Increasing of New CA-MRSA Infections Detected in people living with HIV Who Engage in Chemsex in Barcelona: An Ambispective Study
verfasst von:
Lorena De La Mora, Cristina Pitart, Laura Morata, Ainoa Ugarte, María Martinez-Rebollar, Elisa De Lazzari, Andrea Vergara, Jordi Bosch, Ignasi Roca, Maria Piquet, Ana Rodriguez, Montserrat Laguno, Juan Ambrosioni, Berta Torres, Ana González-Cordón, Alexy Inciarte, Alberto Foncillas, Josep Riera, Irene Fuertes, Iván Chivite, Esteban Martinez, José L. Blanco, Alex Soriano, Josep Mallolas
There are no data on community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA) infections in the context of the chemsex phenomenon. This study aimed to characterize CA-MRSA-related infections in a cohort of people living with HIV (PLWH) who engage in chemsex.
Methods
At the Hospital Clinic of Barcelona, from February 2018 to January 2022, we analyzed CA-MRSA infections diagnosed in a cohort of PLWH who engage in chemsex. Epidemiological, behavioral and clinical variables were assessed. Mass spectrometry identification and antimicrobial susceptibility testing were performed on MRSA isolates. Pulse field electrophoresis was used to assess the clonality of the MRSA strains. The presence of Panton-Valentine leukocidin was also investigated.
Results
Among the cohort of 299 participants who engage in chemsex, 25 (8%) with CA-MRSA infections were identified, 9 at baseline and 16 with incident cases; the cumulative incidence was 5.5% (95% CI: 3.2%, 8.8%). The most common drugs were methamphetamine (96%) and GHB/GBL (92%). Poly-consumption and slamming were reported by 32% and 46%, respectively. CA-MRSA was isolated from the infection sites of 20 participants, and CA-MRSA colonization was confirmed in the remaining 5 persons. Seventy-one percent had used antibiotics in the previous year. All participants presented with skin and soft tissue infections, 28% required hospitalization, and 48% had recurrence. Of the 23 MRSA isolates further studied, 19 (82,6%) belonged to the same clone. Panton-Valentine leukocidin was detected in all isolates.
Conclusion
PLWH who engage in chemsex may present with CA-MRSA infections. Clinical suspicion and microbiological diagnosis are required to provide adequate therapy, and CA-MRSA prevention interventions should be designed.
Lorena De La Mora and Cristina Pitart contributed equally to the study.
Alex Soriano and Josep Mallolas contributed equally to the study as co-senior authors.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Key Summary Points
This study first reports an increasing incidence of community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA) infections in people living with HIV (PLWH) who engage in chemsex in Barcelona, Spain.
All participants presented with skin and soft tissue infections, more than one third required hospitalization, and half had recurrence. Empirical initial antibiotic therapy was not optimal in > 60% of the infections.
Methamphetamine and gamma-hydroxybutyric acid (GHB) were the drugs most prevalent used, and slamming was reported in almost half of the participants.
Panton-Valentin leukocidin was detected in all isolates, and clonality was demonstrated since > 80% of isolates were the same clone.
Clinical suspicion and microbiological diagnosis of CA-MRSA infections in PLWH who have engaged in chemsex are required to provide adequate therapy, and prevention interventions should be designed.
Introduction
There are no reports on community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA) infections in the context of the chemsex phenomenon. Chemsex is described as the intentional use of recreational drugs, before or during sex, among gay, bisexual and other men who have sex with men (gbMSM) with the aim of prolonging, improving and facilitating sexual intercourse; it has been associated with the transmission of HIV and other sexually transmitted diseases (STDs) through sexual risk behaviors [1]. Previously, CA-MRSA infections have been reported separately in gbMSM [2], PLWH [3] and people who use injected drugs [4] and/or smoke methamphetamine [5, 6] or use inhale nitrites and oral erectile dysfunction agents [3, 7]. All these situations described in the literature separately occur simultaneously in people who engage in chemsex. We hereby present the first report to our knowledge on CA-MRSA-related infections in this context, describing prevalence, incidence and clinical characteristics of the infections, MRSA clonality, treatment and prognosis, and patterns of drug use and sexual behavior.
