ABSTRACT.
Visceral leishmaniasis is a tropical disease with a significant global public health burden. This study aimed to determine the social demographic characteristics associated with visceral leishmaniasis in West Pokot of Kenya. A mixed-methods research design was adopted where household questionnaires and key informant interviews were administered. Quantitative data was analyzed using SPSS version 22, and qualitative data were analyzed to establish patterns for interpretation. Male children aged 10 years or younger were the most infected by Leishmania donovani in the community. The hospital record indicated that 60% of previously treated visceral leishmaniasis patients were severely malnourished during admission. Risk factors associated with the disease included low formal education (adjusted odds ratio [aOR] = 4.39; 95% CI = 1.66–11.59; P <0.05), peasant farming (aOR = 8.49; 95% CI = 2.77–26.00; P <0.05), and dog ownership (aOR = 4.86; 95% CI = 1.87–12.60; P <0.05). Social demographic risk factors for visceral leishmaniasis remain a major public health concern in West Pokot.
INTRODUCTION
Leishmaniasis is a neglected tropical disease causing high morbidity and mortality around the globe and remains the second most deadly parasitic disease after malaria.1 The disease affects the poorest of the poor among global communities and receives insufficient research and development investment.1,2 Annually, leishmaniasis has an incidence of approximately 1 million and causes between 14 and 40,000 deaths; more than 1 billion persons are at risk of infection worldwide.1,3–5 Globally, 7,767 post-kala-azar dermal leishmaniasis (PKDL) cases were reported between 2014 to 2018 according to a 2020 WHO report.6 Both PKDL and visceral leishmaniasis relapse cases are believed to play an important role in disease transmission and may negate the disease control efforts in the long term.5,6 Visceral leishmaniasis is 95% fatal if untreated and causes 50,000 to 90,000 cases annually worldwide.1,5 More than three-quarters of visceral leishmaniasis–endemic nations are Third World countries with limited access to basic health services. Generally, less than 45% of visceral leishmaniasis cases are reported, and most of the global incidents occur in India, Brazil, and East Africa where frequent outbreaks have been observed in the recent past.1,5
According to the WHO, East Africa is one of the global regions reporting high kala-azar cases. Visceral leishmaniasis in East Africa is mainly caused by Leishmania donovani.7 Cases of visceral leishmaniasis in Kenya were first documented as early as the 1940s during which there was an outbreak in Lake Turkana among the Kings’ African Rifles Troops.8 In Kenya, L. donovani transmitted by Phlebotomus martini is the major cause of frequent outbreaks of visceral leishmaniasis in more than 11 endemic counties located in the arid and semiarid zones.8,9 According to the WHO and Kenya’s Ministry of Health, Kenya is one of the visceral leishmaniasis high-burden nations with approximately 6 million people at risk and almost 2,000 cases reported annually.1,9 Although vector and reservoir behaviors may be different, climatic patterns, geographic factors, and social dynamics play significant role in enhancing vector infestation or its endemicity in an area.10 Social demographic characteristics such as lack of and/or low formal education, larger household size, herding and peasant farming play important role in the epidemiology of visceral leishmaniasis.11,12 Similarly, demographic risk factors like low household income, residing in mud houses, lack of bed net use, dog ownership, living close to previous visceral leishmaniasis cases, and hunting practices are considered significant determinants of the disease.13,14 Understanding the current visceral leishmaniasis burden and the infection-driving factors is essential, especially when the impact of COVID-19 pandemic interruptions and climate change effect are projected to result in a surge in disease incidence regardless of the setting.10,15 West Pokot is one of the visceral leishmaniasis endemic counties in Kenya recording a high number of cases.16 The significance of establishing the disease trend and its social demographic drivers in the present study was to address the existing information gaps with the aim of improving prevention and control strategies.
MATERIALS AND METHODS
Study area.
