A study of hurdles in mass treatment of schistosomiasis in KwaZulu-Natal, South Africa

Abstract

Background: It has been estimated that 700 million people worldwide and 5.2 million people in South Africa are in need of annual treatment for schistosomiasis. In accordance with the current policy the Department of Health (DoH) in KwaZulu-Natal province, South Africa, aimed to reach 75% treatment coverage in a mass treatment campaign (MTC) of schools in a schistosomiasis-endemic area.

Methods: A cross-sectional study was designed to explore the implementation, coverage, challenges and limitations of a DoH MTC in a middle-income country. The study was conducted by exploring nurses’ and research team records, school enrolment lists and parental consent forms.

Results: Slightly more than 10 000 learners in 43 primary and high schools were treated, achieving treatment coverage of 44.3%. A median of two schools per day were visited over the course of 39 days. We found that older learners, being male and attending a large school were independent significant predictors for low treatment coverage.

Conclusion: Our results indicate a much lower coverage than recommended by the South African National Department of Health and World Health Organization (WHO). Coverage would likely increase through improved consent procedures and repeated schools visits. Further information is needed on how to increase compliance in older teenagers, males and learners in large schools.

Keywords:

• health education
• mass drug administration
• mass-treatment
• praziquantel
• rural health
• schistosomiasis
• treatment

Introduction

Schistosomiasis (bilharziasis) is a water-borne parasitic disease hosted by freshwater snails. It is recognised as one of the major neglected tropical diseases affecting over 249 million people globally.¹ Sub-Saharan Africa carries 85–93% of the global schistosomiasis burden, with the highest prevalence in schoolchildren in poor areas, adolescents and young adults.^1,2 Consequences for individuals affected by schistosomiasis may include anaemia, malnutrition, genital disease, impairment of growth and development, and low school attendance.² Control of schistosomiasis may have a wide range of health and socioeconomic benefits for the poorest populations.

The current strategy recommended by the World Health Organization (WHO) for the control of morbidity is preventive mass drug administration with praziquantel (PZQ), targeting mainly schoolchildren and adults at risk of infection.³ In recent years pre-school children have also been considered for inclusion.⁴ Mass treatment campaigns (MTCs) for schistosomiasis should aim for 75% coverage in order to interrupt or decrease transmission.³ In areas exceeding 50% prevalence, the WHO recommends to treat all school-age children annually, while biennial treatment is sufficient in areas with prevalence between 10% and 50%. In areas with less than 10% prevalence, two treatments during the primary school years are sufficient.

In Brazil, China, Egypt and the Philippines mass screening and treatment have resulted in lasting schistosomiasis control.^5,6 Nonetheless, by 2014 only 17% of people at risk of morbidity due to schistosomiasis worldwide had received treatment.¹ A suboptimal coverage poses a risk of re-infection.³

In 2011, the WHO estimated that 5.2 million people in South Africa require annual preventive drug therapy for schistosomiasis.⁶ Studies from KwaZulu-Natal report prevalence of Schistosoma haematobium in school-age children between 22–55%.⁷ The last mass treatment campaign in South Africa was implemented in KwaZulu-Natal in 2000.⁸ It was a school-based multi-helminth control programme run by the Department of Health (DoH).⁸ In 2008 MTC guidelines were published by The South African Department of Health.⁹ The implementation guidelines, which are based on WHO definitions and recommendations, outline the technical basis for introducing helminth control programmes and identify key factors which need to be in place for successful implementation.

This study aimed to explore the implementation, the coverage, challenges and limitations of an MTC in a middle-income country setting.

