Treatment Failure, Knowledge, Attitude and Practices Related to Schistosomiasis and Soil-Transmitted Helminthic Infections among Basic School Pupils

Abstract

Soil-transmitted helminth (STH) and Schistosomiasis infections remain prevalent in developing countries. In Ghana, periodic mass drug administration (MDA) exercise has been implemented to tackle these infections, however, information on drug treatment failure and knowledge of the infection trend is needed for evaluating and modifying existing control programs. This study assessed the knowledge, attitude and practices (KAP) that predispose Basic School pupils to Schistosomiasis and soil-transmitted helminth infections and determined the rate of treatment failure against the worms after school mass drug administration (MDA). A cross-sectional study with a structured questionnaire was used to obtain information on the KAP among pupils who had undergone a MDA (albendazole and praziquantel) exercise 21 days prior. A majority of the pupils interviewed had knowledge of helminthiasis. There were significant associations between helminthic infection and source of drinking water (river; p = 0.013), the number of individuals who share toilet facilities (p = 0.049) and garbage disposal into a river (p = 0.015). Treatment failure of 7.2% was recorded for all the helminthic infections. Potential drug treatment failure of albendazole against hookworm infection and praziquantel against Schistosomiasis infection was thus evident within the population.

1. Introduction

Soil-transmitted helminthic (STH) infections present a great and silent burden of morbidity and mortality especially in poor populations [1]. It is estimated that STH infections affect more than two billion people worldwide, with the highest prevalence occurring in sub-Saharan Africa, the Americas, China, and East Asia [2]. Helminthic infections are caused by worms such as Ancylostoma duodenale, Necator americanus, Ascaris lumbricoides, Trichuris trichiura, and schistosomes. Predominantly, their mode of transmission is through the ingestion of eggs from food contaminated with human faeces that harbour the eggs of the parasite [3]. STH infections have been observed to be prevalent among people living in rural or deprived urban areas with low socioeconomic status, lack of potable water, and poor sanitation with children, pregnant women, and farmers who come into contact with the soil regularly being the populations most at risk [4]. STH infections are often associated with intestinal damage which results in nutritional loss thus causing poor mental and physical development and anaemia [5, 6]. These pathologies often lead to a low tolerance to other infections in infants, as well as poor birth outcomes in pregnant women [5].

In addressing morbidity and mortality associated with STH infections WHO has recommended the adoption of monitoring and preventive strategies such as promotion of WASH practices like personal hygiene, proper handling of sewage, and improving the quality of water supply [7]. This is also supplemented with periodic mass administration of antihelminthic drugs such as albendazole and praziquantel via school-based recovery services [7, 8, 9].

In Ghana, owing to the high prevalence of STH and Schistosomiasis infections often due to poor sanitary conditions, the country has for the past decades implemented various control measures such as intermittent health education and deworming programs particularly for school children in helminth endemic areas [5, 10, 11, 12]. This however has not been complemented with research to monitor the effectiveness of these programs. It is thus against this background that this study was undertaken to assess the rate of treatment failure, knowledge, attitude, and practice of Basic school pupils towards STH and Schistosomiasis infections. The findings from this study highlight an issue of treatment failure. Therefore, this study serves as a wake-up call to the Ministry of Health about the possible need for a mob up exercise. The research also emphasises the need to promote effective control measures towards the eradication of helminthic infections in Ghana.

2. Methodology

2.1 Study design and site

This was a cross-sectional study conducted in Assin Manso within the Central Region of Ghana. It is located 40 kilometres along the Cape Coast– Kumasi highway. Most of the inhabitants are persistent farmers. The study was conducted among Assin Manso A and B Community Basic Schools pupils in the Assin South District, Ghana.

2.2 Study population and sample size

A total of one hundred and fifty-five (155) pupils from kindergarten to Junior High School who had received Praziquantel and albendazole during MDA exercises were randomly selected to participate in the study. The study excluded all pupils who did not participate in the MDA exercise. Participants in this study were strictly pupils within the age range of 5 to 20 years who reside and attend school at Assin Manso Community Basic Schools (A&B).

