This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Olsen, R. J.
Right arrow Articles by Musser, J. M.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Olsen, R. J.
Right arrow Articles by Musser, J. M.

 Previous Article  |  Next Article 

Journal of Clinical Microbiology, March 2008, p. 1144-1147, Vol. 46, No. 3
0095-1137/08/$08.00+0     doi:10.1128/JCM.02029-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

CASE REPORT

Severe Necrotizing Fasciitis in a Human Immunodeficiency Virus-Positive Patient Caused by Methicillin-Resistant Staphylococcus aureus{triangledown}

Randall J. Olsen,1 Kevin M. Burns,1 Liang Chen,2 Barry N. Kreiswirth,2 and James M. Musser1*

Clinical Microbiology Laboratory, Department of Pathology and Laboratory Medicine, The Methodist Hospital, and Center for Molecular and Translational Human Infectious Diseases Research, The Methodist Hospital Research Institute, Houston, Texas 77030,1 The Public Health Research Institute Tuberculosis Center at the International Center for Public Health, University of Medicine and Dentistry of New Jersey, Newark, New Jersey 071032

Received 17 October 2007/ Returned for modification 26 November 2007/ Accepted 8 January 2008


arrow
ABSTRACT
 
Methicillin-resistant Staphylococcus aureus (MRSA) is a rarely reported cause of necrotizing fasciitis. We report an unusually severe case of MRSA necrotizing fasciitis in a previously undiagnosed AIDS patient. Molecular analysis revealed that the strain had the USA300/spa1 genotype, now an abundant cause of community-acquired MRSA infection.


arrow
CASE REPORT
 
A 36-year-old Hispanic male with no previously recognized significant medical conditions presented to the emergency department (ED) of an outlying community hospital with a chief complaint of exquisite right arm pain, lethargy, fever, and shortness of breath. He had been treated 2 weeks previously with clindamycin for right axillary hidradenitis following a self-reported spider bite. The patient had no recent traumatic injury or known contact with methicillin-resistant Staphylococcus aureus (MRSA). Although the skin infection failed to resolve, he had been otherwise asymptomatic and did not seek further medical attention until awakening that morning with acute distress. Physical examination in the ED revealed a tensely edematous and markedly erythematous right upper arm and shoulder. The right hand and fingers were cool, but they retained complete range of motion. The results shown by a chest X ray were unremarkable despite coarse breath sounds and the deep soft tissue infection. All analytes measured in the initial chemistry and coagulation panels were within normal limits. He was diagnosed with severe cellulitis, septic shock (blood pressure, 58/32; pulse, 130; temperature, 99.4°F; white blood cell count, 1,600/µl), and possible necrotizing fasciitis. Empirical antimicrobial treatment was initiated immediately with vancomycin, piperacillin-tazobactam, and clindamycin. However, his condition deteriorated quickly, and he required ventilator assistance with fluid and vasopressor support. Emergency surgical exploration was undertaken within 24 h of admission, and extensive soft tissue necrosis was observed intraoperatively. The right arm was amputated, and the chest wall was extensively debrided. Sputum and blood cultures collected in the ED prior to administration of empirical therapy, as well as intraoperative wound cultures, grew MRSA that was resistant to erythromycin, clindamycin, and levofloxacin (Table 1). The antimicrobial regimen was then switched to vancomycin, imipenem/cilastatin, rifampin, and voriconazole. Histologic analysis of the surgically excised tissue revealed features typical of necrotizing fasciitis (Fig. 1). Despite initial improvement following surgical intervention and antimicrobial therapy, the septic shock persisted (maximum temperature, 103.4°F; average blood pressure, 100/60) and the necrotizing fasciitis continued to spread to the bilateral chest walls, right abdomen, and right back. He was transferred to a tertiary-care hospital for continued evaluation and management of the severe MRSA infection. Nine additional debridement procedures were performed. Tissues collected during these surgical interventions grew rare MRSA strains with identical susceptibility patterns (Table 1). The hospital course was also complicated by adrenal insufficiency, mild coagulopathy, and iatrogenic anemia. The patient gradually improved, and he was discharged to a rehabilitation center.


