Abstract
Background.
Staphylococcus aureus infections are increasing among pregnant and postpartum women and neonates, but risk factors for S. aureus colonization in pregnancy and the association between maternal colonization and infant infections are not well defined. We sought to identify risk factors for maternal S. aureus rectovaginal colonization and assess colonization as a risk factor for infections among mothers and infants.
Methods.
We conducted a retrospective cohort study of pregnant women and their infants. Demographic and clinical data, including S. aureus infections that occurred in mothers from 3 months before to 3 months after delivery and in infants during the first 3 months of life, were extracted from electronic medical records. Predictors for maternal S. aureus rectovaginal colonization were assessed through multivariable logistic regression analysis.
Results.
The cohort included 2702 women and 2789 infants. The prevalence of maternal rectovaginal colonization with methicillin-susceptible S. aureus and methicillin-resistant S. aureus (MRSA) was 13% and 0.7%. Independent predictors of colonization included multigravidity, human immunodeficiency virus seropositivity, and group B Streptococcus colonization. S. aureus colonization was associated with an increased risk of infection in mothers (odds ratio [OR], 3.5; 95% confidence interval [CI], 1.4–8.8) but not in their infants (OR, 1.9; 95% CI, .6–5.6). The frequency of S. aureus infections was 0.8% in mothers and 0.7% in infants.
Conclusions.
S. aureus rectovaginal colonization was associated with an increased risk of infections in women but not in their infants. The frequency of MRSA infections was low. These data suggest that routine MRSA screening of pregnant women may not be indicated.
Staphylococcus aureus infections are increasing in pregnant and postpartum women and in healthy neonates and infants hospitalized in neonatal intensive care units (NICUs) [1–4]. Much of this increase has been driven by a rise in methicillin-resistant S. aureus (MRSA), specifically community-associated (CA)–MRSA, which most commonly causes infections in patients without traditional risk factors [2, 3, 5]. S. aureus infections appear to be more frequent among individuals who are colonized with S. aureus in the anterior nares and other sites [6, 7].
S. aureus has been reported to colonize the vagina in 4%–22% of pregnant women [8–12]. The prevalence of MRSA rectovaginal colonization has been reported to range 0.5%–10% [8–12]. We previously conducted a prospective surveillance study of pregnant women undergoing routine screening for colonization with group B Streptococcus (GBS) [12]. The prevalence of methicillin-susceptible S. aureus (MSSA) rectovaginal colonization was 11.8%, and the prevalence of MRSA colonization was 0.6%. All 18 MRSA strains were CA-MRSA strains and 12 of 18 (75%) were the epidemic USA300 clone.
The factors that contribute to S. aureus rectovaginal colonization in pregnant women are not well understood. One study identified black race as an independent risk factor for MRSA rectovaginal colonization [10]. We identified younger age and GBS colonization as risk factors for S. aureus rectovaginal colonization but did not explore other demographic or maternal factors associated with S. aureus colonization [12]. A prior case-control study conducted among 117 women at our institution found that GBS colonization was a risk factor for MSSA rectovaginal colonization but was protective against MRSA colonization and that demographic factors and postpartum complications were not associated with colonization [13].
A few studies have examined the association between S. aureus colonization in pregnant women and the frequency of infections in women and/or their infants [9, 10, 14]. In one study, S. aureus colonization of the nares and/or vagina was not associated with an increased risk of S. aureus infections in the women, but infections in their infants were not assessed [9]. Another study did not demonstrate an increased risk of neonatal infections following neonatal S. aureus colonization in the first 48 hours of life, but maternal infections were not assessed [14]. Although vertical transmission has been proposed as a possible mechanism of maternal-to-infant transmission of MRSA [4, 10, 14, 15], the risk of developing early-onset neonatal sepsis caused by MRSA is not increased in infants born to MRSA-colonized women [10].
To date, the clinical significance of S. aureus rectovaginal colonization as a predictor of subsequent infection in mothers and their infants has not been systematically examined in a large cohort. The objectives of this study were to identify risk factors for S. aureus rectovaginal colonization, to assess maternal S. aureus colonization as a risk factor for infection among mothers and infants, and to determine the frequency of S. aureus infections in pregnant and postpartum women and their infants.