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Methods
This is an ambispective longitudinal study carried out between February 2018 and January 2022 in the Hospital Clinic of Barcelona (HCB), Spain. HCB follows a prospective cohort of 299 PLWH who engage in chemsex, as a result of a pilot study [8] within the global cohort of nearly 6000 PLWH. The present study was developed within this prospective cohort. This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Institutional Review Board of the hospital (HCB/2017/0909), and all participants signed an informed consent form.
We included participants who had clinical and laboratory findings consistent with possible MRSA infection, plus (1) MRSA isolate from clinical specimens or (2) MRSA isolate from screening (colonization) specimens. All diagnoses of MRSA infections were detected in the outpatient HIV clinic, emergency department or, during the first 72 h of admission, if hospitalization was required.
Staphylococcus aureus was identified after isolation in agar plates, using MALDI-ToF spectrometry (Bruker Daltonics). Antimicrobial susceptibility was determined by disc diffusion in agar plates and broth microdilution methods using the Phoenix system (Becton Dickinson) following EUCAST guidelines [9]. Pulsed-field gel electrophoresis (PFGE) was chosen to study the clonality of the strains as it is considered the gold standard method and has the highest discriminatory power to assess whether a single clone is being transmitted in a cohort of patients. Isolates were considered within the same PFGE cluster (pulsotype) if their Dice similarity index was > 85%. All isolates were tested by PCR for the presence of lukF/lukS genes encoding Panton-Valentin leukocidin as previously described [10].
Demographic, HIV infection-related and other STD data, drug-use patterns and sexual behaviors in the last 3 months were collected from medical records and standardized surveys. Variables associated with the risk of acquiring CA-MRSA infections, clinical, microbiological characteristics, treatment and evolution of the infections were collected.
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Data were collected in a specific electronic case report form (eCRF) from the medical records system of the HCB (SAP®) and from an electronic survey administered to people who engage in chemsex. The eCRF and e-survey were implemented in the REDCap system hosted at the HCB.
Statistical Methods
Qualitative variables are described using absolute frequencies and percentages over valid values, and quantitative characteristics are described using the mean and standard deviation (SD) in case of normal distribution or median and interquartile range (IQR) in case of non-normality. The prevalence at baseline is calculated as the number of subjects with CA-MRSA infections at baseline over the total subjects included in the study and cumulative incidence over the CA-MRSA follow-up period as the number of subjects newly diagnosed during the follow-up divided by the total subjects included in the study. Both proportions are reported as percentages with 95% exact confidence intervals (95% CIs). Statistical analysis was performed using Stata (StataCorp. 2021. Stata: Release 17. Statistical Software. College Station, TX: StataCorp LLC).
Results
From the cohort of 299 people who engage in chemsex, 25 (8%) with CA-MRSA infections were identified during the study period, 9 at baseline and 16 with incident cases. Cumulative incidence was 5.5% (95% CI: 3.2%, 8.8%). Seventy-two percent were Latin Americans. The median CD4 count was 642 cells/mm3. All participants were treated with antiretroviral therapy, but 28% (7/25) presented a detectable VL. We assessed potential drug interactions with ART as part of the follow-up of individuals who engage in chemsex. To prevent these interactions, we always aim to switch the treatment to non-boosted regimens if possible. More information about sociodemographic and HIV clinical characteristics is described in Table 1.