View this table:
[in this window]
[in a new window]

  		TABLE 1. Antimicrobial susceptibility patterns of the MRSA strain grown from blooda


Figure 1
View larger version (128K):
[in this window]
[in a new window]

  		FIG. 1. Representative photomicrographs of necrotic tissue taken from the patient. (A) Nonviable myocytes and adipocytes are seen in a background of necrotic tissue (hematoxylin-eosin; original magnification, x10). Broad bands of polymorphonuclear cells and macrophages infiltrate along the major fascial planes. Many isolated acute inflammatory cells also dissect along individual muscle fibers. (B) A thrombosed artery is present within the necrotic soft tissue (hematoxylin-eosin; original magnification, x40). No organisms were seen upon performing Gram staining (data not shown).

Of note, screening and confirmatory studies performed during the diagnostic evaluation at the outside hospital were positive for human immunodeficiency virus (HIV) infection. Further evaluation of this new diagnosis was not pursued until the life-threatening MRSA infection completely resolved. At discharge, his CD4+ cell count and HIV viral load were <20 cells/mm3 and 358,000 copies/ml, respectively. These initial laboratory values (CD4+ < 200 cells/mm3 and viral load > 100,000 copies/ml) fulfill criteria for progression to AIDS and initiation of highly active antiretroviral therapy. A multidrug regimen for treatment-naïve patients was prescribed. It included tenofovir, lamivudine, atazanavir, ritonavir, dapsone, and azithromycin. One month later, his CD4+ count was 192 cells/mm3.

S. aureus is an exceptionally versatile pathogen capable of causing human infections that range in severity from impetigo and cellulitis to life-threatening bacteremia and endocarditis. Asymptomatic nasopharyngeal and perineal carriage and uncomplicated skin and soft tissue infections are far more common than invasive infections (2, 28). Of note, S. aureus is a very infrequent cause of necrotizing fasciitis, with an estimated case rate of approximately 0.1/100,000 (7, 15, 24, 25). Colloquially termed the "flesh-eating disease," necrotizing fasciitis is an invasive infection characterized by widespread tissue destruction and significant morbidity and mortality (11). However, most published cases of S. aureus necrotizing fasciitis involve beta-lactam antibiotic-susceptible strains which progress with a relatively indolent clinical course (24, 25). Thus, the MRSA necrotizing fasciitis case presented herein was unusual in that it was rapidly progressive and nearly fatal. Of further interest, this infection was the initial presenting illness for an apparently healthy adult with previously undiagnosed HIV/AIDS.

In an effort to better understand the unusual virulence observed in this MRSA necrotizing fasciitis case, we analyzed the peripheral blood isolate by molecular genotyping. Results were consistent with the USA300 genotype, a strain now causing epidemic disease in the United States (7, 18, 24, 32, 34, 35). DNA sequencing of a polymorphic 24-bp variable-number tandem repeat in the staphylococcal protein A (spa) gene determined that this organism was spa type 1, which is associated with multilocus sequence type 8 (20, 31). Multiplex PCR demonstrated that it had the staphylococcal chromosomal cassette mec type IVa element, the arginine catabolic mobile element, and the genes (lukS-lukF) encoding Panton-Valentine leukocidin (PVL) (8, 10, 20, 31, 35). Western immunoblotting confirmed that the organism expressed alpha-hemolysin and PVL toxin (data not shown).

The USA300 genotype of S. aureus is now a common cause of community-associated skin and soft tissue infection in North America (7, 18, 24, 32, 34, 35). There are also a few reports of healthcare-associated sepsis, pneumonia, and endocarditis (13, 30, 33). Furthermore, recent increases in the overall frequency and severity of MRSA infection, particularly in nontraditional risk groups, have been noted (21, 30). Thus, there is an emerging concern about an evolution toward greater virulence of the MRSA USA300 genotype.