METHODS
Study Design and Subjects
We conducted a retrospective observational cohort study. Subjects included pregnant women screened for GBS and assessed for S. aureus rectovaginal colonization, as previously described, [12] who delivered an infant at NewYork-Presbyterian Hospital/Columbia University Medical Center (NYP/CUMC) and their infants. Women were screened from February 2009 to July 2009 and delivered their infants from February 2009 to November 2009. Women who delivered an infant at another institution (and their infants) were excluded. This study was approved by the Institutional Review Board at CUMC and was conducted in accordance with the ethical standards of the Helsinki Declaration. A waiver of informed consent was granted.
Study Procedures
As previously described, pregnant women in the cohort underwent routine screening for GBS at 35–37 weeks gestation with rectovaginal swabs [12] using established guidelines [16]. These specimens were cultured for S. aureus; 10 µL of the broth was streaked onto a selective differential chromogenic agar plate (BBL CHROMagar Staph aureus, BD Diagnostics) [12]. S. aureus was confirmed by latex agglutination (Staphaurex, Remel Europe), and methicillin susceptibility was determined by the cefoxitin disk diffusion screen [17].
Data Collection Procedures
The electronic medical records (EMRs) of pregnant women and their infants were reviewed by 2 members of the study team (K. T. and A. B.) who were blinded to maternal S. aureus colonization status. Demographic characteristics, prenatal and obstetrical history, including sexually transmitted infections, gravidity, parity, peripartum complications, and mode of delivery, and neonatal outcomes, including Apgar scores, birthweight, and disposition (eg, admission to the newborn nursery or NICU), were collected.
Identifying Staphylococcus aureus Infections
Both MSSA and MRSA infections were identified by positive clinical cultures for S. aureus and/or by International Classification of Diseases (ICD)–9 diagnosis codes pertaining to S. aureus infections, using previously validated ICD-9 codes [18]. To maximize ascertainment of S. aureus infections in infants, the clinical microbiology laboratory generated an epidemiology report of all positive S. aureus cultures sent from pediatric inpatient units, the pediatric emergency department (ED), and pediatric outpatient clinics from 1 February 2009 to 1 February 2010. Cultures were reviewed to identify infants born to women in the study cohort.
Case Definitions
A definite S. aureus infection was defined as isolation of S. aureus from a sterile site (eg, blood, cerebrospinal fluid) or from a nonsterile site (eg, wound, respiratory culture) in the presence of signs and symptoms of infection (eg, fever, erythema, purulent drainage). A probable S. aureus infection was defined if, in the absence of a positive culture, there were signs and symptoms of skin or soft tissue infection (SSTI), including postoperative infections and mastitis, and a clinical response to antistaphylococcal antibiotics was documented in the EMR.
Outcomes
In order to assess colonization as a risk factor for infection, the primary outcomes were S. aureus infections occurring from 3 months prior to delivery to 3 months after delivery in the mothers and S. aureus infections in their infants within the first 3 months of life. The secondary outcomes were perinatal complications including intrapartum maternal fever (>38°C), cesarean delivery, preterm birth, birthweight <2500 g, 5-minute Apgar <7, admission to the NICU, and readmission within 3 months after delivery.
Statistical Analysis
Multivariable logistic regression analysis was conducted to identify independent risk factors for maternal S. aureus rectovaginal colonization. Hierarchical model building was conducted, and the effect of each additional variable on the model was assessed using the −2 log-likelihood test. Odds ratios (OR) and 95% confidence intervals (CIs) were computed for each variable in the model. The χ2 test and Fisher's exact test were used to test for associations between categorical variables when appropriate. Student t test was used to analyze continuous variables. Statistical analysis was conducted using SAS version 9.1 software.
RESULTS
Of 2921 women included in the prior study of the prevalence of S. aureus rectovaginal colonization [12], the current study cohort consisted of 2702 women (93%) who delivered 2789 infants at our institution. The prevalence of maternal rectovaginal colonization with GBS, MSSA, and MRSA was 24%, 13% and 0.7%, respectively, among these 2702 women.
Risk Factors for Rectovaginal Colonization
The demographic and obstetrical characteristics associated with S. aureus colonization in the maternal cohort are shown in Table 1. In this univariate analysis, the factors most strongly associated with S. aureus rectovaginal colonization included black race, government insurance, being unmarried, multigravidity, GBS colonization, and human immunodeficiency virus (HIV) seropositivity. In the multivariable regression analysis, government insurance, multigravidity, HIV seropositivity, and GBS colonization were identified as independent risk factors for S. aureus rectovaginal colonization in the full model analysis (Table 2). Maternal S. aureus colonization status was not associated with adverse peripartum or neonatal outcomes (Table 3).