2.3 Data collection

A structured questionnaire was used to collect data on the knowledge, attitude, and practices of the pupils. This was assessed by asking participants about the signs and symptoms, causes, mode of transmission, prevention, and treatment of helminthic infections. Participant sociodemographic data comprising of age, gender, level of education, occupation of parents, environmental factors concerning potable water, number of water bodies used in the locality and the history of helminthic infections were also collected. Before the commencement of the data collection process, the details of the research were explained to both parents and pupils before questionnaires were administered. The questionnaires were solely developed in clear English language.

Clean stool and urine containers were given to the students to collect stool and urine samples for the parasitological examination. A total of 153 students presented their samples to be used for the parasitological analysis to detect the presence of eggs and worms post Mass Drug Administration (MDA). The urine samples were taken between the hours of 10:00 am and 2:00 pm since this is the appropriate time for optimum egg shedding for Schistosoma sp. It was ensured that stool and urine samples were taken to the laboratory at the Department of Biomedical Sciences and kept in a fridge at a temperature of 4°C until ready for the analysis.

2.4 Urine analysis

About 10 mL of the urine sample were transferred into 15 ml falcon tubes and centrifuged at 1500 rpm for 5 minutes. The supernatants were discarded and the sediments were placed on a glass slide. The slides were covered with a coverslip and viewed under an X10 objective lens and X40 upon observation of a likely helminthic egg.

2.5 Saline preparation method

A few drops of saline were added to a little amount of stool in a container and the solution was mixed. Few drops of the resulting solution were placed on a glass slide and covered with a coverslip. The slide was observed under a microscope using the low power X10 objective lens. Upon observation of a suspicious helminthic egg, the X40 objective lens was used for clearer identification.

2.6 Formalin-ether concentration

A wooden stick was used to pick 1gram of stool into a beaker containing 10 ml of 10% formalin and emulsified it into suspension. The suspension was strained through a double layer of wet gauze directly into a 15 ml centrifuge tube. The gauze was discarded, and the suspension in the tube was topped up with formalin to bring the total volume to 7 ml. 3 ml of ether was added to obtain a total volume of 10 ml and the suspension was shaken vigorously. The mixture was centrifuged at 1200xg for 5 minutes. The supernatant was decanted and a few drops of residual fluid was allowed to flow back unto the sediment. A few drops of physiological saline were added to the sediment and re-suspended to have enough fluid. A few drops of the suspension were transferred onto a microscope slide, covered with a coverslip and examined using the low power (X10) objective. The X40 objective was used upon observation of an organism or suspicious objects for detailed morphological examination/identification of the organism.

2.7 Ethical consideration

Ethical clearance was obtained from the Ministry of Education and Scientific Review Committee of the University of Cape Coast. The assent of the parents and teachers were also sought before samples were taken from the pupils for the study.

2.8 Statistical analysis

Data analysis was performed using IBM SPSS Version 26. The distribution of study participants characteristics and prevalence of helminthic infections were presented as frequencies. Chi-square analysis was used to assess the association between study participant characteristics and helminthic status. A p-value <0.05 was considered statistically significant.

3. Results

3.1 Demographic information

The demographic and background characteristics of the study participants are presented in Table 1. More than half (57.4%) of the study participants were females and the majority (61.9%) of the study participants were within the age group of 10–14 years. Students in lower primary constituted the majority (31%) of the study participant followed by upper primary (28.6%) then, junior high school (27.4%) with the least being kindergarten students (11.9%). The majority (48.4%) of the study participants’ parents are farmers followed by small scale traders (16.1%).

Characteristics	Total (n = 155), n (%)
Gender
Males	66(42.6)
Females	89(57.4)
Age group (years)
5–9	42(27.1)
10–14	96(61.9)
15–19	17(11.0)
Level of Education
Kindergarten	10(11.9)
Lower primary	26(31.0)
Upper primary	24(28.6)
Junior High School	23(27.4)
Occupation of parents
Farmer	93(60)
Small trader	25(16.1)
Tailor/seamstress	10(6.5)
Mason	5(3.2)
Driver	12(7.7)
Hairdresser	3(1.9)
Mechanic	5(3.2)
Others	2(1.3)

Table 1.

Demographic and background characteristics of study participants.

