Skip to main content

Prevalence and risk factors of methicillin-resistant Staphylococcus aureus colonization among HIV patients in Mekelle, Northern Ethiopia


HIV-positive individuals are at higher risk of Methicillin Resistant Staphylococcus aureus (MRSA) colonization and its related infection. There is limited data in the nation on the prevalence and risk factors of MRSA colonization among HIV patients. The aim of this study was to address the existing knowledge gap. Cross sectional study was carried out from September 2014 to February 2015 in three selected health centers and one general hospital. A standardized questionnaire was developed for collection of socio-demographic and clinical data. A total of 498 Nasal and throat swabs (two for each patient) were collected from 249 patients, transported and processed using standard bacteriological procedures. Data was analyzed using Chi square (X2) test and associated risk factors were determined. P < 0.05 was considered statistically significant. Out of 249 study participants, S. aureus was isolated from 81 (32.5 %) patients, with MRSA colonization rate of 6 (2.4 %). MRSA isolates were resistant to Ciprofloxacin and trimethoprim-sulphamethoxazole (16.7 % each), clindamycin (33.3 %) and erythromycin (50 %). However, all MRSA isolates were 100 % sensitive to Amikacin. History of hospitalization, percutaneous device usage, patients with a household member’s hospitalization and low CD4 count (<200 cells/mm3) were significantly associated with S. aureus colonization (p < 0.05).


Methicillin resistant Staphylococcus aureus (MRSA), causes severe and fatal infections such as bloodstream infections, infective endocarditis, pneumonia, skin and soft tissue infections and is a global health issue (National Clinical Effectiveness Committee 2013). Though MRSA can infect all patients, HIV infected patients are more susceptible to MRSA due to their compromised immune system (Hidron et al. 2010; Lee et al. 2005; Bozzett et al. 2001).

The anterior nares are the most consistent site for MRSA colonization (Otto 2012; Wertheim et al. 2005), yet it can also colonize the axilla, inguinal region, throat, oropharynx, wounds and gastrointestinal tract (Otto 2012; Eveillard et al. 2006; Shahin et al. 1999).

MRSA transmission is mainly by direct contact through transient carriage from the hands of health care workers, contaminated equipment or with contaminated environmental surfaces (Lowy 1998).

MRSA infections have become increasingly problematic in both health care and community settings, leading to a greater morbidity, mortality, longer hospital stays, prolonged antibiotic administration and increased treatment costs (Government of Western Australia Department of Health 2013; Wertheim et al. 2005; Filice et al. 2010; Edem et al. 2013). Existing literatures show that, HIV patients are six to 18-fold more susceptible to MRSA than the general population, and is the main cause of bacteremia and endocarditis in these patients (Popovich et al. 2010; Tumbarello et al. 2002; Burkey et al. 2008; Furuno et al. 2011; Franzetti 2006).

There are few studies on MRSA colonization in HIV negative individuals in Ethiopia (Shibabaw et al. 2013; Kejela and Bacha 2013). However, there are no data on the prevalence and risk factors for MRSA colonization among HIV patients in the country. Therefore, this study was conducted to fill the existing knowledge gap by determining the nasal and throat colonization of MRSA and related risk factors in HIV-infected persons.


Study design, study period and study area

A cross-sectional study was conducted from September 2014 to February 2015 in three selected health centers and one hospital giving HIV care services, namely Kasech Health Center, Mekelle Health Center, Semen Health Center and Mekelle Hospital. These health facilities were (as the report on September 2014) providing HIV care services for a total of 5989 HIV-positive patients.