Table 1
Sociodemographic and HIV infection-related characteristics
Demographic characteristics
Variable
Summary statistics
Mean (SD)
Age, years (N = 25)
39 (7)
n (%)
Region of origin (N = 25)
Spain
6 (24%)
Europe (w/o Spain)
1 (4%)
Latin America
18 (72%)
Period of arrival in Spain (N = 19)
< 2010
10 (53%)
2010–2014
2 (11%)
≥ 2015
7 (37%)
Educational level (N = 23)
Secondary
16 (70%)
University
7 (30%)
Serological data
Serology (positive test result)
n (%)
HBsAg (N = 25)
1 (4%)
Anti-HBs (N = 25)
22 (88%)
Anti-HBc (N = 25)
8 (32%)
IgG anti-HAV (N = 25)
21 (84%)
Nontreponemal tests, VDRL* (N = 25)
22 (88%)
IgG anti-HCV (N = 25)
5 (20%)
HCV RNA (N = 5)
1 (20%)
STD data
STD detected by PCR (positive test result)**
n (%)
Chlamydia trachomatis (N = 25)
5 (23%)
Neisseria gonorrheae (N = 25)
7 (32%)
Mycoplasma genitalium (N = 24)
6 (29%)
HIV data
Route of transmission (N = 24)
gbMSM—No intravenous drug use
23 (92%)
gbMSM—Intravenous drug use
1 (4%)
Lymphocyte subpopulations
Median (IQR)
Nadir CD4 + lymphocyte count (cells/mm³) (N = 25)
326 (190; 462)
CD4 + T lymphocyte count (cells/mm³) (N = 25)
642 (565; 812)
CD8 + T lymphocyte count (cells/mm³) (N = 25)
750 (602; 961)
CD4/CD8 ratio (N = 25)
0.9 (0.6; 1.3)
Viral load (VL)
VL
n (%)
VL HIV-1 PCR (N = 25)
Detectable
7 (28%)
Undetectable
18 (72%)
Detectable HIV VL (cp/mL) (N = 7)
Median (IQR) [n]
2170 (115; 95,700)
ART (N = 25)
Treatment
n (%)
NNRTI
5 (20%)
PI
4 (16%)
INSTI
16 (64%)
HBsAg hepatitis B surface antigen, Anti-HBs hepatitis B surface antibody, Anti-HBc hepatitis B core antibody, IgG anti-HAV hepatitis A virus IgG antibody, IgG anti-HCV hepatitis C virus IgG antibody, STDs sexually transmitted diseases, gbMSM gay, bisexual and other men who have sex with men, VL viral load, gbMSM gay, bisexual and other men who have sex with men, NNRTIs nonnucleoside reverse transcriptase inhibitors, PIs protease inhibitors, INSTIs integrase strand transfer inhibitors
*Positive nontreponemal tests refers to an individual's past clinical history
**STDs detected by PCR (overall locations: urethra, pharynx and rectum) at baseline or during follow-up of the chemsex cohort
Methamphetamine was the most used drug (96%). Polydrug use was reported by 32% (8/25) of the individuals. Forty-six participants disclosed injecting drugs (slamming) at least once; complete information about drug use and sexual behaviors can be found in supplementary material.
All CA-MRSA infections involved SSTIs, mainly abscess [68% (17/25)], predominantly located in at groin/buttocks/perineum and lower extremities [88% (22/25)], isolating MRSA from the infection sites in 20 participants. Twenty-eight percent (7/25) required hospitalization and 10 experienced recurrences during the study period. No cases of endocarditis were detected. From 24 participants screened for colonization, 54%, (13/25) were colonized.
Sixty-four percent of the participants (16/25) initially received non-active empirical treatment, later switching to the correct antibiotic therapy according to susceptibility results. Linezolid was the most commonly prescribed active drug. Fifty percent of the individuals (13/25) required surgery. All isolates were resistant to mupirocin, and 30% (6/25) and 45% (9/25) were resistant to clindamycin and cotrimoxazole, respectively. Complete CA-MRSA infection characteristics are reported in Table2.
