The burden of healthcare-associated infection in Ethiopia: a systematic review and meta-analysis

Background Different primary studies in Ethiopia showed the burden of nosocomial infection across geographical setting and variant period. However, the national level of burden and types of healthcare-associated infections were unknown. Hence, this systematic review and meta-analysis estimated the overall nationwide burden and types of healthcare-associated infections in Ethiopia. Methods We searched PubMed, Science Direct, Google Scholar, African Journal Online, and Addis Ababa University repository by date April 7, 2020. To assess publication bias, Egger’s test regression analysis was applied. Weight-inverse random-effect model meta-analysis was used. Subgroup analysis was conducted based on ward type, study region, study design, sample size and diagnostic method, ward type, and study participants. Results A total of 18 studies with 13,821 patients participated in the overall prevalence estimation. The pooled prevalence of healthcare-associated infection was 16.96% (95% CI 14.10–19.82). Specifically, surgical site infection (39.66%), urinary tract infection (27.69%), bloodstream infection (19.9%), dual infections (SSI and UTI) (14.01%), and respiratory tract (13.51%) were the commonest types of healthcare-associated infection. In subgroup analysis, the highest overall prevalence was observed as surgical, gynecology, and obstetrics ward (22.42%). Conclusions The national prevalence of healthcare-associated infection remains high. The most common type of HCAI was surgical site infection, followed by urinary tract infection, bloodstream infection, SSI and UTI, and respiratory tract infection. The overall prevalence was highest in surgical, gynecology, and obstetrics ward. Hence, infection prevention and control should be a priority agenda in healthcare with due emphasis for surgical patients.


Background
Healthcare-associated infection (HCAI) is a preventable infection that a patient can encounter in a healthcare facility while receiving medical care [1,2]. It occurs after 48 h of hospital admission, up to 3 days after discharge, or up to 30 days after the operation when someone was admitted for reasons other than infection [2]. Surgical site infection (SSI), urinary tract infection (UTI), bloodstream infection (BSI), and pneumonia or respiratory tract infection (RTI) were the commonest types of HCAI elsewhere [1].
According to the World Health Organization (WHO) 2019 HCAI fact sheet report, a hundred million patients were affected each year globally. This report added that the point prevalence of HCAI was estimated in the ranges between 3.5-12% and 5.7-19.1% in developed and low-and middle-income countries, respectively [3]. Nosocomial infection (NI) was found between 1.6 and 28.7% in Sub-Saharan Africa [4]. Specifically, the overall prevalence of HCAI was found in Botswana (13.4%) [5] and South Africa (8%) [6]. Regarding types of HCAI, a meta-analysis showed that RTI, UTI, SSI, and BSI from highest to lowest magnitude in order were found worldwide, but SSI (51.1%) was the leading in Africa [7]. Unlikely, nosocomial UTI was the utmost (35%) in Morocco Rabat hospitals [8].
Healthcare infections increase morbidity, mortality, long-term disability [9], hospital stay [10], microbial resistance to antibiotics [11], and healthcare costs for patients and their families [12]. Besides, it upsurges the financial burden on the healthcare system [9]. Hence, "clean care the safer care" program has been launched since 2004 with the WHO patient safety directive, which was aimed to reduce HCAI through improving hand hygiene practice at the center of achieving its aim [13]. Similarly, infection prevention and control guideline was developed for health facilities [14], and infection prevention and control policy recommendations initiated by WHO has been implemented in Ethiopia. Yet, HCAI remains the global public health problem elsewhere.
In the Ethiopian setting, different studies had been conducted to find the overall prevalence of HCAI and its type. The overall prevalence of HCAI was found in the ranges of 9 to 35.8% [15][16][17][18]. Concerning types of HCAI, SSI (13.5 to 52%) [15,17,18], RTI (5 to 19%) [12,17], UTI (9.5 to 48%) [16,18,19], and BSI (4.3 to 46.6%) [20,21] predominated in the country. However, all of the studies showed great variation across geographical setting and variant period. This discrepancy between studies makes it difficult to represent the national prevalence. Having national representative data is real to underpin effective prevention and control strategies. Thus, a need to have a pooled estimation of HCAI was necessitated at the country level. Therefore, this systematic review and meta-analysis aimed to estimate the overall pooled prevalence of HCAI and its types in Ethiopia.