The patient described herein lacked most known risk factors for invasive staphylococcal disease (19). Although immunosuppressive comorbidities such as malnutrition, diabetes mellitus, and hepatic cirrhosis have been associated with poor prognosis and increased mortality in necrotizing fasciitis, there is no evidence that they significantly increase infection susceptibility (3, 22). Similarly, chronic corticosteroid and nonsteroidal anti-inflammatory therapy are linked to necrotizing fasciitis, but dose-response relationships are poorly defined (1, 14). HIV/AIDS is not generally considered to be a substantial predisposing risk factor for invasive MRSA infections (27), and necrotizing fasciitis is uncommonly reported from studies of these patients (4, 24). However, HIV/AIDS is linked to community-acquired MRSA, and an increased rate of skin infections by USA300 genotype strains was recently noted for this population (6, 30).

We reviewed the English-language literature and identified 19 other reported cases of necrotizing fasciitis caused by MRSA, but only one patient was HIV positive (9, 16, 23, 26, 37) (Table 2). Molecular analyses documented that the USA300 genotype caused our case and five others (Table 2, case 1 and cases 2 to 6, respectively). This finding suggests that the USA300 MRSA genotype should be added to the differential diagnosis of pathogens that cause necrotizing fasciitis, including infections within the HIV/AIDS population. Prevalence studies have not been performed on MRSA strains isolated in Houston, but the USA300 genotype has been previously detected in another local adult hospital (13), and it is the predominant strain isolated from pediatric patients treated for uncomplicated infections (12, 13, 17).


View this table:
[in this window]
[in a new window]

  		TABLE 2. Reported characteristics of necrotizing fasciitis cases caused by MRSA

Our report is an important reminder that benign-appearing skin and soft tissue infections caused by MRSA can rapidly progress to potentially fatal illness. The hidradenitis diagnosed in this patient evolved into necrotizing fasciitis and septic shock within a few days of initial clinical presentation. This case also underscores the need for improved early diagnostic procedures and enhanced understanding of the bacterial virulence factors that contribute to necrotizing fasciitis. In recent years, PVL, a leukocyte-lytic exotoxin produced by most USA300 S. aureus strains, has been speculated to be a virulence factor (35). Similarly, the arginine catabolic mobile element encoding multiple gene products that may enable infecting organisms to suppress and/or evade the host immune system also has been thought to contribute to the success of this strain (8, 10). However, patient epidemiological data and experimental infection models have failed to unambiguously demonstrate a direct role in invasive disease (8, 10, 35). Furthermore, there is uncertain therapeutic significance associated with constitutive clindamycin resistance and increased vancomycin MICs (29, 36). This susceptibility profile may have contributed, in part, to the initial treatment failure and subsequent disease progression that occurred in this patient. The USA300 strain may cause more cases of severe necrotizing fasciitis as its prevalence increases in the United States and elsewhere.


arrow
ACKNOWLEDGMENTS
 
We thank G. A. Land and S. A. Shelburne III for critical review of the manuscript. We also thank P. A. Cernoch for technical expertise.

This work was supported in part by American Heart Association grant 0775045N.


arrow
FOOTNOTES
 
* Corresponding author. Mailing address: Center for Molecular and Translational Human Infectious Diseases Research, The Methodist Hospital Research Institute, 6565 Fannin Street, B490, Houston, TX 77030. Phone: (713) 441-5890. Fax: (713) 441-3447. E-mail: jmmusser{at}tmhs.org Back