Material and methods

Study area and inclusion

The DoH MTC was implemented in the Ugu District in south-eastern KwaZulu-Natal, South Africa. The Ugu district covers 5 866 km² and had an estimated population of 709 918 in 2007.¹⁰ It is comprised of two distinct areas; the coastal strip which is largely urban, and the rural inland expanse. The rural area, where the DoH MTC was conducted, is largely populated by two ethnic groups of people, Zulu and Xhosa. It consists of traditional mud homes where agriculture is the primary economic activity. In 2011, 16.6% of households in Ugu district did not have access to piped water.¹¹ Communities rely on unsafe waters from nearby rivers, exposing the inhabitants to water bodies infested with S. haematobium cercaria.

Official education statistics from KwaZulu-Natal report a gross enrolment ratio of 92%.¹² There are 507 schools with a total of 220 708 learners in the District.¹³ High schools were randomly selected for the DoH MTC by assigning a number to each school and making an internet-generated random list. The primary schools feeding most learners to each of these high schools were also included. In all 60 schools were approached. However, due to time constraints, class lists were only collected in 54 schools, covering 31 584 learners. The study did not reach and therefore excluded 11 schools (24% of total learners).

A cross-sectional study was conducted in all reached schools. Family members, teachers and non-enrolled children were also invited to receive treatment. They were informed via the learners' information leaflet to come to the school on the day that the treatment team was there. With this, the DoH aimed to increase the treatment coverage and decrease the risk of re-infection.⁶ These people were, however, not satisfactorily registered and are therefore not included in the data analysis.

A data collection team computerised class lists including learners’ names, date of birth, guardian information, gender, grade and school. Consent status was registered (agreed/refused/blank), as well as weight, the calculated number of tablets, and whether or not the learner received the medication. All data were coded before analysis.

Schools with less than 350 learners were defined as small schools. Schools with 350–700 learners were defined as medium-sized, and schools with more than 700 learners as large.

Methods

Permission to carry out the study was obtained from the Ugu District Departments of Education and Health. School inclusion and practical issues were discussed with the principals, the school governing bodies, parents and staff.

The MTC was implemented in winter, between May 20 and September 12, 2011, when transmission of schistosomiasis is low due to reduced water contact. This reduces the risk of immediate re-infection^3,14 and also increases the effectiveness of the drug, as PZQ is highly effective in killing adult worms, but does not kill immature schistosomes (from recent infections).³

The treatment team size, the quantity of consumables, and the equipment brought to schools were arranged in advance and varied according to the school size. A typical team consisted of 2–4 nurses and 2–4 assistants. Tablet distribution only commenced after the school lunch to ensure that the children had eaten prior to treatment, and to cut food costs for the programme. Bread and bananas were brought to the schools to provide food intake for learners who had not received a school meal.

The MTC was implemented in a classroom or in another assigned room, depending on the advice of school officials. Learners with completed consent forms were weighed and the dose of praziquantel was calculated at 40 mg per kg of body weight.³ A designated health worker directly observed ingestion of all tablets by counting the number of tablets in each learner’s hand and observing hand-to-mouth intake. For smaller children, tablets were split in two. The treatment team remained in the school for an hour after treating the last class, giving the learners the opportunity to report side effects.

In schools with less than 75% treatment coverage a second treatment day was scheduled immediately. New parental consent forms were distributed.

Ethical approval

The research was granted permission from the Biomedical Research Ethics Administration, University of KwaZulu-Natal on March 1, 2011 (Ref. BF029/07), the Department of Health, Pietermaritzburg, KZN, February 3, 2009 (Ref. HRKM010–08), the Norwegian ethics committee, Regional Etisk Komité Øst-Norge (REK-Øst), gave ethical clearance on September 17, 2007 (Ref. 469–07066a1.2007.535), and The European Group on Ethics in Science and New Technologies in June 2011 (Ref. IRSES-2010:269245). The Ugu Departments of Health on February 15, 2008, Education on December 14, 2010 and July 27, 2011. The researchers adhered to the Declaration of Helsinki on Ethical Principles for Medical Research Involving Human Subjects.

