Magnitude and associated factors of cutaneous leishmaniasis among patients visiting Nefas Mewcha primary hospital, Northern Ethiopia, 2022: An institution-based Cross-sectional study

STRENGTHS AND LIMITATIONS OF THIS STUDY

  • The main strength of this study is the use of primary data among the whole population of Ethiopia.

  • Since the study is hospital based, selection bias might be introduced.

  • Indeed, due to the cross-sectional nature of the data, cause-and-effect relationships may not be adequately determined for some predictor variables.

Introduction

Leishmaniasis is 1 of the top 10 neglected tropical diseases caused by an obligate intracellular protozoan parasite of the genus Leishmania that is transmitted by the bite of female phlebotomine sandflies.1 There are three main clinical forms of the disease: cutaneous leishmaniasis (CL), visceral leishmaniasis (VL), also known as kala-azar, and mucocutaneous leishmaniasis (MCL).1 2 CL, however, is the most common form of leishmaniasis that causes skin lesions, mainly ulcers, on exposed parts of the body.1 The disease is endemic in 90 countries in the world, and an estimated 600 000–1 million new cases occur each year globally, but only about 200 000 are reported to the WHO.1 2 African and Middle Eastern countries were highly affected by the overall burden of CL.3 4

Ethiopia, located in east Africa, is one of the nations with a high prevalence of CL, which is thought to affect between 20 000 and 50 000 people annually.5 6 It is highly endemic in highland areas of the country found with an elevation from 1400 to 3175 m above sea level.7 8 Indeed, CL is known to have a profound psychosocial impact due to the stigmatisation of infected and cured individuals, as the disease may leave residual disfiguring scars.9–13 Today, approximately 40 million people worldwide are suffering from stigma due to inactive CL scars.14 It is also the leading cause of stigma, depression and anxiety among the most common tropical skin diseases.10

Despite its severe stigma and psychosocial impacts, policymakers and programme managers overlooked it in favour of focusing on VL, which could be related to its non-fatal nature. In line with this, the incidence of CL is expected to increase in the future, and it is estimated that nearly 30 million people are at risk of developing CL in Ethiopia.15 Environmental and/or climate changes, poverty, immunodeficiency, particularly due to AIDS, sleeping outside the house due to conflict, poor housing conditions, tourism, migration to endemic areas in search of work, and a lack or inappropriate utilisation of protective equipment were the main contributors to increasing the incidence of leishmaniasis in Ethiopia.6 16–21 Apart from the prevention and control strategies of CL, early screening, diagnosis and treatment of identified patients are crucial to reducing the psychological and economic impact of the disease.10 However, there are only a few selected health institutions in the country that have the capacity to diagnose and treat CL, with the majority located in cities far from endemic areas. Nefas Mewcha Primary Hospital (NMPH), located in the Amhara region of north-central Ethiopia, is one of the facilities that provides appropriate care for patients with CL in the surrounding areas.13 Although cases have been reported, up-to-date information on the prevalence, patient presentations and associated factors of CL is limited in Ethiopia, particularly in north-central Ethiopia. Determining the magnitude of the disease is also important for policymakers and programme managers to raise funds to scale up control and preventive measures. Therefore, the aim of this study is to investigate the magnitude, clinical presentation and associated factors of CL among patients visiting NMPH in 2022.

Method and materials

Study setting and design

An institution-based cross-sectional study was conducted among 332 study participants visiting NMPH from June to July 2022. The hospital is located in Lay Gayint district, 739 km from north-central part of Addis Ababa (figure 1). The topography of the Lay Gayint woreda is mostly heaved with hills and valleys encompassing from Tekeze Gorge (1500 m) to Guna Mountain summit (4230 m above sea level).22 23 The hospital starts providing health services including CL identification and treatment for more than 208 000 people who reside in the town and neighbouring woredas since 2018. Currently, more than 1050 patients visit the hospital monthly for different services.

Figure 1
Figure 1

The study area (Lay -Gayint woreda) map located in the Amhara region, north-central Ethiopia, 2022.

Study subjects

The source populations for this study were all patients visiting the outpatient department (OPD) of NMPH, whereas the study populations were all selected patients who visited NMPH OPD during the data collection period. Patients with severe mental impairment and with missing records of the clinical characteristics of CL (types, character of skin lesion and diagnostic modality) were excluded.

