The Prevalence and Risk Factors Associated with Tungiasis Infestations in Uganda: Implications for Vector Borne and Neglected Tropical Disease Control

Abstract

Tungiasis is a neglected parasitic inflammatory tropical skin disease affecting the world’s poorest people caused by a female flea called Tunga penetrans. It is potentially endemic in 88 countries worldwide, with an estimated community prevalence of 60%. The national prevalence is estimated at 50% with recent epidemics re-emergence dimensions in Uganda. The disease burden continues to escalate with high-school dropouts, absenteeism, and poor performance. This study was geared toward assessing the prevalence and risk factors in communities in Uganda. Overall, there is prevalence of 40.6 and 28% among households and individuals. Our findings further indicate prevalence of infection was the highest at household level compared to infected individuals observed; (Jinja; 73.3% vs. 50.0%), (Namutumba; 53.2% vs. 33.3%), (Iganga; 41.1% vs. 25.3%), (Bugiri; 24.4% vs. 27.1%), (Namayingo; 20.5% vs. 12.6%) and (Mayuge; 13.6% vs. 6.2%). Physical examinations revealed the most affected body parts were the toes (6.5%), sole (1.2%), and the heel (0.8%). The common method of prevention and treatment used is self-removal (49.4%), removal by a family member (32.7%), support from medical personnel (14.4%), and use of ointment (1.9%). The findings have implications for the prevention and control of Tungiasis as a public health concern in Uganda. This requires strengthened health education aimed at improved household sanitation and hygiene with community empowerment as a long-term measure.

1. Introduction

Tungiasis is a neglected tropical parasitic inflammatory tropical skin disease (NTD) affecting the world’s poorest people [1] caused by a female flea called Tunga penetrans [2]. It is described as “the greatest curse that has ever afflicted Africa” [3] and is potentially endemic in 88 countries worldwide with an estimated prevalence in community based-settings 60% [4, 5, 6, 7, 8, 9]. It is predominantly a health problem in the tropical areas of Latin America and Africa [10, 11]. It is more common in places with poor hygiene and is closely associated with domestic animals (mainly pigs, dogs, and cattle) [12]. Tungiasis commonly known as emvunza or Nyende in eastern Uganda has reemerged as the national prevalence in Uganda is estimated at 50% and recently reemerged to epidemic dimensions in many countries [13] including Uganda with an estimated prevalence of 50% reported [14, 15].

Tungiasis is a neglected disease of marginalized populations [16] and has been associated with a number of potential reservoirs from pigs, dogs, goats, mice, rats, and wild animals [17, 18, 19, 20]. Studies have shown significant levels of infestations of goats in Uganda with Tungiasis as a serious health concern in domestic animals in Uganda including goats [21], pigs, and dogs [22]. Tungiasis is estimated to affect over 6,000,000 million people who are at risk and an estimated 3 million Ugandans infested with Tungiasis, 50% of whom, are confined to eastern Uganda especially the Busoga sub-region, the rest distributed in other regions of Karamoja and central sub-regions [23].

The ranging disease burden continues to escalate with high school dropouts, absenteeism, poor performance, and low esteem have continued to ruin the areas of Busoga region. There has been no study done to establish the magnitude of this problem and yet resource allocation and interventions can only be appropriately sought when such estimates are made. This study was geared towards assessing the prevalence and risk factors that will help provide the cornerstone for controlling future infections in communities in Uganda.

2. Materials and methods

2.1 Study area and design

This was a cross-sectional and multistage sampling study design that utilized semi-structured questionnaires combined with an observation-checklist to collect quantitative data from 983 individuals and 288 households from Bugiri, Iganga, Jinja, Namutumba, Namayingo, and Mayuge districts in eastern Uganda. The study sites are shown in Figure 1. The study was conducted in Bugiri, Iganga, Jinja, Namutumba, Namayingo and Mayuge districts (Figure 1). These districts were chosen due to the highest epidemiological reports by the Ministry of Health (weekly epidemiological reports). A sampling frame was established and randomization of the villages was performed to generate a proportional number of participants per District.

Figure 1.

Location of study area.

2.2 Survey methodology

The study utilized a census-style survey conducted across all the six districts survey. Overall a total of 983 individuals and 288 households were surveyed and interviewed over an eight-week period beginning February 2018. Before interviews began, an advocacy meeting was held with all the district officials to discuss the study and obtain district approval and support for the survey. Meetings were also held with the local council, chairpersons from the two villages, and the village health teams (VHTs). During mobilization meetings, community members were asked to provide information when the researchers arrived in their homes but were informed that they had no obligation to do so. Households were visited door-to-door; if residents were absent, teams returned to the house at least twice for follow-up. Informed consent from the head of the household and adults present during the interview was obtained. The main interviewers were Ministry of Health Vector Control Officers or the District Health Drug Distributor and each team had a member of the Village Health Team from the respective village. There were three teams performing interviews; team members rotated between groups to ensure uniform questioning across the community.