Table 1.
Univariate Analysis of Demographic and Clinical Risk Factors for Maternal Staphylococcus aureus Rectovaginal Colonization
| Characteristics | S. aureus Positive N = 340 No. (%) | S. aureus Negative N = 2362 No. (%) | OR (95% CI) | P Valuea |
|---|---|---|---|---|
| Maternal age (years) | ||||
| Mean, SD | 29.6 (6.6) | 30.4 (6.7) | … | .03 |
| ≤ 25 | 106 (31) | 672 (28) | 1.41 (1.05–1.89) | .02 |
| 26–35 | 176 (52) | 1147 (49) | 1.53 (1.10–2.11) | .01 |
| ≥ 36b | 58 (17) | 543 (23) | … | |
| Race/Ethnicity | ||||
| Hispanic | 143 (42) | 943 (40) | 1.57 (1.15–2.13) | .004 |
| Black (non-Hispanic) | 59 (17) | 297 (13) | 2.05 (1.41–2.99) | <.001 |
| Other | 86 (25) | 517 (22) | 1.75 (1.22–2.49) | .002 |
| White (non-Hispanic)b | 52 (15) | 595 (25) | … | |
| Insurance | ||||
| Government/Self pay | 235 (69) | 1280 (54) | 1.89 (1.48–2.41) | <.001 |
| Private | 105 (31) | 1082 (46) | … | |
| Marital Status | ||||
| Unmarriedc | 207 (61) | 1208 (51) | 1.50 (1.18–1.88) | <.001 |
| Married/Life partner | 133 (39) | 1154 (49) | … | |
| Gravidity | ||||
| Multigravid (≥2) | 262 (77) | 1591 (67) | 1.63 (1.25–2.13) | <.001 |
| Primigravid | 78 (23) | 771 (33) | … | |
| Parity | ||||
| Multiparous (≥1) | 192 (56) | 1183 (50) | 1.30 (1.03–1.62) | .03 |
| Nulliparous | 148 (44) | 1179 (50) | … | |
| GBS colonization | ||||
| Yes | 119 (35) | 518 (22) | 1.92 (1.50–2.44) | <.001 |
| No | 221 (65) | 1844 (78) | … | |
| HIV status | ||||
| Positive | 4 (1.2) | 4 (0.2) | 7.01 (1.74–28.15) | .001 |
| Negative | 336 (98.8) | 2358 (99.8) | … | |
| Chlamydia trachomatis | ||||
| Yes | 12 (3.8) | 55 (2.5) | 1.50 (0.80–2.83) | .21 |
| No | 308 (96.2) | 2115 (97.5) | … | |
| Syphilis | ||||
| Yes | 3 (0.9) | 15 (0.6) | 1.39 (0.40–4.84) | .61 |
| No | 337 (99.1) | 2347 (99.4) | … |
Abbreviations: CI, confidence interval; GBS, group B Streptococcus; HIV, human immunodeficiency virus; OR, odds ratio; SD, standard deviation.
a Pearson χ2 or Student t test P value comparing S. aureus–positive and S. aureus–negative women.
b Reference group.
c Includes never married, widowed, divorced, separated.
Table 2.
Multivariable Logistic Regression for Staphylococcus aureus Rectovaginal Colonization Among 2692 Pregnant Women
| Characteristics | S. aureus Colonized OR (95 % CI)a | P Value |
|---|---|---|
| Age, years | ||
| ≤ 25 | 1.25 (0.85–1.84) | .26 |
| 26–35 | 1.28 (0.94–1.74) | .12 |
| ≥ 36 (reference) | … | … |
| Black race | 1.32 (0.96–1.80) | .08 |
| Government insurance/Self pay | 1.63 (1.19–2.25) | .003 |
| Unmarriedb | 1.04 (0.78–1.39) | .80 |
| Multigravid (≥2) | 1.70 (1.19–2.41) | .003 |
| Multiparous (≥1) | 0.92 (0.67–1.26) | .59 |
| HIV positive | 6.32 (1.54–25.96) | .01 |
| GBS colonization | 1.82 (1.42–2.33) | <.001 |
Abbreviations: CI, confidence interval; GBS, group B Streptococcus; HIV, human immunodeficiency virus; OR, odds ratio.
a ORs comparing S. aureus–positive and S. aureus–negative women.
b Includes never married, widowed, divorced, separated.
