Infection Prevention and Control at Lira University Hospital, Uganda: More Needs to Be Done

Globally, 5–15% of hospitalized patients acquire infections (often caused by antimicrobial-resistant microbes) due to inadequate infection prevention and control (IPC) measures. We used the World Health Organization’s (WHO) ‘Infection Prevention and Control Assessment Framework’ (IPCAF) tool to assess the IPC compliance at Lira University hospital (LUH), a teaching hospital in Uganda. We also characterized challenges in completing the tool. This was a hospital-based, cross-sectional study conducted in November 2020. The IPC focal person at LUH completed the WHO IPCAF tool. Responses were validated, scored, and interpreted per WHO guidelines. The overall IPC compliance score at LUH was 225/800 (28.5%), implying a basic IPC compliance level. There was no IPC committee, no IPC team, and no budgets. Training was rarely or never conducted. There was no surveillance system and no monitoring/audit of IPC activities. Bed capacity, water, electricity, and disposal of hospital waste were adequate. Disposables and personal protective equipment were not available in appropriate quantities. Major challenges in completing the IPCAF tool were related to the detailed questions requiring repeated consultation with other hospital stakeholders and the long time it took to complete the tool. IPC compliance at LUH was not optimal. The gaps identified need to be addressed urgently.


Introduction
Healthcare-associated infections (HCAIs) are those infections occurring in a patient during the process of care in a hospital or other healthcare facility, which was not present or incubating at the time of admission. This includes infections acquired in the hospital, but appearing after discharge [1]. HCAIs also include occupational infections that occur among the healthcare workers. Globally, 5-15% of hospitalized patients suffer from HCAIs and this is primarily due to poor infection prevention and control (IPC) practices in the hospitals. In low-income and middle-income countries (LMICs), the frequency of HCAIs is estimated to be more than double compared to high-income countries. A total of 16% of patients acquire HCAI at any given time in LMICs as compared to 5-7% of patients in high-income countries, reflecting the differences in compliance to IPC practices [2]. HCAIs result in increased duration of hospitalization, morbidity, mortality, and high costs for patients, families, and health systems. The current COVID-19 pandemic has emphasized the need for high levels of IPC in healthcare facilities and communities. Although not representative, data reported from many countries indicate that around 14-35% of COVID-19 cases reported to WHO are among health workers. Hence, implementation of IPC is crucial in healthcare facilities [3].
HCAIs are often caused by drug-resistant microbes present in water, food, and the environment of a hospital setting and transmitted by both patients and health workers due to poor IPC practices [4]. Decades of excessive antimicrobial use in humans and animals have led to the emergence of antimicrobial resistance (AMR) [5]. Every infection prevented equates to one less instance of antibiotic use. Thus, IPC is one of the main pillars of the global framework to reduce antimicrobial resistance (AMR). AMR is a growing threat to public health, reducing the ability of antimicrobial agents to control infections and causing a high burden of morbidity, mortality, and financial losses for the healthcare systems. Several studies have indicated that appropriate hand hygiene practices significantly reduce the risk of HCAIs, while poor hand hygiene along with overcrowded and understaffed health facilities are associated with steep increases in their prevalence [6][7][8]. Clearly, a high proportion of HCAIs are preventable through simple and effective IPC measures, such as hand hygiene and use of personal, protective equipment [9][10][11][12]. Health workers' knowledge and understanding, accompanied by the correct attitude toward IPC, is important for its effective implementation [13].
In Uganda, infectious diseases account for 18% of all hospital deaths and 37% of hospital admissions [14]. To combat AMR, Uganda has developed policies and guidelines including a "National Action Plan 2018-2023" against AMR to prevent, slow down, and control the spread of resistant microorganisms [14]. As a part of this plan, IPC guidelines are expected to be implemented throughout the country, led by an IPC committee at a national level and in every tertiary health facility.
In 2019, the World Health Organization (WHO) launched a global survey to encourage facility-level assessments of IPC and hand hygiene activities in order to gather a situational analysis on the level of IPC program compliance around the world [15]. Healthcare facilities are encouraged to complete an IPC Assessment Framework (IPCAF), a systematic IPC self-assessment tool. The IPCAF detects relevant problems and shortcomings needing improvements in order to meet international standards and requirements. Through repeated administration, this self-assessment tool, based on eight IPC core components, can document progress overtime and facilitate IPC progress [16].
To date, there is no information on the level of IPC compliance, strengths, and weaknesses in the implementation of IPC and the IPC assessment has never been conducted at Lira University Hospital (LUH), which is a teaching hospital that started in 2019 with the support of the African Development Bank.
The aim of this study was to assess the IPC compliance (i.e., adherence to WHO guidelines, training/education, availability of materials and personnel for IPC) at LUH, using the WHO IPCAF, specifically, (i) assessing the baseline level of IPC compliance, (ii) identifying strengths and gaps in implementing IPC activities at the facility, and (iii) reporting the challenges encountered by the IPC focal person in completing the IPCAF tool.