Table 2
MRSA characterization
n (%)
Health care-associated risk factors
Antibiotic use (past 12 months) (N = 25)
19 (76%)
Dialysis (past 12 months) (N = 25)
0
Surgery (past 12 months) (N = 25)
1 (4%)
Hospitalization or long-term care facility admission, at least a 1-night stay (N = 25)
Prophylaxis for opportunistic infections with cotrimoxazole (past 12 months) (N = 25)
0
Diabetes (N = 25)
0
Liver disease (N = 25)
1 (4%)
Clinical characteristics
SSTI (N = 25)
25 (100%)
Bacteremia (N = 25)
3 (12%)
Pneumonia (N = 25)
1 (4%)
SSTI clinical presentation
Abscess
17 (68%)
Cellulitis*
14 (56%)
Folliculitis
2 (8%)
Furunculosis
7 (28%)
SSTI localization
Head/neck
4 (16%)
Trunk
5 (20%)
Upper extremities
4 (16%)
Groin/buttocks/perineum
11 (44%)
Lower extremities
11 (44%)
Other clinical characteristics
Hospitalization (N = 25)
7 (28%)
Recurrence** (N = 21)
10 (48%)
Colonization (N = 24)
13 (54%)
Nasal colonization (N = 13)
12 (92%)
Perineum colonization (N = 13)
1 (8%)
Treatment
Treatment: incision and drainage or surgery (N = 25)
13 (52%)
No treatment (N = 25)
1 (4%)
Antibiotics (N = 25)
24 (96%)
Ceftaroline (N = 24)
1 (4%)
Clindamycin (N = 24)
2 (8%)
Cotrimoxazole (N = 24)
2 (8%)
Dalbavancin (N = 24)
1 (4%)
Daptomycin (N = 24)
2 (8%)
Linezolid/tedizolid (N = 24)
17 (71%)
Teicoplanin (N = 24)
1 (4%)
Antibiotic resistance of MRSA isolates
n (%)
From the site of infection
Ciprofloxacin (N = 5)
5 (100%)
Clindamycin (N = 20)
6 (30%)
Cotrimoxazole (N = 20)
9 (45%)
Erythromycin (N = 20)
20 (100%)
Gentamicin (N = 20)
2 (10%)
Levofloxacin (N = 19)
18 (95%)
Linezolid (N = 19)
0
Mupirocin (N = 14)
14 (100%)
Oxacillin (N = 20)
20 (100%)
Penicillin (N = 20)
20 (100%)
Rifampicin (N = 20)
0
Teicoplanin (N = 13)
1 (8%)
Tobramycin (N = 13)
3 (23%)
Tetracycline
NDA
Vancomycin (N = 20)
0
SSTI skin and soft tissue infection, NDA no data available
*All patients with cellulitis were associated with other SSTIs
**More than one episode during the follow-up period, after the first diagnosis
Twenty-three CA-MRSA isolates were studied for clonal relatedness. PFGE showed that 19 strains belonged to the same clone, demonstrating high transmission in gbMSM who engage in chemsex (Fig. 1). Gene detection was positive for PVL-leukocidin in all isolates.
Fig. 1
Clonality study of Staphylococcus aureus strains (n = 23) by pulsed-field gel electrophoresis
×
Discussion
This is the first report to our knowledge of CA-MRSA infections in PLWH who engage in chemsex. We found a high prevalence and an increasing cumulative incidence of CA-MRSA infections coinciding with data previously described in PLWH [3, 11] related to immunological, behavioral, biological and environmental factors already communicated [12, 13]. All participants were on antiretroviral treatment, with a median CD4 count high, but almost a third had a detectable HIV viral load (VL). An uncontrolled HIV VL has been identified as another risk factor for CA-MRSA infections and recurrence [14, 15]. We have previously reported that people who engage in chemsex have significantly higher HIV viral load than general PLWH from our cohort [8], as one of the potential consequences of problematic chemsex practice.
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The majority of the participants were Latin Americans, related to the large immigrant population that attends our center and practices chemsex and to the higher risk of CA-MRSA infections that has been described in Latin American migrants living in our geographic area [16].
Regarding sexual behaviors, participants reported high risk sexual practices as well as a high prevalence of STDs. All of these circumstances have been described in the literature as a risks factors for CA-MRSA infections and colonization [2, 7, 17, 18].
Almost all participants reported having used methamphetamine. Non-injected methamphetamine is an independent risk factor for MRSA SSTIs [5] as it can cause skin-scratching behavior and skin breakdown. Additionally, injected methamphetamine can be associated with infections caused by the inoculation of microorganisms through the skin [4]. Almost half of the participants in our study reported having practiced slamming.