Sample size

It was determined by taking the prevalence of MRSA from South Africa, which was 21 % (Heysell et al. 2011) using the following formula: \({\text{n }} = {\text{Z}}^{ 2} \alpha / 2 {\text{ P }}\left( { 1- {\text{P}}} \right),( 1. 9 6)^{ 2} *0. 2 1\left( { 1- 0. 2 1} \right) = { 249}\).

$${\text{d}}^{ 2} \left( {0.0 5} \right)^{ 2}$$

A proportionate allocation formula (Pandey and Verma 2008) was used to determine the sample size from each health facility.

$${\text{n}}_{\text{j}} = \frac{\text{n}}{\text{N}}{\text{ N}}_{\text{j}} \quad\,\,\, {\text{j}} = { 1},{ 2},{ 3},{\text{ k}}$$

where, k is the number of strata and nj is sample size of the jth stratum

Nj is population size of the jth stratum

n = n1 + n2 + … + nk is the total sample size

N = N1 + N2 + … + Nk is the total population size

The sample size of each health facility is calculated as:

n1 (Mekelle Hospital) = 160; n2 (Kasech Health center) = 28; n3 (Semen Heath Center) = 25 and n4 (Mekelle Health Center) = 43.

Data sources and data collection

A well structured questionnaire in combination with a review of medical records were used to collect socio-demographic, risk factors and clinical characteristics of HIV positive individuals. Information collected include age, sex, hospitalization in the past 6 months, hospital visit in the past 12 months, under five children staying in daycare centers, homeless (current or past), prison (current or past), surgery in the past 1 year, household member’s hospitalization in the past 1 year, presence of percutaneous device in the past 1 year, oral antibiotic usage in the past 3 months, current use of Co-trimoxazole, most recent CD4 count.

Specimen collection, transportation, culturing and bacterial isolation

Nasal and throat swabs were collected using sterile cotton swabs pre-moistened with sterile normal saline using the standard procedure (D’Avila et al. 2008; Kumar et al. 2013; Dhuria et al. 2013). Nasal specimens were obtained by rotating a single swab 2–3 times around the inside of the anterior nares, whereas throat specimens were obtained by swabbing the posterior pharynx and lateral walls of the pharynx (tonsillar area), without touching the buccal mucosa or tongue. Swabs were then inoculated into the Stuart’s Transport media and transported to the Ayder referral hospital medical microbiology laboratory within 3–4 h. Swabs were inoculated onto Mannitol Salt Agar (MSA) (Oxiod, Hampshire, UK) and incubated at 37 °C aerobically for 24 h. After incubation, yellowish colonies from the MSA plate were sub-cultured to Nutrient Agar (Oxiod, Hampshire, UK) for further biochemical characterization. Bacterial identification was done based on colony morphology, color of the colonies and the tube coagulase test. MRSA isolates were identified using Cefoxitin disc by the Kirby-Bauer disk diffusion method (CLSI 2013).

Antimicrobial susceptibility pattern of MRSA to other antibiotics

The antimicrobial susceptibility testing of MRSA was detected using the modified Kirby-Bauer disk diffusion method according to the clinical laboratory standard institute (CLSI) guidelines (CLSI 2013). The following antimicrobials were used in their respective concentration: Ciprofloxacin (5 μg), Trimethoprim-Sulfamethoxazole (1.25/23.75 μg), Erythromycin (15 μg), Clindamycin (2 μg), and Amikacin (30 μg) (Hi-Media, India). These antimicrobials were selected based on the local usage to treat MRSA and considering the recommended antimicrobial agents for MRSA infections.

Data processing and analysis

Variables from the demographic and clinical data obtained from the questionnaire and laboratory data were cleaned and entered into a computer. Statistical analysis was done using SPSS version 20.0 for windows. X2 (Chi square) test was used to determine the association of risk factors. P < 0.05, considered as statistically significant and multivariate analysis was used to differentiate the independent risk factors for S. aureus colonization.

Quality control

Standard operating procedures (SOPs) were followed during sample collection, transportation, and processing steps. The quality of the culture media and antimicrobial disks were thoroughly checked using standard American Type Culture Collection (ATCC) reference strain of S. aureus ATCC 25923 obtained from Ethiopian Health and Nutritional Research Institute (EHNRI).

Ethical clearance

This study was ethically approved by the Ethical Review Committee (Ref. No-ERC0453/2014), College of Health Science Mekelle University. Written consent was obtained from the study participants or guardians. Patients who were positive for MRSA were contacted by the respective doctors for further management. All information of participants were kept confidential.


