|Year : 2020 | Volume
| Issue : 3 | Page : 444-447
Staphylococcus aureus colonisation in HIV-infected patients: Incidence, risk factors and subsequent skin- and soft-tissue infections
Aashirwad Panigrahy1, Sanjeev Sinha2, Bimal Kumar Das1, Arti Kapil1, Sreenivas Vishnubhatla3, Benu Dhawan1
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 Submission||03-Jan-2020|
|Date of Decision||31-Jul-2020|
|Date of Acceptance||06-Aug-2020|
|Date of Web Publication||4-Nov-2020|
Dr. Benu Dhawan
Department of Microbiology, All India Institute of Medical Sciences, New Delhi - 110 029
Source of Support: None, Conflict of Interest: None
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 2021 Jan 17];38:444-7. Available from: https://www.ijmm.org/text.asp?2020/38/3/444/299846
| ~ Introduction|| |
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., 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.
S. aureus contributes to 65% of all skin- and soft-tissue infection (SSTI) cases in HIV-infected population. The risk of SSTIs increases with previous colonisation of S. aureus. However, despite highly active antiretroviral therapy (HAART) introduction, the incidence of S. aureus infections continues to remain high. 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|| |
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. 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. 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. 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|| |
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|| |
The incidence of S. aureus colonisation in our patients was similar to that reported in previous studies.,, The nasal colonisation rates (22.3%) were also similar to studies done previously., 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. Our study observed MRSA colonisation rate of 7%, which lies within the range of 0%–17%, as reported previously.
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, 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). 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.
S. aureus colonisation in prior 6 months was observed to be significantly associated with the development of SSTIs. 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
Conflicts of interest
There are no conflicts of interest.
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