In a murine model, Mihu et al. demonstrated that methamphetamine delays wound healing, accelerates collagen degradation and alters host phagocytic functions. Moreover, methamphetamine induces S. aureus biofilm formation [6]. These findings strongly suggest that methamphetamine use may alter immunity and host response to S. aureus infections and may increase virulence of S. aureus by biofilm formation. This, along with the fact that more than half of the participants initially received an incorrect empirical treatment, and that all of them presented the PLV genes, related to a higher MRSA virulence and transmission [19], may have contributed to the hospitalization rate of 28% and the 50% of surgery needed.
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Related to health care-associated risk factors for MRSA infections, the high prevalence of antibiotic use in the last 12 months was remarkable, probably related to the previous STDs treatments.
All the participants in our sample presented with SSTIs coinciding with the most common type of MRSA infections in the general population and PLWH [2, 7, 14, 15], mainly located on the groin, buttocks and perineum, as previously reported by Diep et al. in gbMSM [20].
The high rate of recurrence of CA-MRSA infection is close to 50%. We believe that this may be connected to the lack of evidence for a proper decolonization pattern following treatment as well as the risk of recolonization if people continue in close contact with individuals who may be colonized but are unaware of it. Although people who engage in chemsex usually are not a closed-contact group, we believe that long-term decolonization guidelines should be explored while engaging in a risk practices.
More than half of the participants were initially treated with an incorrect empirical antibiotic treatment, probably because there was no clinical suspicion, because of the lack of data in the context of the chemsex phenomenon, highlighting the importance of communicating our results. We found almost 50% resistance to cotrimoxazole and 30% to clindamycin. This rate of resistance is high, but 82% of the cases belonged to the same clone that had spread among the same collective with this resistance pattern. The rate of cotrimoxazole resistance in our hospital is typically low (5–8%). However, 78% of the group had previously taken antibiotics, which may help to explain why resistance strain selection is more common in this cohort.
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PFGE showed that 19 of 23 strains belonged to the same clone, demonstrating high transmission in gbMSM who engage in chemsex. Gene detection was positive for PVL-leukocidin in all isolates. According to Deap et al. [20] in their analysis, the isolated clones with multiresistance patterns showed clinical characteristics comparable to those in our study. In another study conducted in sub-Saharan Africa, Gabon, [21] found a link between the existence of PVL and cotrimoxazole resistance. However, unlike the participants in our study who had not previously had cotrimoxazole therapy, these findings were made among those who had taken cotrimoxazole previously. Further studies to address the relationship among clones, resistance and virulence should be done.
One of the study limitations is that we were unable to assess all CA-MRSA infections in all people who engage in chemsex because not all were included in the cohort. Moreover, this was a single-center study during the COVID pandemic period; studies from other centers and in different time periods will be useful to confirm our data. We were unable to assess contact tracing for CA-MRSA infections in this study because of the characteristics of the population.
Conclusions
We describe the first series of CA-MRSA infections in PLWH engaged in chemsex, demonstrating clonality in almost all isolates. CA-MRSA should be a causative agent to consider when diagnosing a person who engages in chemsex with an SSTI. Clinical suspicion and microbiological diagnosis are needed, and the subsequent adjustment of empirical treatment should be individualized to avoid serious infections that require hospital admissions and surgery as well as screening for CA-MRSA colonization, and prevention strategies should be considered in this context.
Acknowledgements
We would like to express our gratitude to all of the study participants for their cooperation and their confidence in us.
Funding
The authors declare that no funds, grants or other support were received during the preparation of this manuscript. The journal’s rapid service fee was funded by the authors. We thank Ciber-INF and Fundación Bancaria la Caixa for providing unrestricted funding to develop general HIV research in our center.
