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Methicillin-resistant Staphylococcus aureus colonization in a pediatric intensive care unit: Risk factors
American Journal of Infection Control 40 (2012) 118-22
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American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Major article
Methicillin-resistant Staphylococcus aureus colonization in a pediatric intensive care unit: Risk factors Ira N. Horowitz MD a, *, Elizabeth Baorto MD a, Tuesday Cirillo RN a, Jennifer Davis MD b a b
Department of Pediatrics, Goryeb Children’s Hospital, Morristown Memorial Hospital, Morristown, NJ Department of Pediatrics, Pediatric Critical Care, Broward General Hospital, Fort Lauderdale, FL
Key Words: Methicillin-resistant Staphylococcus aureus Colonization
Background: Both methicillin-resistant Staphylococcus aureus (MRSA) and penicillin-resistant Streptococcus pneumoniae have become significant causes of disease, both in health care and community settings. Objectives: All patients admitted to our pediatric intensive care unit (PICU) currently had a rapid test for methicillin-resistant Staphylococcus aureus (MRSA) performed as per hospital guidelines. This study looked at risk factors for colonization. Methods: Nasal swabs were tested for MRSA on all admissions to the PICU from May 2008 to September 2009 using polymerase chain reaction as per hospital guidelines. All patients enrolled were placed in either a MRSA-positive or a MRSA-negative group, which were compared with each other. Risk factors were assessed from a questionnaire and the resident history. Results: The prevalence of MRSA colonization in our study was 4.5%. Six hundred sixty-six patients were negative for MRSA, and 31 were positive. Patients in the MRSA colonization group were younger, more likely had family (household members) employed in medicine, and were more likely hospitalized or had undergone surgery within the previous 12 months. Prolonged neonatal intensive care unit stay (>1 week) was associated with MRSA colonization (P < .001). Conclusion: The percentage of patients positive for MRSA admitted to a PICU is low. Recent exposure to the health care system, especially a stay in the neonatal intensive care unit, is associated with an increased risk of colonization. Copyright Ó 2012 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
The state of New Jersey implemented a law in 2007 that all patients admitted to an intensive care unit were to be screened for colonization with methicillin-resistant Staphylococcus aureus (MRSA). Both MRSA and penicillin-resistant Streptococcus pneumoniae have become significant causes of disease forcing practitioners to empirically treat infections with vancomycin before culture results become available. MRSA is now a serious cause of surgical wound and soft-tissue infections, the latter typically an outpatient problem. MRSA infections are further categorized as either community-associated MRSA (CA-MRSA) or health careassociated MRSA (HA-MRSA).1 The criteria for CA-MRSA are as follows:
Diagnosis of MRSA was made in the outpatient setting or by a culture positive for MRSA within 48 hours after admission to the hospital; no medical history of MRSA infection or colonization; no medical history in the past year of: B Hospitalization; B admission to a nursing home, skilled nursing facility, or hospice; B dialysis; or B surgery; no permanent indwelling catheters or medical devices that pass through the skin into the body.
* Address correspondence to Ira N. Horowitz, MD, Department of Pediatrics Goryeb Children’s Hospital, Morristown Memorial Hospital, Pediatric Critical Care (Box 89), 100 Madison Ave, P.O. Box 1956, Morristown, NJ 07962-1956. E-mail address: [email protected] (I.N. Horowitz). Conflicts of interest: None to report.
There are marked clinical and genetic characteristics between HA-MRSA and CA-MRSA. S aureus gains its resistance to b-lactams via a gene complex known as staphylococcal cassette chromosome mec (SCCmec), which contains the mecA methicillin-resistance gene.
0196-6553/$36.00 - Copyright Ó 2012 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. doi:10.1016/j.ajic.2011.03.027
I.N. Horowitz et al. / American Journal of Infection Control 40 (2012) 118-22
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Table 1 Risk factors for MRSA colonization in PICU patients Factor Sex Originy Diagnosis groupz Indwelling catheterx Chronic disease Hospital/surgery <12 mo Antibiotics <6 mo Sports team Family employed in medicine Day care Skin infection Eczema ED <1 mo Nosocomial infection Prolonged NICU stay <12-mo agek
MRSAþ, n ¼ 31
MRSA, n ¼ 660
P value*
M ¼ 20 (65); F ¼ 11 (35) ED ¼ 24 (77), floor ¼ 3 (10), OR ¼ 2 (6), other ¼ 2 (6) Neuro ¼ 3 (10), NS ¼ 2 (6), other ¼ 9 (29), resp ¼ 15 (48), trauma ¼ 2 (6) Yes ¼ 2 (6), no ¼ 29 (94) Yes ¼ 12 (39), no ¼ 19 (61) Yes ¼ 13 (42), no ¼ 18 (58) Yes ¼ 15 (48), no ¼ 16 (52) Yes ¼ 4 (13), no ¼ 27 (87) Yes ¼ 9 (29), no ¼ 22 (71) Yes ¼ 8 (26), no ¼ 23 (74) Yes ¼ 0 (0), no ¼ 31 (100) Yes ¼ 5 (16), no ¼ 26 (84) Yes ¼ 3 (10), no ¼ 28 (90) Yes ¼ 1 (<1), no ¼ 30 (99) Yes ¼ 9 (82), no ¼ 2 (18)
M ¼ 399 (60); F ¼ 261 (40) ED ¼ 476 (72), floor ¼ 76 (12), OR ¼ 85 (13), other ¼ 23 (3) Neuro ¼ 79 (12), NS ¼ 75 (11), other ¼ 197 (30), resp ¼ 184 (28), trauma ¼ 125 (19) Yes 43 (7), no 617 (93) Yes 277 (42), no 383 (58) Yes ¼ 234 (35), no ¼ 426 (65) Yes ¼ 292 (44), no ¼ 368 (56) Yes ¼ 163 (25), no ¼ 497 (75) Yes ¼ 81 (12), no ¼ 579 (88) Yes ¼ 153 (23), no ¼ 507 (77) Yes ¼ 28 (4), no ¼ 632 (96) Yes ¼ 106 (16), no ¼ 554 (84) Yes ¼ 134 (20), no ¼ 526 (80) Yes ¼ 6 (2), no ¼ 644 (98) Yes ¼ 26 (26), no ¼ 74 (74)
.65 .60 .11 1.00 .034 .011 .42 .13 .012 .74 .63 1.00 .15 .53 <.001
NOTE. Percentiles are in parenthesis. F, female; M, male; neuro, neurological; NS, neurosurgical; resp, respiratory. *c2 or Fisher exact test; colonized PICU patients compared with uncolonized PICU patients. y Origin: emergency department, operating room, floor, other. z Diagnosis groups analyzed where those with most common reason for admission: neurologic, neurosurgical, respiratory, trauma, other; percentages are in parenthesis. x Tracheostomy, ventriculoperitoneal shunt, baclofen pump, long-term venous access (PICC, port-a-cath, Broviac/Hickman catheter). k N ¼ 11 MRSAþ, n ¼ 100 MRSA.
