Archives of Physical Medicine and Rehabilitation
Volume 88, Issue 8 , Pages 979-983, August 2007

Staphylococcus aureus Colonization in Community-Dwelling People With Spinal Cord Dysfunction

  • Mary-Claire Roghmann, MD, MS

      Affiliations

    • VA Maryland Health Care System, Baltimore, MD
    • Department of Epidemiology and Preventive Medicine, University of Maryland School of Medicine, Baltimore, MD
    • Corresponding Author InformationCorrespondence to Mary-Claire Roghmann, MD, MS, 100 N Greene St (Lower level), Baltimore, MD 21201
    • ,
  • Peter H. Gorman, MD

      Affiliations

    • Department of Neurology, University of Maryland School of Medicine, Baltimore, MD
    • ,
  • Mitchell T. Wallin, MD

      Affiliations

    • Department of Neurology Georgetown University School of Medicine and VA Medical Center, Washington, DC.
    • ,
  • Kristen Kreisel, MS

      Affiliations

    • Department of Epidemiology and Preventive Medicine, University of Maryland School of Medicine, Baltimore, MD
    • ,
  • Simone Shurland, MS

      Affiliations

    • Department of Epidemiology and Preventive Medicine, University of Maryland School of Medicine, Baltimore, MD
    • ,
  • Judith A. Johnson, PhD

      Affiliations

    • VA Maryland Health Care System, Baltimore, MD
    • Department of Pathology, University of Maryland School of Medicine, Baltimore, MD

Article Outline

Abstract 

Roghmann M-C, Gorman PH, Wallin MT, Kreisel K, Shurland S, Johnson JA. Staphylococcus aureus colonization in community-dwelling people with spinal cord dysfunction.

Objectives

To estimate the prevalence of and determine risk factors for Staphylococcus aureus colonization of the perineum.

Design

Cross-sectional study with follow-up of up to 1 year.

Setting

Multiple outpatient sites.

Participants

Eighty-four community-dwelling adults with spinal cord dysfunction (SCD).

Interventions

Not applicable.

Main Outcome Measure

Colonization of perineum with S. aureus.

Results

Overall, 24% of the study cohort carried S. aureus on their perineal skin at enrollment, with 16% having methicillin-susceptible S. aureus and 10% having methicillin-resistant S. aureus (MRSA). Most perineal carriers were also colonized in the anterior nares. Participants with trauma as the cause of their SCD were more likely to be colonized with S. aureus than participants with SCD caused by multiple sclerosis or other causes (relative risk [RR], 2.8; 95% confidence interval [CI], 1.2–6.6; P=.01). Participants with pelvic decubiti were more likely to be colonized with S. aureus than participants without pelvic decubiti (RR=4.3; 95% CI, 2.4–7.7; P<.001). The recent use of any antibiotic was not associated with an increased risk of colonization with S. aureus (RR=1.5; 95% CI, 0.7–3.3; P=.31); however, recent fluoroquinolone use was significantly associated with perineal colonization (RR=2.8; 95% CI, 1.4–5.8; P=.02). Of the 8 participants with MRSA colonization, only 2 (25%) had a history of MRSA colonization.

Conclusions

S. aureus colonization of the perineum is common in this outpatient population of people with SCD. The use of fluoroquinolones was associated with S. aureus colonization. Colonization with MRSA without a history of MRSA was common.

Key Words: Cross-sectional studies, Fluoroquinolones, Multiple sclerosis, Rehabilitation, Spinal cord injuries, Staphylococcus aureus

 

STAPHYLOCOCCUS AUREUS IS a major cause of both community- and hospital-acquired infections.1 S. aureus infection is common in people with spinal cord injury (SCI) or dysfunction (SCD).2 Despite this, little is known about one of the major risk factors for S. aureus infection, colonization with S. aureus. Colonization with S. aureus is clearly important because rates of infection are higher in carriers than noncarriers.3 Studies comparing colonizing and infecting isolates of S. aureus have shown that people are usually infected with their own colonizing isolate.4 Temporary eradication of S. aureus by using topical mupirocin reduces S. aureus infection in certain populations.5, 6 Understanding risk factors for S. aureus colonization can help us identify potential intervention to decrease S. aureus infection.7

Perineal colonization with S. aureus is common, affecting about 20% of the general population.8 Perineal carriers have high levels of colonization based on quantitative cultures.8 In addition, people with perineal or perirectal colonization may be at greater risk of S. aureus infection.9

S. aureus colonization of the nares, perineum, and wounds is common in people with SCI or SCD. Because of frequent hospitalization, these people are often colonized with methicillin-resistant S. aureus (MRSA), which is most commonly transmitted in the health care setting.10, 11, 12 Relatively little is known about S. aureus colonization in community-dwelling people with SCD. Our objectives in this investigation are to estimate the prevalence of S. aureus colonization of the perineum in a cross-sectional study of community-dwelling people with SCD and determine risk factors for perineal colonization. We also describe the patterns of colonization in a longitudinal study.