3.2 Knowledge and self-reported symptoms associated with Schistosomiasis and Soil-transmitted helminthic infections

The knowledge and self-reported symptoms associated with schistosomiasis and soil-transmitted helminthic infections of the study participants are presented in Table 2. Out of the 155 study participants interviewed, more than half (63.9%) had not heard of helminthiasis, with only 32% being knowledgeable of helminthic infection. However, 45.2% of the participants thought personal hygiene is needed to fight against helminthiasis while (25.8%) did not know if personal hygiene affects helminthiasis or not. 36.1%, 6.5%.6.5%, 3.2%, and 1.3% of the study population said they experienced abdominal pain, diarrhoea, vomiting, pain when urinating (dysuria) and blood in the urine (hematuria) respectively.

Characteristics	Total (n = 155), n (%)
Do you know about helminthiasis
Yes	56 (36.1)
No	99 (63.9)
Do you know how to get a helminthic infection
Yes	49 (32.0)
No	72 (47.1)
Do not know	32 (20.9)
Is personal hygiene needed to fight helminthiasis
Yes	70(45.2)
No	45(29)
Do not know	40(25.8)
Symptoms and Experiences	Yes	No
Do you experience abdominal pain	41(36.1)	114(73.5)
Do you experience Diarrhoea	10(6.5)	145(93.5)
Do you experience vomiting	10(.5)	145(93.5)
Do you experience pain when urinating	5(3.2)	150(96.8)
Do you experience blood in the urine	2(1.3)	153(98.7)

Table 2.

Knowledge and self-reported symptoms associated with schistosomiasis and soil-transmitted helminthic infections.

3.3 Domestic attitudes related to schistosomiasis and soil-transmitted helminthic infections

Attitudinal characteristics of study participants are presented in Table 3. Of all the participants the data shows that the majority (45.2%), (31.1%), (43.2%) of the study participants use pipe water as the major source of water for drinking, bathing, and cooking respectively. 23.2% of the participants treat their water by allowing it to sit and settle with only 9.7% and 9.0% of the participants stating that they use alum and boiling as a mode of water treatment respectively.

Characteristics	Total (n = 155), n (%)	Total (n = 155), n (%)
Source of water for drinking	Yes	No
Pipe water	70(45.2)	85(54.8)
Borehole	21(13.5)	134(86.5)
Rainwater	11(7.1)	144(92.9)
Dam	0(0)	155(100)
River water	56(36.1)	99(63.9)
Pond/lake	3(1.9)	152(98.1)
Well	2(1.3)	153(98.7)
Spring	2(1.3)	153(98.7)
Sources of Water for Bathing
Pipe water	49(31.6)	106(68.4)
Borehole	21(13.5)	134(86.5)
Rainwater	8(5.2)	147(94.8)
Dam	0(0.00)	155(100)
River water	56(36.1)	99(63.9)
Pond/lake	3(1.9)	152(98.1)
Well	3(1.9)	152(98.1)
Spring	1(0.6)	154(99.4)
Sources of Water for Cooking
Pipe water	65(43.2)	88(56.8)
Borehole	19(12.3)	136(87.7)
Rainwater	5(3.2)	150(96.8)
Dam	0(0.0)	155(100)
River water	55(35.5)	100(64.5)
Pond/lake	1(0.6)	154(99.4)
Well	1(0.6)	154(99.4)
Spring	0(0.0)	155(100)
Water treatment
Boil	14(9.0)	141(91.0)
Add alum	15(9.7)	140(90.3)
Strain with Cloth	8(5.2)	147(94.8)
Filter	11(7.1)	144(92.9)
Sit and settle	36(23.2)	119(76.8)

Table 3.

Domestic attitudinal characteristics of study participants.

3.4 Practices in relation to schistosomiasis and soil-transmitted helminthic infections

Practices of study participants are presented in Table 4. 66.5% of the participants partake in farming. Also, 82.8%, 79.4%, and 16.3% of the participants wash their hands with water after visiting the toilet, wash their hands with both soap and water after visiting the toilet and wash their hands after playing on the ground respectively. More than half (62.6%) cross a river when going to the farm while 51.8% out of the 155 wear pairs of shoes when going to the farm.

Characteristics	Total (n = 155), n (%)	Total (n = 155), n (%)
Practices/Behaviour	Yes	No
Do you partake in farming	103(66.5)	52(33.5)
Do you wear shoes when going to the farm	88(51.8)	67(43.2)
Do you cross a river when going	97(62.6)	58(37.4)
Do you wash your hands with water after visiting the toilet	128(82.8)	27(17.4)
Do you wash your hands with soap after visiting the toilet	123(79.4)	32(20.4)
Do you wash your hands after playing on the grounds	95(61.3)	60(38.7)
Do you come in contact with water bodies	129(83.2)	26(16.3)

Table 4.