{triangledown} Published ahead of print on 16 January 2008. Back


arrow
REFERENCES
 
    1
  1. Aronoff, D. M., and K. C. Bloch. 2003. Assessing the relationship between the use of nonsteroidal antiinflammatory drugs and necrotizing fasciitis caused by group A streptococcus. Medicine (Baltimore) 82:225-235.[CrossRef][Medline]
    2. 2
  2. Chambers, H. F. 2001. The changing epidemiology of Staphylococcus aureus? Emerg. Infect. Dis. 7:178-182.[Medline]
    3. 3
  3. Cheng, N. C., H. C. Tai, Y. B. Tang, S. C. Chang, and J. T. Wang. 2005. Necrotising fasciitis: clinical features in patients with liver cirrhosis. Br. J. Plast. Surg. 58:702-707.[CrossRef][Medline]
    4. 4
  4. Chidzonga, M. M. 2005. Necrotizing fasciitis of the cervical region in an AIDS patient: report of a case. J. Oral. Maxillofac. Surg. 63:855-859.[CrossRef][Medline]
    5. 5
  5. Clinical and Laboratory Standards Institute. 2005. Performance standards for antimicrobialsusceptibility testing. fifteenth informational supplement. document M100-S15. CLSI, Wayne, PA.
    6. 6
  6. Crum-Cianflone, N. F., A. A. Burgi, and B. R. Hale. 2007. Increasing rates of community-acquired methicillin-resistant Staphylococcus aureus infections among HIV-infected persons. Int. J. STD AIDS 18:521-526.[Abstract/Free Full Text]
    7. 7
  7. Davis, S. L., M. B. Perri, S. M. Donabedian, C. Manierski, A. Singh, D. Vager, N. Z. Haque, K. Speirs, R. R. Muder, B. Robinson-Dunn, M. K. Hayden, and M. J. Zervos. 2007. Epidemiology and outcomes of community-associated methicillin-resistant Staphylococcus aureus infection. J. Clin. Microbiol. 45:1705-1711.[Abstract/Free Full Text]
    8. 8
  8. Diep, B. A., S. R. Gill, R. F. Chang, T. H. Phan, J. H. Chen, M. G. Davidson, F. Lin, J. Lin, H. A. Carleton, E. F. Mongodin, G. F. Sensabaugh, and F. Perdreau-Remington. 2006. Complete genome sequence of USA300, an epidemic clone of community-acquired methicillin-resistant Staphylococcus aureus. Lancet 367:731-739.[CrossRef][Medline]
    9. 9
  9. Dunbar, N. M., and R. C. Harruff. 2007. Necrotizing fasciitis: manifestations, microbiology and connection with black tar heroin. J. Forensic Sci. 52:920-923.[CrossRef][Medline]
    10. 10
  10. Goering, R. V., L. K. McDougal, G. E. Fosheim, K. K. Bonnstetter, D. J. Wolter, and F. C. Tenover. 2007. Epidemiologic distribution of the arginine catabolic mobile element among selected methicillin-resistant and methicillin-susceptible Staphylococcus aureus isolates. J. Clin. Microbiol. 45:1981-1984.[Abstract/Free Full Text]
    11. 11
  11. Golger, A., S. Ching, C. H. Goldsmith, R. A. Pennie, and J. R. Bain. 2007. Mortality in patients with necrotizing fasciitis. Plast. Reconstr. Surg. 119:1803-1807.[CrossRef][Medline]
    12. 12
  12. Gonzalez, B. E., G. Martinez-Aguilar, K. G. Hulten, W. A. Hammerman, J. Coss-Bu, A. Avalos-Mishaan, E. O. Mason, Jr., and S. L. Kaplan. 2005. Severe staphylococcal sepsis in adolescents in the era of community-acquired methicillin-resistant Staphylococcus aureus. Pediatrics 115:642-648.[Abstract/Free Full Text]
    13. 13
  13. Gonzalez, B. E., A. M. Rueda, S. A. Shelburne 3rd, D. M. Musher, R. J. Hamill, and K. G. Hulten. 2006. Community-associated strains of methicillin-resistant Staphylococcus aureus as the cause of healthcare-associated infection. Infect. Control Hosp. Epidemiol. 27:1051-1056.[CrossRef][Medline]
    14. 14
  14. Hashimoto, N., H. Sugiyama, K. Asagoe, K. Hara, O. Yamasaki, Y. Yamasaki, and H. Makino. 2002. Fulminant necrotising fasciitis developing during long term corticosteroid treatment of systemic lupus erythematosus. Ann. Rheum. Dis. 61:848-849.[Free Full Text]