A total of 249 HIV positive individuals attending HIV care service in four health facilities were included in the study. The majority of the participants were females 174 (69.9 %). The age range of participants were 5–72 years with a mean age of 35 years. The majority 103 (41.4 %) of the participants were in the age group of 30–39 (Table 1). The overall rate of S. aureus and MRSA colonization among the 249 study participants were 81 (32.5 %) and 6 (2.4 %) respectively. Distribution of MRSA by nasal, throat and both sites were 3, 2, 1 respectively and for S. aureus was 41 (50.6 %), 28 (34.6 %) and 12 (14.8 %) respectively.

Table 1 Analysis of risk factors for Nasal and Throat colonization of S. aureus in HIV positive individuals attending HIV care service in Northern Ethiopia, September 2014–February 2015

Analysis of risk factors for S. aureus and MRSA colonization

Variables assessed as risk factors and found with a frequency of less than 10 % of the total 249 participants were excluded from the statistical analysis of risk factors for S. aureus. These include child aged under 5 years (0), homeless (4), prisoners (2), surgery in the past 1 year (3), recent intravenous antibiotic usage (0) and HIV positive individuals who have not started antiretroviral therapy (Pre-ART) (7). Two of the homeless, one of these previously prisoners, and two of these Pre-ART HIV patients were colonized with S. aureus. MRSA was not isolated from the prisoners, those with surgery in the past one year, and pre-ART, HIV patients, whereas one person among the homeless participants was colonized with MRSA.

Individuals in the age group of 70–79 years were more colonized by S. aureus; however, there was no statistical significance (p = 0. 59) (Table 1). All the six MRSA was isolated from the age groups of 20–49 years (Table 2). S. aureus colonization rate was higher among females 62 (35.6 %) as compared to males 19 (25.3 %). However, this was not statistically significant (p = 0. 113) (Table 1). All MRSA isolates 6 (3.4 %) were from females (Table 2).

Table 2 Analysis of risk factors for nasal and throat colonization of MRSA in HIV positive individuals attending HIV care service in Northern Ethiopia, September 2014–February 2015

Staphylococcus aureus colonization rate was statistically significant in individuals with the history of hospitalization, percutaneous device usage within the past 1 year, patients with a household member’s hospitalization within past 12 months and patients with CD4 count lower than 200 cells/mm3 (p < 0.05) (Table 1). Similarly, MRSA colonization was higher in patients with a history of hospitalization (Table 2). Risk factors for the colonization of S. aureus with statistical significance in the bivariate analysis were further analyzed using multivariate analysis and were found to be significantly associated (Table 3).

Table 3 Multivariate analysis of independent risk factors associated with S. aureus colonization among HIV positive individuals attending HIV care service in Northern Ethiopia, September 2014–February 2015

Antimicrobial susceptibility pattern of MRSA isolates

Antimicrobial susceptibility testing was performed on the six MRSA isolates against the commonly used antibiotics. Accordingly, 16.7, 33.3 and 50 % resistance were observed against Ciprofloxacin, Trimethoprim-Sulphamethaxazole, Clindamycin and Erythromycin respectively. Interestingly, all the isolates have shown 100 % sensitivity to Amikacin. However, three of the MRSA isolates (50 %) have shown multidrug resistance and all of them were isolated from HIV patients in hospital.


Our result indicates that the prevalence of S. aureus 81 (32.5 %) and MRSA 6 (2.4 %) was lower than similar studies conducted in San Francisco 55.2 % for S. aureus and 27.6 % for MRSA (Miller et al. 2003) and India 50.7–81 % for S. aureus and 18.3–42 % for MRSA (Dhuria et al. 2013). MRSA prevalence of 2.4 % was similar to the 5.1 % reported from Singapore (Kyaw et al. 2012). However, it was lower than report from other African nations with a rate of 20 % in Nigeria (Edem et al. 2013) and 21 % in Kwazu Natal Hospital South Africa (Heysell et al. 2011).