Study Design
This was a hospital-based cross-sectional study.

Setting
Uganda is a land-locked East African country with a population of 41.6 million in June 2020 (Uganda Bureau of Statistics). It borders South Sudan to the north, Kenya to the east, Tanzania and Rwanda to the south, and the Democratic Republic of Congo to the west. Uganda has 13 health regions with five national referral hospitals, 13 regional referral hospitals, 163 general hospitals, and a network of primary health centres. The mandate of implementing healthcare delivery in Uganda lies with the Ministry of Health (MoH), and the health service providers include public (government, including uniformed services and university hospitals), private not-for-profit (faith-based), private for-profit, and nongovernmental organisations (NGOs). Lira municipality, located in the mid-northern region of the country, is around 340 km from Kampala, the capital city of Uganda ( Figure 1). east, Tanzania and Rwanda to the south, and the Democratic Republic of Congo to the west. Uganda has 13 health regions with five national referral hospitals, 13 regional referral hospitals, 163 general hospitals, and a network of primary health centres. The mandate of implementing healthcare delivery in Uganda lies with the Ministry of Health (MoH), and the health service providers include public (government, including uniformed services and university hospitals), private not-for-profit (faith-based), private for-profit, and nongovernmental organisations (NGOs). Lira municipality, located in the mid-northern region of the country, is around 340 km from Kampala, the capital city of Uganda ( Figure 1).

Study Site
The study was conducted at LUH, which is a teaching hospital for the medical students in the University. The hospital has a capacity of 110 beds and is staffed by 97 healthcare workers. The hospital has several specialist departments including obstetrics, gynecology, pediatrics, surgery, medicine, and pathology and provides comprehensive health services to the general public.

Data Collection and Validation
Data were collected using the self-administered WHO IPCAF tool (supplementary Table S1). The tool has eight core components: (i) IPC programme, (ii) IPC guidelines, (iii) IPC education and training, (iv) HCAI surveillance, (v) multimodal strategies for implementation of IPC interventions, (vi) monitoring/audit of IPC practices and feedback, (vii) workload, staffing, and bed occupancy, and (viii) built environment, materials, and equipment for IPC at the facility level [17].
The clinical supervisor of the hospital acted as an IPC focal person and completed the IPCAF tool. Whenever in doubt, the clinical supervisor contacted the most informed people from each of the six departments mentioned above and filled in the information. The principal investigator cross-validated the information filled in by the clinical supervisor. The IPC focal person also reported on the challenges encountered in completing the IPCAF data tool and these were noted. The data were collected at LUH in November 2020.