2.3 Case definition

A short description of Tunga penetrans as an inflammatory of the skin characterized by a white patch with a black spot at the center of a swollen red lesion causing a painful itching constituted a case definition the survey team based on to determine and score observed cases. Individuals were included in the study based on the criteria that they were aged six years and above who had lived in the selected districts for a period of one year and above and excluded in the study when found of unsound mind (very sick, unconscious, mental disturbed).

2.4 Data tools and analysis

One week of training was conducted for all the research assistants involved in this study and deployed on the basis that was able to speak the native language. The data collection tools and questionnaires were pretested in one of the areas known for Tungiasis infections and corrected for errors before use in the study sites. The data collected was entered daily in the field for all the individuals into the computer and cross-checked for consistency and validity of results. A daily data review audit was performed by research to ensure compliance with the standards set.

Household and individual survey data were cleaned and checked for consistency using custom scripts in R v. 3.2.1. Chi-squared tests were used to compare categorical data using the base R function chisq.test. Multivariate logistic regressions were created with the function glm using the binomial family to evaluate two outcome variables.

2.5 Ethical clearance

The methods in the study were reviewed and approved by the Vector Control Division Research Ethic Committee (VCDREC/090) and the graduate of the Nexus International University (VUU-PGDPH-2016-037).

3. Results

3.1 Demographic characteristics of the study respondents

The demographic characteristics of the respondents are presented in Table 1. Overall, a total 983 respondents were interviewed. The majority of 657(66.8%) were male and only 326 (33.2%) were female. The mean age (26.13) years (standard deviation (SD) 22.56). Regarding age, the majority 500 (50.9%) were in the age bracket of 5–17 years, 187 (19%) were above 50 years of age, 120 (12.2%) were 30–39 years, 87 (8.9%) were 40–49 years of age and the least number of respondents were 18–29 years of age. concerning occupation, the majority of the respondents 376 (38.3%) were farmers, 61 (6.2%) were doing business as their occupation and a least respondents 14 (1.4%) were engaged in other activities in order to earn a living. The biggest proportion of the respondents 449 (45.7%) were Moslems, 260 (26.4%) were Catholics, 156 (15.9%) belonged to other religions and only 118 (12%) were Pentecostals.

Variables	Characteristics	Frequency (n = 983)	Percentage (%)
Mean age (SD) = ±26.13 (22.56)
Age in years	5–17 yrs	500	50.9
	18–29 yrs	89	9.1
	30–39 yrs	120	12.2
	40–49 yrs	87	8.9
	>50 yrs	187	19.0
Sex	Male	657	66.8
	Female	326	33.2
Education	None	284	28.9
	Primary	526	53.5
	Secondary	159	16.2
	Tertiary	14	1.4
Marital Status	Single	557	56.7
	Married	225	22.9
	Widow/widower	40	4.1
	Separated/divorced	161	16.4
Occupation	Farmer	376	38.3
	Business	61	6.2
	Others	14	1.4
Religion	Catholic	260	26.4
	Pentecostal	118	12.0
	Moslem	449	45.7
	Others	156	15.9
Source of water	Borehole	141	14.3
	Open well	141	14.3
	Piped/protected water	328	33.3
	River/lake/stream/pond	373	37.9

Table 1.

Demographic characteristics of the study population.

Location of Study area 15.

Tungiasis infestations of the toes, finger-nails and buttocks 17.

Regarding the water source, the majority of the respondents 373 (37.9%) obtained water for household use from the rivers/lakes/streams/pond, 328 (33.3%) used piped/protected water as a source of water, 141 (14.3%) used open well water. Concerning education, the majority 526 (53.5%) had a primary level of education, 284 (28.9%) had none as the education level, 159(16.2%) had a secondary level while the least 14 (1.4%) number of respondents had obtained tertiary education. Furthermore, the majority of 557 (56.7%) were single, 225 (22.9%) were married, 161 (16.4%) were separated/divorced and only 40 (4.1%) were widow/widower. This implies that the study was mainly dominated by single respondents.