Table 3.
Maternal and Infant Outcomes by Staphylococcus aureus Rectovaginal Colonization Status
| Outcomes | S. aureus Positive N = 340 No. (%) | S. aureus Negative N = 2362 No. (%) | OR (95% CI95) | P Valuea |
|---|---|---|---|---|
| Gestation <37 weeks | 30 (8.8) | 200 (8.5) | 0.96 (.64–1.43) | .83 |
| Mode of delivery | ||||
| Vaginal | 215 (63) | 1497 (64) | 1.00 (.79–1.27) | .96 |
| Cesarean | 125 (37) | 865 (37) | ||
| Any peripartum complicationb,c | 74 (22) | 571 (24) | 0.87 (.66–1.15) | .33 |
| 5-minute Apgar <7c | 3 (1) | 32 (1) | 0.65 (.20–2.13) | .61 |
| Birth weight <2500 gc | 22 (6) | 177 (7) | 0.85 (.54–1.35) | .50 |
| Infant disposition at 24 hoursc | ||||
| Well baby nursery | 297 (87) | 2087 (88) | NA | .70 |
| NICU | 41 (12) | 255 (11) | ||
| Infant demise | 2 (0.6) | 20 (0.8) | ||
| Infant S. aureus infectionsd | 4 (1.2) | 15 (0.6) | 1.86 (.61–5.63) | .29 |
Abbreviations: CI, confidence interval; NA, not applicable; NICU, neonatal intensive care unit; OR, odds ratio.
a Pearson χ2 or Student t test P value comparing S. aureus–positive and S. aureus–negative women and their infants.
b Peripartum complications analyzed included maternal fever >38°C, chorioamnionitis, nonreassuring fetal status.
c For multiple births, the outcome of baby A was used in the analysis of categorical variables.
d Two infants with S. aureus infections were twins, and only baby A was included in the analysis.
Association Between Colonization and Infection
The frequency of S. aureus infections in women with S. aureus rectovaginal colonization was 2.1% (7 of 340), compared with 0.6 % (14 of 2362) in uncolonized women. There was a significant association between maternal colonization and risk of infection when women with probable and definite infections were considered (OR, 3.5; 95% CI, 1.4–8.8; P = .004). However, when only definite S. aureus infections were considered in women with concordant colonization and infection based on methicillin-susceptibility, the association between maternal colonization and infection was no longer statistically significant (P = .07). The frequency of S. aureus infections in infants was 1.2% (4 of 340) among those born to S. aureus–positive mothers and 0.6% (15 of 2362) among those born to S. aureus–negative mothers (Table 3), but there was no significant association between maternal S. aureus rectovaginal colonization and the risk of S. aureus infection in their infants (OR, 1.9; 95% CI, 0.6–5.6; P = .29).
Maternal Staphylococcus aureus Infections
During the study period, 14 (0.5%) of 2702 women developed definite S. aureus infections and 7 (0.3%) women had probable S. aureus infections. Surgical site infections were most common (Table 4). Eighty-one percent (17 of 21) of infections occurred within 3 months after delivery, and 19% (4 of 21) occurred in the last 3 months of pregnancy. Three (21%) definite infections were caused by MRSA, and 11 (79%) were caused by MSSA. Seven women developed probable infections with S. aureus: 5 developed incisional erythema 2–4 days after cesarean section and were treated successfully with cephalexin, and 2 were treated in the ED for mastitis with either dicloxacillin or amoxillin-clavulanic acid. Neither of the 2 women was readmitted to the ED or hospital.
Table 4.
Types of Staphylococcus aureus Infections in Mothers and Infants
| Type of Infectiona | Mothers N = 21 No. (%) | Infantsb N = 20 No. (%) |
|---|---|---|
| Mastitis | 3 (14) | 0 (0) |
| Surgical site | 10 (48) | 5 (25) |
| Other skin and soft tissue | 4 (19) | 10 (50) |
| Bacteremia/meningitis | 0 (0) | 5 (25) |
| Conjunctivitis | 0 (0) | 1 (5) |
| Urinary tract infection | 4 (19) | 0 (0) |
a Infection types are as reported in the electronic medical record.
b One infant experienced 2 S. aureus infections during the study period.