The DoH MTC was conducted by the Ugu District School Health Teams in collaboration with the Ugu Department of Education (DoE). Written informed consent was obtained from the learners and participation was voluntary. In South Africa praziquantel can currently only be dispensed by registered nurses or medical doctors (Schedule 4 drug).¹⁵ Consent forms were distributed three to ten days prior to the scheduled treatment day and collected a couple of days before; at the latest on the day of treatment. Only learners who retuned complete, affirmative consent forms were treated.

According to South African regulations, learners below the age of 18 should only be provided school health services with written consent of parent or caregiver. However, learners older than 14 years may consent to their own treatment, but should be advised to inform and discuss their treatment with parent or caregiver.¹⁶ In this study, in accordance with the wishes expressed by teachers and parents, self-consent forms were only accepted from learners above the age of 18.

Data analysis

Data were computed using Statistical Package for the Social Sciences (SPSS), version 19 (SPSS Inc., Chicago, Illinois, USA). Age data was not normally distributed. Chi-square tests and odds ratio (OR) with 95% confidence intervals (95% CI) were used to explore the associations. Logistic regression analysis was used to assess the association between selected predictors and outcome variables. A significance level of 5% was used. Predictor variables were included in the multivariate regression analysis if the p-value from the crude association was less than 0.20. If the Spearman rank correlation between two predictor variables was above 0.70 or below minus 0.70, only one of these variables was included in the multivariate regression analysis.

Results

In 43 schools, 24 005 learners were reached and 10 632 learners were treated (Table 1). These were in 29 primary schools, two intermediate schools, and 12 high schools. Categorised by size, 10 were small schools, 19 were medium-sized, and 14 were large schools.

Table 1: Treatment coverage across gender and school phase

	Treated females/Total reached females (%)	Treated males/Total reached males (%)	Total treated persons/Total reached Persons (%)	Gender not recorded^* (%)
Treated schools (43)	4382/9412 (46.6)	4190/9773 (42.9)	10632/24005 (44.3)	2060/4820 (42.7)
Primary school^†	2878/5357 (53.7)	2882/5846 (49.3)	7159/14162 (50.6)	1399/2959 (47.3)
Intermediate school^‡	279/583 (47.9)	253/610 (41.5)	551/1231 (44.8)	19/38 (50.0)
High school^§	1225/3472 (35.3)	1055/3317 (31.8)	2922/8612 (33.9)	642/1823 (35.2)

^* Gender not stated on class list.

^† Usually grade 1 to 7, but occasionally only to grade 4.

^‡ Usually grade 7 to 9.

^§ Usually grade 8 to 12.

School lists included the following facts for collection: grade, sometimes age and sometimes gender. These facts were collected for all, treated and untreated. Gender was registered for 79.9% (19 185/24 005) of the learners (Table 1). For the remainder, gender was not specified in the school lists. Date of birth was available for 60.9% of learners. The median age was 14 years (range 3–32), 12 years for learners who received treatment and 15 years for those who were not treated.

Treatment coverage

Most schools were approached twice (range 1–4). In Table 1 it is shown that the overall treatment coverage, after a second school visit, was 44.3%, ranging from 14.5 to 82.6% in the different schools. As shown in Figure 1, coverage decreased with age, and fewer males than females were treated in all age groups. The multivariate analysis in Table 2 shows that belonging to an older age group, attending a large school and male gender were all significant predictors for low treatment coverage. A separate analysis shows that significantly fewer high school learners received treatment, independent of school size (OR 0.50, 95% CI 0.47–0.54, P < 0.001).

