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Year : 2017  |  Volume : 10  |  Issue : 6  |  Page : 1809-1813
Methicillin-resistant Staphylococcusaureus nasal colonization in human immunodeficiency virus-infected patients

1 Department of Microbiology, Kasturba Medical College, Manipal University, Manipal, Karnataka, India
2 Department of Medicine, Kasturba Medical College, Manipal University, Manipal, Karnataka, India

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Date of Web Publication11-Jan-2018


Background: Staphylococcusaureus infections account for significant morbidity in human immunodeficiency virus(HIV)-infected individuals. Colonization by methicillin-resistant S. aureus(MRSA) usually precedes the development of subsequent infections. Aim: To study the frequency of MRSA colonization and to analyze its risk factors among HIV-infected adult patients. Materials and Methods: A prospective study was conducted including 194 HIV-infected patients. Anterior nasal swabs were obtained and processed for isolation of MRSA following standard guidelines. Risk factors for MRSA colonization were assessed, and the antimicrobial susceptibility profile of the MRSA isolates including low-level resistance to mupirocin was studied. Data were analyzed using SPSS statistical software. Results: MRSA colonization of anterior nares was found in 49patients(25.3%). Patients put on antibiotics in the prior 3months(P=0.001) and those with percutaneous device in the past year(P=0.001) were more likely to be MRSA colonized. Antiretroviral therapy was found to be protective against MRSA colonization(P=0.004). Low-level mupirocin resistance was found in four(8.2%) isolates of MRSA. Conclusion: A significant proportion of HIV-infected patients were found to have MRSA colonization. Detection and monitoring for MRSA carriage status may be considered to reduce infections caused by MRSA in HIV-infected individuals.

Keywords: Human immunodeficiency virus, methicillin-resistant Staphylococcus aureus, mupirocin, nasal colonization

How to cite this article:
Alexander A, Vishwanath S, Sellvaraj A, Varma M, Saravu K, Chawla K. Methicillin-resistant Staphylococcusaureus nasal colonization in human immunodeficiency virus-infected patients. Ann Trop Med Public Health 2017;10:1809-13

How to cite this URL:
Alexander A, Vishwanath S, Sellvaraj A, Varma M, Saravu K, Chawla K. Methicillin-resistant Staphylococcusaureus nasal colonization in human immunodeficiency virus-infected patients. Ann Trop Med Public Health [serial online] 2017 [cited 2020 Jul 13];10:1809-13. Available from:

   Introduction Top

Staphylococcus aureus infections account for significant morbidity in human immunodeficiency virus(HIV)-infected patients.[1] Methicillin-resistant strains of S. aureus(MRSA) as nosocomial pathogens are isolated with increasing prevalence among hospitals worldwide. MRSA has even emerged worldwide as an important etiological agent of community-associated skin and soft tissue infections.[1],[2]

Enhanced rate of staphylococcal carriage is seen in individuals with diabetes mellitus, hemodialysis, intravenous drug addiction, skin infection, and HIV infection.[3] Although anterior nares is considered the primary site for colonization of S. aureus, other body sites may be involved.[2] Colonization with MRSA is a major risk factor for subsequent MRSA infections by the same colonizing strain in many patients.[4],[5]

In comparison with general population, the risk of MRSA colonization among HIV-infected persons is higher which may be attributed to frequent health-care exposure, frequent antibiotic intake, low CD4+lymphocyte counts, and behavioral risk factors.[2],[6] HIV is also considered as an independent risk factor for MRSA colonization.[6]

Mupirocin(pseudomonic acid A) as a topical antibiotic is used in decolonization regimens for MRSA and for skin and soft tissue infections with S. aureus and streptococcal sp. as etiological agents. Emergence of resistance to mupirocin among MRSA strains is seen in many parts of the globe.[7] It is necessary to monitor the local susceptibility profile of MRSA for mupirocin. Aprospective study was conducted to detect and analyze the risk factors for colonization of MRSA among HIV-infected adults at a tertiary care center and to detect low-level mupirocin resistance(MUP RL) among the MRSA isolates.