3.2 Prevalence of Tungiasis in Busoga region

The overall prevalence of Tungiasis amongst households surveyed was 40.6% (288/984) while 28% (276/984) individuals were found infected with Tungiasis during the study as shown in Table 2. The prevalence at the household level was much higher than at the individual level with some villages having 100% as the case with Butangula-A in Jinja district. The findings further indicate the highest prevalence of infection at the household level versus infected individuals were observed in Jinja (73.3% vs. 50.0%), followed by Namutumba (53.2% vs. 33.3%), Iganga (41.1% vs. 25.3%), Bugiri (24.4% vs. 27.1%), Namayingo (20.5% vs. 12.6%) and Mayuge (13.6% vs. 6.2%). The study findings show that the greatest age group affected by this scourge in all the districts surveyed was 5–17 years as shown in Table 2.

District	Age (years)	Frequency (%) n = 983	Chi-value	P-Values
Bugiri	5–17 yrs	94 (71.8%)
	18–29 yrs	15 (11.5%)
	30–39 yrs	6 (4.5%)	23.934	0.004
	40–49 yrs	4 (3.1%)
	>50 yrs	12 (9.2%)
Mayuge	5–17 yrs	88 (69.8%)
	18–29 yrs	0 (0%)
	30–39 yrs	9 (7.1%)	37.982	0.001
	40–49 yrs	4 (3.2%)
	>50 yrs	25 (19.8%)
Namayingo	5–17 yrs	87 (61.3%)
	18–29 yrs	0 (0%)
	30–39 yrs	14 (9.9%)	39.066	0.001
	40–49 yrs	4 (2.8%)
	>50 yrs	36 (25.4%)
Jinja	5–17 yrs	93 (52.8%)
	18–29 yrs	7 (4.0%)
	30–39 yrs	20 (11.4%)	40.983	0.001
	40–49 yrs	12 (6.8%)
	>50 yrs	44 (25%)
Iganga	5–17 yrs	65 (34.8%)
	18–29 yrs	27 (14.4%)
	30–39 yrs	27 (14.4%)	46.256	0.001
	40–49 yrs	34 (18.2%)
	>50 yrs	34 (18.2%)
Namutumba	5–17 yrs	74 (33.5%)
	18–29 yrs	40 (18.1%)
	30–39 yrs	40 (18.1%)	48.715	0.001
	40–49 yrs	30 (13.6%)
	>50 yrs	36 (16.3%)

Table 2.

Prevalence of Tungiasis infestation in Busoga region.

3.3 The risk factors, morbidities, and management of Tungiasis infestations in the Busoga region

The major environmental risk factors associated with Tungiasis as reported by the respondents were; poor hygiene and sanitation. Other causes reported were; dirtiness, uncommented house, disposal of household wastes, and people sleeping in houses with bare soils. The study findings revealed that 344 (35.0%) agreed that poor hygiene is the most commonest cause of Tungiasis since some just dispose of household wastes outside their compounds. About 6.9% of the respondents reported sharing a residential house with domestic animals while 93.1% reported having a separate shelter for domestic animals. The type of floor material for suspected cases of Tungiasis reported was bare soil, clay, and sand. These observations were seen in zoonotic nature in Uganda [21, 24]. Our findings also show that disposal of household wastes was significantly associated with (p = 0.002) with outside disposal contributing the greatest percentage of 52.3%. The presence of domestic animals at home was also significantly associated with Tungiasis infestations (p = 0.002). The study also noted that knowledge concerning the causes of Tungiasis infestations was equally significantly associated with Tungiasis infestations (p = 0.002) with poor hygiene the biggest contributor accounting for 35%. Similar observations were reported by studies on the knowledge among animal keepers [25] as shown in Table 3.

Variables	Indicators	Frequency & % (n = 983)	Chi- value	P-value
Floor material	Bare soil	327 (33.3%)
	Cow dung	141 (14.3%)
	Concrete	141 (14.3%)	14.62	0.019
	Clay	187 (19%)
	Sand	187 (19%)
Latrine at home	Yes	842 (85.7%)
	No	141 (14.3%)	9.84	0.043
Disposal household wastes	Dispose outside compound	514 (52.3%)
	Disposed in compound	141 (14.3%)	3.66	0.002
	Burnt	141 (14.3%)
	Pit	187 (19.0%)
Share house with animals	Yes	68 (6.9%)
	No	915 (93.1%)
Animals at home	Hens	89 (9.1%)
	Goats	89 (9.1%)
	Cows	89 (9.1%)
	Dogs	89 (9.1%)	23.33	0.001
	Ducks	89 (9.1%)
	Pigs	89 (9.1%)
	Cats	89 (9.1%)
	Pigeons	89 (9.1%)
	Sheep	89 (9.1%)
	None	182 (18.5%)
Causes of Tungiasis	Poor hygiene	344 (35.0%)
	Sleeping on the floor	86 (8.7%)
	Too much sunshine	85 (8.6%)	24.75	0.001
	Doesn’t know	85 (8.6%)
	Un-cemented house	87 (8.9%)
	Dirtiness	296 (30.1%)
Localization of infections	Toes	82 (8.3%)
	Sole	25 (2.5%)
	Heel	25 (2.5%)
	Dorsal area	25 (2.5%)	32.982	0.001
	Fingers	25 (2.5%)
	Hands	42 (4.3%)
	Forearm	42 (4.3%)
Method of treatment used	Doesn’t know	294 (29.9%)
	Health workers	148 (15.1%)	32.243	0.003
	Relatives	196 (19.9%)
	Self-removal	345 (35.1%)