The present study was carried out in 2021 in the Pokot North subcounty of West Pokot County of Kenya. West Pokot is one of the north-rift districts in the former Rift Valley province. The subcounty is located in the northwest of the country, approximately 450 km from the capital city, Nairobi. Pokot North subcounty is located in the arid and semiarid climatic regions of Kenya and is mainly inhabited by pastoral communities that depend on livestock as the main source of livelihood.
Study design.
A mixed-methods cross-sectional research approach involving retrospective and prospective designs was used to establish the social demographic characteristics associated with visceral leishmaniasis in Pokot North subcounty of West Pokot.
Ethical clearance.
The research was approved by the Kenyatta University Ethical Review Committee (PKU/848/1913) and a research permit was granted by the National Commission for Science, Technology and Innovation, Kenya. In addition, permission to carry out the study was granted by the subcounty hospital administration. Written informed consent was signed by research participants following a verbal explanation of the study purpose.
Sampling.
West Pokot County is a visceral leishmaniasis endemic area that registers more than 17 cases every month and 250 to 450 cases annually according to data from the kala-azar diagnostic and treatment center in Kacheliba hospital and thus, the choice of the study site.16,17 Cluster sampling of wards and locations as well as random sampling of households were carried out. Semistructured researcher-administered household-questionnaires were filled and secondary data was obtained from the kala-azar treatment center hosted at Pokot North subcounty hospital. The hospital serves as the center for kala-azar diagnostic and treatment and attends to at least 60 new patients with various illnesses every day. The questionnaire collected data on social demographic factors including household visceral leishmaniasis cases, hospitals visited, and occupation among other factors. Household’s positive visceral leishmaniasis cases were confirmed by laboratory and health records after they were identified by household respondent. Cochran’s 1977 formula was used to attain a sample size of 384 (n = z2p(1 − p)/e2).
Data analyses.
Quantitative data were analyzed using SPSS version 22, and χ2 and logistic regression were used to test associations of social demographic factors with risk of visceral leishmaniasis, and a P-value <0.05 was considered statistically significant. Qualitative data was analyzed to identify trend and patterns.
RESULTS
Trends of visceral leishmaniasis relapse, PKDL and death in Pokot North.
Figure 1 show 13 years of aggregated data starting from August 2007 to July 2020 obtained from Pokot North subcounty hospital kala-azar center. The data obtained comprised patients’ demographic characteristics, diagnoses, and body mass index (BMI). There were at least seven cases of relapse or post-kala-azar dermal leishmaniasis (PKDL) and an average of four deaths as a result of visceral leishmaniasis each year until the end of 2012–2013. Both PKDL and death cases significantly declined to less than 10 and 2, respectively, in the subsequent years, although cases of relapse remained at an average of 10 every year until 2020 (Figure 1).
Figure 1.
The trend of kala-azar relapse, post-kala-azar dermal leishmaniasis (PKDL), and death as obtained from the kala-azar center records in Pokot North subcounty hospital, N = 360 (each year runs from August of the previous to July of the following year).
Visceral leishmaniasis patient’s BMI at the time of admission as obtained from hospital records.
Results in Table 1 show that the majority of the patients treated for visceral leishmaniasis were male (63%; n = 364), compared with female (37%; n = 218). Further, hospital data indicated that most (60%; n = 349) of the patients previously treated for visceral leishmaniasis were severely malnourished at the time of hospital admission with BMI of <16, and 19.1% (n = 94) were moderately malnourished with BMI of 16 to 17 (Table 1). The results also showed that a high percentage (60%, n = 217) of the severely malnourished and 19% (n = 68) of the moderately malnourished individuals were male patients. Considering the visceral leishmaniasis incidence rate against age groups, children under 10 years of age formed almost half (47.4%; n = 276) of all treated cases, whereas those aged between 11 to 20 years were second most affected (26.6%, n = 155) (Table 1). Regarding nutritional status, children less than 10 years remained most affected forming 47.3% (n = 158) of the severely malnourished patients followed by those in the age group between 11 and 20 years that formed approximately 27% (n = 94).