   Materials and Methods Top

Following approval from the Institutional Ethics Committee, a prospective study was conducted between July and October 2014 and included HIV-infected adult patients(n=194), either admitted to various wards of the tertiary care center or presenting as outpatients to HIV clinic. Patients who had applied any medications in their nares within 6weeks prior to enrollment were excluded from the study.

Following informed consent from the study patients, sterile-moist swabs were inserted 1cm into each nasal vestibule and rotated two complete revolutions while in contact with the nasal membrane, following which the swabs were transported immediately to the Microbiology laboratory. The swabs were inoculated on 5% sheep blood agar plates(HiMedia Laboratories, Mumbai, India) and incubated at 37°C for 24h. S. aureus isolates were identified by standard methods.[8] Antimicrobial susceptibility testing for the S. aureus isolates was performed by modified Kirby–Bauer disc diffusion following Clinical Laboratory Standards Institute guidelines.[9] Methicillin resistance among S. aureus isolates was detected using cefoxitin disc (30 μg) test.[9]S. aureus ATCC 25923 and ATCC 43300 were used for quality control. MUP RL was detected with 5 μg mupirocin discs(HiMedia Laboratories, Mumbai, India). Strains showing zone diameters of≥14mm were considered susceptible.[10] The study patients were classified as MRSA colonized if MRSA was detected from either nares' culture. Participants were classified as non-MRSA colonizers when either the cultures grew methicillin-susceptible S. aureus(MSSA) or had negative results of culture. Participants colonized with both MSSA and MRSA were classified as MRSA colonized. The data obtained were analyzed by SPSS (Statistical Package for the Social Sciences) statistical software, version 17.0 (SPSS Inc., Chicago, Ill., USA).

   Results Top

Majority of the study patients were males(55.7%) with M:F 1.27:1. The age group31–50years(66.5%) was the most predominant[Table1]. Mean age of the study group was 43years (range, 18–72years). Median CD4+lymphocyte count was 354.5cells/mm 3 (range, 19–1090cells/mm 3). HIV-1 viral load testing(Taqman 48, Roche) was performed in three patients and the results were <34 copies/mL, 289 copies/mL, and 39,844 copies/mL.
Table 1: Demographic and clinical characteristics of study group (n=194)

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MRSA colonization in the anterior nares was found in 49patients(25.3%). Among them, 30(61.2%) were males with M:F 1.58:1. Mean age and median CD4+lymphocyte count among MRSA-colonized HIV-infected patients was 42years and 285cells/mm 3, respectively.

Analyzing the risk factors for MRSA nasal carriage, patients with antibiotic intake in the previous 3months(P=0.001) or those who had a percutaneous device in the previous year(P=0.001) were more likely to be MRSA colonized[Table2].
Table 2: Risk factors associated with methicillin-resistant Staphylococcus aureus colonization in study patients (n=194)

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Twenty-eight(19.6%) of 143patients on antiretroviral therapy(ART) had MRSA colonization. With a risk estimate of 0.4, patients on ART were less likely to be colonized with MRSA(P=0.004). Fewer number of HIV-infected patients with CD4+lymphocyte counts of≥500cells/mm 3 were colonized with MRSA[Table3].
Table 3: CD4+ lymphocyte counts (n=140) and methicillin-resistant Staphylococcus aureus colonization in study patients

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MUP RL was seen in 4(8.2%) isolates of MRSA. All strains of MRSA(49, 100%) were found to be sensitive to linezolid and vancomycin. Lower susceptibility rates were noted for erythromycin(8, 16.3%), ciprofloxacin (10, 20.4%), trimethoprim-sulfamethoxazole (19, 38.8%), clindamycin(33, 67.3%), and tetracycline(33, 67.3%).

