical suspicion of pneumonia. The following day the patient was found unconscious in his home by his son. When the ambulance arrived, the patient was in cardiac arrest with asystole. Resuscitation was started and the patient transported to a community hospital for emergency treatment. Spontaneous circulation (ROSC) was achieved several times, lasted 8–10 min, and followed by new episodes of asystole. Echocardiogram revealed massive mitral valve vegetations with prolapse of the posterior valve leaflet and mitral regurgitation. Emergency cardiac surgery was discussed,
S. LUGDUNENSIS ENDOCARDITIS AND VASECTOMY
but found contraindicated due to recurrent circulatory collapse. The patient died few hours after arriving in the hospital. An autopsy was requested. Autopsy revealed several recent-onset cerebral embolisms, hemorrhages, and septic infarctions. The mitral valve had massive vegetations and ulcerations as well as a partial rupture involving one-third of the diameter (Fig. 1A). Microscopic examination showed endocarditis with combined acute and chronic inflammatory infiltrates, areas of granulation tissue and gram positive bacteria in the inflammatory infiltrates (Fig. 1B, C and D). In addition, a slight hypertrophy of the left cardiac ventricle was seen, pulmonary congestion, a small, peripheral lung infarction and adrenal hypertrophy. The remaining organ findings were normal. Especially, there were no signs of pneumonia or bronchitis on gross and microscopic examination. Staphylococcus lugdunensis (S. lugdunensis) was identified in both blood cultures and mitral valve tissue samples from the patient at autopsy, primarily identified by typical colony morphology and odor. Mass spectrometric analysis, MALDI-TOF MS (matrix-assisted laser desorption ionizationtime of flight mass spectrometry) gave spectral score of 2,3, consistent with accurate species identification with high confidence. The isolate was resistant to penicillin, but sensitive to oxacillin, clindamycin, vancomycin, gentamycin, tetracycline,
trimethoprim-sulfamethoxazole, and fusidic acid. Mec-A gene was not detected. The conclusion in the autopsy report was that the patient died of S. lugdunensis encocarditis with complications. The most likely port of entry for the pathogen was the scrotal skin related to the recent vasectomy procedure.
REVIEW OF THE LITERATURE Staphylococcus lugdunensis is a coagulase-negative Staphylococcus (CoNS). Like other CoNS, S. lugdunensis is part of the normal skin flora. It has been identified in cultures from the entire body (1), in particular from the perineum and breast areas (2, 3). In a comprehensive study of 525 cultures obtained from eight sites in 75 healthy subjects (2), swabs from the groin, toes, and axilla yielded S. lugdunensis most frequently. Staphylococcus lugdunensis was first described in 1988 by Freney. Lugdunum is the Latin adjective of Lyon (4), where the bacteria were first isolated. Since then, S. lugdunensis is increasingly recognized as an emerging pathogen, causing both communityacquired and nosocomial infections (5). Unlike other CoNS, S. lugdunensis infections resemble Staphylococcus aureus infections in virulence, tissue destruction, and clinical course. Toxic shock
A
B
C
D
Fig. 1. (A) Mitral valves with massive vegetations and destruction. (B) Gram positive cocci in colonies (Magnification with objective 4). (C) Histopathology overview of mitral valve with thrombotic vegetations and colonies of bacteria (Magnification with objective 2). (D) Partially destroyed mitral valve with acute necrotizing endocarditis, granulation tissue and thrombotic vegetations with colonies of bacteria (Magnification with objective 4) © 2015 APMIS. Published by John Wiley & Sons Ltd
727
SCHANDIZ et al.