    15. 15
  15. Huang, H., N. M. Flynn, J. H. King, C. Monchaud, M. Morita, and S. H. Cohen. 2006. Comparisons of community-associated methicillin-resistant Staphylococcus aureus (MRSA) and hospital-associated MSRA infections in Sacramento, California. J. Clin. Microbiol. 44:2423-2427.[Abstract/Free Full Text]
    16. 16
  16. Imamura, Y., Y. Kudo, Y. Ishii, H. Shibuya, and S. Takayasu. 1995. A case of subacute necrotizing fasciitis. J. Dermatol. 22:960-963.[Medline]
    17. 17
  17. Kaplan, S. L., K. G. Hulten, B. E. Gonzalez, W. A. Hammerman, L. Lamberth, J. Versalovic, and E. O. Mason, Jr. 2005. Three-year surveillance of community-acquired Staphylococcus aureus infections in children. Clin. Infect. Dis. 40:1785-1791.[CrossRef][Medline]
    18. 18
  18. King, M. D., B. J. Humphrey, Y. F. Wang, E. V. Kourbatova, S. M. Ray, and H. M. Blumberg. 2006. Emergence of community-acquired methicillin-resistant Staphylococcus aureus USA 300 clone as the predominant cause of skin and soft-tissue infections. Ann. Intern. Med. 144:309-317.[Abstract/Free Full Text]
    19. 19
  19. Kluytmans-Vandenbergh, M. F., and J. A. Kluytmans. 2006. Community-acquired methicillin-resistant Staphylococcus aureus: current perspectives. Clin. Microbiol. Infect. 12(Suppl. 1):9-15.[Medline]
    20. 20
  20. Koreen, L., S. V. Ramaswamy, E. A. Graviss, S. Naidich, J. M. Musser, and B. N. Kreiswirth. 2004. spa typing method for discriminating among Staphylococcus aureus isolates: implications for use of a single marker to detect genetic micro- and macrovariation. J. Clin. Microbiol. 42:792-799.[Abstract/Free Full Text]
    21. 21
  21. McCaig, L. F., L. C. McDonald, S. Mandal, and D. B. Jernigan. 2006. Staphylococcus aureus-associated skin and soft tissue infections in ambulatory care. Emerg. Infect. Dis. 12:1715-1723.[Medline]
    22. 22
  22. McHenry, C. R., C. P. Brandt, J. J. Piotrowski, D. G. Jacobs, and M. A. Malangoni. 1994. Idiopathic necrotizing fasciitis: recognition, incidence, and outcome of therapy. Am. Surg. 60:490-494.[Medline]
    23. 23
  23. Miller, L. G., F. Perdreau-Remington, G. Rieg, S. Mehdi, J. Perlroth, A. S. Bayer, A. W. Tang, T. O. Phung, and B. Spellberg. 2005. Necrotizing fasciitis caused by community-associated methicillin-resistant Staphylococcus aureus in Los Angeles. N. Engl. J. Med. 352:1445-1453.[Abstract/Free Full Text]
    24. 24
  24. Morgan, W. R., M. D. Caldwell, J. M. Brady, M. E. Stemper, K. D. Reed, and S. K. Shukla. 2007. Necrotizing fasciitis due to a methicillin-sensitive Staphylococcus aureus isolate harboring an enterotoxin gene cluster. J. Clin. Microbiol. 45:668-671.[Abstract/Free Full Text]
    25. 25
  25. Omland, L. H., S. W. Rasmussen, J. Hvolris, and A. Friis-Moller. 2007. Necrotizing fasciitis caused by TSST-1 producing penicillin-sensitive Staphylococcus aureus—a case report. Acta Orthop. 78:296-297.[CrossRef][Medline]
    26. 26
  26. Roth, A., R. Fuhrmann, M. Lange, J. Mollenhauer, E. Straube, and R. Venbrocks. 2003. Overwhelming septic infection with a multi-resistant Staphylococcus aureus (MRSA) after total knee replacement. Arch. Orthop. Trauma. Surg. 123:429-432.[Medline]
    27. 27
  27. Roy, P. K., S. C. Patel, and Y. P. Kataria. 2001. Necrotizing fasciitis of abdominal wall in AIDS. Dig. Dis. Sci. 46:1139-1142.[CrossRef][Medline]
    28. 28
  28. Sanford, M. D., A. F. Widmer, M. J. Bale, R. N. Jones, and R. P. Wenzel. 1994. Efficient detection and long-term persistence of the carriage of methicillin-resistant Staphylococcus aureus. Clin. Infect. Dis. 19:1123-1128.[Medline]
