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BRIEF COMMUNICATION
Year : 2020  |  Volume : 38  |  Issue : 3  |  Page : 444-447
 

Staphylococcus aureus colonisation in HIV-infected patients: Incidence, risk factors and subsequent skin- and soft-tissue infections


1 Department of Microbiology, All India Institute of Medical Sciences, New Delhi, India
2 Department of Medicine, All India Institute of Medical Sciences, New Delhi, India
3 Department of Biostatistics, All India Institute of Medical Sciences, New Delhi, India

Date of Submission03-Jan-2020
Date of Decision31-Jul-2020
Date of Acceptance06-Aug-2020
Date of Web Publication4-Nov-2020

Correspondence Address:
Dr. Benu Dhawan
Department of Microbiology, All India Institute of Medical Sciences, New Delhi - 110 029
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijmm.IJMM_20_5

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 ~ Abstract 


We evaluated the incidence and risk factors of Staphylococcus aureus colonisation in 300 treatment-naïve HIV patients. Swabs from anterior nares and pharynx were cultured. Eighty-eight patients (29.3%) were colonised with S. aureus (47.7% nasal, 23.8% pharyngeal and 28.5% at both sites), which yielded 112 isolates. Methicillin-resistant S. aureus was detected in 25.9% (29/112) of isolates. Panton–Valentine leucocidin gene was present in 18.8% (21/112) of isolates. Multiple logistic regression analysis identified CD4 count <200 cells/mm3, public bath use, alcohol intake and other sexually transmitted infections as independent predictors for S. aureus colonisation. On follow-up, 22.7% of patients with S. aureus colonisation developed skin- and soft-tissue infections. Strategies for behavioural changes would be helpful in controlling S. aureus colonisation and subsequent infection.


Keywords: HIV patients, methicillin-resistant Staphylococcus aureus, Panton–Valentine leucocidin, skin- and soft-tissue infection, Staphylococcus aureus


How to cite this article:
Panigrahy A, Sinha S, Das BK, Kapil A, Vishnubhatla S, Dhawan B. Staphylococcus aureus colonisation in HIV-infected patients: Incidence, risk factors and subsequent skin- and soft-tissue infections. Indian J Med Microbiol 2020;38:444-7

How to cite this URL:
Panigrahy A, Sinha S, Das BK, Kapil A, Vishnubhatla S, Dhawan B. Staphylococcus aureus colonisation in HIV-infected patients: Incidence, risk factors and subsequent skin- and soft-tissue infections. Indian J Med Microbiol [serial online] 2020 [cited 2020 Nov 24];38:444-7. Available from: https://www.ijmm.org/text.asp?2020/38/3/444/299846





 ~ Introduction Top


Staphylococcus aureus is a commensal on human skin, with anterior nares being the most common site of colonisation. Being immunocompromised, HIV-positive patients present with higher colonisation as compared to a healthy population.[1],[2] Panton–Valentine leucocidin (PVL) helps in the colonisation, invasion and evasion of the immune system by S. aureus. It is a pore-forming toxin causing neutrophil lysis and apoptosis and contributes to tissue necrosis.[3]

S. aureus contributes to 65% of all skin- and soft-tissue infection (SSTI) cases in HIV-infected population.[4] The risk of SSTIs increases with previous colonisation of S. aureus.[5] However, despite highly active antiretroviral therapy (HAART) introduction, the incidence of S. aureus infections continues to remain high.[6] Therefore, additional information is required to define incidence rates and also to ascertain immunological and behavioural factors associated with staphylococcal colonisation in HIV-infected patients.


 ~ Materials and Methods Top


This prospective study was conducted from February 2018 to October 2019. Patients attending the Integrated Counselling and Testing Centre of AIIMS, New Delhi, were enrolled if they fulfilled the following inclusion criteria: treatment-naïve HIV-positive patients >18 years of age, whereas patients on antitubercular therapy and topical mupirocin use in anterior nares in the last 2 weeks were excluded from the study. Sociodemographic, clinical and behavioural data were collected through individual interviews in a structured pro forma. This study was approved by the institute's ethics committee (IECPG-699/31.01.2018).

Sample collection and microbiological analyses

A total of 300 patients were enrolled after obtaining written consent. Swabs were collected from the anterior nares and pharynx. Subsequently, they were cultured on Mannitol salt agar and blood agar and incubated aerobically overnight at 37°C. Suspected S. aureus colonies were isolated. Matrix-assisted laser desorption ionisation-time-of-flight mass spectrometry (VITEK MS, BioMerieux, India) was performed to confirm their identity. Patients with S. aureus colonisation were followed up 12 months for the development of SSTI.