Sample size determination and sampling technique

The sample size required to conduct this study was estimated through Epi Info software V.7.2.3.1 with the assumption of 80% power, a 95% CI, a 10% non-response rate proportion of outcome in the unexposed group (39.6%) and an OR of 1.9 from a prior study conducted in Borumeda Hospital, northeastern Ethiopia.18 Finally, a total of 332 patients were taken as the final sample. A systematic random sampling technique (k=every sixth interval) was used to select eligible study participants.

Study variables

The main outcome variable for this study was the presence or absence of CL (yes or no), whereas sociodemographic variables (age, sex, education status, knowledge of CL, occupation and residence), environmental factors (housing condition, travel history, use of bed net, forest condition, sleeping site, presence of animals and vegetables, presence and absence of gorge and its distance from the house) and clinical factors (presence of comorbidities) were categorised as independent or predictor variables of CL.

Operational definitions

The residence of an individual was categorised as urban or rural based on the area where he or she lived for the last 6 months.24 Knowledge about CL was assessed according to the responses given to 12 items. Knowledge scores above and equal to the mean/median score were categorised good knowledge, while scores below the mean/median value were considered poor knowledge.25

Data collection instrument and procedures

A pretested interviewer-administered standard questionnaire was developed after thoroughly reviewing the work of prior related literature. The pretest was conducted on 5% (17) of study participants to ensure the consistency of the English and Amharic version of the questionnaire. The tool was initially prepared with an English version consisting of 9 sociodemographic, 2 comorbidity-related, 12 knowledge-related, 11 environmental-related and 9 clinical questions, which were initially translated into Amharic and then back into English to assure consistency (online supplemental file 1). The data were collected through a face-to-face interview and review of the patient’s medical chart. The patient’s chart (medical record) was reviewed to obtain clinical parameters, such as the clinical characteristics of CL and the presence of comorbidities. The data were collected by two BSc nurses under the close supervision of one adult health nursing professional with a master’s degree. To assure data quality, 1-day training was given for both data collectors and supervisors about the purpose of the study, and the way to extract relevant data and ensure the confidentiality issue of the patient information.

Supplemental material

Data processing and analysis procedures

The data were initially coded, entered into EpiData V.4.6.0 and simultaneously exported to SPSS software V.26 for further statistical analysis. Mean with SD, median with IQR and frequency with percentage were used to summarise the data. Moreover, texts, tables and graphs were also used to present data. Both simple binary and multivariable binary logistic regression models were fitted to identify the risk factors for CL. Variables with a p value of <0.25 in the simple binary logistic regression model were fitted to the multivariable binary logistic regression model, and finally, the level of significance was declared at a p value of <0.05. The backward likelihood ratio elimination method was used to select predictor variables by removing the least contributing variables until all variables left in the model were significantly associated with the outcome variable. The overall goodness of the model with the fitted data was evaluated using the Hosmer-Lemeshow goodness-of-fit test. Furthermore, the final model’s discriminative power was examined using the receiver operating characteristic (ROC) curve, which is created by plotting the sensitivity against the 1−specificity (false-positive rate) of the model. When the area under the curve (AUC) value in the ROC is ≥70, the model is considered to be ‘good’ at differentiating between patients who have and do not have CL.

Patient and public involvement

Patients and the public were not involved in the planning and design of the study.

Results

Sociodemographic characteristics of the study participants

A total of 332 (100%) participants were included in this study. Majority of the study participants were male (183, 55%) and unable to read and write (124, 37.3). The median age of the participants was 24 (IQR 18–42) years. Additionally, more than two-thirds of them were from rural areas (232, 70%) (table 1).

Table 1

Sociodemographic characteristics of study participants with cutaneous leishmaniasis in NMPH, north-central Ethiopia, 2022

Environmental health and housing condition of the study participants

According to the study participants, almost all respondents (334, 96.8%) had a habit of sleeping indoors, and more than half (309, 89.6%) of them had a house where by the roof is covered with tin. On the other hand, 275 (79.8%) of the respondents had no habit of using bed nets (table 2).