Table 1.
Visceral leishmaniasis patients’ BMI at the time of admission as obtained from kala-azar center in Pokot North subcounty hospital
| BMI | |||||
|---|---|---|---|---|---|
| Factor | <16 | 16–17 | 18–24 | >25 | Total |
| Sex, n (%) | |||||
| Female | 132 (22.7) | 43 (7.4) | 41 (7.0) | 2 (0.3) | 218 (37.4) |
| Male | 217 (37.3) | 68 (11.7) | 77 (13.2) | 2 (0.4) | 364 (62.6) |
| Total | 349 (60) | 111 (19.1) | 118 (20.2) | 4 (0.7) | 582 (100) |
| Age group, years, n (%) | |||||
| 0–10 | 158 (27.1) | 58 (10.0) | 57 (9.8) | 3 (0.5) | 276 (47.4) |
| 11–20 | 94 (16.2) | 25 (4.3) | 35 (6.0) | 1 (0.2) | 155 (26.7) |
| 21–30 | 66 (11.3) | 17 (2.9) | 16 (2.7) | 0 (0.0) | 99 (16.9) |
| 31–40 | 15 (2.6) | 3 (0.5) | 4 (0.7) | 0 (0.0) | 22 (3.8) |
| 41–50 | 7 (1.2) | 2 (0.3) | 3 (0.5) | 0 (0.0) | 12 (2.0) |
| >51 | 9 (1.5) | 6 (1.0) | 3 (0.5) | 0 (0.0) | 18 (3.0) |
Body mass index (BMI) range: <16 = severely malnourished; 17–18 = moderately malnourished; 18–24 = normal; >25 = overweight (BMI calculation adapted from HCC Informant 2022, Oregon Health and Science University).18
Descriptive and bivariate analyzes of respondent’s social demographic risk factors.
Results in Table 2 show that almost half (47.9%) of the participants had no formal education, and livestock herding (33.1%) and peasant farming (32%) were the most practiced occupations. Most participants lived in households with seven to nine members (40.2%), and almost half (47.9%) of the households earned less than 50 USD per month. Concerning house type, the majority (69.7%) of the respondents lived in grass-roofed, mud-walled houses, and most (62%) respondents had at least one bed net in their house. With regard to hunting practices, more than half (53.4%) of the participants practiced hunting for either household consumption or as a source of income. The majority (64.7%) of the respondents reported none of their immediate neighbors ever had visceral leishmaniasis, and 18.2% of the study respondents owned dogs. Among respondents, 17.6% reported gold-mining activities as a source of income. The majority (64.7) of the study participants used herbal medication in the treatment of all ailments including visceral leishmaniasis and participated in traditional night dance events. Bivariate analysis was carried out to test the association of these factors with the risk of visceral leishmaniasis, and significant factors included education level, occupation, household size, house type, and household monthly income.
Table 2.