Susceptibility to oxacillin was determined using cefoxitin (30 μg) disc diffusion method.[7] Disc diffusion method was used for susceptibility testing of penicillin (10 IU), gentamicin (10 μg), linezolid (30 μg), chloramphenicol (30 μg), ciprofloxacin (5 μg), cotrimoxazole (1.25/23.75 μg), rifampicin (5 μg), erythromycin (15 μg), clindamycin (2 μg) and mupirocin (5 μg) (HiMedia Mumbai, Maharashtra, India), and inducible resistance to clindamycin was detected by standard disc approximation test.[7] The minimum inhibitory concentrations of vancomycin were determined by E-test (AB Biodisk, Solna, Sweden).

PVL genes luk F and luk S were identified as described by previous polymerase chain reaction protocol.[3] Reference isolates 05-01290t127/STI/she luk PV and 06-01172t008/ST8/arc A luk PV (B. Strommenger, Robert Koch Institute, Germany) were used as controls. Amplicon of 433-bp size following agarose gel electrophoresis was indicative of the presence of PVL gene [Figure 1].
Figure 1: Polymerase chain reaction for Panton–Valentine leucocidin gene of Staphylococcus aureus. Lane 1: 100 bp DNA Ladder; lane 2: 756U Panton–Valentine leucocidin positive control (433 bp); lane 3, 5, 6: positive for Panton–Valentine leucocidin gene; lanes 4, 7, 8 and 9: negative for Panton–Valentine leucocidin gene; lane 10: negative control

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All statistical tests were two tailed, with P ≤ 0.05 considered statistically significant. Multivariable logistic regression analysis was performed to identify the variables independently associated with S. aureus colonisation. Stata software version 12.1 (StataCorp., Texas, USA) was used for analyses.


 ~ Results Top


The mean age of HIV patients was 34 10.39 years, with 218 (72.6%) being males, with 218 (72.6%) being males. Six hundred swabs were collected from the 300 patients. Eighty-eight patients (29.3%) were colonised with S. aureus (47.7% nasal, 23.8% pharyngeal and 28.5% at both sites), which yielded 112 isolates. Methicillin-resistant S. aureus (MRSA) was detected in 25.9% (29/112) of isolates. MRSA colonisation was observed in 7% (21/300) of the patients.

All the isolates were uniformly susceptible to rifampicin, linezolid, mupirocin and vancomycin. Inducible clindamycin resistance phenotype was observed in 16.1% of the isolates. MRSA isolates showed higher level of resistance to non-β-lactam antimicrobials compared to MSSA isolates, with difference being statistically significant for ciprofloxacin, gentamicin, erythromycin and cotrimoxazole (P < 0.05). PVL gene was present in 18.8% (21/112) of isolates, which were obtained from 18 patients.

Multiple logistic regression analysis identified four independent factors to be significantly associated with S. aureus colonisation, namely, CD4 count <200 cells/mm3, public bath use, alcohol intake and other sexually transmitted diseases. Current intake of antibiotics appeared to have a protective effect [Table 1].
Table 1: Association of study characteristics of patients with Staphylococcus aureus colonisation (n=300)

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Amongst the HIV-infected patients with S. aureus colonisation (n = 88), 22.7% developed SSTI during the study period. The most common type of SSTIs was pustules (30%), followed by abscesses (25%), furuncles (25%), folliculitis (10%) and cellulitis (5%). Culture specimens were obtained from eight of the twenty SSTI cases. Culture was positive for S. aureus in four patients, of which one isolate was MRSA. Other organisms isolated were Staphylococcus haemolyticus (three patients) and Staphylococcus epidermidis (one patient). PVL gene was positive in all the four S. aureus isolates from SSTI.


 ~ Discussion Top


The incidence of S. aureus colonisation in our patients was similar to that reported in previous studies.[2],[5],[6] The nasal colonisation rates (22.3%) were also similar to studies done previously.[8],[9] Culturing of swabs from anterior nares is commonly used for the detection of S. aureus carriers, but in our study, an additional culture of pharyngeal swab increased detection by 23.8%, as was also observed by Crum-Cianflone et al.[5] Our study observed MRSA colonisation rate of 7%, which lies within the range of 0%–17%, as reported previously.[10]

MRSA isolates showed higher level of resistance to non-β-lactam antimicrobials compared to MSSA isolates, suggesting careful use of antibiotics for empirical antimicrobial treatment of infections due to MRSA. Mupirocin has been effectively used topically for eradication of S. aureus nasal carriage,[2] and none of the S. aureus isolates showed resistance to mupirocin, in our study.