Figure 1: Treatment coverage by the different age groups (in years) and gender

Table 2: Bivariate and multivariate analysis for factors influencing the treatment coverage

			Bivariate analysis		Multivariate analysis
		Treatment given (%)	OR* (95% CI)	P	Adj. OR (95% CI)^†	P
Age group	3–9	1894/3232 (58.6)	1		1
	10–14	2646/5364 (49.3)	0.69 (0.63–0.75)	<0.001	0.70 (0.63–0.78)	<0.001
	15–19	1728/5128 (33.7)	0.36 (0.33–0.39)	<0.001	0.39 (0.35–0.43)	<0.001
	20–24	223/866 (25.8)	0.25 (0.21–0.29)	<0.001	0.28 (0.23–0.33)	<0.001
	25–35	3/26 (11.5)	0.09 (0.03–0.31)	<0.001	0.10 (0.03–0.35)	<0.001
School level	Primary school	7159/14162 (50.6)	1
	Intermediate school	551/1231 (44.8)	0.79 (0.71–0.89)	<0.001
	High school	2922/8612 (33.9)	0.50 (0.48–0.53)	<0.001
Gender	Female	4382/9412 (46.6)	1		1
	Male	4190/9773 (42.9)	0.86 (0.81–0.91)	<0.001	0.91 (0.85–0.99)	0.02
School size	<350 learners	1185/2108 (56.2)	1		1
	350–700 learners	4597/9753 (47.1)	0.69 (0.63–0.76)	<0.001	0.48 (0.40–0.58)	<0.001
	>700 learners	4850/12144 (39.9)	0.52 (0.47–0.57)	<0.001	0.47 (0.39–0.56)	<0.001

^* Odds ratio (OR) with 95% confidence interval (CI).

^† School level was not included in the multivariate analysis as there is a causal factor between school level and age.

Consent procedure

Consent forms for parental signature were collected a few days after distribution, but were only returned by 56.4% (13 549/24 005) of the learners. Of these, 86.9% (11 773/13 549) consented, while 13.1% (1 776/13 549) refused. The remaining 43.6% (10 456/24 005) of consent forms were either not returned or illegible. Table 3 shows that high school learners were less likely to return forms. There were 2 099 consenting learners who were not treated and 958 learners were registered as treated whose consent status was not recorded.

Table 3: Bivariate and multivariate analysis for factors influencing the percentage of consent forms returned

	Consent form returned (%)	OR (95% CI)^*	P	Adj OR(95% CI)^†	P
Female	5735/9412 (60.9)	1		1
Male	5314/9773 (54.4)	0.76 (0.72–0.81)	<0.001	0.74 (0.70–0.79)	<0.001
School size<350^‡	1363/2108 (64.7)	1		1
School size 350–700	5878/9753 (60.3)	0.83 (0.75–0.92)	<0.001	0.92 (0.82–1.03)	0.15
School size >700	6308/12144 (51.9)	0.59 (0.54–0.65)	<0.001	0.62 (0.55–0.69)	<0.001
Primary school^§	8739/14162 (61.7)	1		1
Intermediate school^||	660/1231 (53.6)	0.72 (0.64–0.81)	<0.001	0.75 (0.66–0.84)	<0.001
High school^**	4150/8612(48.2)	0.58 (0.55–0.61)	<0.001	0.57 (0.53–0.61)	<0.001

^* Odds ratio (OR) with 95% confidence interval (CI).

^† Adjusted odds ratio, all three factors were included in the multivariate analysis.

^‡ Number of learners in the school.

^§ Usually grade 1 to 7, but occasionally only to grade 4.

^|| Usually grade 5 to 7.

^** Usually grade 8 to 12.

Table 3 shows that 60.9% of female learners returned consent forms, compared to 54.4% of male learners. Multivariate analysis shows that learners in small schools and primary schools returned significantly more consent forms than learners in large schools and high schools.

Of learners who returned consent forms, 91.3% consented to treatment in large schools compared to 84.1% in small schools (OR 2.32, 95% CI 1.91 – 2.81, P < 0.001). Additionally, the odds of consenting to treatment was 44% lower for learners in high schools compared with learners in primary schools (OR 0.56, 95% CI 0.49 – 0.63, P < 0.001). There was no roll call upon the distribution of consent forms or on the treatment days.

On average three learners per school reported side effects such as transient nausea, vomiting, stomach pains or headache.

