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Background: To determine the prevalence of intestinal S. aureus colonization of patients at a large teaching hospital and determine the molecular characteristics of the identified strains. The second objective of this research was to determine risk factors associated with S. aureus intestinal colonization. Methods: A cross-sectional study of 781 specimens from inpatients and outpatients at the University of Iowa Hospitals and Clinics Clinical Microbiology Laboratory was conducted. S. aureus was identified using traditional culture methodologies. Methicillin-resistance was determined via PCR of the mecA gene. PVL PCR, spa typing, and antimicrobial sensitivity testing were also done. A nested case-control study was done on a subset of patients with all colonized patients defined as cases and non-colonized controls. Medical record abstractions were done to identify risk factors for intestinal colonization in the nested study. Results: Out of 625 patients included in the final study, 58 were positive for S. aureus (9.3%). One isolate was positive for the PVL gene. A high number of isolates were resistant to multiple antibiotics including oxacillin (43.1%), erythromycin (51.7%), and levofloxacin (41.4%). All isolates were susceptible to vancomycin, daptomycin, linezolid, and quinupristin- dalfopristin. In the nested study, having a disease or condition of the gastrointestinal tract significantly increased the odds of intestinal colonization (OR: 1.96, 95% CI: 1.04–3.7; aOR: 13.9, 95% CI: 1.67–115.7). No other variables were significantly associated with increased odds of colonization. Conclusions: S. aureus was identified from the stool of patients at the University of Iowa Hospitals and Clinics, with a large number of those isolates being resistant to antibiotics and may serve a reservoir for subsequent infections as well as asymptomatic transmission. Keywords: Methicillin-resistant Staphylococcus aureus, Hospitals, Antibiotic resistance, Intestinal carriage Background S. aureus, an in particular methicillin-resistant S. Staphylococcus aureus is a commensal bacterium and aureus (MRSA) intestinal colonization, may be more important cause of healthcare-associated infections [1]. common than previously thought and has been shown Nasal carriage is considered to be the most important to be clinically important [10, 11]. Rectal carriers have site of S. aureus colonization [2] and is the best-studied been found to be at increased risk of developing S. [3]. However, other extra-nasal body sites, including the aureus infections [10] and gastrointestinal carriage of gastrointestinal tract, are known to harbor S. aureus MRSA has been associated with nosocomial antibiotic- [4–6]. Recent studies have found S. aureus in the intes- associated diarrhea [11]. Screening for gastrointestinal tines of healthy humans [7, 8] aswellasthe intestines carriage has been shown to identify colonized patients of hospitalized patients [9]. who would have been otherwise missed [12]. S. aureus gastrointestinal carriage may be an overlooked reservoir, contributing to hospital infection and transmission. * Correspondence: margaret-chorazy@uiowa.edu The objectives of this study were to determine the Department of Epidemiology, College of Public Health, University of Iowa, prevalence of S. aureus and MRSA in human stool Iowa City, IA, USA Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Kates et al. Antimicrobial Resistance and Infection Control (2018) 7:42 Page 2 of 9 samples at a large university hospital, to characterize the Pastorex Staph Plus rapid latex agglutination (Bio-Rad, identified isolates by molecular methods, and to assess Redmond,Washington,USA)tests.Any patientwho potential risk factors for intestinal carriage. We hypothe- was culture positive for S. aureus and/or MRSA in the sized S. aureus and MRSA prevalence in stool will be stool was considered intestinally colonized. similar to what has been reported previously in the lit- All S. aureus isolates were tested for antimicrobial erature [3]. Furthermore, we hypothesized having a susceptibility using broth dilution