Women who had a cesarean delivery were at significantly higher risk of developing a S. aureus infection compared with women who had a vaginal delivery (14 of 990 [1.4%] vs 7 of 1712 [0.4%]; OR, 3.5; 95% CI, 1.4–8.7; P = .008). Women who were HIV-seropositive were also significantly more likely to develop a S. aureus infection than women who were HIV-seronegative (2 of 8 [25%] vs 19 of 2694 [0.7%]; P = .002). There was no association between insurance status, gravidity, or GBS colonization and S. aureus infections.
Neonatal Staphylococcus aureus Infections
Twelve (0.4%) of 2789 infants had 13 definite S. aureus infections, and 8 (0.3%) infants had probable S. aureus infections. The median age at diagnosis of the first S. aureus infection was 27 days (range, 8–84 days). Of the 12 infants with definite S. aureus infections, 1 had an MRSA SSTI and 11 had MSSA infections, including 1 infant with MSSA bacteremia followed by an SSTI 6 weeks later. Two infants in the NICU with a history of MSSA colonization based on positive cultures from the conjunctiva or respiratory tract without concomitant signs and symptoms of infection developed MSSA infections 3–6 weeks after colonization was detected. The types of infant infections are shown in Table 4. Ten of 20 (50%) infants with S. aureus infections were born preterm (<37 weeks gestational age), 7 (35%) were of multiple gestation, and 15 (75%) were admitted to our NICU. These 3 factors were all significantly associated with S. aureus infection (P < .001).
DISCUSSION
This large retrospective cohort study identified risk factors for S. aureus rectovaginal colonization in late pregnancy and assessed the risk of peripartum and neonatal infections. Independent predictors of S. aureus rectovaginal colonization included multigravidity, HIV infection, government insurance, and GBS colonization. Although maternal rectovaginal S. aureus colonization may be a risk factor for maternal infections, maternal colonization was not significantly associated with neonatal infections. Overall, the frequency of serious S. aureus infections in pregnant and postpartum women and infants was low.
Women who were multigravid had 1.7 times the odds of being colonized with S. aureus in the rectum and genital tract, an association that has not been previously reported. A prior study showed that multiparous women had a higher rate of CA-MRSA infections, which may be attributed to transmission from young children in the home [1]. However, in the current study, multiparous women were not at increased risk of S. aureus colonization, suggesting that another factor was important among multigravid women. We speculate that the discrepancy between multigravidity and multiparity could be due to a higher frequency of prior spontaneous or therapeutic abortions among S. aureus–colonized women, although this was not specifically addressed in the current study. Multigravid women may have increased contact with the healthcare system (eg, outpatient visits and medical procedures) and thus have increased opportunities to contract MRSA or MSSA [19]. Further studies may help to clarify the importance of an increased number of pregnancies and increased contact with the healthcare system on S. aureus transmission and colonization.
Prior studies have shown an association between HIV infection and S. aureus colonization and infection, particularly in those with lower CD4+ T-cell counts and higher viral loads [20, 21]. Asymptomatic HIV patients have also been shown to be at increased risk of S. aureus and MRSA colonization and infection compared with HIV-negative controls [21]. In the current study, HIV-positive women were at significantly greater risk of both rectovaginal S. aureus colonization and S. aureus infection than HIV-negative women. Of note, there were only 8 HIV-positive women in the current study, and no information was available on the status of their HIV infection (eg, CD4+ T-cell counts or HIV RNA levels). However, S. aureus rectovaginal colonization has not been previously demonstrated in pregnant women with HIV infection, suggesting the need for further studies in different populations.
Women with government insurance had 1.6-fold greater odds of S. aureus colonization. Another large cohort of pregnant women also identified government insurance as a possible risk factor for MRSA rectovaginal colonization in the univariate but not in the multivariable analysis [10]. Studies in other patient populations have similarly shown an association between MRSA colonization in the anterior nares and lower household income [19]. Crowding and poor hygiene may facilitate S. aureus transmission among populations of lower socioeconomic status, which could include those with government insurance [19].