These DNA cassettes vary between CA-MRSA and HA-MRSA. Whereas CA-MRSA has been found to be less resistant to antibiotics, it is also more virulent because of production of the cytotoxin Panton-Valentine leukocidin and capable of causing a spectrum of illnesses. More than 95% of Panton-Valentine leukocidin-positive MRSA strain contain SCCmec IVa.2 However, as more patients are hospitalized with CA-MRSA, the distinction between which strains are community in origin and which are hospital acquired has become blurred. Established risk factors for MRSA infection in adults include recent hospitalization or surgery, stay at long-term care facility, history of prolonged antibiotic use, injection drug use, indwelling catheters, or chronic illnesses.3 Risk factors for infection and colonization in children have not been studied to the same extent as in adults. Our pediatric intensive care unit (PICU) implemented universal screening with a nasal probe, and positive patients were decolonized with intranasal antibiotics. Whether this strategy prevents the outbreak of nosocomial and postoperative infections has not been determined. METHODS Goryeb Children’s Hospital at Morristown Memorial Hospital is a 3-floor, community-based tertiary pediatric facility providing care from birth to age 21 years. The PICU has 9 private rooms, and the pediatric inpatient floor has 18 rooms and 26 beds, both located on the third level. All patients admitted to the PICU were eligible for the study. All patients were screened for MRSA from a nasal specimen obtained by the bedside nurse or respiratory therapist using an S/P Brand CultureSwab (Cardinal Health, McGaw Park, IL) unto a Remel Spectra MRSA plate (Remel, Lenexa, KS). This is a qualitative detection system using a differential chromogenic medium that yields a denim blue color as a result of phosphatase activity, an enzyme present in all MRSA. In addition, antibacterial compounds in the medium inhibit the growth of a wide variety of competitor organisms. Patients were initially placed in contact isolation, which was discontinued once the screen returned a negative result. Those
found to be colonized continued with contact precautions combined with decolonization by intranasal mupirocin. Exclusion criteria were an inpatient stay at our hospital or a referring hospital >24 hours before transfer to the PICU. The Institutional Review Board waived the need for informed consent. Risk factors were determined from a questionnaire that the admitting nurse asked of the primary caregivers in addition to the routine resident history. This questionnaire supplemented demographic data and medical data. The patient’s medical record was also reviewed retrospectively. All statistical analyses were performed using MINITAB (MINITAB Release 15.1.1.0.; Minitab Inc, State College, PA). Those found to be colonized with MRSA were compared with those who were not colonized using c2 and Fisher exact tests. Multivariate logistic regression was used in the analysis of risk factors. RESULTS There were 732 admission to the PICU from May 2008 to September 2009, of which 31 were MRSA positive and 660 MRSA negative; 41 patients were excluded for the following reasons: an indeterminate result, an inadequate specimen, a missing questionnaire, or an inpatient stay >24 hours before arrival to PICU (Tables 1 and 2). Patients in the MRSA colonized group were younger (mean standard deviation age in the MRSA colonized group ¼ 68.9 76.3 months vs 101.3 77.8 months in the not colonized group), P ¼ .027. The results in Tables 1 and 2 show that patients whose family (household members) was employed in medicine had a significantly higher risk of MRSA infection compared with those not employed in medicine (odds ratio [OR], 2.79; P ¼ .016). Older age was marginally associated with lower risk of MRSA infection (OR, 0.95; per 10 months increase; P ¼ .074). Patients who were hospitalized or who had surgery within 12 months had a significantly higher risk of MRSA infection (OR, 2.95; P ¼.006). Those children with chronic disease had a higher risk of colonization (6%) than those without underlying medical conditions (3%) (P ¼ .034). Patients with an emergency department visit within the month prior to admission had a significantly lower risk of MRSA infection compared with others by multivariate logistic regression (OR, 0.26; P ¼ .033).
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Table 2 Multivariate logistic regression model for MRSA colonization Factor Age (per 10 mo) Gender Hospital/surgery within 12 mo Employed in medicine ED < 1 mo
Mean or %
OR
CI
P value*
99.9 39.4 36.5 13.0 19.8
0.95 0.80 2.95 2.79 0.26
0.90-1.00 0.37-1.72 1.37-6.34 1.21-6.42 0.07-0.90
.074 .56 .006 .016 .033
NOTE. Table 2 includes factors with a P value of 0.1 with the exception of gender, which was forced into the model regardless of its P value. CI, 95% confidence interval; ED, emergency department. *A value of P < .05 indicates significance.