The low prevalence of S. aureus and MRSA colonization in our study might be due to the rare visit of these HIV patients to the health facilities, since repeated visits to health care centers, or contact with hands of health care workers in HIV infected individuals is the major risk factor for the colonization (Hidron et al. 2010; Lowy 1998; Government of Western Australia Department of Health 2013).

In our study, the inclusion of throat swabs increased the sensitivity of nasal screening of S. aureus and MRSA by 34.6 and 33.3 %, respectively, which was also shown by other studies conducted in Bristol, UK (Chow et al. 2012), Singapore (Kyaw et al. 2012) and Switzerland (Mertz et al. 2007).

In this study, recent hospitalization was associated with S. aureus colonization. This was also showed by other studies conducted in Singapore (Kyaw et al. 2012; Villacian et al. 2004) and TX, USA (Onorato et al. 1999). S. aureus and MRSA colonization rate was higher among those who visited hospitals, in the last twelve months; this is in line with the result of other study conducted in Singapore (Kyaw et al. 2012). Presence of percutaneous device within the past year was found to have a strong association with S. aureus and MRSA colonization. This result was supported by other studies conducted in Singapore (Kyaw et al. 2012) and in TX, USA (Onorato et al. 1999).

MRSA colonization was higher in those with Low CD4 count (less than 200/mm3) which was also shown by other studies conducted in Singapore (Villacian et al. 2004) and in Dallas, TX, USA (Cenizal et al. 2008). In our study the antimicrobial susceptibility pattern of MRSA isolates showed 100 % sensitivity to Amikacin which was similar to the study in India (Dhuria et al. 2013).


In this study there was a lower prevalence of MRSA; however, high degree of S. aureus colonization among the HIV patients. History of hospitalization, percutaneous device usage, patients with a household member’s hospitalization and CD4 count lower than 200 cells/mm3 were significantly associated with S.aureus colonization. MRSA isolates from HIV patients in hospital were more resistant than MRSA isolates obtained from health centers. All MRSA isolates were 100 % sensitive to Amikacin.


  • Bozzette SA, Joyce G, Mccaffrey DF, Leibowitz AA, Morton SC, Berry SH et al (2001) Expenditures for the care of HIV-infected patients in the era of highly active antiretroviral therapy. N Engl J Med 344:817–823

    Article  Google Scholar 

  • Burkey MD, Wilson LE, Moore RD, Lucas GM, Francis J, Gebo KA (2008) The incidence of and risk factors for MRSA bacteremia in an HIV-infected cohort in the HAART era. HIV Med 9:858–862

    Google Scholar 

  • Cenizal MJ, Hardy RD, Anderson M, Kathy Katz BS, Skiest DJ (2008) Prevalence of and risk factors for methicillin-resistant Staphylococcus aureus (MRSA) nasal colonization in HIV-infected ambulatory patients. J Acquir Immune Defic Syndr 48:567–571

    Article  Google Scholar 

  • Chow A, Win MK, Wong CS, Leo YS (2012) Universal methicillin-resistant Staphylococcus aureus (MRSA) screening: comparison of anatomic screening sites for patients with high and low prevalence of MRSA carriage. Infect Control Hosp Epidemiol 33:315–317

    Article  Google Scholar 

  • CLSI (2013) Performance standards for antimicrobial susceptibility testing. CLSI approved standard M100-S23. Clinical and Laboratory Standards Institute, Wayne

    Google Scholar 

  • D’Avila NE, Zhang L, Miller RG, D’Avila AC, Conceição AP, Boffo MS (2008) High prevalence of nasopharyngeal colonization by Staphylococcus aureus among children with HIV-1 infection in extreme southern Brazil. J Trop Pediatr 54(6):410–412

    Article  Google Scholar 

  • Dhuria N, Devi P, Devi B, Malhotra S (2013) Prevalence and risk factors for methicillin-resistant Staphylococcus aureus colonization in anterior nares of HIV- positive individuals. Wudpecker J Med Sci 2:026–029