Back to Article Outline

Methods 

Study Design 

We prospectively enrolled community-dwelling adults with SCI or SCD (hereafter referred to collectively as SCD) from April 2003 to June 2004. The perineum of participants was cultured for S. aureus. We then assessed risk factors for S. aureus colonization in a cross-sectional study. We repeated their perineal cultures quarterly for up to 1 year to determine if colonization was persistent. We added a culture of the anterior nares to the protocol after the first 38 participants were enrolled when it became apparent from perineal culture results that S. aureus carriage was common. This assessment of S. aureus colonization was part of a larger review of antibiotic-resistance colonization patterns in this patient population, part of which was already published.13 Eligibility criteria and recruitment sites are described in detail in the prior publication.13, 14

Participants provided informed consent and were followed longitudinally for up to 1 year. The institutional review boards of the University of Maryland, Baltimore, MD, and the Washington, DC, Veterans Affairs Medical Centers approved the study protocol. Implementation of this study conformed to the approved protocol, as well as the ethical and humane principles of research.

Study Variables 

We collected age, sex, ethnic background, etiology of SCD, years since onset of SCD, level of disability as measured by the Eastern Cooperative Oncology Group (ECOG),15 presence of decubiti, method of emptying bladder, and previous hospitalizations and antibiotics within the last 90 days at enrollment from participants and their medical records. We classified participants with multiple sclerosis (MS) by disease subtype.16 We classified participants with SCI caused by trauma by their American Spinal Injury Association (ASIA) Impairment Scale.17 We categorized the 6-point ECOG score as 0 to 2 and 3 to 5 because people with an ECOG score of 0 to 2 are capable of all self-care, whereas people with an ECOG score of 3 to 5 are capable of only limited self-care or completely disabled.

We obtained cultures of the perineal skin on enrollment and then quarterly. Cultures were obtained by a single research coordinator. Perineal cultures were obtained after positioning the participant on his/her back with open legs by using a moistened, single-sterile Dacron fiber-tipped swab starting under the scrotum (male) or under the vagina (female) in a side-to-side pattern toward the anus, making a total of 3 swipes and rotating the swab to allow contact with the entire swab. We also cultured the anterior nares. Anterior nares cultures were obtained after positioning the participant upright by using a moistened, single-sterile Dacron fiber-tipped swab, inserting it into 1 anterior naris, rotating it around, and then repeating in the other nares.

Swabs were cultured for the presence of S. aureus including MRSA by using standard microbiologic methods. Swabs were inoculated on T-soy agar plates with 5% sheep blood agar, phenylethyl alcohol agar,a and mannitol salt agar with and without 6μg/mL of oxacillin. Plates were incubated at 35°C and examined at 1- and 2-day growth. S. aureus was identified with BactiStaph latex agglutination.a Methicillin resistance was confirmed on Mueller Hinton agar with 4% NaCL and 6μg/mL of oxacillin.a Cultures negative for S. aureus on direct plating were tested via enrichment broth culture by using 2.5% NaCl broth18 and then direct plated as described earlier.

Persistent carriage was defined as greater than or equal to 80% of at least 5 perineal cultures positive for S. aureus; intermittent carriage was defined as 1% to 79% of at least 5 cultures positive for S. aureus, and no carriage was defined as 0% of at least 5 cultures. This definition is adapted from definitions used by VandenBergh et al19 to define patterns of nasal carriage over time. Standard deoxyribonucleic acid (DNA) amplification and sequencing with the “universal” 27F and 519R primers of 16s recombinant DNA was performed to confirm all isolates as S. aureus.20 Each isolate was typed by DNA sequencing analysis of the protein A (spa) gene hypervariable region as previously described.21

Study Analysis 

Summary statistics included means and standard deviations (SDs) or continuous variables and proportions for categorical variables. Group means were compared by using a t test or 1-way analysis of variance and proportions by the Pearson chi-square test or Fisher exact test, as appropriate. All statistical analyses were performed by using SPSS statistical software.b