   Discussion Top

Colonization and infections with MRSA have been increasingly reported in individuals infected with HIV. A6–18-fold increased risk has been noted for MRSA-attributable infections in HIV-infected individuals compared to that of general population.[11] One-fourth(25.3%) of our HIV-infected study patients had MRSA anterior nare colonization. Prior literature review reveals varying rates of MRSA colonization among HIV-infected adults[Table4]. This may be attributed to varied geographical locations, different patient populations, sample size, sampling techniques, intermittent MRSA colonization, and prevalence of ART in the study population.[1],[12] Extranasal sampling which was not done in our study can identify unrecognized carriers who can be potential reservoirs for transmission.[6] Inclusion of screening oropharynx, axilla, groin, perianal, wounds, and catheter insertion sites is known to increase the sensitivity of MRSA detection by up to one-third as compared to nasal screening alone.[13] This underlines the importance of extranasal sampling and including chlorhexidine bath in decolonization regimens along with intranasal mupirocin application.[11] It has been estimated that multiple sampling obtained at different time periods will help in identifying additional 20% S. aureus colonizers who may be missed if single sample is obtained.[14] It is also essential that we should be vigilant about the rise of multidrug-resistant(MDR) Gram-positive organisms even in those centers where high prevalence of MDR Gram-negative bacilli is an usual cause of concern.
Table 4: Methicillin-resistant Staphylococcus aureus colonization rates and risk factors for methicillin-resistant Staphylococcus aureus colonization among human immunodeficiency virus-infected individuals in various studies

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Over the years, increasing rates of MRSA infections preceded by colonization have been noted in HIV-positive patients.[1],[2] Among these infections, skin and soft-tissue infections predominate and include abscesses, cellulitis, furunculosis, impetigo, folliculitis, and carbuncles. Other common infections are bacteremia, endocarditis, pneumonia, and necrotizing fasciitis.[1] Shet et al. observed that all HIV-infected individuals(n=10) with MRSA skin and soft-tissue infections were colonized with the same strain that caused the infection.[15] Immune dysfunction, behavioral risk factors, and increased exposure to the health-care facilities have been the proposed mechanisms for increased infection rates with S. aureus.[2] Several defects in innate immunity have been suggested to predispose HIV-infected individuals to infections by S. aureus. These include decreased chemotaxis, neutropenia, reduced neutrophil bactericidal function, B-lymphocyte abnormalities, production of dysfunctional antibodies, and monocyte dysfunction.[1]

The risk factors for MRSA colonization as noted in various studies have been summarized in [Table4]. Recent antibiotic use(β-lactams), health-care exposure, central venous catheter, and dermatologic disease are the common risk factors for MRSA colonization. There are contradicting reports of high HIV viral load and low CD4+T-lymphocyte count predisposing for MRSA colonization. Trimethoprim-sulfamethoxazole prophylaxis has been found to be protective in some studies.[1] We found receipt of ART within the previous year to be associated with decreased risk for MRSA colonization, similar to the earlier observations.[12] Institution of ART according to standard guidelines, antibiotic stewardship, use of proper contact precautions in health-care facilities, and patient education on good hygiene practices can reduce the prevalence of MRSA colonization.

Increasing use of mupirocin has led to the reports of its resistance in MRSA strains.[7] Mupirocin resistance which reduces the effectiveness of decolonization is classified into MUP RL with MICs of 8–256 μg/mL and high-level mupirocin resistance(MUP RH) categories with MICs of≥512 μg/mL.[10] We noted MUP RL in 8.2% MRSA isolates. Chaturvedi et al.[23] found mupirocin resistance in 18.3%(15/82) MRSA clinical isolates of which Mu RL was found in 46.7%(n=7) strains. Recolonization is more commonly noted among isolates exhibiting low-level resistance.[7] MUP RH which was not determined in this study is associated with failure to eradicate MRSA in patients on mupirocin.[24] MUP RH isolates exhibit zone diameters of<14mm with 200μg mupirocin discs.[24] There is a need to generate local data on the prevalence of mupirocin resistance among MRSA isolates to aid in the selection of appropriate decolonization regimens.

The limitation of the study was that extranasal body sites were not screened and we did not have follow-up data of the colonized patients for the development of skin and soft-tissue infections and/or invasive disease or for determining persistent or transient carrier status. Efficacy of decolonization regimens in preventing infections can also be further studied in a cohort of HIV-infected patients.

   Conclusion Top

A significant proportion of HIV-infected patients had nasal MRSA colonization. Detection and monitoring for MRSA carriage status may be considered to reduce infections caused by MRSA in HIV-infected individuals.

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Conflicts of interest

There are no conflicts of interest.

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Correspondence Address:
Shashidhar Vishwanath
Department of Microbiology, Kasturba Medical College, Manipal University, Manipal - 576 104, Karnataka
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ATMPH.ATMPH_794_16

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