    Google Scholar 

  • Edem EN, Onwuezobe IA, Ochang EA, Etok CA, Eyakndue EO (2013) Antibiogram of nasal isolates of Staphylococci in anterior nares of human immunodeficiency virus patients in the University of Uyo Teaching Hospital (UUTH) Uyo, Akwa Ibom State, Nigeria. J Microbiol Microb Res 1:7–12

    Google Scholar 

  • Eveillard M, De Lassence A, Lancien E, Barnaud G, Ricard JD, Joly-Guillou ML (2006) Evaluation of a strategy of screening multiple anatomical sites for methicillin-resistant Staphylococcus aureus at admission to a Teaching Hospital. Infect Control Hosp Epidemiol 27:181–184

    Article  Google Scholar 

  • Filice GA, Nyman JA, Lexau C, Lees CH, Bockstedt LA, Como-Sabetti K et al (2010) Excess costs and utilization associated with methicillin resistance for patients with Staphylococcus aureus infection. Infect Control Hosp Epidemiol 31:365–373

    Article  Google Scholar 

  • Franzetti F, Grassini A, Piazza M, Degl’innocenti M, Bandera A, Gazzola L et al (2006) Nosocomial bacterial pneumonia in HIV-infected patients: risk factors for adverse outcome and implications for rational empiric antibiotic therapy. Infection 34:9–16

    Article  Google Scholar 

  • Furuno JP, Johnson JK, Schweizer ML, Uche A, Stine OC, Shurland SM et al (2011) Community-associated methicillin-resistant Staphylococcus aureus bacteremia and endocarditis among HIV patients: a cohort study. BMC Infect Dis 11:1–7

    Article  Google Scholar 

  • Government of Western Australia Department of Health (2013). Infection Prevention and Control of methicillin-resistant Staphylococcus aureus (MRSA) in Western Australian Healthcare Facilities. Western Australia: Healthcare Associated Infection Unit (HAIU), Communicable Disease Control Directorate, Department of Health

  • Heysell SK, Shenoi SV, Catterick K, Thomas TA, Friedland G (2011) Prevalence of methicillin-resistant Staphylococcus aureus nasal carriage among hospitalized patients with tuberculosis in rural Kwazulu-Natal. S Afr Med J 101:332–334

    Article  Google Scholar 

  • Hidron AI, Kempker R, Moan A, Rimland D (2010) Methicillin-resistant Staphylococcus aureus in HIV-infected patients. Infect Drug Resist 3:73–86

    Article  Google Scholar 

  • Kejela T, Bacha K (2013) Prevalence and antibiotic susceptibility pattern of methicillin-resistant Staphylococcus aureus (MRSA) among Primary school children and prisoners in Jimma Town. Ann Clin Microbiol Antimicrob 12:1–11

    Article  Google Scholar 

  • Kumar S, Bandopadhyay M, Banerjee P, Laskar S (2013) Nasal methicillin-resistant Staphylococcus aureus colonization in HIV-infected patients from Eastern India. Saudi J Health Sci 2:14–17

    Article  Google Scholar 

  • Kyaw WM, Lee LK, Siong WC, Li Ping AC, Ang B, Leo YS (2012) Prevalence of and risk factors for MRSA colonization in HIV-positive outpatients in Singapore. AIDS Res Ther 9:1–6

    Article  Google Scholar 

  • Lee NE, Taylor MM, Bancroft E, Ruane PJ, Morgan M, Mccoy L et al (2005) Risk factors for community-associated methicillin-resistant Staphylococcus aureus skin infections among HIV-positive men who have sex with men. Clin Infect Dis 40:1529–1534

    Article  Google Scholar 

  • Lowy FD (1998) Staphylococcus aureus infections. N Engl J Med 1998(339):520–532

    Article  Google Scholar 

  • Mertz D, Frei R, Jaussi B, Tietz A, Stebler C, Fluckiger U et al (2007) Throat swabs are necessary to reliably detect carriers of Staphylococcus aureus. Clin Infect Dis 45:475–477

    Article  Google Scholar 

  • Miller M, Cespedes C, Vavagiakis P, Klein RS, Lowy FD (2003) Staphylococcus aureus colonization in a community sample of HIV-infected and HIV-uninfected drug users. Eur J Clin Microbiol Infect Dis 22:463–469