Concurrent colonization with GBS was independently associated with an increased risk of S. aureus rectovaginal colonization in the multivariable regression model, confirming our prior finding [12]. Previous studies have demonstrated an association between GBS and S. aureus in the vaginal flora of both pregnant and nonpregnant women [10, 22]. Isolation of GBS and S. aureus as part of the vaginal flora has been associated with asymptomatic alterations in the microbiota and with symptomatic vaginitis [23, 24]. In both settings, elevated levels of cytokines and chemokines including interleukin 1, interleukin 6, and interleukin 8 have been detected in vaginal secretions [23, 24]. In vitro studies have shown that GBS inhibits growth of other streptococcal but not staphylococcal species [25]. The inhibition of competing bacterial species may provide an opportunity for S. aureus to proliferate in the setting of GBS colonization and thus contribute to alterations in the vaginal flora [13]. The impact of bacterial inhibition by GBS on the vaginal microbiota in vivo and the extent to which GBS and S. aureus contribute to mucosal inflammation are unclear.
Colonization with S. aureus, and MRSA in particular, has been associated with an increased risk of infections [3, 6, 7]. In the current study, women with S. aureus rectovaginal colonization had 3.5-fold greater odds of infection (P = .004). However, infants born to S. aureus–colonized mothers did not appear to be at higher risk of S. aureus infections (P = .29). Prior reports have demonstrated that infants born to mothers with S. aureus rectovaginal colonization can develop colonization of the anterior nares and skin [10, 14, 15], but neonatal S. aureus colonization within the first 48 hours of life was not associated with an increased risk of infection [14]. Two studies that employed active surveillance to identify postpartum and neonatal infections, respectively, reported higher frequencies of S. aureus infections of 6.3% and 2.4% [9, 14]. In both studies, all of the reported infections were SSTIs, most commonly surgical site infections or postpartum mastitis. No patient in either study developed an invasive S. aureus infection, supporting our finding of a low frequency of invasive S. aureus infections in mothers and infants. Infants who became infected with S. aureus were more likely to have been hospitalized in the NICU, suggesting unique risk factors for infection in this population.
The study had limitations. This was a single-center study conducted at an academic referral center located in an area of relatively low prevalence of MRSA colonization [26], thereby limiting the generalizability of the results. The study did not examine colonization at body sites other than the genital tract; thus, some women with S. aureus colonization may have been missed. All data collection, excluding S. aureus colonization and GBS status, was conducted retrospectively through the hospital EMR and relied on existing documentation. There may have been inaccuracies in the medical record, including in recording ICD-9 diagnosis codes. However, if the study team noted discrepancies in the EMR, multiple data sources (eg, laboratory results, clinical notes written by multiple providers) were reviewed in efforts to resolve the discrepancies. Ascertainment of S. aureus infections, particularly minor infections, may have been incomplete because patients may have sought care at another facility or from a physician who did not use the institution's EMR or they may have been managed by telephone. Approximately 45% of infants had an outpatient visit recorded in the EMR. Among these infants, all infections requiring a physician visit should have been captured in the study. In addition, serious infections requiring an ED visit or hospitalization would have been captured for infants followed by private practices affiliated with our medical center. Due to the low frequency of S. aureus infections observed in the current study there was reduced statistical power to identify risk factors for S. aureus infections.
In conclusion, this large cohort study identified several independent risk factors for maternal S. aureus rectovaginal colonization, notably multigravidity and HIV infection, which have not been previously associated with rectovaginal colonization. Further studies in other populations of pregnant women are needed to characterize the association between S. aureus colonization, multigravidity, and HIV infection. The frequency of serious S. aureus infections in S. aureus–colonized women and their infants was low. Maternal rectovaginal colonization was associated with an increased risk of S. aureus infections in women but was not associated with a significantly increased risk of infection in their infants. Furthermore, MSSA infections were more common than MRSA infections in both mothers and infants in our population. Together, these data suggest that routine surveillance for MRSA colonization in pregnant women may not be indicated.
Acknowledgments
The authors thank Ms Jiang Yao and Ms Alla Babina of the Department of Biomedical Informatics for assistance with data extraction, Mr Jonathan Sury for assistance with data analysis, Dr Katherine Chen and Dr Franklin Lowy for helpful discussion of the manuscript, Ms Dana O'Toole for assistance with data entry, and Dr Shing Lee of the Biostatistics Consulting Service and Mr Jimmy K. Duong of the Irving Institute for Clinical and Translational Research (NIH grant UL1 RR024156) at Columbia University Medical Center for assistance with the statistical analysis.
Financial support. This work was supported by the Thrasher Research Fund (NR-0091 to K. T.) and the National Institutes of Health (R01 NR010821 to L. S., T32 AI007531 to K. T., and R01 AI092743 to A. J. R).
Potential conflicts of interest. All authors: No reported conflicts.
All authors have submitted the ICMJE Form for Disclosure of Potential. Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed.
References
- 1.Laibl VR, Sheffield JS, Roberts S, McIntire DD, Trevino S, Wendel GD., Jr. Clinical presentation of community-acquired methicillin-resistant Staphylococcus aureus in pregnancy. Obstet Gynecol. 2005;106:461–5. doi: 10.1097/01.AOG.0000175142.79347.12. [DOI] [PubMed] [Google Scholar]
- 2.Fortunov RM, Hulten KG, Hammerman WA, Mason EO, Jr., Kaplan SL. Community-acquired Staphylococcus aureus infections in term and near-term previously healthy neonates. Pediatrics. 2006;118:874–81. doi: 10.1542/peds.2006-0884. [DOI] [PubMed] [Google Scholar]
- 3.Seybold U, Halvosa JS, White N, Voris V, Ray SM, Blumberg HM. Emergence of and risk factors for methicillin-resistant Staphylococcus aureus of community origin in intensive care nurseries. Pediatrics. 2008;122:1039–46. doi: 10.1542/peds.2007-3161. [DOI] [PubMed] [Google Scholar]
- 4.Carey AJ, Duchon J, Della-Latta P, Saiman L. The epidemiology of methicillin-susceptible and methicillin-resistant Staphylococcus aureus in a neonatal intensive care unit, 2000–2007. J Perinatol. 2010;30:135–9. doi: 10.1038/jp.2009.119. [DOI] [PubMed] [Google Scholar]
- 5.Weber JT. Community-associated methicillin-resistant Staphylococcus aureus. Clin Infect Dis. 2005;41(Suppl 4):269–72. doi: 10.1086/430788. [DOI] [PubMed] [Google Scholar]
- 6.Ellis MW, Hospenthal DR, Dooley DP, Gray PJ, Murray CK. Natural history of community-acquired methicillin-resistant Staphylococcus aureus colonization and infection in soldiers. Clin Infect Dis. 2004;39:971–9. doi: 10.1086/423965. [DOI] [PubMed] [Google Scholar]
- 7.Kluytmans J, van Belkum A, Verbrugh H. Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev. 1997;10:505–20. doi: 10.1128/cmr.10.3.505. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Chen KT, Huard RC, Della-Latta P, Saiman L. Prevalence of methicillin-sensitive and methicillin-resistant Staphylococcus aureus in pregnant women. Obstet Gynecol. 2006;108:482–7. doi: 10.1097/01.AOG.0000227964.22439.e3. [DOI] [PubMed] [Google Scholar]
- 9.Beigi R, Hanrahan J. Staphylococcus aureus and MRSA colonization rates among gravidas admitted to labor and delivery: a pilot study. Infect Dis Obstet Gynecol. 2007;2007:70876. doi: 10.1155/2007/70876. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Andrews WW, Schelonka R, Waites K, Stamm A, Cliver SP, Moser S. Genital tract methicillin-resistant Staphylococcus aureus: risk of vertical transmission in pregnant women. Obstet Gynecol. 2008;111:113–8. doi: 10.1097/01.AOG.0000298344.04916.11. [DOI] [PubMed] [Google Scholar]
- 11.Creech CB, Litzner B, Talbot TR, Schaffner W. Frequency of detection of methicillin-resistant Staphylococcus aureus from rectovaginal swabs in pregnant women. Am J Infect Control. 2010;38:72–4. doi: 10.1016/j.ajic.2009.06.015. [DOI] [PubMed] [Google Scholar]
- 12.Top KA, Huard RC, Fox Z, et al. Trends in methicillin-resistant Staphylococcus aureus anovaginal colonization in pregnant women in 2005 versus 2009. J Clin Microbiol. 2010;48:3675–80. doi: 10.1128/JCM.01129-10. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Chen KT, Campbell H, Borrell LN, Huard RC, Saiman L, Della-Latta P. Predictors and outcomes for pregnant women with vaginal-rectal carriage of community-associated methicillin-resistant Staphylococcus aureus. Am J Perinatol. 2007;24:235–40. doi: 10.1055/s-2007-976551. [DOI] [PubMed] [Google Scholar]