Table 3.

Risk factors and management of Tungiasis infestation in Busoga in region.

Table 3 presents the commonest methods of prevention and treatment used by the infected individuals; self-removal accounted for 49.4%), removal by a family member (32.7%), support from medical personnel (14.4%), and use of ointment (1.9%). As concerns the methods of treatment for infected individuals, a bigger percentage acknowledged self-removal, 35.1%, by health workers, 15.1%, removal by relatives 19.9% and 29.9% had no idea of any interventions.

Physical examination of the respondents showed 27% (266/983) which was significantly associated with Tungiasis infections (p = 0.001) as shown in Table 3. The highest cumulative number of Tungiasis infections recorded was 8.35% on the toes, 2.5% on the sole, 2.5% on the heel, and 2.5% on the dorsal area. Other body parts localized with infections were the fingers (2.5%), hands (4.3%), and forearm (4.3%). The commonest body parts affected by Tungiasis infections as shown in Figure 2 are the fingernails, toes, buttocks, and knees.

Figure 2.

Tungiasis infestations of the toe, finger-nails and buttocks.

4. Discussions

The overall prevalence of Tungiasis amongst households surveyed was 40.6% (288/984) while 28% (276/984) (95%CI, 0.0001–0.0290, p < 0.0001) individuals were found infected with Tungiasis during the study as shown in Table 2. The study findings further show that females were 2.4 times more infected with Tungiasis compared to males as observed in other studies from studies by [6, 26]. The prevalence at the household level was much higher than at the individual level with some villages having 100% as the case with Butangula-A in Jinja district. The findings further indicate the highest prevalence of infection at the household level versus infected individuals were observed in Jinja (73.3% vs. 50.0%), followed by Namutumba (53.2% vs. 33.3%), Iganga (41.1% vs. 25.3%), Bugiri (24.4%vs. 27.1%), Namayingo (20.5% vs.12.6%) and Mayuge (13.6% vs. 6.2%). The results of this study indicate that Tungiasis is a major public health problem amongst households in rural communities in eastern Uganda. The present-day study areas had previously been known as a hot spot and problematic for Tungiasis infestation in humans [15, 27] and animals [21, 22, 24, 25, 28, 29]. This could have been due to repetitive infestations of the affected households. These findings were in conformity with similar studies [28, 30].

Previous studies [26, 31] have shown that the prevalence of Tungiasis amongst 5–14 years was higher during the dry season similar to the trends observed in our study as indicated in Table 2. The study further points out that the prevalence of Tungiasis varied across different age groups though more significantly amongst 5–17-year-olds in almost all villages surveyed. This trend has been observed in similar studies by [8, 32], mostly attributed to the poor hygiene and exposure behaviors of these youngsters. This is made worse with the limited knowledge to take good care of themselves, frequently playing in dusty environments where the parasite thrives most.

It was a common observation that the majority of those suffering from Tungiasis infections had problems with walking because they had multiple infections on the toenails, fingernails and even to the extent some buttocks of the elderly were severely affected. Similar levels of morbidities were reported in many studies both in animals [21, 22, 29] and humans [18, 32, 33, 34, 35] and a common cause of serious secondary bacterial infections [36].