Reporting
The results of this review were reported based on the Preferred Reporting Items for Systematic Review and Meta-analysis (PRISMA) statement guideline [22] (Additional file 1 research checklist), and it is registered in the PROSPERO database:(PROSPERO ID CRD42020183158).

Study selection
Retrieved studies were exported to the Endnote version 8 (Thomson Reuters, London) reference manager software to remove duplicate studies. Two independent reviewers screened the title and abstract. The disagreement was handled based on established article selection criteria. Two independent authors conducted the abstract and full-text review.

Eligibility criteria Inclusion criteria
Included studies were articles that reported the prevalence in general and/or at least one type of healthcareassociated infection. It also included studies published in English and studies conducted only in Ethiopia.

Exclusion criteria
Articles without full-text available and qualitative studies were excluded. Likewise, reviews, commentaries, consultants' corners, letters, and conference abstracts were not considered.

Quality assessment
We used Joanna Briggs Institute (JBI) quality appraisal criteria [23]. The tool consists of nine major items. The first item is appropriate to the sample frame. The second is the appropriate sampling technique. The third is the adequacy of the sample size. The fourth is a description of the study subjects and settings. The fifth is enough coverage of data analysis. The sixth is the validity of the method for identification of the condition. The seventh item is a standard and reliable measurement for all participants. The eighth is the appropriateness of statistical analysis. And the last item is adequacy and management of response rate. Studies were considered low-risk when it would fit 5 or above quality assessment checklists. Two independent authors appraised the quality of studies. The disagreement was resolved by the interference of a third reviewer.

Data extraction
Two authors extracted data using the standardized format. The name of the first author and year, study region, study design, ward type, diagnostic method(s), sample size, the prevalence for overall, and types of HCAI were extracted. Whenever variations are observed, the phase was repeated. If discrepancies between data extractors continued, the third reviewer was involved.

Statistical analysis
The required data were collected using a Microsoft Excel 2013 workbook. Then, the STATA version 11 statistical software was used for meta-analysis. Publication bias was objectively checked using Egger's regression test analysis [33]. Heterogeneity of studies was quantified using the I-squared statistic, in which 25, 50, and 75% represented low, moderate, and high heterogeneity, respectively [34]. Pooled analysis was conducted using a weighted inverse variance random-effects model [35]. Subgroup analysis was done by the region, study design, diagnostic method, and sample size. Besides, subgroup analysis was done based on ward type and study participants to overcome the inflation of the pooled effect from the inclusion of studies done across various wards and study participants with the age difference. Sensitivity analysis was employed to see the effect of a single study on the overall estimation.

Literature search
The search strategy retrieved 1440 articles from PubMed, 398 from Science Direct, 3 from African Journal Online, 79 from Google Scholar, and 3 from Addis Ababa University repository. After duplication was removed, 1882 remained. Eighty studies were screened for full-text review. Finally, 18 studies were used for meta-analysis (Fig. 1).
Eleven of the studies have reported types of HCAI [10, 12, 15-18, 20, 21, 26, 28, 32] (Additional file 2). We assessed studies with JBI quality appraisal checklists. Based on this, none of the included studies was of poor quality status.

Meta-analysis
The burden of healthcare-associated infection The absence of publication bias was assessed with Egger's regression test analysis (p = 0.456), which showed no publication bias.

Sensitivity analysis
Endalafer et al. [15] and Sahile et al. [20] had shown an impact on the overall estimation of the meta-analysis result (Fig. 6).