There were 111 patients of age <12 months who were enrolled in our study. We hypothesized, in this age group, that a lengthy neonatal intensive care unit (NICU) course might influence colonization rate. In this subgroup, 26 of 35 (74%) babies with a prolonged NICU stay (>1 week) were colonized (P < .001). DISCUSSION CA-MRSA is responsible for many serious skin, soft-tissue, and severe lung infections. Up to 75% of S aureus isolates are CA-MRSA in certain areas of the country.4 There is no standard definition of CA-MRSA infection as compared with hospital-acquired MRSA. Typically, a MRSA infection is considered community associated if there are no known or suspected risk factors in the host. Analysis of MRSA isolates is not performed on most inpatients. MRSA strains in the community have a different resistance and virulence pattern than nosocomial isolates using DNA sequencing and polymerase chain reaction analysis. CA-MRSA isolates tend to be susceptible to antimicrobial classes other than penicillin, typically clindamycin and trimethoprim-sulfamethoxazole. However, a recent study utilizing molecular testing identified strains historically associated with community-associated disease outbreaks from cultures in both hospital-onset and community-onset health care-associated infections. Therefore, definitions of CA-MRSA may soon not be applicable.5 The data on the incidence of MRSA infections in children are conflicting and scarce. A Centers for Disease Control and Prevention study that included outpatients with health care exposure over a 4-year period from 2005 through 2008 in 9 diverse metropolitan areas found the incidence low and minimally changed in children.6 In contrast, a retrospective, observational study of MRSA infections using a database from 140 freestanding US children’s hospitals showed an increase from 6.7 cases per 1,000 admissions in 2002 to 21.1 cases per 1,000 admissions in 2007, predominately of skin and soft-tissue infections.7 Investigators of hospitalized children in central New York reported an increased prevalence of invasive Staphylococcus aureus infections from 35.8 to 47.8 of 10,000 pediatric admissions between the periods of 1996 to 1999 and 2003 to 2006. MRSA prevalence also increased, from an observed frequency of 1.0 to 7.9 of every 10,000 pediatric admissions, although methicillinsensitive S aureus (MSSA) prevalence remained constant. Nevertheless, MRSA still only accounted for 10% of invasive S aureus infections.8 What seems to be a more consistent trends is the increasing proportion of Staphylococcal infections caused by MRSA in both the inpatient and outpatient population regardless of the overall incidence of Staphylococcal infections.8,9 An analysis of 824,307 S aureus isolates in The Surveillance Network showed an increase in MRSA from 33% of all S aureus (MRSA and MSSA) infections in 1998 in all age groups to 54% by 2007, with CA-MRSA accounting for less than 5% of all S aureus infections in children under age 15 years in 1998 but 45% a decade later.10 By 2007, 82% of all MRSA infections in
children under age 15 years had the CA-MRSA phenotype. Contradicting this trend was a study in a suburban community hospital pediatric emergency department where the percentage of MRSA isolates of cultured simple abscesses remained at 30% from 2004 to 2007 without an increase relative to MSSA.11 In a large pediatric study, Fritz et al12 followed 1,300 children for skin and soft tissue infection (SSTIs) up to 12 months after a prevalence study measuring S aureus nasal colonization finding 56 of 708 (8.1%) respondents to a survey reported an SSTI during the initial 6-month interval. SSTI developed in 6 of 26 (23%) children colonized with MRSA, 16 of 194 (8%) children colonized with methicillin-sensitive S aureus, and 34 of 474 (7%) not colonized with S aureus (MRSA vs not MRSA, univariate analysis, P ¼ .014). In multivariable analysis, factors associated with SSTI included history of SSTI in the child during the year preceding enrollment (P < .01) and SSTI in household contacts during the follow-up interval (P < .01). Whereas univariate analysis identified baseline MRSA colonization as a significant risk factor for subsequent SSTI both till 6 months and 12 months after a positive nasal swab in the study participants, it was of borderline significance in multivariate analysis (P ¼ .076, P ¼ .063, respectively). McNamara et al13 did not find an increase in nasal or skin staphylococcal colonization among caretakers of children with community-associated SSTI. Family and personal histories of community associated SSTI were the only identified risk factors for developing this infection. However, in a study of Staphylococcal colonization from Israel, parental carriage with MRSA was not associated with MRSA carriage in young children.14 Of 13 MRSA colonized individuals (4 children and 9 parents), there was only 1 concordant pair of a child and his parent. Previous health care interaction was documented in 8 of the 13 patients, with the majority of individuals having hospitalassociated strains. A prospective study of MRSA colonization in children scheduled for elective surgery showed 28% colonization but less than 1% wound infection.15 Colonization rate and infections somewhat parallel rate each other. Colonization rates, usually reported for outpatients, not only vary country to country, but even within different regions of the United States. The rate of colonization of MRSA in 1,300 ambulatory children was 2.4% and, for MSSA, 25.5% in the St. Louis metropolitan area.16 In children 3 months to < 7 years of age seen for well child or sick visits in primary care offices in Massachusetts, the prevalence of S aureus and MRSA colonization remained stable between 20032004 and 2006-2007 (MSSA and MRSA, 14.6% vs 14.1%, respectively), (MRSA, 0.2% vs 0.9%, P ¼ .09) among children <7 years.17 At a university-based ambulatory clinic in Illinois for children less than 5 years, the MRSA colonization rate was 1.7%.18 Investigators in Tennessee reported an increasing incidence of MRSA colonization in ambulatory children from .8% to 9.2% from 2001 to 2004.19 For inpatients, colonization rate also vary geographically. The rate of nasal carriage of S aureus in children admitted to hospital in Switzerland was recently 41%, although the rate for MRSA was <1%.20 At Driscoll Children’s in Texas, 22% of children upon admission were colonized with MRSA, with total S aureus colonization at 36 %.21 A US study published involving a PICU determined a MRSA colonization rate (surveillance nasal culture or clinical culture with 3 days of admission) similar to ours of 6.0%.22 In this population, a reduction to a 50% rate of colonization occurred rapidly (in <1 month). The same investigators, when screening 979 PICU patients (65% of admissions) weekly by a nasal specimen, discovered 42 (4.3%) who were colonized with MRSA. Of note, admission surveillance cultures were not obtained.23 Investigators recently discovered pharyngeal screening of S aureus in neonates and children in ICUs to be more sensitive than nasal screening (P < .0001).24 Because their MRSA colonization rate was only 3.6%, the higher sensitivity of pharyngeal screening was
I.N. Horowitz et al. / American Journal of Infection Control 40 (2012) 118-22