as described by the gastrointestinal condition would increase the risk of Clinical and Laboratory Standards Institute [13]. intestinal S. aureus carriage. Isolates were tested for susceptibility to oxacillin, tetracycline, erythromycin, clindamycin, trimethoprim- Methods sulfamethoxazole, gentamycin, levofloxacin, vanco- Population and design mycin, daptomycin, quinupristin/dalfopristin, linezolid, We conducted a cross-sectional study of 781 stool speci- and rifampin. mens retrieved from the University of Iowa Hospitals Whole, genomic DNA was extracted using the and Clinics (UIHC) Clinical Microbiology Laboratory Wizard Genomic DNA purification kit (Promega Cor- between September 2010 and March 2011. UIHC is poration, Madison, Wisconsin, USA) adapted for S. Iowa’s only comprehensive academic medical center, aureus.Presenceofthe mecA [14]and PVL[15] genes consisting of 811 beds. Though patients are primarily were determined through end-point PCR. spa typing drawn from eastern Iowa, the hospital serves the entire was carried out using the primers and methodologies state and into the region beyond (including parts of described by Ridom Bioinformatics and sequences Illinois, Wisconsin, Minnesota). The specimens were were interpreted utilizing the Ridom StaphType soft- provided from a bank of existing biologic specimens ware (Ridom GmbH, Würzburg, Germany). For pheno- originally collected for the purpose of patient clinical typically MRSA isolates negative for the mecA gene, care as part of standard clinical practice. Samples thepresenceof the mecC gene was determined [16]. remaining after completion of diagnostics that would All molecular procedures were carried out using have otherwise been disposed by the Clinical Microbiol- known positive and negative controls, including ogy Laboratory were collected by the researchers and USA300 (mecA, PVL) and LGA251 (mecC). stored at − 80 °C for further analysis. This convenience sample included both inpatients and outpatients from Medical record abstraction Iowa, Northern Missouri, and Western Illinois. A nested Medical record abstractions were done on all S. aureus case-control study was conducted using electronic pa- and MRSA-positive patients (cases) and two culture- tient medical records to assess potential risk factors for negative patients (controls). Controls were chosen based S. aureus intestinal carriage. All patients positive for on date of admission and time of sample collection intestinal S. aureus carriage were included in the nested relative to cases. Demographic information (gender, age, study and considered cases. Two controls were chosen and race/ethnicity), reason for specimen collection, hos- for every case based on admission date and time of stool pital admission and discharge dates, ICU admission and sample collection within ± 24 h. Only one stool sample discharge dates, death date, co-infections, recent per patient was included. If more than one stool sample antimicrobial use, recent anti-motility medication use, per patient was included in the biobank, only the first history of gastrointestinal disorders, and history of stool provided by the patient was included in this immunosuppressive conditions were abstracted from the analysis. electronic medical record. Ethics, consent, and approval Statistical analysis The University of Iowa Institutional Review Board Statistical analyses were performed using SAS, version approved all study protocols. 9.3 (SAS Institute, Cary, NC). There were 781 banked samples available to the investigators from the UIHC. Identification and characterization of S. aureus Two controls for each case was decide upon because it 50 μL of stool was plated onto Baird-Parker Agar and has been shown more than two controls per case does CHROMagar MRSA media (Becton Dickinson and not greatly increase the statistical power of the analysis Company, Sparks, Maryland, USA) and incubated for [17]. Logistic regression was performed to assess risk 48 h at 35 °C. Presumptive positive colonies were factors for intestinal colonization. The primary exposure streaked onto Columbia CNA with 5% sheep blood of interest, having a