The bacterial profile and antibiotic susceptibility pattern in respiratory tract samples from art-experienced HIV-positive adults in Uganda

PLOS ONE RESEARCH ARTICLE The bacterial profile and antibiotic susceptibility pattern in respiratory tract samples from art-experienced HIV-positive adults in Uganda Gloria Lubega ID1*, Andrew Abaasa1,2, Willyfred Ochola1, Bernard Kikaire3,4, Joseph Lutaakome1, Eugene Rugazira1,2, Yunia Mayanja ID1,2 a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 1 Medical Research Council /Uganda Virus Research Institute and London School of Hygiene and Tropical Medicine Uganda Research Unit, Entebbe, Uganda, 2 London School of Hygiene and Tropical Medicine, London, United Kingdom, 3 Uganda Virus Research Institute, Entebbe, Uganda, 4 Department of Paediatrics, College of Health Sciences, Makerere University, Kampala, Uganda * Abstract OPEN ACCESS Citation: Lubega G, Abaasa A, Ochola W, Kikaire B, Lutaakome J, Rugazira E, et al. (2023) The bacterial profile and antibiotic susceptibility pattern in respiratory tract samples from art-experienced HIV-positive adults in Uganda. PLoS ONE 18(8): e0282936. https://doi.org/10.1371/journal. pone.0282936 Editor: Giuseppe Vittorio De Socio, Azienda Ospedaliera Universitaria di Perugia, ITALY Received: February 26, 2023 Accepted: August 6, 2023 Published: August 31, 2023 Copyright: © 2023 Lubega et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: The author(s) received no specific funding for this work. Competing interests: The authors have declared that no competing interests exist. Introduction Microbial infections are a major cause of morbidity and mortality among people living with HIV (PLWH). Respiratory tract infections (RTIs) are responsible for approximately 70% of illnesses among PLWH. Drug resistant bacteria are highly prevalent among PLWH and this is a public health concern. Methods This is a retrospective analysis of data collected during the COSTOP trial between 2011 and 2013. Sputum collected on spot from participants presenting with a productive cough was examined using Gram, Ziehl-Neelsen stains and cultured on suitable bacteriological media. Antimicrobial sensitivity testing was done on isolated pathogens, by disc diffusion technique. Results We included 687 participants with mean age 41.3 (SD 8.2) years of whom 76.4% were female. Two hundred one sputum samples grew bacteria; Moraxella species (27.4%), Streptococcus pneumoniae(25.4%), Haemophilus influenza(22.4%), Mycobacterium species(4.5%), Pseudomonas species(4.0%), Staphylococcus aureus(4.0%), Escherichia coli (1.0%), Klebsiella species (1.0%), other bacteria (10.4%). A higher monthly income greater than or equal to 30$ (aOR = 0.63, 95%CI: 0.40–0.99) and longer duration since HIV diagnosis (aOR = 1.06, 95%CI: 1.0–1.11) were found to be independently associated with a positive bacterial culture. Moraxella sp, H. influenza and Pseudomonas had zero sensitivity towards cotrimoxazole. Sensitivity to erythromycin was low among Moraxella sp (28.6%), H. PLOS ONE | https://doi.org/10.1371/journal.pone.0282936 August 31, 2023 1 / 10 PLOS ONE Bacterial profile and antibiotic susceptibility in respiratory tract samples from HIV-positive adults influenza (31.6%) and S. aureus(42.9%) and other bacteria (42.9%). Most isolates were sensitive to Amoxicillin + Clavulanic acid and ceftriaxone. Conclusion There is a very low sensitivity of isolated bacteria to commonly prescribed antibiotics that are more available through the national supply chain, which is of public health concern. Urgent steps to tackle the high antimicrobial resistance among PLWH is required. Introduction For over three decades, Human Immunodeficiency Virus (HIV) infection remains a disease of public health importance with approximately 37.6 million people living with HIV (PLWH) globally in 2020 [1]. Sub-Saharan Africa (SSA) suffers the highest burden of HIV with nearly 70% of global HIV infections [2]. Since the introduction of antiretroviral therapy (ART), PLWH have an improved quality of life however, microbial infections are still a major cause of morbidity and mortality among this population [3], with approximately 70% of illnesses being respiratory tract infections (RTIs) [4, 5]. Ojha et al. reported a high prevalence (47%) of respiratory tract infections caused by bacterial pathogens among PLWH [5] and, factors associated with these infections include low CD4 counts (<200 cells/μl) and detectable viral loads [5, 6]. HIV infection causes a progressive depletion of CD4 T cells as well as an impairment of cellular and humoral immunity through a dysfunction of the T and B cells respectively [7]. A dysfunction of T cells leads to abnormal cellular responses while a dysfunction of B cells leads to a lack of antibody responses to infections. The resultant immune dysfunction, deregulation and depletion of CD4 lymphocytes causes an increased susceptibility to infections and the subsequent risk of other complications like resistant pathogens [8, 9]. HIV infection causes an alteration in lung host defences for example, it affects mucociliary function which may contribute to an increase RTIs among PLWH [9]. PLWH are at increased risk of hospital acquired infections due to their frequent contact with health care system through frequent clinic visits and admissions [10]. The frequent infections and admissions among PLWH, pill burden leading to unfinished doses and inappropriate use of drugs through self-medication due to easy access to over the counter drugs are some of the factors that have led to the development of antimicrobial resistance among this population [11]. Antimicrobial resistance is an emerging global problem of public health importance [4]. Previous studies have reported a much higher prevalence of drug resistant bacteria among PLWH (79%) compared to their HIV negative counterparts (30%) [10, 12]. Prophylactic cotrimoxazole given to PLWH over prolonged periods of time to prevent opportunistic infections has been reported to give rise to antibiotic resistance [13]. Resistant microbes are more difficult to manage since they require alternative medications and or higher doses of drugs, both of which are more expensive, not readily available in SSA and or toxic to the patient [13]. Additionally, laboratory capacity for identifying AMR is still limited in many parts of SSA; data are therefore still limited on antimicrobial susceptibility patterns among PLWH in SSA [10]. It is important to understand the common disease-causing pathogens among PLWH and current antibiotic susceptibility patterns for better management. We studied the susceptibility pattern of microorganisms isolated from respiratory samples taken from PLWH in central Uganda. PLOS ONE | https://doi.org/10.1371/journal.pone.02829 (...truncated)