not statistically significant for this subgroup. In a study of colonization of adult patients presenting to the emergency department, 5% were MRSA colonized, 80% with extranasal MRSA, and 45% exclusively with extranasal MRSA.25 Dental investigators found that S aureus nasal screening was more effective than pharyngeal screening, with nasal screening missing some colonized patients.26 For newborns and young children, a review of the literature found that intestinal colonization with MRSA was in 1% to 2% of patients screened, with higher rates in the first 6 months of life.27 Therefore, current screening methods may underestimate the true colonization rate of MRSA using the nasal site alone. Fritz et al16 investigating risk factors for MRSA and MSSA colonization in ambulatory healthy children in St. Louis area found employment of household members in health care, antibiotic usage, hospitalization or surgery in the prior year, and emergency department or urgent care visit in past 6 months to be significant by univariate analysis. Surprisingly, colonization was less likely in children less than 5 years who attended day care (OR, .10). Factors that were not found to be significant for colonization included sports participation, past skin infection in either the child or a family member, a family member with eczema, and chronic health problems. Creech et al19 only found family members working in a hospital to be a risk factors for MRSA colonization. Our data also support employment of household members in a medical setting as a risk factor for colonization. Although MRSA is considered a disease of households, in an outpatient Israeli study of parents and their children (<40 months) where 13 individuals were found to have the isolate, there was only 1 pair of a child and his parent who were colonized.14 In a study at a university-based ambulatory clinic in a population less than 5 years of age, factors associated with colonization with S aureus were attending day care 5 days/week and prolonged antibiotic use, at levels of significance of <.05 and <.1, respectively.28 We found age, hospitalization within the past year, employment of household members in a medical setting, and visit to emergency department within the past 1 month to be risk factors. Eczema was not a risk factor for colonization in our study, in contrast to other investigators.29 Review of the literature also suggests that risk factors for MSSA may not necessarily be the same as for MRSA. There is sparse data on eradication of MRSA colonization in children. There is little evidence, however, that decolonization reduces the risk of more meaningful end points such as staphylococcal infection or transmission. Despite uncertainty regarding the efficacy of this approach, Robiscek et al30 showed that mupirocinbased decolonization therapy of MRSA-colonized inpatients temporarily reduced the risk of continued colonization but did not decrease the risk of subsequent infection, although there was a trend toward delayed infection. Although our numbers are small, prolonged NICU stay appears to be associated with acquisition of MRSA. This is borne out by larger studies such as at the Children’s National Medical Center in Washington, DC, from 2004 to 2008, where 2,280 newborns from a level II-IV NICU had nasal swab. Samples were obtained from study patients on admission and weekly thereafter during their stay. One hundred ninety-one neonates (8.4%) were colonized or infected with MRSA, which was associated with significant morbidity and financial burden but not independently with increased mortality.31 Supporting that hospitalization is associated with acquisition of MRSA is a study from a New Jersey NICU where only 1.9% of babies were colonized on admission screening, which rose to 9.3% during an outbreak.32 The proportion of S aureus isolates that were MRSA increased from 9.1% to 34.4%. Of note, using antibiotic sensitivity as a proxy for strain type, the proportion that were MRSA community phenotype did not vary significantly
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during the study period (P ¼ .3). This study also did not investigate colonization, whether on admission or any time subsequent. Our study of a PICU within a community hospital suggests that MRSA colonization is infrequent and that life-threatening MRSA infections are uncommon. The data suggest that children exposed to health care directly or indirectly are at higher risk of colonization. CONCLUSION Major foci of the health care system are reducing nosocomial infections and cost. It is unclear whether the use of routine surveillance improves the outcomes of children hospitalized in the PICU. Other unanswered questions are the value of decolonization to prevent recurrent SSTI, decolonization as an infection control measure, and decolonization as surgical prophylaxis in children. Acknowledgment The authors thank Rami Bustami, PhD, for statistical assistance. References 1. Center for Disease Control and Prevention. Community-associated MRSA information for clinicians. Available from: http://www.cdc.gov/ncidod/dhqp/ ar_mrsa_ca_clinicians.html#7. Accessed June 8, 2010. 2. Marquez S, Bellman G. Treating community and health-care associated MRSA. Is there a difference and does it matter? Society of Critical Care Connections, February 2009. Available from: http://www.sccm.org/Publications/Critical_ Connections/Archives/February2009/Pages/TreatingMRSA.aspx. Accessed March 9, 2010. 3. Naimi TS, LeDell KH, Como-Sabetti K, Borchardt SM, Boxrud DJ, Etienne J, et al. Comparison of community- and health careeassociated methicillin-resistant Staphylococcus aureus infection. JAMA 2003;290:2976-84. 4. Fergie J, Purcell K. The epidemic of methicillin-resistant Staphylococcus aureus colonization and infection in children: effects on the community, health systems, and physician practices. Pediatr Ann 2007;36:404-12. 5. Klevens RM, Morrison MA, Nadle J, Petit S, Gersham K. Invasive methicillinresistant Staphylococcus aureus infections in the United States. JAMA 2007; 298:1763-71. 6. Kallen AJ, Mu Y, Bulens S, Reingold A, Petit S, Gershman K, et al. Health careassociated invasive MRSA infections, 2005-2008. JAMA 2010;304:641-8. 7. Gerber JS, Coffin SE, Smathers SA, Zaoutis TE. Trends in the Incidence of methicillin-resistant Saphylococcus aureus infection in children’s hospitals in the United States. Clin Infect Dis 2009;49:65-71. 8. Suryadevara M, Moro MR, Rosenbaum PF, Kiska D, Riddell S, Weiner LB, et al. Incidence of invasive community-onset Staphylococcus aureus infections in children in Central New York. J Pediatr 2010;156. 152-4.e1. 9. Tucker ME. Keep tabs on CA-MRSA infection by obtaining cultures. Hospitalist News 2010;3:11. Available from: www.Ehospitalistnews.com. Accessed January 11, 2011. 10. Jancin B. CA-MRSA accounts for 66% of MRSA infections. Hospitalist News 2010; 3:5. Available from: www.Ehospitalistnews.com. Accessed January 11, 2011. 11. Kairam N, Siverman ME, Salo DF, Baorto E, Lee B, Amato CS. Cutaneous methicillin-resistant Staphyloccus aureus in a suburban community hospital pediatric emergency department. J Emerg Med. 2009 Jul 8. [Epub ahead of print.] 12. Fritz SA, Epplin EK, Garbutt EK, Storch GA. Skin infection in children colonized with community-associated methicillin-resistant Staphylococcus aureus. J Infect 2009;59:394-401. 13. McNamara WF, Flak MJ, Lee YH. Staphylococcal colonization of caretakers of children who have community-acquired skin and soft tissue infections. J Ped Surg 2010;45:1294-8. 14. Regev-Yochay G, Raz M, Carmeli Y, Shainberg B, Navon-Venezia S, Pinco E, et al. Parental Staphylococcus aureus carriage is associated with Staphylococcal carriage in young children. Pediatr Infect Dis J 2009;28:960-5. 15. Vegunta RK, Gray B, Wallace LJ, Mongkolrattanothai K, Mankin P, Stanfill AB, et al. A prospective study of methicillin-resistant Staphylococcus aureus colonization in children scheduled for elective surgery. J Pediatr Surg 2009;44: 1197-200. 16. Fritz SA, Garbutt J, Elward A, Shannon W, Storch GA. Prevalence of and risk factors for community-acquired methicillin-resistant and methicillin-sensitive Staphylococcus aureus colonization in children seen in a practice-based research network. Pediatrics 2008;121:1090-8. 17. Lee GM, Huang SS, Rifas-Shiman SL, Hinrichsen VL, Pelton SI, Kleinman K, et al. Epidemiology and risk factors for Staphylococcus aureus colonization in children in the post-PCV7 era. BMC Infect Dis 2009;9:110.