disorder of the gastrointestinal tract, (Becton Dickinson and Company, Sparks, Maryland, was modeled as dichotomous (yes/no). Backwards selec- USA), and incubated for 24 h at 35 °C. All isolates were tion was used to determine which variables to include tested for S. aureus using the catalase, coagulase, and into the model (p > 0.2 threshold to stay in the model). Kates et al. Antimicrobial Resistance and Infection Control (2018) 7:42 Page 3 of 9 Interaction terms were assessed between all covariates. If Thirty unique spa types were identified, with t002 being the term was significantly associated with S. aureus the most prevalent at 66.7% (n = 20) followed by t012 infections, it was included into the final model and the and t1635 both at 10% (n = 3). The BURP analysis Akaike information criterion (AIC) was assessed. If the resulted in one major cluster with the hospital- model including the interaction term increased the AIC associated strain t002 as the founder. The spa cc-002 by more than three over the model without the term, grouping accounted for 24 strains (42% of all strains) the interaction term was not included in the final model. and four spa types (13% of all spa types). Two spa types Odds ratios and 95% Confidence Intervals were calcu- (three isolates) were excluded as they had less than 5 lated and a significance level of p = .05 was used. repeat sequences present in the spa gene. Antimicrobial susceptibility testing was performed Results on all isolates positive for S. aureus (Fig. 2). Resistance Of the 781 samples retrieved from the UIHC Clinical was observed for most antibiotics tested. The highest Microbiology Laboratory, six samples were excluded due prevalence of resistance was to erythromycin at to the tubes breaking during the freezing process. An 51.7% (n = 37) followed by oxacillin at 43.1% (n =25) additional 148 samples were excluded due to patients and levofloxacin at 41.4% (n = 24). Resistance to clin- providing more than one stool sample and six additional damycin was observed at 22.4% (n =16). No isolates samples were excluded due to medical records that were were resistant to vancomycin, daptomycin, or quinu- not able to be located, leaving 621 patients included in pristin/dalfopristin. Resistance to all other antimicro- the study (Fig. 1). Demographic and clinical characteris- bials was low (Fig. 3). Twenty-six (44.8%) isolates tics of the 621 patients included in the study are met the definition for multi-drug resistance (MDR) described in Table 1. The average age for all patients was with having acquired non-susceptibility to at least 51.6 years (stan. Dev.: 19 years, range: 0 to 94 years). A one agent in three or more antimicrobial categories majority of patients were female (320, 51.5%) and Cauca- [18]. Of the MDR isolates, one isolate was resistant sian (560, 90.2%). A majority were inpatients (487, to at least one agent in six antimicrobial categories 78.4%) with 20.1% (126/625) being outpatients, and 1.3% and one isolate was resistant to ≥1agent in five (8/625) being housed outpatients. The average length of categories. Twelve isolates were resistant to ≥1agent stay for inpatients as defined as the entire time they in four categories and 9 isolates were resistant to ≥1 were admitted for the stay when their stool samples was agent in 3 categories. Three isolates met the defin- collected was 15.8 days (stan. Dev.: 28.6 days). There ition of MDR by being MRSA. Twenty-two of the 58 were no significant differences between carriers and isolates (37.9%) were susceptible to all antibiotics non-carriers for any variables listed in Table 1. tested. Six isolates (10.3%) were resistant to only one Of the 621 samples, 58 (58/621, 9.3%) were positive antimicrobial and two were resistant to two antimi- for S. aureus, 26 of which (26/621, 4.2%) were MRSA via crobials (3.4%). Two isolates were phenotypically the presence of the mecA gene, with an MRSA preva- resistant to oxacillin according to the AST (both lence of 44.8% (26/58). One isolate was positive for PVL. isolates had a minimum inhibitory concentration Fig. 1 Flow chart of the participant inclusion and exclusion