Descriptive and bivariate analyzes of respondent’s social demographic risk factors in Pokot North subcounty, Kenya, 2021
| Visceral Leishmaniasis | ||||||
|---|---|---|---|---|---|---|
| Factor | Overall, n (%) | Positive (%) | Negative (%) | χ2 | df | P-Value |
| Education level | ||||||
| No formal education | 174 (47.9) | 61 (16.8) | 113 (31.1) | 36.66 | 3 | <0.000 |
| Primary | 104 (28.7) | 9 (2.5) | 95 (26.2) | |||
| Secondary | 56 (15.4) | 6 (1.7) | 50 (13.8) | |||
| Tertiary | 29 (8) | 2 (0.6) | 27 (7.4) | |||
| Occupation | ||||||
| Herder | 120 (33.1) | 39 (10.7) | 81 (22.3) | 39.75 | 4 | <0.000 |
| Farmer | 116 (32) | 7 (1.9) | 109 (30) | |||
| Housewife | 52 (14.3) | 14 (3.9) | 38 (10.5) | |||
| Business | 44 (12.1) | 17 (4.7) | 27 (7.4) | |||
| Salaried | 31 (8.5) | 1 (0.3) | 30 (8.3) | |||
| Household size | ||||||
| Less than 3 persons | 31 (8.5) | 2 (0.6) | 29 (8) | |||
| 4–6 persons | 131 (36.1) | 25 (6.9) | 106 (29.2) | |||
| 7–9 persons | 146 (40.2) | 35 (9.6) | 111 (30.6) | 9.49 | 4 | 0.044 |
| 10–12 persons | 45 (12.4) | 15 (4.1) | 30 (8.3) | |||
| More than 13 persons | 10 (2.8) | 1 (0.3) | 9 (2.5) | |||
| Household monthly income | ||||||
| Don’t know | 83 (22.9) | 20 (5.5) | 63 (17.4) | |||
| Less than 50 (USD) | 174 (47.9) | 52 (14.3) | 122 (33.6) | 25.42 | 4 | <0.000 |
| 60–100 (USD) | 86 (23.7) | 5 (1.4) | 81 (22.3) | |||
| 110–150 (USD) | 9 (2.5) | 0 (0) | 9 (2.5) | |||
| More than 160 (USD) | 11 (3) | 1 (0.3) | 10 (2.8) | |||
| House type | ||||||
| Entirely mud | 7 (1.9) | 1 (0.3) | 6 (1.7) | 8.09 | 3 | 0.033 |
| Grass roof mud wall | 253 (69.7) | 64 (17.6) | 189 (52.1) | |||
| Iron sheet roof mud wall | 92 (25.3) | 13 (3.6) | 79 (21.8) | |||
| Brick | 11 (3) | 0 (0.0) | 11 (3) | |||
| Bed net | ||||||
| Present | 225 (62) | 25 (6.9) | 200 (55.1) | |||
| Absent | 138 (38) | 53 (14.6) | 85 (23.4) | 37.77 | 1 | <0.000 |
| Hunting practice | ||||||
| Yes | 194 (53.4) | 50 (13.8) | 144 (39.7) | 4.54 | 1 | 0.033 |
| No | 169 (46.6) | 28 (7.7) | 141 (38.8) | |||
| Kala-azar case in neighborhood | ||||||
| Yes | 128 (35.3) | 55 (15.2) | 73 (20.1) | 54.08 | 1 | <0.000 |
| No | 235 (64.7) | 23 (6.3) | 212 (58.4) | |||
| Domestic dog | ||||||
| Yes | 66 (18.2) | 26 (7.2) | 40 (11) | 15.33 | 1 | <0.000 |
| No | 297 (81.8) | 52 (14.3) | 245 (67.5) | |||
| Mining activity | ||||||
| Yes | 64(17.6) | 16 (4.4) | 48 (13.2) | 0.56 | 1 | 0.451 |
| No | 299(82.4) | 62 (17.1) | 237 (65.3) | |||
| Kala-azar herbal medication | ||||||
| Yes | 235 (64.7) | 39 (10.7) | 196 (54) | 9.45 | 1 | 0.002 |
| No | 128 (35.3) | 39 (10.7) | 89 (24.5) | |||
| Night dance practice | ||||||
| Yes | 235 (64.7) | 59 (16.3) | 176 (48.5) | 5.17 | 1 | 0.023 |
| No | 128 (35.3) | 19 (5.2) | 109 (30) | |||
Multivariate analyzes of social demographic risk factors.