Author Contributions
Lorena De La Mora, Maria Martínez-Rebollar, Josep Mallolas and Laura Morata designed the study. Lorena De La Mora, Laura Morata, Maria Martínez-Rebollar, Ana Rodriguez, Ainoa Ugarte, Montserrat Laguno, Juan Ambrosioni, Berta Torres, Ana González-Cordón, Alexy Inciarte, Alberto Foncillas, Josep Riera, Irene Fuertes, Ivan Chivite, Esteban Martínez, José Luís Blanco, Alex Soriano and Josep Mallolas recruited patients for the study. Cristina Pitart, Andrea Vergara, Jordi Bosch, Ignasi Roca and Maria Piquet were responsible for performing all microbiological analyses. Elisa De Lazzari, Lorena De La Mora, Maria Martínez-Rebollar, Ainoa Ugarte, Elisa De Lazzari, Montserrat Laguno and Cristina Pitart wrote the first version of the manuscript. Alex Soriano, Josep Mallolas, Esteban Martínez, Juan Ambrosioni, Alexy Inciarte, Irene Fuertes and Berta Torres reviewed the first version and made changes. All authors reviewed and approved the last version of the manuscript. Lorena De La Mora And Cristina Pitart contributed equally to the study. Alex Soriano and Josep Mallolas contributed equally to the study as co-senior authors. Maria Martínez-Rebollar is the corresponding author.
Prior Presentation
Part of these results has been presented in XIII Congreso Nacional GESIDA, 27–30 November 2022, Sitges, Barcelona, Spain, as an oral communication PO-28.
Disclosures
Lorena De La Mora has received fees to give lectures from Gilead, MSD, ViiV, AbbVie and Janssen-Cilag. Laura Morata has received honoraria for lectures from Pfizer, MSD, Menarin and Angelini. Ainoa Ugarte has received fees to give lectures from Gilead, MSD, ViiV, AbbVie and Janssen-Cilag. Maria Martínez-Rebollar has received fees to give lectures from Gilead, MSD, ViiV, AbbVie and Janssen-Cilag. Montserrat Laguno has received fees to give lectures from Gilead, MSD, ViiV, AbbVie and Janssen-Cilag. Juan Ambrosioni has participated in advisory boards and received consulting honoraria, research grants, or both, from Gilead Sciences, Janssen Pharmaceuticals, and ViiV Healthcare, all outside of this work. Berta Torres has received fees to give lectures from Gilead, MSD, ViiV, AbbVie and Janssen-Cilag. Ana González-Cordón has received fees to give lectures from Gilead, MSD, ViiV, AbbVie and Janssen-Cilag. Alexy Inciarte has received fees to give lectures from Gilead, MSD, ViiV, AbbVie and Janssen-Cilag. Ivan Chivite has received fees to give lectures from Gilead, MSD, ViiV, AbbVie and Janssen-Cilag. Esteban Martínez has received honoraria for lectures or advisory boards from Gilead and Janssen, and his institution has received research grants from MSD and ViiV. José Luís Blanco has received honoraria for lectures or advisory boards from Gilead, Janssen, and MSD. Alex Soriano has received honoraria for lectures and advisory boards from Pfizer, MSD, Menarini, Shionogi, Angelini and Gilead, and grants from Pfizer and Gilead. Josep Mallolas has received honoraria, speaker fees, consultant fees or funds for research from MSD, Roche, Boehringer-Ingelheim, ViiV, Gilead, Janssen, BMS, and AbbVie. Cristina Pitart, Elisa De Lazzari, Andrea Vergara, Jordi Bosch, Ignasi Roca, Maria Piquet, Ana Rodriguez, Alberto Foncillas, Josep Riera and Irene Fuertes have no conflicts of interest to declare.
Compliance with Ethics Guidelines
This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Institutional Review Board of the hospital (HCB/2017/0909), and all participants signed an informed consent form.
Data Availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
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Increasing of New CA-MRSA Infections Detected in people living with HIV Who Engage in Chemsex in Barcelona: An Ambispective Study
verfasst von
Lorena De La Mora Cristina Pitart Laura Morata Ainoa Ugarte María Martinez-Rebollar Elisa De Lazzari Andrea Vergara Jordi Bosch Ignasi Roca Maria Piquet Ana Rodriguez Montserrat Laguno Juan Ambrosioni Berta Torres Ana González-Cordón Alexy Inciarte Alberto Foncillas Josep Riera Irene Fuertes Iván Chivite Esteban Martinez José L. Blanco Alex Soriano Josep Mallolas
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