Data Analysis and Statistics
The responses were assessed and scored as per the WHO guidelines. Every component of the IPCAF tool contributed to a score of 100 and, thus, the maximum score that could be obtained was 800. Based on the overall score, the IPC compliance was categorized as inadequate (0-200), basic (201-400), intermediate (401-600), and advanced (601-800) (see Table 1). Based on the responses in each component, a score was obtained and a percentage score was calculated (score obtained divided by the maximum component score multiplied by 100). Compliance against each component was graded based

Study Site
The study was conducted at LUH, which is a teaching hospital for the medical students in the University. The hospital has a capacity of 110 beds and is staffed by 97 healthcare workers. The hospital has several specialist departments including obstetrics, gynecology, pediatrics, surgery, medicine, and pathology and provides comprehensive health services to the general public.

Data Collection and Validation
Data were collected using the self-administered WHO IPCAF tool (supplementary Table S1). The tool has eight core components: (i) IPC programme, (ii) IPC guidelines, (iii) IPC education and training, (iv) HCAI surveillance, (v) multimodal strategies for implementation of IPC interventions, (vi) monitoring/audit of IPC practices and feedback, (vii) workload, staffing, and bed occupancy, and (viii) built environment, materials, and equipment for IPC at the facility level [17].
The clinical supervisor of the hospital acted as an IPC focal person and completed the IPCAF tool. Whenever in doubt, the clinical supervisor contacted the most informed people from each of the six departments mentioned above and filled in the information. The principal investigator cross-validated the information filled in by the clinical supervisor. The IPC focal person also reported on the challenges encountered in completing the IPCAF data tool and these were noted. The data were collected at LUH in November 2020.

Data Analysis and Statistics
The responses were assessed and scored as per the WHO guidelines. Every component of the IPCAF tool contributed to a score of 100 and, thus, the maximum score that could be obtained was 800. Based on the overall score, the IPC compliance was categorized as inadequate (0-200), basic (201-400), intermediate (401-600), and advanced (601-800) (see Table 1). Based on the responses in each component, a score was obtained and a percentage score was calculated (score obtained divided by the maximum component score multiplied by 100). Compliance against each component was graded based on the component score percentage: (i) inadequate (0-25%), (ii) basic (25.1-50%), (iii) intermediate (50.1-75%), and (iv) advanced (75.1-100%). IPC sub-components attaining the maximum score were considered "strengths" and components with zero or less-than-full scores were considered to be "gaps." The strengths and gaps are summarized in the tables segregated by each core component. The challenges encountered by the IPC focal person in filling the IPCAF tool were summarized as a narrative.

401-600 Intermediate
Most aspects of IPC core components are appropriately implemented. Continue to improve the scope and quality of implementation and focus on the development of long-term plans to sustain and further promote the existing programs.

601-800 Advanced
The IPC core components are fully implemented, according to the WHO recommendations, and appropriate to the needs of your facility.

Baseline Level of IPC Compliance at LUH
All the six departments of the Lira University Hospital were assessed. The overall IPC compliance score was 220/800 (27.5%), which equates to a 'basic' level of compliance. For the individual components of IPCAF, scores ranged from 0% to 77.5%. The scores for most of the IPCAF components ranged from 0-25%, which is considered an 'inadequate' level of compliance. The best compliance was observed in the 'Built Environment, materials, and equipment' component ( Table 2). The full details of the responses to the IPCAF questionnaire are shown in Supplementary Table S1.