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18. Immergluck Cheng L, Kanungo S, Schwartz A, McIntyre A, Schreckenberger PC, Diaz PS. Prevalence of Streptococcus pneumoniae and Staphylococcus aureus nasopharyngeal colonization in healthy children in the United States. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2870090/. Accessed January 11, 2011. 19. Creech II CB, Kernodle DS, Alsentzer A, Wilson C, Edwards KM. Increasing rates of nasal carriage of methicillin-resistant Staphylococcus aureus in healthy children. Pediatr Infect Dis J 2005;24:617-21. 20. Heininger U, Datta F, Gervaix A, Schaad UB, Berger C, Vaudaux B, et al. Prevalence of nasal colonization with methicillin-resistant Staphylococcus aureus (MRSA) in children: a multicenter cross-sectional study. Pediatr Infect Dis J 2007;26:544-6. 21. Alfaro C, Mascher-Denen M, Fergie J, Purcell K. Prevalence of methicillinresistant Staphylococcus aureus nasal carriage in patients admitted to Driscoll Children’s Hospital. Pediatr Infect Dis J 2006;25:459-61. 22. Milstone AM, Carroll KC, Ross T, Shangraw KA, Perl TM. Communityassociated methicillin-resistant Staphylococcus aureus strains in pediatric intensive care unit. Available from: www.cdc.gov/eid. Accessed January 11, 2011. 23. Milstone AM, Song X, Beers C, Berkowitz I, Carroll KC, Perl TM. Unrecognized burden of methicillin-resistant Staphylococcus aureus and vancomycinresistant Enterococcus Carriage in the pediatric intensive care unit. Infect Control Hosp Epidemiol 2008;29:1174-6. 24. Nakamura MM, McAdam AJ, Sandora TJ, Moreira KR, Lee GM. Higher prevalence of pharyngeal than nasal Staphylococcus aureus carriage in pediatric intensive care units. J Clin Microbiol 2010;48:2957-9. 25. Schechter-Perkins EM, Mitchell PM, Murray KA, Rubin-Smith JE, Weir S, Gupta K. Prevalence and predictors of nasal and extranasal staphylococcal
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Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Major article
Methicillin-resistant Staphylococcus aureus colonization in a pediatric intensive care unit: Risk factors Ira N. Horowitz MD a, *, Elizabeth Baorto MD a, Tuesday Cirillo RN a, Jennifer Davis MD b a b
Department of Pediatrics, Goryeb Children’s Hospital, Morristown Memorial Hospital, Morristown, NJ Department of Pediatrics, Pediatric Critical Care, Broward General Hospital, Fort Lauderdale, FL
Key Words: Methicillin-resistant Staphylococcus aureus Colonization
Background: Both methicillin-resistant Staphylococcus aureus (MRSA) and penicillin-resistant Streptococcus pneumoniae have become significant causes of disease, both in health care and community settings. Objectives: All patients admitted to our pediatric intensive care unit (PICU) currently had a rapid test for methicillin-resistant Staphylococcus aureus (MRSA) performed as per hospital guidelines. This study looked at risk factors for colonization. Methods: Nasal swabs were tested for MRSA on all admissions to the PICU from May 2008 to September 2009 using polymerase chain reaction as per hospital guidelines. All patients enrolled were placed in either a MRSA-positive or a MRSA-negative group, which were compared with each other. Risk factors were assessed from a questionnaire and the resident history. Results: The prevalence of MRSA colonization in our study was 4.5%. Six hundred sixty-six patients were negative for MRSA, and 31 were positive. Patients in the MRSA colonization group were younger, more likely had family (household members) employed in medicine, and were more likely hospitalized or had undergone surgery within the previous 12 months. Prolonged neonatal intensive care unit stay (>1 week) was associated with MRSA colonization (P < .001). Conclusion: The percentage of patients positive for MRSA admitted to a PICU is low. Recent exposure to the health care system, especially a stay in the neonatal intensive care unit, is associated with an increased risk of colonization. Copyright Ó 2012 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
The state of New Jersey implemented a law in 2007 that all patients admitted to an intensive care unit were to be screened for colonization with methicillin-resistant Staphylococcus aureus (MRSA). Both MRSA and penicillin-resistant Streptococcus pneumoniae have become significant causes of disease forcing practitioners to empirically treat infections with vancomycin before culture results become available. MRSA is now a serious cause of surgical wound and soft-tissue infections, the latter typically an outpatient problem. MRSA infections are further categorized as either community-associated MRSA (CA-MRSA) or health careassociated MRSA (HA-MRSA).1 The criteria for CA-MRSA are as follows:
Diagnosis of MRSA was made in the outpatient setting or by a culture positive for MRSA within 48 hours after admission to the hospital; no medical history of MRSA infection or colonization; no medical history in the past year of: B Hospitalization; B admission to a nursing home, skilled nursing facility, or hospice; B dialysis; or B surgery; no permanent indwelling catheters or medical devices that pass through the skin into the body.
* Address correspondence to Ira N. Horowitz, MD, Department of Pediatrics Goryeb Children’s Hospital, Morristown Memorial Hospital, Pediatric Critical Care (Box 89), 100 Madison Ave, P.O. Box 1956, Morristown, NJ 07962-1956. E-mail address: [email protected] (I.N. Horowitz). Conflicts of interest: None to report.
There are marked clinical and genetic characteristics between HA-MRSA and CA-MRSA. S aureus gains its resistance to b-lactams via a gene complex known as staphylococcal cassette chromosome mec (SCCmec), which contains the mecA methicillin-resistance gene.
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Table 1 Risk factors for MRSA colonization in PICU patients Factor Sex Originy Diagnosis groupz Indwelling catheterx Chronic disease Hospital/surgery <12 mo Antibiotics <6 mo Sports team Family employed in medicine Day care Skin infection Eczema ED <1 mo Nosocomial infection Prolonged NICU stay <12-mo agek
MRSAþ, n ¼ 31
MRSA, n ¼ 660
P value*
M ¼ 20 (65); F ¼ 11 (35) ED ¼ 24 (77), floor ¼ 3 (10), OR ¼ 2 (6), other ¼ 2 (6) Neuro ¼ 3 (10), NS ¼ 2 (6), other ¼ 9 (29), resp ¼ 15 (48), trauma ¼ 2 (6) Yes ¼ 2 (6), no ¼ 29 (94) Yes ¼ 12 (39), no ¼ 19 (61) Yes ¼ 13 (42), no ¼ 18 (58) Yes ¼ 15 (48), no ¼ 16 (52) Yes ¼ 4 (13), no ¼ 27 (87) Yes ¼ 9 (29), no ¼ 22 (71) Yes ¼ 8 (26), no ¼ 23 (74) Yes ¼ 0 (0), no ¼ 31 (100) Yes ¼ 5 (16), no ¼ 26 (84) Yes ¼ 3 (10), no ¼ 28 (90) Yes ¼ 1 (<1), no ¼ 30 (99) Yes ¼ 9 (82), no ¼ 2 (18)
M ¼ 399 (60); F ¼ 261 (40) ED ¼ 476 (72), floor ¼ 76 (12), OR ¼ 85 (13), other ¼ 23 (3) Neuro ¼ 79 (12), NS ¼ 75 (11), other ¼ 197 (30), resp ¼ 184 (28), trauma ¼ 125 (19) Yes 43 (7), no 617 (93) Yes 277 (42), no 383 (58) Yes ¼ 234 (35), no ¼ 426 (65) Yes ¼ 292 (44), no ¼ 368 (56) Yes ¼ 163 (25), no ¼ 497 (75) Yes ¼ 81 (12), no ¼ 579 (88) Yes ¼ 153 (23), no ¼ 507 (77) Yes ¼ 28 (4), no ¼ 632 (96) Yes ¼ 106 (16), no ¼ 554 (84) Yes ¼ 134 (20), no ¼ 526 (80) Yes ¼ 6 (2), no ¼ 644 (98) Yes ¼ 26 (26), no ¼ 74 (74)
.65 .60 .11 1.00 .034 .011 .42 .13 .012 .74 .63 1.00 .15 .53 <.001
NOTE. Percentiles are in parenthesis. F, female; M, male; neuro, neurological; NS, neurosurgical; resp, respiratory. *c2 or Fisher exact test; colonized PICU patients compared with uncolonized PICU patients. y Origin: emergency department, operating room, floor, other. z Diagnosis groups analyzed where those with most common reason for admission: neurologic, neurosurgical, respiratory, trauma, other; percentages are in parenthesis. x Tracheostomy, ventriculoperitoneal shunt, baclofen pump, long-term venous access (PICC, port-a-cath, Broviac/Hickman catheter). k N ¼ 11 MRSAþ, n ¼ 100 MRSA.