Practices/behavioural characteristics of study participants (n = 155).

3.5 Prevalence of schistosomiasis and other soil-transmitted helminths

The overall prevalence of helminthic infection among the school pupil after 21 days of mass drug administration was 11 (7.2%). There were only hookworm and Schistosoma haematobium treatment failure positives cases recorded after the MDA of the study participants. The study observed treatment failure of 3.3% and 3.9% for hookworm and Schistosoma haematobium infection respectively (Table 5).

Categories	Positives (n = 153)	Prevalence (%)
Hookworm	5	3.3
Schistosoma haematobium	6	3.9
Overall Helminthic infections	11	7.2

Table 5.

Prevalence of helminthiasis after mass drug administration.

3.6 Association between risk factors and helminthic infection

Helminthic infection was significantly associated with participants’ source of drinking water (p = 0.013), number of individuals who share toilet facility (p = 0.049) and whether participants disposed garbage into a river (p = 0.015) (Table 6).

Variables	Helminth Positive n(%)	Helminth Negative n(%)	P-value
Source of drinking
River
Yes	8(13.8)	50(86.2)	0.013
No	3(7.2)	92(96.8)
How many use toilet facility
<5	1(4.2)	23(95.8)	0.049
>5	3(3.7)	79(96.3)
Do not know	7(14.9)	40(85.1)
Garbage disposal (River)
Yes	2(20)	8(80)	0.015
No	8(5.7)	133(94.3)
Do not know	1(50)	1(50)

Table 6.

Association between risk factors and helminth infection.

Associations between helminthic infection status and all other variables were assessed however, the only statistically significant association have been reported here.

4. Discussion

Helminthic infection is very common among school children in Ghana. The Ministry of Health has been organising periodic MDA for school pupils. However, there have not been followed up exercises to assess the efficacy of the MDA among the school children in the Assin Manso community. Therefore, this study evaluates the effectiveness of the MDA and the knowledge, attitude and practice related to Schistosomiasis and STHs infection among the school pupils. This study revealed that most of the Basic School pupils have low knowledge (36.0%) about the modes of transmission of helminthic infections. This suggests that health education on helminthic infections as a control measure has not been effectively instituted particularly among pupils in the area, thus increasing their risk of acquiring helminthic infections. This observation is consistent with other findings in Bangladesh [13], Kenya [14], South Africa [15] and Ethiopia [16]. However, the finding contradicts the report by Sady, Al-Mekhlafi [17], who recorded higher awareness on the modes of transmissions among rural populations in Yemen. As highlighted in a study by Dawaki, Al-Mekhlafi [18], individuals living in remote rural neighbourhoods often lack the requisite knowledge on the causes, mode of transmission, signs, and symptoms, and preventive measures of schistosomiasis due to their poor economic status as reported by Murnane [19].

We found that the majority (70%) of the school children use untreated water for domestic purposes, which agrees with a report by Addo, Addo [20] in a Ghanaian community that 93% of the households do not treat their water before drinking. The continuous domestic use of untreated water is a risk factor for helminthic infections seeing that the river is the major source of water in the community. Unprotected surface water such as rivers, lakes, or springs or groundwater can easily become contaminated by human or animal faeces thus making the need for water treatment urgent [21].

The study also found that more than 60% of the participants engage in farming activities, with 62.6% reporting that they cross-river when going to their farms and 42.6% reporting that they do not wear shoes when going to the farm. This observation corroborates with the studies by Midzi, Mtapuri-Zinyowera [22], who reported that 82.6% of helminthiasis patients engage in farming. This could be an important risk factor for helminth infection since most of the farmers practise open range defecation and may shed some of the helminths eggs through their stools into the soil that could be picked up during farming practices thus increasing the risk of helminthic infections. Also, most of the farmers may come into body contact with water body sources that they cross to their various farms and these water bodies may be a major risk factor of schistosomiasis infection, since schistosomes present in the water bodies may penetrate the skin during surface body contact to cause the infections [23].