syndrome, osteomyelitis, septic arthritis, postoperative endopthalmitis, and endocarditis have been observed and reported (6–9). Colonies of S. lugdunensis can be misidentified as a clinically more indolent form of CoNS or identified only at the genus level. They can appear unpigmented, cream-colored or pale yellow after 5 days of incubation. Tube coagulase test can help distinguish S. lugdunensis from S. aureus. It can also be identified through commercially available phenotypic identification systems using the biochemical reaction with pyrrolidonyl arylamidase (PYR) and ornithine decarboxylase (ODC). Recently MALDITOF has been introduced in many microbiology laboratories. Our isolates gave a MALDI-TOF MS spectral score of 2.3, which reflects high confidence in identification to species level. Next best score value was 1.5. Staphylococcus capitis ssp. capitis. Antimicrobial susceptibility testing was performed by disk diffusion (Becton Dickinson) using EUCAST breakpoints. Our isolate was resistant to penicillin, but sensitive to oxacillin, clindamycin, vancomycin, gentamicin, tetracycline, trimethoprim-sulfamethoxazole, and fusidic acid. Mec-A gene was not detected. The technique is straightforward, rapid, and has accuracy equivalent to molecular methods (10–12). Recent studies confirm CoNS as an emerging and important cause of NVE in both community and healthcare settings (13, 14). S. lugdunensis may lead to rapidly progressive native valve endocarditis, first described in an 11-case series in 1993 (8). To date, more than 80 cases of S. lugdunensis endocarditis have been reported, mainly involving native aortic and mitral valves (15), with a reported mortality rate up to 70% (8). In 2008, Frank et al. reported five cases of S. lugdunensis endocarditis diagnosed one to 3 months after vasectomy. All these cases required valve replacement; four urgent (15,16,17). In a 3-year retrospective microbiological and clinical review study from a single medical center, Klotchko et al. (18) identified 77 S. lugdunensis isolates. Of these, seventy had complete data. Seventeen had infections above, eighteen below the waist. Thirteen had infection in urinary tract, including four cases after urological instrumentation. Twenty others had the bacteria found in cerebrospinal fluid and bloodstream with neither endocarditis nor endocarditis. Soft tissue, bone, joint, central nervous system, urine, and bloodstream infections occurred with soft tissue infections described as primarily abscesses. There were four infections of prosthetic joints and nine cases of osteomyelitis. Of the 21 bacteremias reported, five were associated with endocarditis. Two of these patients died. Most isolates were penicillin resistant.
728
DISCUSSION The frequency of S. lugdunensis infections has probably been underestimated in the past. Many clinical laboratories do not routinely identify CoNS to species level. Additionally, cultures are not always performed prior to antibiotic therapy for skin infections following minor surgery. Prior to the vasectomy procedure, patients in Norway receive written and oral information about possible complications. They are informed to not delay contact in case of any discomfort. Serious side effects are rare. The few patients that experience side effects or discomfort after the vasectomy, usually have minor reactions that do not require further treatment. In concordance with International guidelines (19), the Norwegian guidelines do not recommend prophylactic antimicrobial treatment routinely prior to vasectomy. It is our belief that the outcome of this case might have been different, had the patient been seen by the surgeon. We hope to raise the awareness on potential risks of S. lugdunensis infections after minor surgeries like vasectomy procedures. Our patient underwent a vasectomy with fatal outcome due to infection by this bacterium. This also stresses the importance of relevant oral and written information to patients on possible complications, and what signs to look for following such procedures.
REFERENCES 1. Herchline TE, Ayers LW. Occurrence of Staphylococcus lugdunensis in consecutive clinical cultures and relationship of isolation to infection. J Clin Microbiol 1991;29:419–21. 2. Bieber L, Kahlmeter G. Staphylococcus lugdunensis in several niches of the normal skin flora. Clin Microbiol Infect 2010;16:385–8. 3. Hellbacher C, T€ ornqvist E, S€ oderquist B. Staphylococcus lugdunensis: clinical spectrum, antibiotic susceptibility, and phenotypic and genotypic patterns of 39 isolates. Clin Microbiol Infect 2006;12:43–9. 4. Freney J. Staphylococcus lugdunensis sp. nov. and Staphylococcus schleiferi sp. nov., two species from human clinical specimens. Int J Syst Bacteriol 1988;38:168–72. 5. Seifert H, Oltmanns D, Becker K, Wisplinghoff H, von Eiff C. Staphylococcus lugdunensis pacemakerrelated infection. Emerg Infect Dis 2005;11:1283–6. 6. Babu E, Oropello J. Staphylococcus lugdunensis: the coagulase-negative staphylococcus you don’t want to ignore. Expert Rev Anti-Infect Ther 2011;9:901–7. 7. Murillo J, McMahon C, Starr J. Large vegetations in Staphylococcus lugdunensis endocarditis. Heart Lung 2008;37:479–80. 8. Vandenesch F, Etienne J, Reverdy ME, Eykyn SJ. Endocarditis due to Staphylococcus lugdunensis:
© 2015 APMIS. Published by John Wiley & Sons Ltd
S. LUGDUNENSIS ENDOCARDITIS AND VASECTOMY
9.