Table 2

Environmental health and housing characteristics of study participants in NMPH, north-central Ethiopia, 2022

Knowledge of the study participants about CL

Concerning the knowledge level of study participants, more than half (191, 57.5%) of them have poor knowledge about CL. More explicitly, only 15.06% of study participants did know the cause of the disease, while majority (271, 81.6%) of the participants mentioned that the disease manifested as a disfiguring lesion (281, 81.3%) (table 3).

Table 3

Knowledge status of study participants about CL in NMPH, north-central Ethiopia, 2022

Magnitude of CL

Out of the 332 study participants, 63 patients seek medical care with skin lesion, and 61 (18.37%, 95% CI: 14.5% to 22.9%) were patients with CL. Localised CL (LCL) was the most common type of leishmaniasis (55, 86.9%), followed by MCL (11.48%). In relation to the characteristics of the skin lesion, ulcerated lesions are the most frequently observed type of lesion (75.4%), followed by nodular (11.5 %), macule (8.2%) and papule (4.9%) (figure 2).

Figure 2
Figure 2

Magnitude of cutaneous leishmaniasis among outpatient department visitors in Nefas Mewcha Primary Hospital, north-central Ethiopia, 2022.

Predictors of the presence of CL

During the bivariable logistic regression analysis, a total of nine variables with a p value of <0.25 were fitted to the multivariable logistic regression model. In the final multivariable logistic regression model, at 5% level of significance, the following five variables, namely age, sex, educational status, knowledge of CL and living with dogs and other animals were found to be significant predictors of the presence or absence of CL. In this regard, the odds of CL are nearly five times higher in males than females (adjusted OR (AOR): 4.51; 95% CI: 1.94 to 10.45). As the age of the participants increases by 1 year, the probability of having CL decreases by 9% (AOR: 0.91, 95% CI: 0.87 to 0.94). Additionally, the odds of having CL among individuals with a secondary and tertiary level of education were 0.18 and 0.04 times higher than those of individuals who are unable to read and write, respectively. Individuals who live with dogs and other domestic animals were 5.29 (AOR: 5.29; 3.24 to 7.50) times at risk of suffering with CL compared with those who had no animals. Finally, study participants with poor knowledge of the overall aspect of CL were nearly four times (AOR: 4.02; 1.81 to 9.76) at greater risk of developing CL compared with their counterparts (table 4).

Table 4

Bivariable and multivariable logistic regression analyses results of CL and related factors in OPD visitors, NMPH, north-central Ethiopia, 2022

Assumption of binary logistic regression

The Hosmer-Lomeshow goodness-of-fit test result indicated that the model is good at predicting the occurrence or non-occurrence of the outcome variable, that is, CL (p=0.8749). Indeed, the ROC curve analysis was used to assess the model’s discriminative power, and the AUC value in the ROC (AUC=0.894) showed that the model is excellent at distinguishing between individuals with true positives and individuals without CL (figure 3).

Figure 3
Figure 3

Receiver operating characteristic curve graph showing the model discriminative power on the presence/absence of cutaneous leishmaniasis among outpatient department visitors in Nefas Mewcha Primary Hospital, north-central Ethiopia, 2022.

Discussion

This study attempted to assess the burden, clinical presentations and associated factors of CL in relation to the study population’s sociodemographic, environmental and housing conditions. The magnitude of CL among patients visiting NMPH was estimated to be 18.37% (95% CI 14.5% to 22.9%). This finding is consistent with prior studies conducted in Borumeda Hospital in northeastern Ethiopia,18 and in highland areas of Yemen.26 On the other hand, the prevalence was relatively lower when compared with other similar studies conducted in Gondar University Comprehensive Specialized Hospital in northwestern Ethiopia,9 Ochollo primary school students in southwest Ethiopia,27 Saudi Arabia,28 Iraq,29 Sri Lanka30 and the rainforest areas of Bolivia.31 The relatively lower prevalence of CL in the study area might be due to the following conditions: first, the hospital had faced a big challenge due to the consequences of the recent war in the northern region of Ethiopia, which significantly reduced patients’ healthcare utilisation status.32 Second, since this study is conducted at the institution level, patients who are in the community will not be routinely screened and diagnosed in Ethiopia compared with studies conducted abroad. On the other hand, this figure is higher than a study conducted in rural communities in Tigray and in Mekelle city, northern Ethiopia.33 34 The possible discrepancy with the above finding might be due to the variation in environmental conditions of the study areas, in which the current study area had more favourable conditions for the propagation of sandflies compared with the above-mentioned areas.35 36 Regarding the clinical features of CL, LCL was the most common type, which is similar to a prior study conducted in Borumeda Hospital, northeastern Ethiopia.19

