Antiseptics, disinfectants and hand hygiene products as reservoirs of antimicrobial resistance in healthcare facilities in sub-Saharan Africa: frequency, bacterial species and risk factors

Antimicrobial resistance is a worldwide public health problem, with low- and middle-income countries severely hit. Healthcare associated infections promote the spread of antimicrobial resistance, as associated pathogens are able to contaminate and survive in the hospital environment. These infections can be prevented by implementation of infection prevention standards and guidelines.

Hospital environment gained interest as reservoir of pathogens causing infections these last decades. In a Scoping review focused on high-income countries, we described the bacterial contamination of antiseptics, disinfectants and hand hygiene products (AS, DI and HH products). The affected products, the bacterial species and the risk factors across the life cycle of the products were addressed. Data from low- and middle-income countries is scarce, and the reasons behind the contamination of these products were not well described.

This thesis aimed to address these knowledge gaps. It focuses on bacterial contamination of AS, DI and HH products used in healthcare facilities in low- and middle-income countries. Gram-negative bacteria were of particular interest.

We conducted a systematic review (Chapter 1) according to a structured protocol registered in PROSPERO and based on the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) checklists. Articles published in low- and middle-income countries on outbreak investigations and cross-sectional surveys addressing bacterial contamination of AS, DI and HH products were included. This review showed that the problem of bacterial contamination of antiseptics, disinfectants and hand hygiene products in low- and middle-income countries, particularly sub-Saharan Africa, is overlooked. However, risk factors, the inaccessibility of quality water, hygiene and sanitation services, and the lack of functional infection prevention and control policies in the healthcare facilities of these countries suggest a more prominent and persistent presence of this problem. In the existing studies, water-based products such as quaternary ammonium compounds, chlorhexidine and liquid soaps were found to be affected. The laboratory methods used in the published studies were not standardized, generating low-quality data. Furthermore, the risk factors associated with bacterial contamination of the products were not well addressed.

To achieve further insight into the problem of the bacterial contamination of AS, DI and HH products in low- and middle-income countries, a cross-sectional survey (Chapter 2) was conducted in Burkina Faso and Benin. This cross-sectional survey used standardized microbiology methods including the use of neutralizer, selective media to optimize the growth of different Gram-negative bacterial species, and total bacterial colony count. Gram-negative isolates from in-use product containers, and from distribution and stock containers were identified by MALDI-TOF and their susceptibility to antibiotics tested. Close to three quarters of liquid soaps used in different hospital wards including neonatology, surgery and dialysis were contaminated by Gram-negative bacteria. The majority of these liquid soaps had a total bacterial count greater than 10,000 CFU/mL. Non-fermentative Gram-negative bacteria with Pseudomonas and Acinetobacter species were the most frequent. Enterobacterales, including Klebsiella pneumoniae and Enterobacter cloacae, and Vibrio non-cholerae/Aeromonas represented less than one-third of isolates. Half of Enterobacterales species were multidrug resistant organisms. Risk factors contributing to the contamination of the products included: the type of the product, the use/reuse of recycled containers, large volume-containers, the absence of labeling, the topping-up of containers, dilution of the products with tap water, expiry dates and the period after opening. These risk factors were mostly related to healthcare workers awareness, attitudes and practices.

A questionnaire-based survey (Chapter 3) was initiated to achieve a greater understanding of the risk factors behind the bacterial contamination of AS, DI and HH products in healthcare facilities in resource-limited settings. The questionnaire developed on KoboToolbox, and deployed on electronic tablets was self-administrated to the participating healthcare workers in presence of the investigating team. For this study, healthcare workers’ knowledge, awareness and practices regarding the products used in the hospital wards was assessed in three countries: Burkina Faso, Benin and DR Congo. Among the 617 (para)medical and auxiliary staff who consented to participate to the study, a moderate knowledge about the different categories of products, the storage conditions, the expiry date and date-after-opening, and their use was reported. Healthcare workers were not always aware about the vulnerability of chlorine 0.5%, alcohol-based hand rub and povidone iodine. Some common risk practice observed in the healthcare facilities when handling antiseptics were not considered as at risk. Although participants trained in IPC scored better than those not trained, the scores remained unsatisfactory. These findings suggest an urgent need for the training of healthcare workers in infection prevention and control. In addition to infection prevention and control, a focus on training in the management of AS, DI and HH products will be useful.

The findings from this thesis provide avenues for future investigations and highlight perspectives to improve the quality of use of AS, DI and HH products in hospitals in low- and middle-income countries.