Strengths and Gaps in Implementing IPC Activities at LUH
The strengths and gaps related to the different components of the IPC framework are detailed in Tables 3-5. Consistent with the scores, there were gaps in all the components, but the most numerous were observed under the IPC programme, IPC guidelines, and monitoring/audit components of the IPCAF tool.    Table 3 details the strengths and gaps in the IPC programme, guidelines, education, and training. There was no IPC programme in the hospital, no IPC team with full-time dedicated professionals trained in IPC and no IPC committee, comprised of multi-disciplinary staff members. Even the focal person identified for IPC did not have dedicated time to focus on IPC. No budgets were allocated for IPC activities in the hospital. Barring guidelines on hand hygiene, no other WHO-recommended guidelines were present in the facility. While the expertise to conduct the training was present, training programmes were rarely carried out for healthcare workers and no trainings were ever conducted for administrative and managerial staff, patients, or their family members. Table 4 details the strengths and gaps in surveillance and monitoring. None of the multimodal strategies recommended to promote IPC (system change, education and training, monitoring and feedback, communication and reminders, safety climate, and culture change) were used. While personnel responsible for surveillance were present and trained, no surveillance activities were conducted. Surveillance methods were not defined. Case definitions were not as per international standards and there were no processes to monitor data quality. Table 5 details the strengths and gaps in the 'built environment, materials, and equipment' and 'workload, staffing, and bed occupancy' components. Bed occupancy was maintained at one patient per bed and there was a system in place to assess and respond when adequate bed capacity was exceeded. All the essential services such as safe water for drinking and other purposes, electricity supply, sanitation, and disposal of hospital waste were available for the facility. Gaps in the built environment component included inadequate documentation of hygiene practices, presence of non-functional toilets, latrines, and waste management equipment. Disposable items and PPE equipment were not available in adequate quantities at all times.

Challenges Encountered by the IPC Focal Person in Completing the IPCAF Tool
The major challenge in filling the IPCAF tool was lack of knowledge on part of the IPC focal person about the contents of the questionnaire. It was observed that the tool is lengthy with many questions in different areas, which required consultation with several departmental heads. Due to the length, it took a long time to fill the questionnaire (1 to 3 h) and needed focused time away from the demands of routine work, which was perceived to be a major challenge.