These DNA cassettes vary between CA-MRSA and HA-MRSA. Whereas CA-MRSA has been found to be less resistant to antibiotics, it is also more virulent because of production of the cytotoxin Panton-Valentine leukocidin and capable of causing a spectrum of illnesses. More than 95% of Panton-Valentine leukocidin-positive MRSA strain contain SCCmec IVa.2 However, as more patients are hospitalized with CA-MRSA, the distinction between which strains are community in origin and which are hospital acquired has become blurred. Established risk factors for MRSA infection in adults include recent hospitalization or surgery, stay at long-term care facility, history of prolonged antibiotic use, injection drug use, indwelling catheters, or chronic illnesses.3 Risk factors for infection and colonization in children have not been studied to the same extent as in adults. Our pediatric intensive care unit (PICU) implemented universal screening with a nasal probe, and positive patients were decolonized with intranasal antibiotics. Whether this strategy prevents the outbreak of nosocomial and postoperative infections has not been determined. METHODS Goryeb Children’s Hospital at Morristown Memorial Hospital is a 3-floor, community-based tertiary pediatric facility providing care from birth to age 21 years. The PICU has 9 private rooms, and the pediatric inpatient floor has 18 rooms and 26 beds, both located on the third level. All patients admitted to the PICU were eligible for the study. All patients were screened for MRSA from a nasal specimen obtained by the bedside nurse or respiratory therapist using an S/P Brand CultureSwab (Cardinal Health, McGaw Park, IL) unto a Remel Spectra MRSA plate (Remel, Lenexa, KS). This is a qualitative detection system using a differential chromogenic medium that yields a denim blue color as a result of phosphatase activity, an enzyme present in all MRSA. In addition, antibacterial compounds in the medium inhibit the growth of a wide variety of competitor organisms. Patients were initially placed in contact isolation, which was discontinued once the screen returned a negative result. Those
found to be colonized continued with contact precautions combined with decolonization by intranasal mupirocin. Exclusion criteria were an inpatient stay at our hospital or a referring hospital >24 hours before transfer to the PICU. The Institutional Review Board waived the need for informed consent. Risk factors were determined from a questionnaire that the admitting nurse asked of the primary caregivers in addition to the routine resident history. This questionnaire supplemented demographic data and medical data. The patient’s medical record was also reviewed retrospectively. All statistical analyses were performed using MINITAB (MINITAB Release 15.1.1.0.; Minitab Inc, State College, PA). Those found to be colonized with MRSA were compared with those who were not colonized using c2 and Fisher exact tests. Multivariate logistic regression was used in the analysis of risk factors. RESULTS There were 732 admission to the PICU from May 2008 to September 2009, of which 31 were MRSA positive and 660 MRSA negative; 41 patients were excluded for the following reasons: an indeterminate result, an inadequate specimen, a missing questionnaire, or an inpatient stay >24 hours before arrival to PICU (Tables 1 and 2). Patients in the MRSA colonized group were younger (mean standard deviation age in the MRSA colonized group ¼ 68.9 76.3 months vs 101.3 77.8 months in the not colonized group), P ¼ .027. The results in Tables 1 and 2 show that patients whose family (household members) was employed in medicine had a significantly higher risk of MRSA infection compared with those not employed in medicine (odds ratio [OR], 2.79; P ¼ .016). Older age was marginally associated with lower risk of MRSA infection (OR, 0.95; per 10 months increase; P ¼ .074). Patients who were hospitalized or who had surgery within 12 months had a significantly higher risk of MRSA infection (OR, 2.95; P ¼.006). Those children with chronic disease had a higher risk of colonization (6%) than those without underlying medical conditions (3%) (P ¼ .034). Patients with an emergency department visit within the month prior to admission had a significantly lower risk of MRSA infection compared with others by multivariate logistic regression (OR, 0.26; P ¼ .033).
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Table 2 Multivariate logistic regression model for MRSA colonization Factor Age (per 10 mo) Gender Hospital/surgery within 12 mo Employed in medicine ED < 1 mo
Mean or %
OR
CI
P value*
99.9 39.4 36.5 13.0 19.8
0.95 0.80 2.95 2.79 0.26
0.90-1.00 0.37-1.72 1.37-6.34 1.21-6.42 0.07-0.90
.074 .56 .006 .016 .033
NOTE. Table 2 includes factors with a P value of 0.1 with the exception of gender, which was forced into the model regardless of its P value. CI, 95% confidence interval; ED, emergency department. *A value of P < .05 indicates significance.