The significant factors on bivariate analysis were adjusted at P <0.05 in association with risk of visceral leishmaniasis before multivariate analysis was carried out using binary logistic regression and only significant factors were retained in the reduced model (Table 3). The results shown in Table 3 indicate that those with a low level of formal education were 4.39 times more likely to suffer from visceral leishmaniasis compared with those with a secondary education level (adjusted odds ratio [aOR] = 4.39; 95% CI = 1.66–11.59; P <0.05). Concerning participants’ occupation type, those who engaged in peasant farming were more likely to suffer visceral leishmaniasis compared with salaried individuals (aOR = 8.49; 95% CI = 2.77–26.00; P <0.05). Regarding household use of bed nets, those who owned bed nets were 5.98 times less likely to get visceral leishmaniasis compared with those households who did not own bed nets (aOR = 5.98; 95% CI = 2.73–13.10; P <0.05). In considering the presence of previous visceral leishmaniasis cases in the neighborhood, members living in homesteads without previous visceral leishmaniasis cases were 6.84 times less likely to experience visceral leishmaniasis (aOR = 6.84; 95% CI = 3.19–14.68; P <0.05). Similarly, members of households without dog were 4.86 times less likely to suffer from visceral leishmaniasis compared with those living in houses with dog (aOR = 4.86; 95% CI = 1.87–12.60; P <0.05).
Table 3.
Multivariate analyzes of respondent’s social demographic risk factors in Pokot North subcounty, Kenya, 2021
| 95% CI | ||||
|---|---|---|---|---|
| Factor | aOR | Lower | Upper | P-Value |
| Education level | ||||
| No formal education | Ref | |||
| Primary | 4.392 | 1.663 | 11.598 | 0.003 |
| Secondary | 0.717 | 0.209 | 2.456 | 0.597 |
| Tertiary | 1.776 | 0.156 | 20.162 | 0.643 |
| Occupation | ||||
| Herder | Ref | |||
| Farmer | 8.495 | 2.775 | 26.001 | <0.000 |
| Housewife | 1.4 | 0.5 | 3.919 | 0.521 |
| Business | 0.381 | 0.13 | 1.116 | 0.79 |
| Salaried | 2.078 | 0.205 | 21.026 | 0.536 |
| Bed net | ||||
| Present | 5.985 | 2.732 | 13.108 | <0.000 |
| Absent | Ref | |||
| Kala-azar case in neighborhood | ||||
| Yes | Ref | |||
| No | 6.844 | 3.191 | 14.681 | <0.000 |
| Domestic dog | ||||
| Yes | Ref | |||
| No | 4.865 | 1.879 | 12.6 | 0.001 |
aOR = adjusted odds ratio; Ref = reference.
DISCUSSION
Despite the significant progress achieved in reducing the community visceral leishmaniasis burden, cases of relapse remain widespread in the study area. According to the Pokot North subcounty hospital records, there was a significant reduction in the visceral leishmaniasis burden particularly mortalities, and PKDL from mid-2012 to 2020. The observed reduction in cases of PKDL and mortality may be attributed to the measures put in place by the health sector to curb the disease. These efforts included equipment of kala-azar diagnosis and treatment center and nutritional package for the weak inpatients as well as the inception of the combined treatment regimen. The current treatment regimen came into use in 2012 and consists of a 17-day injection of sodium stibogluconate and paromomycin to the middle-aged population, and amphotericin-B to the minors and aged patients.19 According to the WHO expert committee on leishmaniasis control 2010 report, the current drugs were thought to demonstrate desirable characteristics including a significant reduction in treatment duration and cost, thereby increasing patient turnover during the outbreak.20 Our findings support a 2010 WHO report and a randomized control trial study carried out by Musa in East Africa that reported improved survival and cure level achieved by using the combined drugs despite some side effects.19–21 Children under 10 years of age and male gender are significant risk factors for visceral leishmaniasis in the present study area. The higher visceral leishmaniasis prevalence among children could be attributed to poor clothing habits, lack of proper housing, more time spent roaming in rangeland, malnutrition, and immune system not fully developed. These findings are in agreement with a spatial study by Jiang in 2021 on visceral leishmaniasis risk factors in China and a 2005 study by Barnett in India, both of which reported higher kala-azar occurrence among children.22,23 Similarly, higher visceral leishmaniasis incidence among males may be a result of outdoor exposure encountered during field activities including guarding livestock from wild animals at night or herding, as well as engaging in farm field activities.24 These findings also support those of Braz in Brazil and Kolaczinski in East Africa on kala-azar risk factors that associated higher disease prevalence among