criteria Kates et al. Antimicrobial Resistance and Infection Control (2018) 7:42 Page 4 of 9 Table 1 Patient demographic data by S. aureus intestinal [MIC] of ≥4 μg/mL); however, both isolates were negative colonization status for the presence of the mecA and mecC genes. Carriers Non-carriers P Total Medical record abstractions were completed on 189 pa- n =58 n = 567 n = 621 tients (58 cases and 131 controls). A majority of cases were Age (Mean years ± 51.2 (±20.4) 51.6 (±18.9) 0.897 51.6 (±19.0) Caucasian (n = 168, 88.9%) and slightly over half were male Std. dev.) (n = 98, 51.8%). In the univariate analysis, most covariates Sex were not significantly associated with S. aureus intestinal Male 24 (41.4%) 277 (49.2%) 301 (48.5%) colonization. We observed a borderline significant associ- ation with sex with females having increased odds of intes- Female 34 (58.6%) 286 (50.8%) 0.256 320 (51.5%) tinal colonization, though the confidence interval included Race/ Ethnicity 1.0 (OR: 1.84, 95% CI: 0.98–3.44). Having a history of a Caucasian 52 (89.7%) 508 (90.2%) 560 (90.2%) gastrointestinal condition, theprimary predictor, wassig- African American 2 (3.5%) 24 (4.3%) 26 (4.2%) nificant in the unadjusted, univariate model with those hav- Hispanic or Latino 3 (5.2%) 8 (1.4%) 11 (1.8%) ing any disorder of the gastrointestinal tract having Other 1 (1.7%) 24 (4.2%) 0.486 25 (4.0%) increased odds of intestinal colonization (OR: 1.96, 95% CI: 1.04–3.7). The most prevalent disorder of the GI tract was Visit Type gastroesophageal reflux disease (GERD) at 31 of the 189 Inpatient 44 (75.9%) 443 (78.7%) 487 (78.4%) patients (16.4%) of the total population analyzed for the Outpatient 13 (22.4%) 113 (20.1%) 126 (20.3%) nested study. The second most prevalent condition was Housed outpatient 1 (1.7%) 7 (1.2%) 0.865 8 (1.3%) lower GI bleed (n = 16, 7.4%) followed by Crohn’sdisease Length of Stay (Mean 21.7 (±51.7) 15.2 (± 25.1) 0.992 15.8 (± 28.6) (n = 13, 6.9%) and any inflammatory disorder of the intes- days ± Std. dev.) tines including inflammatory bowel disorder (n = 13, 6.9%). Other includes American Indian or Alaskan Natives, Asian, Native Hawaiian or No other covariates were significantly associated with intes- Pacific Islander, as well as individuals who declined to provide a race or ethnicity tinal colonization in the univariate analyses (Table 2). Housed outpatient refers to patients being held for observation The final adjusted model included having a disorder of the gastrointestinal tract, age, sex, laxative usage, anti- motility agent usage, having a S. aureus infection, whether the patient died, ICU length of stay, and the reason for specimen collection. An interaction between having a gastrointestinal disorder and age was forced Fig. 3 Based Upon Repeat Pattern Analysis of all positive S. aureus isolates (n = 58). Based Upon Repeat Pattern (BURP) analysis was used to group all 58 S. aureus isolates into cluster complexes. Cost distances Fig. 2 Antibiotic susceptibility testing using minimum inhibitory of ≤4wereused to define clusters and spa types with 5 or fewer concentrations (n = 58) repeats were excluded from the analysis Kates et al. Antimicrobial Resistance and Infection Control (2018) 7:42 Page 5 of 9 Table 2 Associations between potential risk factors and S. aureus intestinal colonization Risk Factor Cases Controls Unadjusted Adjusted (N = 58) (N = 131) OR (95% CI) OR (95% CI) Age 0–29 years 9 13 Ref Ref 30–49 years 14 34 0.58 (0.020–1.65) 2.94 (0.43–19.88) 50–69 years 28 60 0.67 (0.026–1.77) 5.02 (0.81–30.9) Over 70 years 7 23 0.44 (0.13–1.5) 1.42 (0.15–13.6) Sex Male 24 74 Ref Ref Female 33 58 1.84 (0.98–3.44) 1.93 (0.94–3.96) Race/ Ethnicity Caucasian 53 115 Ref African American 2 5 0.9 (0.17–4.8) Hispanic/ Latino 3 2 3.35 (0.54–20.63) Other 1 8 0.28 (0.03–2.29) S. aureus Infection No 53 121 Ref Ref Yes 5 10 1.14 (0.37–3.50) 0.83 (0.19–3.54) Other Coinfections No Coinfections 26 46 Ref One 21 60 0.62 (0.34–1.23) Two 4 18 0.49 (0.16–1.48) Three or more 7 7 0.67 (0.19–2.34) Collection Reason Abdominal pain 5 13 Ref Ref Clostridium difficile 23 37 1.61 (0.51–5.13) 1.87 (0.49–7.11) Diarrhea 11 72 0.67 (0.21–2.14) 0.59 (0.15–2.25) Other 19 9 2.25 (0.63–8.03) 2.74 (0.64–11.7) Deceased No 44 83 Ref Ref Yes-within 30 days 3 11 0.71 (0.18–2.8) 0.74 (0.13–4.67) Yes- after 30 days 14 26 0.4 (0.16–0.98) 0.29 (0.1–0.86) Undeterminable 4 7 1.08 (0.3–3.9) 0.71 (0.17–2.96) Gastrointestinal Disease No 21 69 Ref Ref Yes 37 62 1.96 (1.04–3.7) 13.9 (1.67–115.7) Immunocompromised No 15 34 Ref Yes 43 97 1.01 (0.47–2.04) ICU Stay No 47 98 Ref Yes 11 33 0.69 (0.32–1.5) ICU Unit No ICU stay 47 98 Ref MICU 5 21 0.5 (0.18–1.4) Kates et al. Antimicrobial Resistance and Infection Control (2018) 7:42 Page 6 of 9 Table 2 Associations between potential risk factors and S. aureus intestinal colonization (Continued) Risk Factor Cases Controls Unadjusted Adjusted (N = 58) (N = 131) OR (95% CI) OR (95% CI) SICU 2 6 0.7 (0.14–3.58) Other 4 6 1.4 (0.4–5.2) ICU Length of Stay 0 days 47 99 Ref Ref 1 to 4 days 1 14 0.15 (0.02–1.18) 0.15 (0.02–1.36) Greater than 4 days 10 18 1.18 (0.5–2.73) 1.38 (0.46–4.15) Total Length of Stay 0 days 12 23 Ref 1 to 10 days 23 59 0.75 (0.32–1.75) 11 to 29 days 10 26 0.74 (0.27–2.02) Greater than 30 days 13 23 1.08 (0.41–2.87) Antibiotics used No 26 40 Ref Yes 32 91 0.54 (0.29–1.02) Laxatives used No 43 100 Ref Ref Yes 15 31 1.13 (0.56–2.3) 1.94 (0.8–4.6) Anti-motility agent used No 57 122 Ref Ref Yes 1 9 0.238 (0.03–1.92) 0.16 (0.02–1.53) S. aureus infections are defined as clinical infections extracted from the patients medical record Mortality is not considered a risk factor colonization. For this variable, S. aureus colonization is a risk factor for mortality into the model as the interaction term was verging on rate of intestinal colonization in hospitalized patients is significance (p = 0.058) and did not increase the AIC by roughly 20% [3], though the number of studies included more than 3. In the final model, having a disorder of the in reaching this estimate is small and the populations GI tract was significantly associated with increased odds vary greatly. Our observed prevalence of 9.3% is lower of being intestinally colonized with S. aureus, though the than the estimated average and lower than most studies confidence interval is very wide (OR: 13.9, 95% CI: 1.67– have reported to date. This may be due to the fact the 115.7). No other covariates included in the final model population screened for this study included patients were significantly associated with intestinal S. aureus from many departments across a large teaching hospital colonization (Table 2). as well as outpatients seen in the emergency department. Use of frozen instead of fresh stools may also have Discussion reduced our recovery rate. We identified S. aureus in the intestines of patients at Many of the studies in recent years have focused on UIHC and report an intestinal colonization rate of 9.3%. MRSA carriage and have reported MRSA intestinal car- During the 1950’s, S. aureus intestinal colonization was riage rates frequently ranging from 5% [22, 23] to 10% studied in greater detail than seen in the current litera- [24] with some studies finding a MRSA prevalence as ture [19]. Studies from this time report carriage preva- high as 22% in high-risk populations [25]. The observed lence ranges between 8% and 30% [3, 20, 21]. While prevalence of MRSA reported here is 4.2%, which is researchers have known of the relationship between lower than others have reported. Of the S. aureus intestinal S. aureus carriage and antibiotic-associated isolates identified, 44.8% met the definition for MDR-SA. diarrhea, as well as the increased risk of other S. aureus Two of these isolates were phenotypically resistant to infections, intestinal carriage has been studied far less oxacillin; however, they were not positive for either than carriage at other anatomical sites, particularly the resistance gene – mecA or mecC –tested for. nares. Recent studies of S. aureus intestinal carriage have Wefoundone isolatetobepositivefor thePVL gene detected intestinal carriage rates ranging from 10% [22] [26]. As PVL genes are mainly associated with commu- to as high as 37% [10]. It has been estimated the average nity- associated S. aureus, it is not