    29. 29
  29. Schreckenberger, P. C., E. Ilendo, and K. L. Ristow. 2004. Incidence of constitutive and inducible clindamycin resistance in Staphylococcus aureus and coagulase-negative staphylococci in a community and a tertiary care hospital. J. Clin. Microbiol. 42:2777-2779.[Abstract/Free Full Text]
    30. 30
  30. Seybold, U., E. V. Kourbatova, J. G. Johnson, S. J. Halvosa, Y. F. Wang, M. D. King, S. M. Ray, and H. M. Blumberg. 2006. Emergence of community-associated methicillin-resistant Staphylococcus aureus USA300 genotype as a major cause of health care-associated blood stream infections. Clin. Infect. Dis. 42:647-656.[CrossRef][Medline]
    31. 31
  31. Shopsin, B., M. Gomez, S. O. Montgomery, D. H. Smith, M. Waddington, D. E. Dodge, D. A. Bost, M. Riehman, S. Naidich, and B. N. Kreiswirth. 1999. Evaluation of protein A gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains. J. Clin. Microbiol. 37:3556-3563.[Abstract/Free Full Text]
    32. 32
  32. Tenover, F. C., L. K. McDougal, R. V. Goering, G. Killgore, S. J. Projan, J. B. Patel, and P. M. Dunman. 2006. Characterization of a strain of community-associated methicillin-resistant Staphylococcus aureus widely disseminated in the United States. J. Clin. Microbiol. 44:108-118.[Abstract/Free Full Text]
    33. 33
  33. Vayalumkal, J. V., H. Whittingham, O. Vanderkooi, T. E. Stewart, D. E. Low, M. Mulvey, and A. McGeer. 2007. Necrotizing pneumonia and septic shock: suspecting CA-MRSA in patients presenting to Canadian emergency departments. CJEM 9:300-303.[Medline]
    34. 34
  34. Voyich, J. M., K. R. Braughton, D. E. Sturdevant, A. R. Whitney, B. Said-Salim, S. F. Porcella, R. D. Long, D. W. Dorward, D. J. Gardner, B. N. Kreiswirth, J. M. Musser, and F. R. DeLeo. 2005. Insights into mechanisms used by Staphylococcus aureus to avoid destruction by human neutrophils. J. Immunol. 175:3907-3919.[Abstract/Free Full Text]
    35. 35
  35. Voyich, J. M., M. Otto, B. Mathema, K. R. Braughton, A. R. Whitney, D. Welty, R. D. Long, D. W. Dorward, D. J. Gardner, G. Lina, B. N. Kreiswirth, and F. R. DeLeo. 2006. Is Panton-Valentine leukocidin the major virulence determinant in community-associated methicillin-resistant Staphylococcus aureus disease? J. Infect. Dis. 194:1761-1770.[CrossRef][Medline]
    36. 36
  36. Wang, G., J. F. Hindler, K. W. Ward, and D. A. Bruckner. 2006. Increased vancomycin MICs for Staphylococcus aureus clinical isolates from a university hospital during a 5-year period. J. Clin. Microbiol. 44:3883-3886.[Abstract/Free Full Text]
    37. 37
  37. Wong, C. H., S. H. Tan, A. Kurup, and A. B. Tan. 2004. Recurrent necrotizing fasciitis caused by methicillin-resistant Staphylococcus aureus. Eur. J. Clin. Microbiol. Infect. Dis. 23:909-911.[Medline]

Journal of Clinical Microbiology, March 2008, p. 1144-1147, Vol. 46, No. 3
0095-1137/08/$08.00+0     doi:10.1128/JCM.02029-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Adeyemi, O. A., Qi, C., Zembower, T. R., Ison, M. G., Grant, T. H., Hartigan, B. J., Malczynski, M., Stosor, V. (2008). Invasive Infections with Community-Associated Methicillin-Resistant Staphylococcus aureus after Kidney Transplantation. J. Clin. Microbiol. 46: 2809-2813 [Abstract] [Full Text]  

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Olsen, R. J.
Right arrow Articles by Musser, J. M.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Olsen, R. J.
Right arrow Articles by Musser, J. M.

Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»