10. 11.
12.
13.
Report of 11 cases and review. Clin Infect Dis 1993;17:871–6. Anguera I, Rıo A, Mir o JM, Matınez-Lacasa X, Marco F, Guma JR, et al. Staphylococcus lugdunensis infective endocarditis: description of 10 cases and analysis of native valve, prosthetic valve, and pacemaker lead endocarditis clinical profiles. Heart 2005;91:e10. Patel R. Matrix-assisted laser desorption ionizationtime of flight mass spectrometry in clinical microbiology. Clin Infect Dis 2013;57:564–72. Elamin WF, Ball D, Millar M. Unbiased species-level identification of clinical isolates of Coagulase-negative staphylococci: does it change the perspective on Staphylococcus lugdunensis? J Clin Microbiol 2015;53:292–4. Szabados F, Woloszyn J, Richter C, Kaase M, Gatermann S. Identification of molecularly defined Staphylococcus aureus strains using matrix-assisted laser desorption/ionization time of flight mass spectrometry and the Biotyper 2.0 database. J Med Microbiol 2010;59:787–90. Chu VH, Cabell CH, Abrutyn E, Corey GR, Hoen B, Miro JM, et al. Native valve endocarditis due to coag-
© 2015 APMIS. Published by John Wiley & Sons Ltd
14.
15.
16. 17. 18. 19.
ulase-negative staphylococci: report of 99 episodes from the International Collaboration on Endocarditis Merged Database. Clin Infect Dis 2004;39:1527–30. Chu VH, Woods CW, Miro JM, Hoen B, Cabell CH, Pappas PA, et al. Emergence of coagulase-negative staphylococci as a cause of native valve endocarditis. Clin Infect Dis 2008;46:232–42. Frank KL, del Pozo JL, Patel R. From clinical microbiology to infection pathogenesis: how daring to be different works for Staphylococcus lugdunensis. Clin Microbiol Rev 2008;21:111–33. Lessing MP, Crook DW, Bowler IC, Gribbin B. Native-valve endocarditis caused by Staphylococcus lugdunensis. QJM 1996;89:855–8. Walsh B, Mounsey JP. Staphylococcus lugdunensis and endocarditis. J Clin Pathol 1990;43:171–3. Klotchko A, Wallace MR, Licitra C, Sieger B. Staphylococcus lugdunensis: an emerging pathogen. South Med J 2011;104:509–14. American Urological Association (AUA) Guideline. 2012;http://www.auanet.org/common/pdf/education/ clinical guidance/Vasectomy.pdf.
729
© 2015 APMIS. Published by John Wiley & Sons Ltd. DOI 10.1111/apm.12396
Case Report
Staphylococcus lugdunensis endocarditis following vasectomy – report of a case history and review of the literature HOSSEIN SCHANDIZ,1 NILS OLAV HERMANSEN,2 TROND JØRGENSEN3 and BORGHILD ROALD1,4 1
Departments of Pathology; 2 Microbiology, Oslo University Hospital, Oslo; 3Volvat Medical Centre; and 4 Faculty of Medicine, Institute of Clinical Medicine, University of Oslo, Oslo, Norway
Schandiz H, Olav Hermansen N, Jørgensen T, Roald B. Staphylococcus lugdunensis endocarditis following vasectomy – report of a case history and review of the literature. APMIS 2015; 123: 726–729 Staphylococcus lugdunensis is a coagulase-negative Staphylococcus (CoNS), and part of the normal skin flora. The bacterium is an emerging pathogen that, unlike other CoNS, resembles coagulase-positive Staphylococcus aureus infections in virulence, tissue destruction, and clinical course. We report a fatal case following minor surgery. The frequency of S. lugdunensis infections has probably been underestimated and under-reported in the past as few clinical laboratories routinely identify coagulase-negative Staphylococci. Key words: Staphylococcus lugdunensis; Staphylococcus aureus; coagulase-negative staphylococcus; valve endocarditis; vasectomy; surgery. Hossein Schandiz, Department of Pathology, Oslo University Hospital, P. O. Box 4950 Nydalen, N-0424 Oslo, Norway. e-mail: [email protected]
We report a serious complication after a simple vasectomy procedure in a healthy male. Postoperative infections, regardless of the extent of the surgical procedure, are important, sometime fatal complications that must be addressed swiftly and accurately. The bacteria found in this case, Staphylococcus lugdunensis, is an emerging pathogen that, in some instances, has attributed to death. We discuss the case and review the literature.