surprising we found Kates et al. Antimicrobial Resistance and Infection Control (2018) 7:42 Page 7 of 9 such a low prevalence in clinical cohort. Spa type t002 model (OR: 13.9, 95% CI: 1.67–115.7), though the 95% was the most frequently identified spa type accounting for confidence interval was very wide due to a small sample 66.7% of all identified spa types. This spa type is most size. No other variables abstracted from the medical record frequently associated with hospital strains and typically were significantly associated with an increased risk of in- belongs to the pulsed-field type USA100 [27]. Spa type testinal colonization in either the univariate or adjusted t012, the second most prevalent spa type observed in this models. Other studies have reported several potential risk study (10% of all spa types) is frequently found in commu- factors for intestinal S. aureus colonization. It has been nity settings and may be associated with younger age [28]. shown that a stay in an extended care facility or nursing Prevalence of intestinal carriage is dependent on the home can significantly increase the risk of intestinal method of specimen collection employed. Varying rates colonization [36]; however, we were unable to assess nurs- of colonization are seen by method and anatomical site ing home stays in the present study. Studies have also used to define “gastrointestinal.” The two main methods reported length of stay [37], a recent history of antimicro- used to collect specimens are swabs and stool samples. bial usage [37–39], a history of MRSA infection [38], and Swabs collected from the rectum, anus, perineum, and dependence on healthcare workers to perform activities of the groin or inguinal region are typically accepted as daily living [37] all significantly increasing the risk of intes- representing intestinal carriage of S. aureus in addition tinal S. aureus carriage. While we were not able to assess to stool specimens [3]. Several studies have assessed activities of daily living in the medical record, we did not which method and region provide the most consistent detect a significant association with LOS, antibiotic usage, rate of colonization, but these studies are few and do or the history of MRSA infections and colonization in our not provide a consensus. Rectal swabbing has been population. This may be due to the inclusion of a single shown to yield more S. aureus than stool cultures [29]. hospital in this study, smaller sample size, and the reliance This may explain why our study reports a lower preva- on medical record data. lence compared to many of the studies cited above Our study has several limitations. The first is the speci- which used rectal or perineal swabbing. mens analyzed were not collected for research purposes, Intestinal colonization may be an important reservoir but for routine medical care and as such we were only able for the dissemination of S. aureus in the health care to address intestinal colonization in a cross-sectional study setting. Intestinal colonization is known to lead to and were unable to determine the duration of colonization increased risk of infection [30–32], though the mech- in these patients. Future studies are needed to determine anism is not clear. It has been hypothesized intestinal colonization duration, as well as the rates of persistent ver- colonization increases colonization or contamination sus intermittent carriage. Furthermore, we were unable to of the skin which in turn increases contamination of determine if the S. aureus strain the patient was colonized the patient’s environment. Environmental contamin- with was the same strain causing an S. aureus infection, or ation then increases both the risk of infection as well otherwise present in other locations of the patient’sbody as the potential for nosocomial transmission [31]. or environment. This study was conducted in a single hos- While we were unable to investigate colonization of pital in Iowa with a predominantly white population which other body sites in this study, S. aureus intestinal may limit the generalizability of the study findings. How- colonization has been associated