Back to Article Outline

Results 

Table 1 shows a description of our participants. Forty-four participants (52%) had MS, and 36 (45%) had trauma as a cause of their SCD. Of those with MS, 45% were classified as relapsing-remitting and 43% as secondary progressive. The remaining were classified as primary progressive (n=3) or not specified (n=2). Of those with SCD caused by trauma, 58% were ASIA grade A, 11% were grade B, 19% were grade C, and 11% were grade D. Of the remaining participants, 1 had Brown-Séquard syndrome, 2 had central cord syndrome, and 1 had cauda equina syndrome. Twenty-six percent had used antibiotics in the 90 days before study enrollment, and 12% had used fluoroquinolone antibiotics. Six percent had a history of MRSA colonization. Overall, 24% of the study cohort carried S. aureus on their perineal skin at enrollment, with 16% having methicillin-sensitive S. aureus (MSSA) and 10% having MRSA. One participant had both MRSA and MSSA colonization. Of the 8 participants with MRSA colonization, only 2 (14%) had a history of MRSA colonization. All but one of the MRSA isolates had spa motifs (MDMGMK) associated with the hospital-acquired MRSA clones USA100 or USA800.22

Table 1. Overall Description of Community-Dwelling People With SCD and Characteristics Associated With Perineal Colonization With S. aureus at Enrollment
Overall PopulationPerineal Colonization With S. aureus at Enrollment
Variables(N=84)Yes (n=20)No (n=64)P
Demographics
Male, n (%)70(83)16(80)54(84).647
Mean age ± SD (y)50±1048±1051±10.295
Ethnic background .427
White, non-Hispanic, n (%)55(65)11(55)44(69)
African American, non-Hispanic, n (%)27(32)8(40)19(30)
Other, n (%)2(2)1(5)1(2)
Characteristics of SCD
Etiology of SCD .035
Trauma, n (%)38(45)14(70)24(38)
MS, n (%)44(52)6(30)38(59)
Other, n (%)2(2)0(0)2(3)
Mean years with SCD ± SD17±1214±1018±12.232
ECOG score of 3–5, n (%)14(17)4(20)10(16).647
Presence of skin breakdown in pelvic area, n (%)16(19)8(40)8(13).006
Method of emptying bladder .012
Continent, n (%)42(50)6(30)36(56)
Condom catheter, n (%)12(14)2(10)10(16)
Intermittent catheterization, n (%)15(18)4(20)11(17)
Suprapubic catheter, n (%)3(4)3(15)0(0)
Urethral catheter, n (%)6(7)3(15)3(5)
Incontinent (no catheter use), n (%)6(7)2(10)4(6)
Potential risk factors
History of MRSA colonization, n (%)5(6)3(16)2(3).081
Hospitalizations >48h in last 90d, n (%)5(6)1(5)4(6).837
Antibiotics in last 90d, n (%)22(26)7(35)15(23).305
Fluoroquinolone antibiotics in last 90d, n (%)11(13)6(30)5(8).010

Table 1 also shows characteristics associated with S. aureus colonization of the perineal skin. Participants with trauma as the cause of their SCD were more likely to be colonized with S. aureus than participants with SCD caused by MS or other causes (relative risk [RR], 2.8; 95% confidence interval [CI], 1.2–6.6; P=.01). Participants with pelvic decubiti were more likely to be colonized with S. aureus than participants without pelvic decubiti (RR=4.3; 95% CI, 2.4–7.7; P<.001). The recent use of any antibiotic was not associated with an increased risk of colonization with S. aureus (RR=1.5; 95% CI, 0.7–3.3; P=.31); however, recent fluoroquinolone use was significantly associated with perineal colonization (RR=2.8; 95% CI, 1.4–5.8; P=.02). Among 38 participants with trauma as the cause of their SCI, a greater proportion of those who had taken fluoroquinolones in the past 90 days were S. aureus colonized compared with those who had not (60% vs 29%, P=.126). Most perineal carriers were also colonized in the anterior nares. Of the 46 participants who were cultured in the anterior nares, 13 of 16 perineal carriers were also nasal carriers, and only 4 of the 30 nonperineal carriers were nasal carriers (81% vs 13%, P<.0001).