There were 111 patients of age <12 months who were enrolled in our study. We hypothesized, in this age group, that a lengthy neonatal intensive care unit (NICU) course might influence colonization rate. In this subgroup, 26 of 35 (74%) babies with a prolonged NICU stay (>1 week) were colonized (P < .001). DISCUSSION CA-MRSA is responsible for many serious skin, soft-tissue, and severe lung infections. Up to 75% of S aureus isolates are CA-MRSA in certain areas of the country.4 There is no standard definition of CA-MRSA infection as compared with hospital-acquired MRSA. Typically, a MRSA infection is considered community associated if there are no known or suspected risk factors in the host. Analysis of MRSA isolates is not performed on most inpatients. MRSA strains in the community have a different resistance and virulence pattern than nosocomial isolates using DNA sequencing and polymerase chain reaction analysis. CA-MRSA isolates tend to be susceptible to antimicrobial classes other than penicillin, typically clindamycin and trimethoprim-sulfamethoxazole. However, a recent study utilizing molecular testing identified strains historically associated with community-associated disease outbreaks from cultures in both hospital-onset and community-onset health care-associated infections. Therefore, definitions of CA-MRSA may soon not be applicable.5 The data on the incidence of MRSA infections in children are conflicting and scarce. A Centers for Disease Control and Prevention study that included outpatients with health care exposure over a 4-year period from 2005 through 2008 in 9 diverse metropolitan areas found the incidence low and minimally changed in children.6 In contrast, a retrospective, observational study of MRSA infections using a database from 140 freestanding US children’s hospitals showed an increase from 6.7 cases per 1,000 admissions in 2002 to 21.1 cases per 1,000 admissions in 2007, predominately of skin and soft-tissue infections.7 Investigators of hospitalized children in central New York reported an increased prevalence of invasive Staphylococcus aureus infections from 35.8 to 47.8 of 10,000 pediatric admissions between the periods of 1996 to 1999 and 2003 to 2006. MRSA prevalence also increased, from an observed frequency of 1.0 to 7.9 of every 10,000 pediatric admissions, although methicillinsensitive S aureus (MSSA) prevalence remained constant. Nevertheless, MRSA still only accounted for 10% of invasive S aureus infections.8 What seems to be a more consistent trends is the increasing proportion of Staphylococcal infections caused by MRSA in both the inpatient and outpatient population regardless of the overall incidence of Staphylococcal infections.8,9 An analysis of 824,307 S aureus isolates in The Surveillance Network showed an increase in MRSA from 33% of all S aureus (MRSA and MSSA) infections in 1998 in all age groups to 54% by 2007, with CA-MRSA accounting for less than 5% of all S aureus infections in children under age 15 years in 1998 but 45% a decade later.10 By 2007, 82% of all MRSA infections in
children under age 15 years had the CA-MRSA phenotype. Contradicting this trend was a study in a suburban community hospital pediatric emergency department where the percentage of MRSA isolates of cultured simple abscesses remained at 30% from 2004 to 2007 without an increase relative to MSSA.11 In a large pediatric study, Fritz et al12 followed 1,300 children for skin and soft tissue infection (SSTIs) up to 12 months after a prevalence study measuring S aureus nasal colonization finding 56 of 708 (8.1%) respondents to a survey reported an SSTI during the initial 6-month interval. SSTI developed in 6 of 26 (23%) children colonized with MRSA, 16 of 194 (8%) children colonized with methicillin-sensitive S aureus, and 34 of 474 (7%) not colonized with S aureus (MRSA vs not MRSA, univariate analysis, P ¼ .014). In multivariable analysis, factors associated with SSTI included history of SSTI in the child during the year preceding enrollment (P < .01) and SSTI in household contacts during the follow-up interval (P < .01). Whereas univariate analysis identified baseline MRSA colonization as a significant risk factor for subsequent SSTI both till 6 months and 12 months after a positive nasal swab in the study participants, it was of borderline significance in multivariate analysis (P ¼ .076, P ¼ .063, respectively). McNamara et al13 did not find an increase in nasal or skin staphylococcal colonization among caretakers of children with community-associated SSTI. Family and personal histories of community associated SSTI were the only identified risk factors for developing this infection. However, in a study of Staphylococcal colonization from Israel, parental carriage with MRSA was not associated with MRSA carriage in young children.14 Of 13 MRSA colonized individuals (4 children and 9 parents), there was only 1 concordant pair of a child and his parent. Previous health care interaction was documented in 8 of the 13 patients, with the majority of individuals having hospitalassociated strains. A prospective study of MRSA colonization in children scheduled for elective surgery showed 28% colonization but less than 1% wound infection.15 Colonization rate and infections somewhat parallel rate each other. Colonization rates, usually reported for outpatients, not only vary country to country, but even within different regions of the United States. The rate of colonization of MRSA in 1,300 ambulatory children was 2.4% and, for MSSA, 25.5% in the St. Louis metropolitan area.16 In children 3 months to < 7 years of age seen for well child or sick visits in primary care offices in Massachusetts, the prevalence of S aureus and MRSA colonization remained stable between 20032004 and 2006-2007 (MSSA and MRSA, 14.6% vs 14.1%, respectively), (MRSA, 0.2% vs 0.9%, P ¼ .09) among children <7 years.17 At a university-based ambulatory clinic in Illinois for children less than 5 years, the MRSA colonization rate was 1.7%.18 Investigators in Tennessee reported an increasing incidence of MRSA colonization in ambulatory children from .8% to 9.2% from 2001 to 2004.19 For inpatients, colonization rate also vary geographically. The rate of nasal carriage of S aureus in children admitted to hospital in Switzerland was recently 41%, although the rate for MRSA was <1%.20 At Driscoll Children’s in Texas, 22% of children upon admission were colonized with MRSA, with total S aureus colonization at 36 %.21 A US study published involving a PICU determined a MRSA colonization rate (surveillance nasal culture or clinical culture with 3 days of admission) similar to ours of 6.0%.22 In this population, a reduction to a 50% rate of colonization occurred rapidly (in <1 month). The same investigators, when screening 979 PICU patients (65% of admissions) weekly by a nasal specimen, discovered 42 (4.3%) who were colonized with MRSA. Of note, admission surveillance cultures were not obtained.23 Investigators recently discovered pharyngeal screening of S aureus in neonates and children in ICUs to be more sensitive than nasal screening (P < .0001).24 Because their MRSA colonization rate was only 3.6%, the higher sensitivity of pharyngeal screening was