Discussion
The Sustainable Development Goal (SDG) goal-3 is implemented to ensure access to quality essential healthcare services in every country [37]. However, HCAI confronts quality in healthcare systems that fail to build strong principles to reduce the risks and spread of nosocomial infection [38]. Thus, HCAI has been continued as preventable causes of morbidity, mortality, and spending health system cost.
This meta-analysis estimated the country level overall pooled prevalence of healthcare-associated infection and types in Ethiopia. Accordingly, the overall pooled prevalence of HCAI was 16.94% (95% CI 14.06-19.81) (Fig. 2). This result was higher than studies done in China (3.12%) [39], Morocco (10.3%) [8], Botswana (13.54%) [5], and South Africa (7.67%) [6]. The possible reasons for high prevalence in this study might be very low hand hygiene practice, low adherence to infection prevention practice, low level of job satisfaction, morally distressed nurses, resource constraints, low implementation of the nursing process, and less attention given to healthcareassociated infection.
Keeping hand hygiene before patient contact is vital to prevent NI. However, only 7% of physicians working at two university hospitals in Addis Ababa Ethiopia performed hand hygiene before patient contact [40]. Evidence also showed that 35% of nurses were nonadherent to infection prevention practices in Southwest Ethiopia [41]. Besides, nearly 68% of health professionals were less satisfied with their work in the Amhara region [42]. Additionally, about 84% of nurses were morally distressed in the northwestern part of the country [43]. As a result, acquisition of HCAI from unsafe hands of unsatisfied healthcare providers augmented by less adherence to infection prevention and morally less prepared nurses might limit the quality of patient care in healthcare facilities. These may in turn increase HCAI in the country. Healthcare workers (HCWs) disposed of that lack of hand hygiene agents and sinks in public hospitals of Addis Ababa Ethiopia [40]. The implementation of the nursing process was below half (49%) in the northwestern part of the country [44]. Furthermore, healthcare providers, patients, and/or families are more  curious about the primary reason for admission or healthcare visits. Therefore, resource shortage preclude infection prevention practice, patients at risk of HCAI followed without the nursing process would not get nursing intervention, and less attention given for HCAI could justify high prevalence. This systematic review and meta-analysis found that the most prevalent HCAI is SSI. This is greater than studies done in Morocco [8], Botswana [5], South Africa [6], and a meta-analysis done in mainland China [39]. The higher prevalence in the current finding might be due to poor surgical instrument processing, inadequate knowledge of healthcare workers (HCWs) about SSI prevention, the highest occurrence of HCAI in the surgery ward, poor SSI prevention practice by HCWs, and surgical procedure errors in Ethiopian settings. None of the HCWs in Addis Ababa Ethiopia were using biological indicators of steam (Bacillus stearothermophilus) or dry (Bacillus subtilis) heat sterilization [45]. Knowledge of SSI prevention was found inadequate, and SSI prevention was practiced poorly at two referral hospitals in northwest Ethiopia [46]. Besides, as shown in Fig. 4 the prevalence of HCAI was the second highest in the surgery ward (20.98%). Regarding surgical procedure errors, surgical and medical error claims in the country showed that medical error was 26.7%, and the majority (72%) of the complaints were surgical related and emerged from the operation room [47]. As a result of the above antecedents, prevalence of nosocomial SSI could be higher in the country.
A higher prevalence of SSI and an abundance of NI in the surgery ward reported in the current meta-analysis might be explained by the low density of healthcare providers in Ethiopia. The density of physicians (per 1000 population) was 0.0, 0.6, and 0.8 in Ethiopia, Morocco, and South Africa respectively while the density of nursing and midwifery personals (per 1000 population) was 0.3, 0.9, and 5.2 in Ethiopia, Morocco, and South Africa orderly [48]. Nurses, midwives, and physicians serving many people every day might be unable to maintain healthcare quality, so this might be another reason for higher HCAI in the surgery ward. On top of the abovementioned reasons, nurse's burnout might contribute to the high prevalence of SSI and an abundance of HCAI in the surgery ward. In the United States (US) nurse's burnout was found as a single most important associated factor for increased nosocomial UTI and SSI [49].

Strength and limitation
This systematic review and meta-analysis was the first national estimation conducted in Ethiopia. However, it may lack national representativeness because no data were found from Benishangul Gumuz, Afar, Gambella, Somalia, Dire Dawa, and Harare regions of Ethiopia.

Conclusions
In this finding, the burden of HCAI remains high. SSI was the first most common type of HCAI, followed by UTI, BSI, SSI and UTI, and RTI from highest to lowest magnitude respectively. The highest overall burden was observed in surgery, gynecology, and obstetrics ward followed by surgical ward. Hence, infection prevention and control should be strengthened and held as the priority agenda in healthcare with due emphasis for surgical site infection.