with an increased risk ever, UIHC is a large teaching hospital with a catchment of skin colonization [10]. Nasal and intestinal carriage area including several surrounding mid-western states.S are also frequently observed in the same patient; how- aureus was identified from the stool of patients at the ever, intestinal colonization alone does increase the de- UIHC. Lastly, the samples used for this study were col- tection sensitivity [3, 22, 23, 33–35]. In a meta-analysis lected as part of routine clinical care and as such, all partic- by McKinnell et al., it was found rectal screening ipants had some degree of gastrointestinal symptoms. A increased yield by 20%, with rectal screening having history of gastrointestinal conditions increased the risk of the greatest impact in hospitals with a low MRSA intestinal S. aureus carriage. Many of those isolates are prevalence (23% increase) [35]. resistant to antibiotics and may serve as a reservoir for To assess potential risk factors for intestinal colonization, subsequent infections and transmission events. we performed a nested case-control study. We hypothe- sized having a disease or condition of the gastrointestinal Conclusions tractwould putpatientsatincreased risk of S. aureus S. aureus colonization was found in 9.3% of tested stool intestinal colonization. In the univariate analysis we found samples. Having a disease or condition of the gastrointes- gastrointestinal conditions did significantly increase the tinal tract significantly increased the odds of intestinal odds of being colonized with S. aureus (OR: 1.96, 95% CI: colonization. A diverse array of molecular types were iso- 1.04–3.7) and this association remained significant after lated, and antibiotic resistance was common, including adjusting for the other variables included in the final methicillin resistance and multi-drug resistant strains. Kates et al. Antimicrobial Resistance and Infection Control (2018) 7:42 Page 8 of 9 Abbreviations vancomycin-resistant enterococcus in healthy children. Antimicrob Agents AIC: Akaike information criterion; BURP: Based Upon Repeat Pattern.; Chemother. 2014;58(2):1261–2. GERD: Gastroesophageal reflux disease; LOS: Length of stay; MDR: Multi-drug 9. Nakao A, Ito T, Han X, Lu YJ, Hisata K, Tsujiwaki A, Matsunaga N, Komatsu M, resistant; MIC: Minimum inhibitory concentration; MRSA: Methicillin-resistant Hiramatsu K, Shimizu T. Intestinal carriage of methicillin-resistant Staphylococcus aureus; UIHC: University of Iowa Hospitals and Clinics Staphylococcus aureus in nasal MRSA carriers hospitalized in the neonatal intensive care unit. Antimicrob Resist Infect Control. 2014;3:14. Acknowledgements 10. Bhalla A, Aron DC, Donskey CJ. Staphylococcus aureus intestinal The authors would like to thank the Clinical Microbiology Laboratory and the colonization is associated with increased frequency of S. Aureus on skin of University of Iowa Hospitals and Clinics and Dr. Bradley Ford for their assistance hospitalized patients. BMC Infect Dis. 2007;7:105. with medical record abstraction. Thanks to Yesenia C. Romero-Herazo for 11. Boyce JM, Havill NL. Nosocomial antibiotic-associated diarrhea associated retrieving the specimens. with enterotoxin-producing strains of methicillin-resistant Staphylococcus aureus. Am J Gastroenterol. 2005;100(8):1828–34. 12. 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Euro j clin microb infect dis off publ Euro Soc Clin Microbiol. 2015; 34(10):1947–55. Submit your next manuscript to BioMed Central and we will help you at every step: • We accept pre-submission inquiries � Our selector tool helps you to find the most relevant journal � We provide round the clock customer support � Convenient online submission � Thorough peer review � Inclusion in PubMed and all major indexing services � Maximum visibility for your research Submit your manuscript at www.biomedcentral.com/submit
Antimicrobial Resistance and Infection Control – Springer Journals
Published: Mar 20, 2018
Keywords: Methicillin-resistant Staphylococcus aureus; Hospitals; Antibiotic resistance; Intestinal carriage
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