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not statistically significant for this subgroup. In a study of colonization of adult patients presenting to the emergency department, 5% were MRSA colonized, 80% with extranasal MRSA, and 45% exclusively with extranasal MRSA.25 Dental investigators found that S aureus nasal screening was more effective than pharyngeal screening, with nasal screening missing some colonized patients.26 For newborns and young children, a review of the literature found that intestinal colonization with MRSA was in 1% to 2% of patients screened, with higher rates in the first 6 months of life.27 Therefore, current screening methods may underestimate the true colonization rate of MRSA using the nasal site alone. Fritz et al16 investigating risk factors for MRSA and MSSA colonization in ambulatory healthy children in St. Louis area found employment of household members in health care, antibiotic usage, hospitalization or surgery in the prior year, and emergency department or urgent care visit in past 6 months to be significant by univariate analysis. Surprisingly, colonization was less likely in children less than 5 years who attended day care (OR, .10). Factors that were not found to be significant for colonization included sports participation, past skin infection in either the child or a family member, a family member with eczema, and chronic health problems. Creech et al19 only found family members working in a hospital to be a risk factors for MRSA colonization. Our data also support employment of household members in a medical setting as a risk factor for colonization. Although MRSA is considered a disease of households, in an outpatient Israeli study of parents and their children (<40 months) where 13 individuals were found to have the isolate, there was only 1 pair of a child and his parent who were colonized.14 In a study at a university-based ambulatory clinic in a population less than 5 years of age, factors associated with colonization with S aureus were attending day care 5 days/week and prolonged antibiotic use, at levels of significance of <.05 and <.1, respectively.28 We found age, hospitalization within the past year, employment of household members in a medical setting, and visit to emergency department within the past 1 month to be risk factors. Eczema was not a risk factor for colonization in our study, in contrast to other investigators.29 Review of the literature also suggests that risk factors for MSSA may not necessarily be the same as for MRSA. There is sparse data on eradication of MRSA colonization in children. There is little evidence, however, that decolonization reduces the risk of more meaningful end points such as staphylococcal infection or transmission. Despite uncertainty regarding the efficacy of this approach, Robiscek et al30 showed that mupirocinbased decolonization therapy of MRSA-colonized inpatients temporarily reduced the risk of continued colonization but did not decrease the risk of subsequent infection, although there was a trend toward delayed infection. Although our numbers are small, prolonged NICU stay appears to be associated with acquisition of MRSA. This is borne out by larger studies such as at the Children’s National Medical Center in Washington, DC, from 2004 to 2008, where 2,280 newborns from a level II-IV NICU had nasal swab. Samples were obtained from study patients on admission and weekly thereafter during their stay. One hundred ninety-one neonates (8.4%) were colonized or infected with MRSA, which was associated with significant morbidity and financial burden but not independently with increased mortality.31 Supporting that hospitalization is associated with acquisition of MRSA is a study from a New Jersey NICU where only 1.9% of babies were colonized on admission screening, which rose to 9.3% during an outbreak.32 The proportion of S aureus isolates that were MRSA increased from 9.1% to 34.4%. Of note, using antibiotic sensitivity as a proxy for strain type, the proportion that were MRSA community phenotype did not vary significantly
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during the study period (P ¼ .3). This study also did not investigate colonization, whether on admission or any time subsequent. Our study of a PICU within a community hospital suggests that MRSA colonization is infrequent and that life-threatening MRSA infections are uncommon. The data suggest that children exposed to health care directly or indirectly are at higher risk of colonization. CONCLUSION Major foci of the health care system are reducing nosocomial infections and cost. It is unclear whether the use of routine surveillance improves the outcomes of children hospitalized in the PICU. Other unanswered questions are the value of decolonization to prevent recurrent SSTI, decolonization as an infection control measure, and decolonization as surgical prophylaxis in children. Acknowledgment The authors thank Rami Bustami, PhD, for statistical assistance. References 1. Center for Disease Control and Prevention. Community-associated MRSA information for clinicians. Available from: http://www.cdc.gov/ncidod/dhqp/ ar_mrsa_ca_clinicians.html#7. Accessed June 8, 2010. 2. Marquez S, Bellman G. Treating community and health-care associated MRSA. Is there a difference and does it matter? Society of Critical Care Connections, February 2009. Available from: http://www.sccm.org/Publications/Critical_ Connections/Archives/February2009/Pages/TreatingMRSA.aspx. Accessed March 9, 2010. 3. Naimi TS, LeDell KH, Como-Sabetti K, Borchardt SM, Boxrud DJ, Etienne J, et al. Comparison of community- and health careeassociated methicillin-resistant Staphylococcus aureus infection. JAMA 2003;290:2976-84. 4. Fergie J, Purcell K. The epidemic of methicillin-resistant Staphylococcus aureus colonization and infection in children: effects on the community, health systems, and physician practices. Pediatr Ann 2007;36:404-12. 5. Klevens RM, Morrison MA, Nadle J, Petit S, Gersham K. Invasive methicillinresistant Staphylococcus aureus infections in the United States. JAMA 2007; 298:1763-71. 6. Kallen AJ, Mu Y, Bulens S, Reingold A, Petit S, Gershman K, et al. Health careassociated invasive MRSA infections, 2005-2008. JAMA 2010;304:641-8. 7. Gerber JS, Coffin SE, Smathers SA, Zaoutis TE. Trends in the Incidence of methicillin-resistant Saphylococcus aureus infection in children’s hospitals in the United States. Clin Infect Dis 2009;49:65-71. 8. Suryadevara M, Moro MR, Rosenbaum PF, Kiska D, Riddell S, Weiner LB, et al. Incidence of invasive community-onset Staphylococcus aureus infections in children in Central New York. J Pediatr 2010;156. 152-4.e1. 9. Tucker ME. Keep tabs on CA-MRSA infection by obtaining cultures. Hospitalist News 2010;3:11. Available from: www.Ehospitalistnews.com. Accessed January 11, 2011. 10. Jancin B. CA-MRSA accounts for 66% of MRSA infections. Hospitalist News 2010; 3:5. Available from: www.Ehospitalistnews.com. Accessed January 11, 2011. 11. Kairam N, Siverman ME, Salo DF, Baorto E, Lee B, Amato CS. Cutaneous methicillin-resistant Staphyloccus aureus in a suburban community hospital pediatric emergency department. J Emerg Med. 2009 Jul 8. [Epub ahead of print.] 12. Fritz SA, Epplin EK, Garbutt EK, Storch GA. Skin infection in children colonized with community-associated methicillin-resistant Staphylococcus aureus. J Infect 2009;59:394-401. 13. McNamara WF, Flak MJ, Lee YH. Staphylococcal colonization of caretakers of children who have community-acquired skin and soft tissue infections. J Ped Surg 2010;45:1294-8. 14. Regev-Yochay G, Raz M, Carmeli Y, Shainberg B, Navon-Venezia S, Pinco E, et al. Parental Staphylococcus aureus carriage is associated with Staphylococcal carriage in young children. Pediatr Infect Dis J 2009;28:960-5. 15. Vegunta RK, Gray B, Wallace LJ, Mongkolrattanothai K, Mankin P, Stanfill AB, et al. A prospective study of methicillin-resistant Staphylococcus aureus colonization in children scheduled for elective surgery. J Pediatr Surg 2009;44: 1197-200. 16. Fritz SA, Garbutt J, Elward A, Shannon W, Storch GA. Prevalence of and risk factors for community-acquired methicillin-resistant and methicillin-sensitive Staphylococcus aureus colonization in children seen in a practice-based research network. Pediatrics 2008;121:1090-8. 17. Lee GM, Huang SS, Rifas-Shiman SL, Hinrichsen VL, Pelton SI, Kleinman K, et al. Epidemiology and risk factors for Staphylococcus aureus colonization in children in the post-PCV7 era. BMC Infect Dis 2009;9:110.
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