S. aureus colonisation was observed to be higher in patients with low CD4 count (<200 cells/mm3).[11] In our study, specific behaviours were significant predictors for S. aureus colonisation, suggesting that increased colonisation rates during the HAART era may no longer be attributed to immunosuppression only. We observed the presence of PVL gene in 18.8% of all S. aureus isolates. This is an issue of potential concern because isolates with PVL have been largely associated with SSTIs.[12]

S. aureus colonisation in prior 6 months was observed to be significantly associated with the development of SSTIs.[5] Almost one-fourth of the HIV-infected patients with S. aureus colonisation developed SSTIs during the follow-up period. Fifty percent of all patients with SSTI had prior PVL-positive S. aureus colonisation.

In summary, the high proportions of MRSA and concomitant occurrence of PVL is a matter of concern. Dissemination of PVL-positive MRSA represents a significant challenge to infection control. We observed that besides immunological factor, certain behavioural factors also determine S. aureus colonisation. Therefore, this information will be useful to define strategies for behavioural changes to prevent S. aureus colonisation and subsequent infection in HIV-infected patients.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
 ~ References Top

1.
Kotpal R, Krishna Prakash S, Bhalla P, Dewan R, Kaur R. Incidence and risk factors of nasal carriage of Staphylococcus aureus in HIV-infected individuals in comparison to HIV-uninfected individuals: A case-control study. J Int Assoc Provid AIDS Care 2016;15:141-7.  Back to cited text no. 1
    
2.
Neupane K, Rayamajhee B, Acharya J, Rijal N, Shrestha D, Binod GC, et al. Comparison of nasal colonization of methicillin-resistant Staphylococcus aureus in HIV-infected and Non-HIV patients attending the national public health laboratory of central Nepal. Can J Infect Dis Med Microbiol 2018;2018:4508757.  Back to cited text no. 2
    
3.
Lina G, Piémont Y, Godail-Gamot F, Bes M, Peter MO, Gauduchon V, et al. Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis 1999;29:1128-32.  Back to cited text no. 3
    
4.
Hemmige V, McNulty M, Silverman E, David MZ. Recurrent skin and soft tissue infections in HIV-infected patients during a 5-year period: Incidence and risk factors in a retrospective cohort study. BMC Infect Dis 2015;15:455.  Back to cited text no. 4
    
5.
Crum-Cianflone NF, Wang X, Weintrob A, Lalani T, Bavaro M, Okulicz JF, et al. Specific behaviors predict Staphylococcus aureus colonization and skin and soft tissue infections among human immunodeficiency virus-infected persons. Open Forum Infect Dis 2015;2:ofv034.  Back to cited text no. 5
    
6.
Nguyen MH, Kauffman CA, Goodman RP, Squier C, Arbeit RD, Singh N, et al. Nasal carriage of and infection with Staphylococcus aureus in HIV-infected patients. Ann Intern Med 1999;130:221-5.  Back to cited text no. 6
    
7.
Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing. Twenty-Eighth Informational Supplement CLSI Document MP100-S28, Wayne, PA: Clinical and Laboratory Standards Institute; 2018.  Back to cited text no. 7
    
8.
Villacian JS, Barkham T, Earnest A, Paton NI. Prevalence of and risk factors for nasal colonization with Staphylococcus aureus among human immunodeficiency virus-positive outpatients in Singapore. Infect Control Hosp Epidemiol 2004;25:438-40.  Back to cited text no. 8
    
9.
Miller M, Cespedes C, Bhat M, Vavagiakis P, Klein RS, Lowy FD. Incidence and persistence of Staphylococcus aureus nasal colonization in a community sample of HIV-infected and -uninfected drug users. Clin Infect Dis 2007;45:343-6.  Back to cited text no. 9
    
10.
Hidron AI, Moanna A, Rimland D. The rise and fall of methicillin-resistant Staphylococcus aureus infections in HIV patients. AIDS 2011;25:1001-3.  Back to cited text no. 10
    
11.
Reinato LA, Pio DP, Lopes LP, Pereira FM, Lopes AE, Gir E. Nasal colonization with Staphylococcus aureus in individuals with HIV/AIDS attended in a Brazilian teaching hospital. Rev Lat Am Enfermagem 2013;21:1235-9.  Back to cited text no. 11
    
12.
Boan P, Tan HL, Pearson J, Coombs G, Heath CH, Robinson JO. Epidemiological, clinical, outcome and antibiotic susceptibility differences between PVL positive and PVL negative Staphylococcus aureus infections in Western Australia: A case control study. BMC Infect Dis 2015;15:10.  Back to cited text no. 12
    


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