Patterns of S. aureus carriage were assessed in 30 participants who were followed for 1 year with at least 5 perineal cultures. The demographics, characteristics of SCD, and potential risk factors for S. aureus colonization of these participants did not differ from the participants who dropped out (data not shown). Overall, 10% were persistently colonized with 80% or more of perineal cultures positive, 63% were intermittently colonized with 20% to 60% of cultures positive, and 27% were never positive for S. aureus. Among 23 participants with S. aureus colonization, we detected 22 different spa types. Three of the 19 intermittent carriers showed evidence of a switch in spa type, whereas 1 of the 3 persistent carriers had a modification in spa type (16% vs 33%, P=1.0). We had cultures of the anterior nares on 22 of the 30 participants in the longitudinal component of the study. Among perineal carriers of S. aureus with a nares culture, 11 of 16 were nasal carriers of S. aureus; among nonperineal carriers of S. aureus with a nares culture, 1 of 6 were nasal carriers. Among the 11 with nasal and perineal carriage, all but 1 carried the same spa type in the anterior nares as in the perineum.

Back to Article Outline

Discussion 

Summary of Main Results Placed in Context of Other Studies 

Overall, 24% of the study population carried S. aureus on their perineal skin at enrollment. People without SCD are also known to carry S. aureus in their perineum with similar frequency. In 1959, Ridley8 cultured 50 male medical students. He found that overall 48% were S. aureus carriers with 26% in the nose only, 12% in the nose and perineum, and 10% in the perineum. Importantly, the 22% with perineal carriage had high colony counts of S. aureus and could disperse S. aureus into the air with exercise even with negative nares cultures. Thus, perineal carriage may increase the risk of S. aureus transmission to others. Squier et al9 reported that liver transplant patients colonized with S. aureus in the perirectal area, and the anterior nares had a significantly higher risk of infection compared with those patients colonized only in the anterior nares. Thus, people with perineal carriage may be at an increased risk for S. aureus infection particularly in an SCD population with skin breakdown in the perineal area.

Although overall antibiotic use was not associated with S. aureus colonization of the perineum, the use of fluoroquinolone antibiotics was strongly associated with perineal colonization. Patients who receive fluoroquinolones may be more likely to have other risk factors for perineal colonization such as skin breakdown; however, a similar trend, although not statistically significant, was also noted in a subset analysis of those with trauma as the etiology of their SCI. It is plausible that the use of fluoroquinolones increases the risk of S. aureus colonization. Both MRSA and MSSA rapidly develop resistance to ciprofloxacin.23 Bisognano et al24 showed that isolates of S. aureus increased their tissue-binding abilities when exposed to fluoroquinolones by upregulation of fibronectin-binding proteins. Dziekan et al25 showed that fluoroquinolone use was an independent risk factor for MRSA colonization in a case-control study during an MRSA outbreak. Thus, treatment with fluoroquinolone antibiotics could increase the risk of S. aureus acquisition or promote persistent carriage of S. aureus once acquired.

Many of the S. aureus isolates were MRSA, despite relatively few participants with a history of MRSA colonization or infection. This shows the importance of surveillance cultures for determining MRSA colonization; relying on clinical cultures to identify those with MRSA consistently underestimates the prevalence of MRSA colonization.26 The use of surveillance cultures to identify MRSA colonization in high-risk populations is now recommended by the U.S. Centers for Disease Control and Prevention for preventing the transmission of MRSA in the health care setting.27 Early identification through surveillance cultures allows for appropriate isolation to prevent transmission to others. Information from surveillance cultures for MRSA can also be used to guide empiric antibiotic therapy for skin and soft tissue infections.

In our longitudinal study of perineal carriage of S. aureus, we found that 10% of the participants had persistent carriage, 63% had intermittent carriage, and 27% had no carriage. This is consistent with what has been noted in other populations when assessing rates of nasal carriage.28 Previous work29 in other populations have found that patients with intermittent carriage are more likely to have different S. aureus strains over time, implying that these people are becoming colonized, then losing their isolates, and then acquiring a new isolate. The majority of our participants with intermittent carriage were colonized with a single spa type of S. aureus despite intermittent carriage. This implies that in this population, the intermittent carriers are truly persistently colonized with a single strain and that negative cultures are false-negatives.

In those participants for whom we had both perineal and nares cultures, we found that perineal cultures were strongly associated with nasal cultures. Eighty-one percent of those with positive perineal cultures had positive nares culture, and 76% of those with positive nares cultures had positive perineal cultures. This is in contrast to other studies that found that the anterior nares was more commonly colonized than the perineum11, 12; our use of enrichment broth cultures may explain the difference. Alternatively, perineal colonization may be more common in this population. This strong correlation suggests that our results may apply to S. aureus colonization at either site.

Study Strengths 

Our study has a number of important strengths. We studied a unique population of people with SCD in a prospective manner, thereby optimizing the accuracy of our data. Few, if any, studies have looked at S. aureus colonization in a community-dwelling population of people with SCI; most studies have been performed in the inpatient setting.10, 11, 12 We also used surveillance cultures, not clinical cultures (which are taken in response to the clinical suspicion of an infection), to measure the presence of S. aureus, and our culture methods included the use of enrichment broth for the detection of S. aureus maximizing the sensitivity of the cultures to detect S. aureus.

Study Limitations 

Our cross-sectional study was limited by a relatively small sample size. Because of this, we cannot say whether the use of fluoroquinolones is an independent risk factor for S. aureus colonization. The longitudinal study was limited because of loss to follow-up; however, those lost to follow-up were similar to those who participated for a full year. Thus, our estimates of the distribution of S. aureus carriage over time should be accurate for our target population.

Back to Article Outline

Conclusions 

S. aureus colonization of the perineum is common in this outpatient population of people with SCD; if colonized, most carry a single strain for over a year. The use of fluoroquinolones may promote S. aureus colonization, which is associated with an increased risk of S. aureus infection.3 Thus, we need to use fluoroquinolones to treat only symptomatic infections, not asymptomatic colonization or contamination.

Suppliers

Back to Article Outline

Acknowledgments 

We thank Debbie Grady, RN, for her critical role in coordinating the project. We thank the clinical staff of enrollment sites and other members of the research team including the VA MS Center of Excellence-East. This assessment of S. aureus colonization was part of a larger review of antibiotic resistance colonization patterns in this patient population, part of which was previously published.13

Back to Article Outline

References 

  1. Laupland KB, Church DL, Mucenski M, Sutherland LR, Davies HD. Population-based study of the epidemiology of and the risk factors for invasive Staphylococcus aureus infections. J Infect Dis. 2003;187:1452–1459
  2. Montgomerie JZ. Infections in patients with spinal cord injuries. Clin Infect Dis. 1997;25:1285–1290
  3. Wertheim HF, Melles DC, Vos MC, et al. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis. 2005;5:751–762
  4. Wertheim HF, Vos MC, Ott A, et al. Risk and outcome of nosocomial Staphylococcus aureus bacteraemia in nasal carriers versus non-carriers. Lancet. 2004;364:703–705
  5. Yu VL, Goetz A, Wagener M, et al. Staphylococcus aureus nasal carriage and infection in patients on hemodialysis (Efficacy of antibiotic prophylaxis). N Engl J Med. 1986;315:91–96
  6. Perl TM, Cullen JJ, Wenzel RP, et al. Mupirocin and the Risk of Staphylococcus Aureus Study Team (Intranasal mupirocin to prevent postoperative Staphylococcus aureus infections). N Engl J Med. 2002;346:1871–1877
  7. Peacock SJ, de Silva I, Lowy FD. What determines nasal carriage of Staphylococcus aureus?. Trends Microbiol. 2001;9:605–610
  8. Ridley M. Perineal carriage of Staph aureus. Br Med J. 1959;1(5117):270–273
  9. Squier C, Rihs JD, Risa KJ, et al. Staphylococcus aureus rectal carriage and its association with infections in patients in a surgical intensive care unit and a liver transplant unit. Infect Control Hosp Epidemiol. 2002;23:495–501
  10. Olona-Cabases M, Tico-Falguera N, Ramirez-Garceran L, Del Valle-Ortiz O, Castello-Verdu T, Garcia-Fernandez L. Methicillin-resistant Staphylococcus aureus: a four-year experience in a spinal cord injury unit in Spain. Spinal Cord. 1996;34:315–319
  11. Maeder K, Ginunas VJ, Montgomerie JZ, Canawati HN. Methicillin-resistant Staphylococcus aureus (MRSA) colonization in patients with spinal cord injury. Paraplegia. 1993;31:639–644
  12. Aeilts GD, Sapico FL, Canawati HN, Malik GM, Montgomerie JZ. Methicillin-resistant-Staphylococcus aureus colonization and infection in a rehabilitation facility. J Clin Microbiol. 1982;16:218–223
  13. Roghmann MC, Wallin MT, Gorman PH, Johnson JA. Prevalence and natural history of colonization with fluoroquinolone-resistant gram-negative bacilli in community-dwelling people with spinal cord dysfunction. Arch Phys Med Rehabil. 2006;87:1305–1309
  14. Multiple Sclerosis Council for Clinical Practice Guidelines. In: Urinary dysfunction and multiple sclerosis: evidence-based management strategies for fatigue in multiple sclerosis. Washington (DC): Paralyzed Veterans of America; 1999;p. 1–16
  15. Oken MM, Creech RH, Tormey DC, et al. Toxicity and response criteria of the Eastern Cooperative Oncology Group. Am J Clin Oncol. 1982;5:649–655
  16. Kurtzke JF. Clinical definition for multiple sclerosis treatment trials. Ann Neurol. 1994;36(Suppl):S73–S79
  17. American Spinal Injury Association. International standards for neurological classification of SCI. Atlanta: ASIA; 2002;
  18. Jones EM, Bowker KE, Cooke R, Marshall RJ, Reeves DS, MacGowan AP. Salt tolerance of EMRSA-16 and its effect on the sensitivity of screening cultures. J Hosp Infect. 1997;35:59–62
  19. VandenBergh MF, Yzerman EP, van Belkum A, Boelens HA, Sijmons M, Verbrugh HA. Follow-up of Staphylococcus aureus nasal carriage after 8 years: redefining the persistent carrier state. J Clin Microbiol. 1999;37:3133–3140
  20. Hugenholtz P, Goebel BM, Pace NR. Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol. 1998;180:4765–4774
  21. Harmsen D, Claus H, Witte W, Rothganger J, Turnwald D, Vogel U. Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol. 2003;41:5442–5448
  22. McDougal LK, Steward CD, Killgore GE, Chaitram JM, McAllister SK, Tenover FC. Pulsed-field gel electrophoresis typing of oxacillin-resistant Staphylococcus aureus isolates from the United States: establishing a national database. J Clin Microbiol. 2003;41:5113–5120
  23. Blumberg HM, Rimland D, Carroll DJ, Terry P, Wachsmuth IK. Rapid development of ciprofloxacin resistance in methicillin-susceptible and -resistant Staphylococcus aureus. J Infect Dis. 1991;163:1279–1285
  24. Bisognano C, Vaudaux P, Rohner P, Lew DP, Hooper DC. Induction of fibronectin-binding proteins and increased adhesion of quinolone-resistant Staphylococcus aureus by subinhibitory levels of ciprofloxacin. Antimicrob Agents Chemother. 2000;44:1428–1437
  25. Dziekan G, Hahn A, Thune K, et al. Methicillin-resistant Staphylococcus aureus in a teaching hospital: investigation of nosocomial transmission using a matched case-control study. J Hosp Infect. 2000;46:263–270
  26. Salgado CD, Farr BM. What proportion of hospital patients colonized with methicillin-resistant Staphylococcus aureus are identified by clinical microbiological cultures?. Infect Control Hosp Epidemiol. 2006;27:116–121
  27. Siegel JD, Rhinehart E, Jackson M, Chiarello L Healthcare Infection Control Practices Advisory Committee. Management of multidrug-resistant organisms in healthcare settings. 2006;Available at: URL: http://www.cdc.gov/ncidod/dhqp/pdf/ar/mdroGuideline2006.pdf. Accessed April 17, 2007.
  28. Kluytmans J, van Belkum A, Verbrugh H. Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev. 1997;10:505–520
  29. Eriksen NH, Espersen F, Rosdahl VT, Jensen K. Carriage of Staphylococcus aureus among 104 healthy persons during a 19-month period. Epidemiol Infect. 1995;115:51–60
  • a Remel Inc, 12076 Santa Fe Dr, PO Box 14428, Lenexa, KS 66215.
  • b Version 12.1; SPSS Inc, 233 S Wacker Dr, 11th Fl, Chicago, IL 60606.

 Supported by a VA Merit Review Grant, University of Maryland School of Medicine General Clinical Research Center (grant no. M01-RR-16500), and a Merck Medical School Grant.

 No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the author(s) or upon any organization with which the author(s) is/are associated.

 Reprints are not available from the author.

PII: S0003-9993(07)00348-6

doi:10.1016/j.apmr.2007.05.005

Archives of Physical Medicine and Rehabilitation
Volume 88, Issue 8 , Pages 979-983, August 2007

Article Tools