Discussion

Unreturned consent forms were the most important reason for low treatment coverage. Unreturned consent forms could represent a difficult consent form retrieval system, illiteracy or absent guardians. However, it could also encompass indirect refusals and hesitations by children and/or care-givers.

Moreover, we found that older age, being male and attending a large school were other independent, significant predictors of low treatment coverage. This has also been found in previous studies and may partly be attributed to parental control and a closer teacher follow-up in younger children and in small schools.^17,18 In addition, males have been found to be less likely to visit health facilities and may be less likely to follow mainstream health recommendations.¹⁸ Lastly, a research project on schistosomiasis in girls in the area may have made boys think this is a female problem.¹⁹ Misconceptions may have influenced participation in treatment. Schistosomiasis is perceived as a self-healing disease, and the chronicity of the disease is not known to the general population.¹⁹

Upon making roll calls from returned consent forms, we observed that many consenting learners were absent on the treatment days. However, the exact number of absentees was not recorded. Previous studies in South Africa have found that school absenteeism may reach 30% on some days, and schistosomiasis in itself may cause school absenteeism.^8,14,20–22

Mass treatment campaigns in South Africa have the disadvantage that tablets must be distributed by health professionals.¹⁵ There are reports that external treatment teams lack credibility, whereas trained teachers distributing treatment may tap into already existing trust.³ Furthermore, they know every learner by name and may know how to reach many absentees.^3,19 A study of an MTC in Uganda, where teachers distributed the treatment, showed significant increase in coverage after teacher motivation was provided.²³ In their report on promoting health in schools, the WHO emphasises that collaboration between ministries of health and education, as well as their representatives at a local level, is essential for implementation of successful school health programmes.²⁴

Several administrative challenges occurred during the MTC. Schools were reluctant to provide more than one day for treatment, as they wanted to minimise disturbance (personal communication). Further, class lists were made at the beginning of the year and occasionally we found that learners were recorded in several schools, grades or sections. The learners did not have unique identification numbers, and many had several names, such as clan names, praise names, different surnames, English and Zulu names. Many did not know their date of birth and there was discrepancy between care-givers’ recordings, the official school list and the learners’ own information.

Increased coverage may be achieved by repeated treatment days, relentless distribution and collection of consent forms, and by adhering to the new guidelines, granting learners between the ages of 14 and 18 years the possibility to self-consent to treatment.¹⁶ It has also been suggested to request consent (or refusal) as part of the schools’ yearly registration procedure.⁸

Conclusion

The reported programme in the schools of Ugu District only reached 44% of the learners, whereas WHO and the National Department of Health in South Africa recommend that regular mass-treatment should reach 75% coverage with Praziquantel.⁹ Although the regimen is highly effective killing adult worms and preventing morbidity,^6,24 a low treatment coverage renders communities at higher risk of re-infection. Being non-toxic, Praziquantel has minor side effects, and in many countries delivery is integrated with other school health programmes, such as vaccination campaigns. Teachers are instrumental in building trust, and active participation by them in advocacy and implementation is highly desirable.^6,24 Further avenues must be explored to communicate the medical consequences of the disease and the importance of participation in MTCs to the rural populations. Most important, however, would be a national commitment to control schistosomiasis of rural South Africa.

Acknowledgements

Technical and professional assistance were provided by the school health nurses, research nurses of Child Development Research Unit, research assistants, security guards, logisticians, data enterers and laboratory staff. The authors are very grateful for the financial support from the European Research Council under the European Union’s Seventh Framework Programme (FP7/2007-2013)/ERC Grant agreement no. PIRSES-GA-2010-269245 and from the University of Copenhagen with the support from the Bill and Melinda Gates Foundation grant number OPPGH5344. We are indebted to the Ugu Department of Health, District Health Manager Mr Veeran Chetty, Dr. Olowookorum, Mrs Sokhulu, the Ugu Department of Education, teachers and headmasters of Ugu schools, teenagers, children and parents.