CASE HISTORY 56-year-old married male, self-employed with two children. The patient’s prior medical history revealed hypertension, otherwise unremarkable. In Autumn 2012, the patient underwent bilateral vasectomy (sterilization) at a private medical clinic. Few days following the procedure, he complained of a painful swelling in his scrotum. He contacted the surgeon after 2 weeks due to persisting sympReceived 8 January 2015. Accepted 8 March 2015
726
toms. The surgeon adviced him to contact him again if the problems persisted. The patient never did. Some days later he experienced flu-like symptoms with chills, high fever, asthenia, and headache. His wife noticed cognitive alterations and amnesia. The symptoms escalated and the patient’s general condition started to deteriorate. Six weeks following the vasectomy procedure, the patient visited his family practitioner (GP) due to general malaise. Creactive protein (CRP) was 200 mg/L in capillary blood. Oral penicillin treatment was prescribed under the clinical suspicion of pneumonia. The following day the patient was found unconscious in his home by his son. When the ambulance arrived, the patient was in cardiac arrest with asystole. Resuscitation was started and the patient transported to a community hospital for emergency treatment. Spontaneous circulation (ROSC) was achieved several times, lasted 8–10 min, and followed by new episodes of asystole. Echocardiogram revealed massive mitral valve vegetations with prolapse of the posterior valve leaflet and mitral regurgitation. Emergency cardiac surgery was discussed,
S. LUGDUNENSIS ENDOCARDITIS AND VASECTOMY
but found contraindicated due to recurrent circulatory collapse. The patient died few hours after arriving in the hospital. An autopsy was requested. Autopsy revealed several recent-onset cerebral embolisms, hemorrhages, and septic infarctions. The mitral valve had massive vegetations and ulcerations as well as a partial rupture involving one-third of the diameter (Fig. 1A). Microscopic examination showed endocarditis with combined acute and chronic inflammatory infiltrates, areas of granulation tissue and gram positive bacteria in the inflammatory infiltrates (Fig. 1B, C and D). In addition, a slight hypertrophy of the left cardiac ventricle was seen, pulmonary congestion, a small, peripheral lung infarction and adrenal hypertrophy. The remaining organ findings were normal. Especially, there were no signs of pneumonia or bronchitis on gross and microscopic examination. Staphylococcus lugdunensis (S. lugdunensis) was identified in both blood cultures and mitral valve tissue samples from the patient at autopsy, primarily identified by typical colony morphology and odor. Mass spectrometric analysis, MALDI-TOF MS (matrix-assisted laser desorption ionizationtime of flight mass spectrometry) gave spectral score of 2,3, consistent with accurate species identification with high confidence. The isolate was resistant to penicillin, but sensitive to oxacillin, clindamycin, vancomycin, gentamycin, tetracycline,
trimethoprim-sulfamethoxazole, and fusidic acid. Mec-A gene was not detected. The conclusion in the autopsy report was that the patient died of S. lugdunensis encocarditis with complications. The most likely port of entry for the pathogen was the scrotal skin related to the recent vasectomy procedure.