The major environmental risk factors associated with Tungiasis as reported by the respondents were; poor hygiene and sanitation. Other causes reported were; dirtiness, uncemented house, disposal of household wastes, and people sleeping in houses with bare soils. The study findings revealed that 344 (35.0%) agreed that poor hygiene is the most commonest cause of Tungiasis since some just dispose of household wastes outside their compounds. About 6.9% of the respondents reported sharing a residential house with domestic animals while 93.1% reported having a separate shelter for domestic animals. The type of floor material for suspected cases of Tungiasis reported was bare soil, clay, and sand. These observations were seen in zoonotic nature in Uganda [21, 24]. Our findings also show that disposal of household wastes was significantly associated with (p = 0.002) with outside disposal contributing the greatest percentage of 52.3%. The presence of domestic animals at home was also significantly associated with Tungiasis infestations (p = 0.002). The study also noted that knowledge concerning the causes of Tungiasis infestations was equally significantly associated with Tungiasis infestations (p = 0.002) with poor hygiene the biggest contributor accounting for 35%. Similar observations were reported by studies on the knowledge among animal keepers [25]. These observations were made on studies of zoonotic nature in Uganda [21, 24]. Our findings also show that 55.4% were knowledgeable about Tungiasis infection with 23.8% reporting poor hygiene, 23.9% reporting sleeping on the floor, 24.0% stating too much sunshine, and 22.0% reporting uncemented floors as the major causes of Tungiasis infestations. Similar observations were reported by studies on the knowledge among animal keepers [25]. Only 4.5% had reported using regular footwear. The majority reported bathing with soap (73.3%) as a good strategy for the prevention of infections although only 11.5% reported having good personal hygiene as one of the prevention strategies. Physical removal of Tunga penetrans using manipulation with safety pin/needles accounted for 14.4%.

4.1 The National elimination Policy for Uganda

In Uganda, the disease outbreak came to light in 2010 when deaths were reported in the Bugiri district. This has resulted in a series of activities that have led to the proper understanding and recognition of Tungiasis is a neglected tropical disease. The disease is endemic in the whole country, with an estimated 6 million people are at risk and at least 2.4 million infected with Tungiasis [23]. However, 50% of total cases in Uganda come from Busoga and Karamoja Subregions. This has been included as a priority disease under the NTDs by the year 2020 through mapping to assess the distribution, Capacity building on vector control treatment and rehabilitation, Advocacy and community mobilization, Personal and Environmental hygiene, and identifying partners to support the program [23]. The warm dusty weather and environment of these regions have certainly played an amenable role in breeding Tungiasis. More so, exposed dirty floors, walls, and compounds mean Tungiasis-eggs can incubate inside homes. There are many rural families who keep animals and chickens inside their houses at night as a measure of theft. This close proximity of animals enables the transmission of eggs from animals to humans to happen with much ease.

The Ministry of Health has proposed the use of Benzyl-benzoate emulsion (BBE) combined with petroleum jelly as the medication for treating and managing cases. These have been provided to health facilities for use by the affected communities. This will be incorporated and run alongside the national control program implemented through the community-based village health teams (VHTs) geared towards community involvement and ownership. The government has proposed to strengthen and enforce the current public health act on household sanitation and hygiene, which will include smearing, cleaning, and prohibiting sharing of human dwelling houses with domestic animals. Also, strengthen community social norms with community engagement.

5. Conclusions

Based on the study findings, it’s noted that Tungiasis infections present a serious health hazard to communities living in Busoga where many people live and suffer quietly under poor housing conditions. This is worsened by sharing housing and accommodation with domestic animals that are reservoirs for the infection. The following lessons have been learned during the study and recommended for further studies to advance solutions as regards the need to make a sound decision as to which drug to use during the community treatment intervention for Tungiasis. We have to choose between the scientifically backed Dimethicone (BBE) and the locally recommended interventions but data lacking on the Country's use of BBE for Tungiasis Control and elimination. There is a need to develop a training manual, IEC Materials, and Community/Civil Societies Organizations Materials for sensitizations to support those affected and the need for integrated coordinated community disease surveillance mechanisms with a comprehensive approach. Vector-Borne and Neglected Tropical Disease control division will be critical in providing solutions to this problem.

6. Recommendations

It is therefore suggested that countrywide studies are required to establish the exact prevalence and magnitude of Tungiasis infections in Uganda, assessing the epidemiological, socio-cultural context, behavioral and ecological risk factors. There is a need to assess the impact on school-age children (SAC) attendance 5–14 years and the disability-adjusted life years associated with the infections.

Acknowledgments

The authors would like to thank in particular the research assistants who were involved in the data collection. We are also grateful for the contribution of District NTD focal Persons for their efforts in mobilizing the communities for the study. Approval for the surveys was gratefully received from the Ethics committee of the Virtual University of Uganda (VUU-PGDPH-2016-037) and Vector Control Division Research Ethics (VCDREC/090) and Uganda National Council of Science & Technology (UNCST). Individuals who participated in the study provided written consent and assent before the study took place.

Conflict of interest

The authors declare no conflict of interest.

Authors contributions

Conceptualization, Data curation, Formal analysis, Funding acquisition, Methodology, Project administration, Visualization, Writing – original draft, Writing – review & editing all by the author.

Funding

This study was a student lead study supported by primary healthcare funds from the Ministry of Health, Republic of Uganda.