males with certain occupational activities.24–26 Further, we observed widespread severe malnutrition among visceral leishmaniasis patients at the time of admission, which could suggest that malnutrition may be a risk factor for visceral leishmaniasis in West Pokot County where the poverty rate stands high as described by the county-integrated development plan.27,28 The high rate of severe malnutrition could be a result of poor dietary intake that may be contributing to disease relapse as well as full-blown infection as it impact both innate and adaptive immunity. Our findings are in conformity with previous report by Mengesha et al. in Ethiopia that associated malnutrition with the risk of visceral leishmaniasis.28–31
Exacerbated by the predominant nomadic lifestyle in the study setting, the demographic characteristics of the present study participants such as lack of formal education and engaging in livestock herding are significant risk factors and may compromise disease prevention and control efforts. The higher percentage of study participants lacking formal education established by the present study is further evident in the county-integrated development plan.27 According to members of key informants, literacy is essential in health promotion and is a significant predictor of the welfare and quality of life. Our findings agree with a previous report by Margonari regarding knowledge and risk factors of kala-azar in Brazil that identified low education level as a significant risk factor for visceral leishmaniasis.11,32,33 Livestock herding and peasant farming are the most common occupations in our study area and remain significant determinants of visceral leishmaniasis status. The risk could be attributed to significant time spent outdoors by individuals while undertaking occupational duties such as herding in the field and the risk of vector attraction posed by livestock housed around human-inhabited houses. Moreover, farm fields are believed to be frequented by the vector because they provide a preferred atmosphere; thus, residing near farm fields poses the risk of attracting vector.34 These findings are in accordance with those of a case–control study on the risk factors of visceral leishmaniasis by Yared in Ethiopia and a study by Mandal in Nepal that both associated peasant farming and livestock ownership with the risk of kala-azar.34,35
Social demographic risk factors that are both economically and culturally entrenched; these include lack of bed net, presence of a previous visceral leishmaniasis patient in the neighborhood, and presence of dog in the home. Such factors are significant predictors of the disease in the current study. Sleeping without protective night gear (e.g., lack of bed net and protective clothing in vector-endemic areas) poses the risk of exposure to vector bite. These findings are in agreement with a previous report by Gebremichael in Ethiopia, in which the use of bed nets was associated with reduced risk of infection.13,24 Living in close proximity to previously visceral leishmaniasis–infected individuals is believed to be a risk factor. Previous visceral leishmaniasis cases play an important role in disease transmission or act as reservoir in endemic areas; thus, those living in the same homestead or in the neighborhood are at higher risk of infection. Our findings are in agreement with a study carried out by Oryan on global leishmaniasis risk factors, which reported the presence of previous visceral leishmaniasis cases as a risk factor.36 A domestic dog is believed to serve various purposes at the household level in the study area, including acting as home security, guarding livestock from wild animals, and hunting. However, dogs are known to be a principal reservoir for the Leishmania parasite; thus, their presence in the homestead in visceral leishmaniasis–endemic areas may pose a risk for propagating the infection by harboring the parasite. Our findings support a study on risk factors carried out in Ethiopia by Bashaye et al., who reported dog ownership as a significant risk factor for visceral leishmaniasis.37,38 In conclusion, despite the gains achieved in curbing the burden of visceral leishmaniasis, particularly mortalities, relapse and social demographic risk factors may negate disease prevention and control efforts in West Pokot County of Kenya.
ACKNOWLEDGMENTS
We are grateful to the residents of Pokot North for their study participation. We appreciate the support and cooperation of the Pokot North subcounty hospital and the West Pokot department of health services. The American Society of Tropical Medicine and Hygiene (ASTMH) assisted with publication expenses.
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