REVIEW OF THE LITERATURE Staphylococcus lugdunensis is a coagulase-negative Staphylococcus (CoNS). Like other CoNS, S. lugdunensis is part of the normal skin flora. It has been identified in cultures from the entire body (1), in particular from the perineum and breast areas (2, 3). In a comprehensive study of 525 cultures obtained from eight sites in 75 healthy subjects (2), swabs from the groin, toes, and axilla yielded S. lugdunensis most frequently. Staphylococcus lugdunensis was first described in 1988 by Freney. Lugdunum is the Latin adjective of Lyon (4), where the bacteria were first isolated. Since then, S. lugdunensis is increasingly recognized as an emerging pathogen, causing both communityacquired and nosocomial infections (5). Unlike other CoNS, S. lugdunensis infections resemble Staphylococcus aureus infections in virulence, tissue destruction, and clinical course. Toxic shock
A
B
C
D
Fig. 1. (A) Mitral valves with massive vegetations and destruction. (B) Gram positive cocci in colonies (Magnification with objective 4). (C) Histopathology overview of mitral valve with thrombotic vegetations and colonies of bacteria (Magnification with objective 2). (D) Partially destroyed mitral valve with acute necrotizing endocarditis, granulation tissue and thrombotic vegetations with colonies of bacteria (Magnification with objective 4) © 2015 APMIS. Published by John Wiley & Sons Ltd
727
SCHANDIZ et al.
syndrome, osteomyelitis, septic arthritis, postoperative endopthalmitis, and endocarditis have been observed and reported (6–9). Colonies of S. lugdunensis can be misidentified as a clinically more indolent form of CoNS or identified only at the genus level. They can appear unpigmented, cream-colored or pale yellow after 5 days of incubation. Tube coagulase test can help distinguish S. lugdunensis from S. aureus. It can also be identified through commercially available phenotypic identification systems using the biochemical reaction with pyrrolidonyl arylamidase (PYR) and ornithine decarboxylase (ODC). Recently MALDITOF has been introduced in many microbiology laboratories. Our isolates gave a MALDI-TOF MS spectral score of 2.3, which reflects high confidence in identification to species level. Next best score value was 1.5. Staphylococcus capitis ssp. capitis. Antimicrobial susceptibility testing was performed by disk diffusion (Becton Dickinson) using EUCAST breakpoints. Our isolate was resistant to penicillin, but sensitive to oxacillin, clindamycin, vancomycin, gentamicin, tetracycline, trimethoprim-sulfamethoxazole, and fusidic acid. Mec-A gene was not detected. The technique is straightforward, rapid, and has accuracy equivalent to molecular methods (10–12). Recent studies confirm CoNS as an emerging and important cause of NVE in both community and healthcare settings (13, 14). S. lugdunensis may lead to rapidly progressive native valve endocarditis, first described in an 11-case series in 1993 (8). To date, more than 80 cases of S. lugdunensis endocarditis have been reported, mainly involving native aortic and mitral valves (15), with a reported mortality rate up to 70% (8). In 2008, Frank et al. reported five cases of S. lugdunensis endocarditis diagnosed one to 3 months after vasectomy. All these cases required valve replacement; four urgent (15,16,17). In a 3-year retrospective microbiological and clinical review study from a single medical center, Klotchko et al. (18) identified 77 S. lugdunensis isolates. Of these, seventy had complete data. Seventeen had infections above, eighteen below the waist. Thirteen had infection in urinary tract, including four cases after urological instrumentation. Twenty others had the bacteria found in cerebrospinal fluid and bloodstream with neither endocarditis nor endocarditis. Soft tissue, bone, joint, central nervous system, urine, and bloodstream infections occurred with soft tissue infections described as primarily abscesses. There were four infections of prosthetic joints and nine cases of osteomyelitis. Of the 21 bacteremias reported, five were associated with endocarditis. Two of these patients died. Most isolates were penicillin resistant.
728
DISCUSSION The frequency of S. lugdunensis infections has probably been underestimated in the past. Many clinical laboratories do not routinely identify CoNS to species level. Additionally, cultures are not always performed prior to antibiotic therapy for skin infections following minor surgery. Prior to the vasectomy procedure, patients in Norway receive written and oral information about possible complications. They are informed to not delay contact in case of any discomfort. Serious side effects are rare. The few patients that experience side effects or discomfort after the vasectomy, usually have minor reactions that do not require further treatment. In concordance with International guidelines (19), the Norwegian guidelines do not recommend prophylactic antimicrobial treatment routinely prior to vasectomy. It is our belief that the outcome of this case might have been different, had the patient been seen by the surgeon. We hope to raise the awareness on potential risks of S. lugdunensis infections after minor surgeries like vasectomy procedures. Our patient underwent a vasectomy with fatal outcome due to infection by this bacterium. This also stresses the importance of relevant oral and written information to patients on possible complications, and what signs to look for following such procedures.