We observed that the majority (79.4%) of the children wash their hands with soap and water before eating, after visiting the toilet, and after playing on the grounds. This could be as a result of the promotion and enforcement of personal hygiene by school authorities, thus reducing the pupils’ susceptibility to helminthic infections.

4.1 Association between risk factors and helminth infection

We found a significant association between the source of drinking water and helminthic infections which confirms the report by Tiruneh, Geshere [24], Adu-Gyasi, Asante [25], Simon-Oke, Afolabi [26], who identified the source of drinking water as a significant risk factor of helminthic infection. These studies revealed that the use of protected water sources such as pipe was associated with a reduced odds of helminthic infection [25], whereas the use of unprotected water sources such as rivers was associated with increased odds of infection [24]. Studies by Simon-Oke, Afolabi [26] also identified a high prevalence (45%) of helminthic infection among individuals whose major source of drinking water was the river and a relatively lower prevalence (10%) among pipe water users.

The study also observed a significant association between the sharing of toilet facilities and helminthic infections, which agrees with findings by Mahfouz, el-Morshedy [27], Heijnen, Cumming [28], who observed sharing of toilet facilities as a risk factor for helminthic infection. This could be attributed to the poor sanitary practices and the ease of disease spread which could be observed at shared toilet facilities, particularly communal toilet facilities.

Evidence from our study also indicates that poor garbage disposal practices such as the disposal of refuse into the river are associated with the contraction of helminthic infection. This was actually in line with studies by Curtale, Pezzotti [29], Asady, Ismail [30], who observed that improper garbage disposal was significantly associated with STH infection. This results from the fact that improper disposal of waste contaminated with helminth into soil often facilitates the spread of STH infection, particularly through the ingestion of eggs.

4.2 Treatment failure

We found a treatment failure rate of 7.2% among the school children who had received MDA less than a month ago. This indicates that some of the worms may have developed resistance to albendazole and praziquantel and this could pose a serious problem towards the eradication of these worms in the community. This finding is consistent with studies by Humphries, Mosites [31], Jaske [32], who both observed higher treatment failure of 39% and 36.8% respectively among individuals treated with albendazole. As highlighted by Humphries, Mosites [31], Humphries, Nguyen [33] this high rate of albendazole failure raises concern about emerging resistance particularly among STH endemic communities. A recent study done in the middle belt of Ghana found that comorbidity of STH with malaria parasites could increase albendazole treatment failure among individuals [34]. Thus we recommend if possible to screen the school children for malaria infection before MDA and possibly treating individuals with concurrent infection with both antimalaria and anthelminthic drugs. A recent study by Djune-Yemeli, Nana-Djeunga [35] also suggested that the use of Mebendazole- or Albendazole-based MDA alone among high-risk populations may not be sufficient to eliminate soil-transmitted helminthic infections thus necessitating the urgent need for new antihelminthics [36].

We found some treatment failure of praziquantel (PZQ) treatment against schistosomiasis infection among the school children and this is supportive of other studies findings of increased treatment failure of PZQ in certain communities in Ghana [37, 38, 39, 40, 41, 42, 43]. This finding is also supported by a systemic review and meta-analysis by Danso-Appiah and De Vlas [42], who provide corroborative evidence of the unexpectedly low cure rate associated with the use of praziquantel.

Whilst it is unclear the reason for the relatively high prevalence of treatment failures being recorded globally, particularly in endemic areas, various studies have suggested that factors underlying this observation include; the sub-curative efficacy of the typical dose of 40–60 mg/kg [44], the presence of immature worms and insufficient drug uptake particularly due to unique metabolic characteristics of specific patients [45] and helminths comorbidity with malaria [34].

5. Conclusion

This study revealed treatment failure of both albendazole and praziquantel against STH and Schistosomiasis infection, respectively among the Basic school children. Thus, we recommend mob up screening exercises after the MDA and treatment of children who may still test positive. This will contribute to the prevention and management of helminthic infections among school children. There is also the need to raise awareness about the issue of MDA failure to encourage all stakeholders to contribute towards control of helminthic infection through the development of better water purification systems to provide potable water and the provision of effective incinerators for proper waste disposal, to promote environmental hygiene… It is also necessary to improve health education, to enable pupils to avoid habits that lead to STH and schistosomiasis.