In the current study, we found that male individuals were 4.52 times more at risk of developing CL than their female counterparts. This could be due to the higher engagement rate of males than females in outdoor activities like farming, irrigation, harvesting, keeping animals and other agricultural activities, which all increase the probability of being exposed to the bite of sandflies. This finding is in line with prior studies conducted in different settings in Ethiopia, Sri Lanka and Bolivia.8 19 30 31 33 37 On the contrary, this finding opposed a report from Yemen and Iran,38 39 which might be due to the differences in sociodemographic, agricultural and cultural practices between these countries.

Age also has a significant association with the prevalence of CL. As the age of the individual increases by one unit, the probability of developing CL decreases by 10%. It is also supported by studies conducted in Ethiopia,33 40 Kenya, Colombia and Turkey.4 41 42 This may also be explained by the fact that the immune system of children and young adults is not strong, leading to a weaker immune response against the parasite, which allows the infection to persist and develop CL. Indeed, as the individual gets older, exposure to some environmental factors, such as farming and visiting endemic areas, will decrease.

Moreover, educational status has a strong relationship with CL, with the high educational status of the respondent decreasing the likelihood of being affected by CL. This is because education is the great power that makes individuals become informed and aware of the different aspects of CL so that they can easily comply with its preventive measures. Indeed, people with better education may have a better socioeconomic status, better housing, and therefore reduced exposure to sandflies and better access to healthcare services. A study conducted in the rural Marigat subcounty of Kenya is in parallel with this finding.43 In line with this, the current study has also revealed that individuals with poor knowledge about CL were four or more times at risk of developing CL more than their counterparts. This is because individuals who have good knowledge about CL will strictly adhere to the preventive and control strategies of the disease, including minimising the number of uncovered areas of the skin, proper use of bed nets, spraying living and sleeping areas, and staying in well-screened areas.44 45 It is known that good awareness and perception of people towards leishmaniasis have a great impact on averting disease transmission in endemic areas.

Finally, living with domestic animals has a strong association with an increased incidence of CL. This is congruent with prior studies conducted in Ethiopia,6 18 46Iran47 and Colombia.42 The observed association might be justified by the fact that the presence of livestock and their manure further creates favourable breeding grounds for the sandfly vectors in peridomestic environments. Most of the time, sandflies congregate around human dwellings and breed in particular organic wastes, such as dung, excrement, rodent burrows, leaf litter, and cracks and fissures in walls that experience high temperatures and humidity.48

Conclusion and recommendation

In the study area, the magnitude of CL among patients visiting the hospital was found to be high. Being male and young, having a low educational status, having poor awareness and knowledge, and living with domestic animals were the main identified risk factors that increased the probability of acquiring CL. Further large-scale, community-based epidemiological studies need to be undertaken. Moreover, increasing the knowledge of the community through scaling up of health education programmes and reducing activities that increase individual exposure to sandflies need to be considered as main strategies to reduce the burden of CL.

Data availability statement

All data relevant to the study are included in the article or uploaded as supplemental information.

Ethics statements

Patient consent for publication

Ethics approval

This study involves human participants and was approved by the Ethical Review Committee (ERC) of Debre Tabor University, College of Health Science with a protocol number of CHS1874/2014. Verbal informed consent was obtained from all study participants. Detailed information regarding the objective of the study, measures taken to ensure the confidentiality of the information that the study participants gave and the risk and benefits of participating in the study were given to each study participant. No personal identifiers were collected and the confidentiality of the information was assured.

Acknowledgments

We would like to express our deepest gratitude to Debre Tabor University, College of Health Science, for letting us conduct this research and for timely approving ethical clearance. Next, we also extend our profound thanks to the administration bodies at NMPH for facilitating a conducive environment to conduct our research successfully. Last but not least, our special thanks go to the data collectors, supervisors and study participants for their willingness and commitment.

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