    Article  Google Scholar 

  • National Clinical Effectiveness Committee (2013) Prevention and control methicillin-resistant Staphylococcus aureus: national clinical guide line No. 2. Royal College of Physicians Ireland, Dublin, pp 1–20

    Google Scholar 

  • Onorato M, Borucki MJ, Baillargeon G, Paar DP, Freeman DH, Cole CP et al (1999) Risk factors for colonization or infection due to methicillin-resistant Staphylococcus aureus in HIV-positive patients: a retrospective case-control study. Infect Control Hosp Epidemiol 20:26–30

    Article  Google Scholar 

  • Otto M (2012) MRSA virulence and spread. Cell Microbiol 14:1513–1521

    Article  Google Scholar 

  • Pandey R, Verma R (2008) Samples allocation in different Strata for impact evaluation of developmental programme. Rev Bras Biom 26:103–112

    Google Scholar 

  • Popovich KJ, Weinstein RA, Aroutcheva A, Rice T, Hota B (2010) Community-associated methicillin resistant Staphylococcus aureus and HIV: interesting epidemics. Clin Infect Dis 50:979–987

    Article  Google Scholar 

  • Shahin R, Johnson IL, Jamieson F, Mcgeer A, Tolkin J, Ford-Jones EL (1999) Methicillin-resistant Staphylococcus aureus carriage in a child care following a case of disease. Arch Pediatr Adolesc Med 153:864–868

    Article  Google Scholar 

  • Shibabaw A, Abebe T, Mihret A (2013) Nasal carriage rate of methicillin-resistant Staphylococcus aureus among Dessie Referal Hospital health care workers; Dessie, Northeast Ethiopia. Antimicrob Resist Infect 2:1–5

    Article  Google Scholar 

  • Tumbarello M, Donati KG, Tacconelli E, Citton R, Spanu T, Leone F et al (2002) Risk factors and predictors of mortality of methicillin-resistant Staphylococcus aureus (MRSA) bacteraemia in HIV-infected patients. J Antimicrob Chemother 50:375–382

    Article  Google Scholar 

  • Villacian JS, Barkham T, Earnest A, Paton NI (2004) Prevalence of and risk factors for nasal colonization with Staphylococcus aureus among human immunodeficiency virus-positive outpatients in Singapore. Infect Control Hosp Epidemiol 25:438–440

    Article  Google Scholar 

  • Wertheim HF, Melles DC, Vos MC, van Leeuwen W, van Belkum A, Verbrugh HA, Nouwen JL (2005) The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis 5:751–762

    Article  Google Scholar 

Download references

Authors’ contributions

GG was the principal investigator, conceived the study, designed and data collection, laboratory works, data analyzed and drafted the manuscript for publication. MS was the Principal advisor for this study, designed the complete study, data collection, laboratory works, data analyzed and prepared for final version of the manuscript for publication. TT was the Co-Advisor, contributed designing of the study, data collection, Laboratory works and data analysis. AG and TA prepared and reviewed the initial and final draft of the manuscript. All authors read and approved the final manuscript.


We would like to acknowledge to the Tigray Regional Health Bureau and Tigray Health and Research Laboratory for financial and resource support. We would also like to acknowledge Mekelle Hospital, Mekelle Health center, Kasech health center and Semen Health center to conduct this study in the health facilities. We greatly acknowledge staff members of the ART clinic in each health facilities for their support during data collection and to the study participants. We would like to thank to the staff of microbiology laboratory of the Ayder Referral Hospital and Mekelle University.

Competing interests

The authors declare that they have no competing interests.

Author information

Authors and Affiliations


Corresponding author

Correspondence to Muthupandian Saravanan.

Rights and permissions

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (, 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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gebremedhn, G., Gebremariam, T.T., Wasihun, A.G. et al. Prevalence and risk factors of methicillin-resistant Staphylococcus aureus colonization among HIV patients in Mekelle, Northern Ethiopia. SpringerPlus 5, 877 (2016).

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: