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Impact on malaria morbidity of a programme supplying insecticide treated nets in children aged under 2 years in Tanzania: community cross sectional study

Salim Abdulla, research scientist ^a, Joanna Armstrong Schellenberg, project manager ^b, Rose Nathan, research scientist ^a, Oscar Mukasa, research scientist ^a, Tanya Marchant, research scientist ^a, Tom Smith, project leader ^b, Marcel Tanner, director ^b, Christian Lengeler, project leader ^b. 

^a Ifakara Health Research and Development Centre, PO Box 53, Ifakara, Tanzania, ^b Swiss Tropical Institute, PO Box 4002, Basle, Switzerland

Correspondence to: C Lengeler Christian.Lengeler{at}unibas.ch

	Abstract

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Objective: To assess the impact of a social marketing programme for distributing nets treated with insecticide on malarial parasitaemia and anaemia in very young children in an area of high malaria transmission.
Design: Community cross sectional study. Annual, cross sectional data were collected at the beginning of the social marketing campaign (1997) and the subsequent two years. Net ownership and other risk and confounding factors were assessed with a questionnaire. Blood samples were taken from the children to assess prevalence of parasitaemia and haemoglobin levels.
Setting: 18 villages in the Kilombero and Ulanga districts of southwestern Tanzania.
Participants: A random sample of children aged under 2 years.
Main outcome measures: The presence of any parasitaemia in the peripheral blood sample and the presence of anaemia (classified as a haemoglobin level of <80 g/l).
Results: Ownership of nets increased rapidly (treated or not treated nets: from 58% to 83%; treated nets: from 10% to 61%). The mean haemoglobin level rose from 80 g/l to 89 g/l in the study children in the successive surveys. Overall, the prevalence of anaemia in the study population decreased from 49% to 26% in the two years studied. Treated nets had a protective efficacy of 62% (95% confidence interval 38% to 77%) on the prevalence of parasitaemia and of 63% (27% to 82%) on anaemia.
Conclusions: These results show that nets treated with insecticide have a substantial impact on morbidity when distributed in a public health setting.

	Introduction

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Several studies have shown that malarial parasitaemia is positively correlated with anaemia and that parasitaemia is the primary cause of anaemia in very young children in Africa.¹ As a result, because malarial infection is the norm in high transmission areas, anaemia is common in young children. Assessment of the impact of chemoprophylaxis in Tanzanian infants showed that over 60% of the anaemia could be due to malaria.² The emergence and spread of parasite resistance to commonly used antimalarial agents has exacerbated the problem of anaemia in sub-Saharan Africa.³

Hopes for controlling malaria and malarial anaemia have recently been revitalised by the demonstration that nets treated with insecticide can reduce morbidity and mortality. A summary of randomised controlled trials showed an average protective effect of about 50% on mild malaria episodes in areas where the rate of transmission of malaria was stable.⁴ Moreover, protective effects were shown on the prevalence of parasitaemia with a high level (>5000/µl) of trophozoites (31%) and on overall mortality (19%). A modest improvement in packed cell volume (a rise of 0.02 (2%)) and weight gain was also observed in children sleeping under treated nets.⁴ Large scale implementation of programmes to supply treated nets is under way in several African countries.⁵

It is not known whether the impact of treated nets in the context of well controlled randomised controlled trials can be replicated under programme conditions.⁶ We report the first assessment of the impact of treated bed nets when supplied in the context of a large scale social marketing programme (an approach using marketing techniques to promote and distribute socially beneficial interventions rather than commercial products) on morbidity indicators in children aged under 2 years in an area of Tanzania with a high prevalence of malaria.

	Methods

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Study area and population
Social marketing of treated bed nets started in the Kilombero net project (KINET) in 1997,⁷ covering the Kilombero and Ulanga districts (population 350 000) in southwestern Tanzania. Nets and insecticide (branded Zuia Mbu) are now being promoted, distributed, and sold through public and private outlets and a system of community door to door distributors. When the project began, the retail price of a treated net was $5 (£3.60). Although this amount was not a negligible part of the average annual income in this community, many of the residents bought a net.⁷ The impact of the programme on morbidity and mortality indicators is being monitored in 18 villages under demographic surveillance. Population characteristics of this area of high perennial malaria transmission have been described elsewhere.⁸ Moderate anaemia (packed cell volume <0.25 ( <25%)) and severe anaemia occur in 61% and 14% respectively of children aged under 5 years who are admitted to the local St Francis District Hospital.⁹ Resistance to chloroquine is common: 65% of malaria infections do not clear within one week of chloroquine treatment.¹⁰

Design
Three annual, cross sectional surveys were conducted in a sample of children aged under 2 years living in the villages in the demographic surveillance area.⁷ The first survey was done at the time of launching the social marketing campaign in June 1997, and two other surveys were carried out at the same period (June to August) in the subsequent two years. A simple random sample was selected from the demographic surveillance database for the first survey, and a two stage, random sampling (of six villages then sampling children from these) was done for the subsequent surveys. A different sample was selected for each survey.