- 14.Pinter DM, Mandel J, Hulten KG, Minkoff H, Tosi MF. Maternal-infant perinatal transmission of methicillin-resistant and methicillin-sensitive Staphylococcus aureus. Am J Perinatol. 2009;26:145–51. doi: 10.1055/s-0028-1095179. [DOI] [PubMed] [Google Scholar]
- 15.Andrews JI, Fleener DK, Messer SA, Kroeger JS, Diekema DJ. Screening for Staphylococcus aureus carriage in pregnancy: usefulness of novel sampling and culture strategies. Am J Obstet Gynecol. 2009;201(396):e1–5. doi: 10.1016/j.ajog.2009.06.062. [DOI] [PubMed] [Google Scholar]
- 16.Schrag S, Gorwitz R, Fultz-Butts K, Schuchat A. Prevention of perinatal group B streptococcal disease. Revised guidelines from CDC. MMWR Recomm Rep. 2002;51:1–22. [PubMed] [Google Scholar]
- 17.Clinical and Laboratory Standards Institute. 10th. Clinical and Laboratory Standards Institute; Wayne, PA: 2009. Performance standard for antimicrobial disk susceptibility tests—approved standard. CLSI document M02-A10. [Google Scholar]
- 18.Tracy LA, Furuno JP, Harris AD, Singer M, Langenberg P, Roghmann MC. Predictive ability of positive clinical culture results and International Classification of Diseases, Ninth Revision, to identify and classify noninvasive Staphylococcus aureus infections: a validation study. Infect Control Hosp Epidemiol. 2010;31:694–700. doi: 10.1086/653206. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Gorwitz RJ, Kruszon-Moran D, McAllister SK, et al. Changes in the prevalence of nasal colonization with Staphylococcus aureus in the United States, 2001–2004. J Infect Dis. 2008;197:1226–34. doi: 10.1086/533494. [DOI] [PubMed] [Google Scholar]
- 20.Cenizal MJ, Hardy RD, Anderson M, Katz K, Skiest DJ. Prevalence of and risk factors for methicillin-resistant Staphylococcus aureus (MRSA) nasal colonization in HIV-infected ambulatory patients. J Acquir Immune Defic Syndr. 2008;48:567–71. doi: 10.1097/QAI.0b013e31817e9b79. [DOI] [PubMed] [Google Scholar]
- 21.Imaz A, Pujol M, Barragan P, Dominguez MA, Tiraboschi JM, Podzamczer D. Community associated methicillin-resistant Staphylococcus aureus in HIV-infected patients. AIDS Rev. 2010;12:153–63. [PubMed] [Google Scholar]
- 22.Carson HJ, Lapoint PG, Monif GR. Interrelationships within the bacterial flora of the female genital tract. Infect Dis Obstet Gynecol. 1997;5:303–9. doi: 10.1155/S1064744997000525. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Donders GG, Vereecken A, Bosmans E, Dekeersmaecker A, Salembier G, Spitz B. Definition of a type of abnormal vaginal flora that is distinct from bacterial vaginosis: aerobic vaginitis. BJOG. 2002;109:34–43. doi: 10.1111/j.1471-0528.2002.00432.x. [DOI] [PubMed] [Google Scholar]
- 24.Nikolaitchouk N, Andersch B, Falsen E, Strombeck L, Mattsby-Baltzer I. The lower genital tract microbiota in relation to cytokine-, SLPI- and endotoxin levels: application of checkerboard DNA-DNA hybridization (CDH) APMIS. 2008;116:263–77. doi: 10.1111/j.1600-0463.2008.00808.x. [DOI] [PubMed] [Google Scholar]
- 25.Chaisilwattana P, Monif GR. In vitro ability of the group B streptococci to inhibit gram-positive and gram-variable constituents of the bacterial flora of the female genital tract. Infect Dis Obstet Gynecol. 1995;3:91–7. doi: 10.1155/S1064744995000391. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Miller M, Cook HA, Furuya EY, et al. Staphylococcus aureus in the community: colonization versus infection. PLoS One. 2009;4:e6708. doi: 10.1371/journal.pone.0006708. [DOI] [PMC free article] [PubMed] [Google Scholar]