REFERENCES 1. Herchline TE, Ayers LW. Occurrence of Staphylococcus lugdunensis in consecutive clinical cultures and relationship of isolation to infection. J Clin Microbiol 1991;29:419–21. 2. Bieber L, Kahlmeter G. Staphylococcus lugdunensis in several niches of the normal skin flora. Clin Microbiol Infect 2010;16:385–8. 3. Hellbacher C, T€ ornqvist E, S€ oderquist B. Staphylococcus lugdunensis: clinical spectrum, antibiotic susceptibility, and phenotypic and genotypic patterns of 39 isolates. Clin Microbiol Infect 2006;12:43–9. 4. Freney J. Staphylococcus lugdunensis sp. nov. and Staphylococcus schleiferi sp. nov., two species from human clinical specimens. Int J Syst Bacteriol 1988;38:168–72. 5. Seifert H, Oltmanns D, Becker K, Wisplinghoff H, von Eiff C. Staphylococcus lugdunensis pacemakerrelated infection. Emerg Infect Dis 2005;11:1283–6. 6. Babu E, Oropello J. Staphylococcus lugdunensis: the coagulase-negative staphylococcus you don’t want to ignore. Expert Rev Anti-Infect Ther 2011;9:901–7. 7. Murillo J, McMahon C, Starr J. Large vegetations in Staphylococcus lugdunensis endocarditis. Heart Lung 2008;37:479–80. 8. Vandenesch F, Etienne J, Reverdy ME, Eykyn SJ. Endocarditis due to Staphylococcus lugdunensis:
© 2015 APMIS. Published by John Wiley & Sons Ltd
S. LUGDUNENSIS ENDOCARDITIS AND VASECTOMY
9.
10. 11.
12.
13.
Report of 11 cases and review. Clin Infect Dis 1993;17:871–6. Anguera I, Rıo A, Mir o JM, Matınez-Lacasa X, Marco F, Guma JR, et al. Staphylococcus lugdunensis infective endocarditis: description of 10 cases and analysis of native valve, prosthetic valve, and pacemaker lead endocarditis clinical profiles. Heart 2005;91:e10. Patel R. Matrix-assisted laser desorption ionizationtime of flight mass spectrometry in clinical microbiology. Clin Infect Dis 2013;57:564–72. Elamin WF, Ball D, Millar M. Unbiased species-level identification of clinical isolates of Coagulase-negative staphylococci: does it change the perspective on Staphylococcus lugdunensis? J Clin Microbiol 2015;53:292–4. Szabados F, Woloszyn J, Richter C, Kaase M, Gatermann S. Identification of molecularly defined Staphylococcus aureus strains using matrix-assisted laser desorption/ionization time of flight mass spectrometry and the Biotyper 2.0 database. J Med Microbiol 2010;59:787–90. Chu VH, Cabell CH, Abrutyn E, Corey GR, Hoen B, Miro JM, et al. Native valve endocarditis due to coag-
© 2015 APMIS. Published by John Wiley & Sons Ltd
14.
15.
16. 17. 18. 19.
ulase-negative staphylococci: report of 99 episodes from the International Collaboration on Endocarditis Merged Database. Clin Infect Dis 2004;39:1527–30. Chu VH, Woods CW, Miro JM, Hoen B, Cabell CH, Pappas PA, et al. Emergence of coagulase-negative staphylococci as a cause of native valve endocarditis. Clin Infect Dis 2008;46:232–42. Frank KL, del Pozo JL, Patel R. From clinical microbiology to infection pathogenesis: how daring to be different works for Staphylococcus lugdunensis. Clin Microbiol Rev 2008;21:111–33. Lessing MP, Crook DW, Bowler IC, Gribbin B. Native-valve endocarditis caused by Staphylococcus lugdunensis. QJM 1996;89:855–8. Walsh B, Mounsey JP. Staphylococcus lugdunensis and endocarditis. J Clin Pathol 1990;43:171–3. Klotchko A, Wallace MR, Licitra C, Sieger B. Staphylococcus lugdunensis: an emerging pathogen. South Med J 2011;104:509–14. American Urological Association (AUA) Guideline. 2012;http://www.auanet.org/common/pdf/education/ clinical guidance/Vasectomy.pdf.
729