Discussion
Our findings indicate that the IPC compliance at LUH was 'basic', meaning many aspects of the IPC core components were either not in place or not adequately implemented. Out of eight components on IPC compliance, five were graded 'inadequate.' Another related to IPC education and training was graded 'basic'. The one related to bed occupancy, staffing, and workload was graded 'intermediate' and only the last one related to the built environment, materials, and training was graded as 'advanced.' Additionally, major challenges were detected while filling in the WHO framework, linked mostly to the inadequate knowledge of the IPC focal person about the content of the tool and the length of time it took to respond to all the items on the questionnaire.
Previous studies conducted in Ghana and Uganda have reported similar findings. The study from Ghana using five of the WHO IPCAF core components found that 41.1% of the health facilities had a 'basic' level of compliance similar to what we found [17]. However, unlike LUH, 37.5% of these facilities in Ghana had senior level leaders participating in IPC activities and a dedicated budget was allocated [17]. In a study on implementation of IPC in health facilities in the Arua district of Uganda [18], 93.8% of these did not have an IPC committee, 93.8% reported an irregular supply of disposables and other supplies (such as gloves, soap, disinfectants), most facilities had no structures to monitor HCAI, and 72.6% never had in-service IPC training. However, the capacity to respond with adequate bed occupancy was present, which is similar to our findings. In contrast to LUH, a study from Germany revealed that 84.5% of the hospitals surveyed were in an 'advanced' level of IPC compliance [19]. While the overall compliance was good, multimodal strategies were graded 'inadequate' in the German study in line with our findings. The study from Germany also reported gaps in the components related to workload, staffing and bed occupancy, and built environment, materials, and equipment, where LUH performed better.
From a review in China, where 56 articles (including seven on hand hygiene and five on IPC education/training) qualified for data analysis, unlike LUH, where 98.1% of tertiary hospitals had an IPC committee, 67.2% had HAI surveillance, 85.8% had IPC guidelines, 75.5% provided post qualification IPC training, and 93.6% provided feedback on IPC performance indicators [20].
In a national survey conducted in Uganda in 2019, which included 42 health facilities including a national referral hospital, regional referral hospitals, general hospitals, private not for profit (PNFP) hospitals, private hospitals, and health centres. A total of 9.6% attained an advanced level, 52.4% had an intermediate level, 30.9% had a basic level like LUH, and 7.1% reached an inadequate level [21]. The overall average (433/800) level of compliance was graded 'intermediate', which was better than for LUH (Basic). Compared to LUH (basic), at least 60% of the health facilities had an 'intermediate' or better IPC level. Of the eight general hospitals, 37.5% had a 'basic' level like LUH. However, 37.5% had an 'intermediate' level and 12.5% had 'advanced' levels, which were better than LUH and 12.5% had a lower level (inadequate). In the five PNFP health facilities, 20% were at a 'basic' IPC level like LUH and the other 80% were at 'intermediate' (40%) and 'advanced' IPC levels. Unlike LUH, 78.5% had an IPC program, 71% had customized guidelines, 57% HCAI surveillance, 37% monitoring plan and targets, and 69% applied multimodal strategies. Like LUH, 50% had uninterrupted water, 67% adequate toilets, 67% adequate waste management supplies, and 93% adequate electricity supply, but, like LUH, 81% did not have an adequate supply of PPE and, in 40%, there was an unreliable supply of sterile and disposables items.
While testing the usability of WHO IPCAF in 46 countries, 52% of the respondents completed the tool in less than one hour [22], unlike, at LUH, where it took about two hours. This could be due to IPC trainings and exposure to the implementation in other countries, unlike LUH, which never had training and exposure to implementation. This implies that, with training and on-going IPC implementation, completing the tool becomes easier.
Our study had several strengths. We used a standardized tool recommended by the WHO to measure compliance to IPC policies and practices. Thus, the findings can be compared with those of other studies, which have used the same tool. This study provides a baseline assessment of IPC in LUH, which can be used to track progress when future assessments are done. We reported our study findings in line with STROBE (Strengthening the Reporting of Observational Studies in Epidemiology) guidelines. One limitation was that we conducted the study in a single hospital, and, thus, the findings have limited generalizability to other health care settings of Uganda.
Despite these limitations, the study has important implications. Based on the study findings, we make the following recommendations categorized into 3 groups: (i). "Easy to address recommendations", which include: starting an IPC programme led by an IPC committee consisting of multidisciplinary professionals, designating one of the committee members as the IPC focal person with dedicated time to focus on IPC activities, constituting an IPC team consisting of full-time professionals trained to implement IPC activities, drawing an IPC action plan, which will guide the team to implement improvement practices, based on strengths and gaps, reviewing IPC activities periodically in executive meetings attended by senior level staff, putting in place IPC guidelines and adapting them to the local context, (ii)"Recommendations with moderate resource implications", which include: instituting regular IPC monitoring, audit, and feedback, training all the health care providers, cleaners, and other personnel (such as administrative and managerial staff), patients and their family members in IPC practices utilizing in-house IPC expertise, putting in place a system of monitoring whether IPC practices are being implemented, providing feedback regularly to all the providers, providing adequate quantities of PPE and other disposable items, supplied in an uninterrupted manner since they are very vital even to prevent the spread of infections in the COVID-19 era, (iii) "Recommendations with major resource implications" which include: instituting HCAI surveillance, and putting in place a system for tracking the most important and relevant HCAIs in healthcare workers, e.g., tuberculosis, surgical site infections, hepatitis B, COVID-19, and Clostridium difficile, rolling out IPC guidelines and activities in other health facilities in Uganda to support IPC implementation, instituting follow-up assessments in future using the same tool in LUH and other health facilities so as to track the progress in implementing IPC policies and practice, and putting in place multimodal strategies to enhance IPC and allocating budgets for IPC activities.

Conclusions
In conclusion, the overall compliance to IPC in LUH in Uganda was not optimal. We identified serious gaps in multimodal strategies, supplies, and monitoring/surveillance. We have made specific recommendations for putting in place multimodal strategies and monitoring systems as well as for ensuring adequate and consistent supplies to address the gaps. The above recommendations include the drawing of an action plan, which must be implemented, with follow-up assessments using the same tool and feedback to track progress in LUH and other health facilities. We hope that such assessments will go a long way in improving IPC and in preventing HCAIs.