Procedures
The selected children were visited at home, and oral consent obtained from the parent or guardian. A questionnaire was used to assess use of treated nets and other potential risk factors. A physical examination was performed, and temperature, weight, and height were also measured. A finger prick blood sample was taken to determine haemoglobin level and assess whether parasitaemia was present. Haemoglobin levels were measured with a portable kit, HemoCue (HemoCue, Ängelholm, Sweden). Slides were stained in Giemsa and were read (without the microscopists knowing the child's net status) using standard procedures as described elsewhere.⁹ An inspection of the children's sleeping places to assess their use of nets was done only in 1999 because this was strongly perceived as an intrusion of their privacy.

Data analysis
Analysis was done for the three cross sectional surveys combined. We estimated impact of the nets on haemoglobin level, anaemia, parasitaemia, and splenomegaly using multiple linear and logistic regression models, taking into account the sampling methods for years 2 and 3, and using robust regression approaches in STATA software.¹² We included the effect of different time points of observation (surveys) as one of the explanatory variables.

	Results

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We identified 985 eligible children; the mothers of 16 of these children refused consent, and 142 mothers could not be traced at their homes. Therefore, mothers (or guardians) of 827 children were interviewed during the three cross sectional surveys. Sixty eight children were over 24 months old at the time of sampling, and the net status was not known for 11 children; therefore only 748 (91%) children were included in the analysis. Similar proportions of anaemia and of reported net ownership were found in the children analysed and those not analysed (data not shown).

We observed an increase in the mean haemoglobin level from 80 g/l to 89 g/l and a decline in the proportion of children with anaemia (49% to 26%), parasitaemia (63% to 38%), and splenomegaly (86% to 49%) during the successive surveys (table 1). The proportion of children with a net (treated or untreated) increased from 58% (140/240) to 83% (199/239), and those with treated nets increased substantially during the three years (from 10% to 61%), indicating a rapid uptake of the socially marketed treated nets, especially during the first year (table 1).

Ownership and use of nets
Predictors of net ownership included family income: families with a high income (highest quarter) were almost three times more likely to have a bed net than those with a low income (lowest quarter) (table 2). This was expected as the treated nets were being sold. By the end of the second year of the marketing campaign (1999), only 17% of the children were without a net. Children with no access to covered wells (piped clean water)that is, not at the centre of the villageswere less likely to have nets (table 2). Mothers who mentioned that they would advise their neighbours to send their sick children to a formal health facility were more likely to have nets for their own children (odds ratio 2.27; likelihood ratio test ²=3.90, P value=0.048) than mothers who advised care by a traditional healer. This might reflect an association between health seeking patterns or perceptions about the value of the formal health system and the decision to have a net or not.

Health impact of treated nets
We observed a protective efficacydefined as (1 odds ratio)×100on the prevalence of parasitaemia of 62% (95% confidence interval 38% to 77%) and 51% (0% to 76%) for treated and untreated nets respectively, when compared with children without nets (table 3). The prevalence of parasitaemia was also related to ethnic group, religion, use of the net in the previous month, and age of the child, with the prevalence in those aged over 1 year being four times higher than that in those aged under 7 months (table 3). This is consistent with earlier studies in Tanzania that showed that prevalence of parasitaemia increased with age. ^{13 14}

	Discussion

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These results have shown that the social marketing approach of distributing bed nets treated with insecticide was highly successful and resulted quickly in more than 80% of children aged under 2 years having access to a net. Our results suggest a good overall impact of social marketing of treated nets on health outcomes in the community, with an improvement of mean haemoglobin levels (from 80 g/l to 89 g/l) and a decline in the total proportion of children with anaemia (from 49% to 26%), parasitaemia, or splenomegaly. The treated nets had an apparent individual protective efficacy of over 60% on the prevalence of anaemia, parasitaemia, and splenomegaly. In this study untreated nets were also found to be protective. Overall, most of the changes occurred in the first year of the study.

These efficacy estimates are higher than those found in most controlled trials (see table on the BMJ 's website).^w1-w11 May this finding be the result, therefore, of residual confounding despite efforts to control for it? This question is especially pertinent because our comparison group comprised children who did not own nets in the same community. The tools used to measure confounding factors such as socioeconomic status and health seeking behaviour may not be sensitive enough to allow for proper control of confounding. Factors related to the dynamics of the malaria infection and the associated disease presentation, however, may also explain this finding. Variations in transmission, for example, strongly affect the estimates of morbidity and mortality in very young children.¹⁵ Therefore at a given transmission intensity, the age of the study participants may be crucial in determining the level of protection. Our finding of high impact in children under 2 years is in line with other studies that included very young children (see website table).

Lower impact estimates than ours were observed in a randomised study near Ifakara in a similar age group.^w11 This may be because our study covered a larger geographical area and included study children with a lower mean haemoglobin level (mean level in those without nets 77 g/l in our study, 87 g/l in the Ifakara study, t test=3.9, P=0.0001). Children with more severe anaemia are probably more likely to benefit from intervention than children with milder anaemia.

Nets treated with insecticide distributed through a social marketing programme rapidly and substantially reduced the prevalence of parasitaemia and anaemia in children aged under 2 years. This strategy has high potential in the control of malaria in sub-Saharan Africa.

	Acknowledgments

We thank the children and guardians who participated in the study; Dr H Mshinda, the director, and the other staff of the Ifakara Health Research and Development Centre for facilitating the conduct of the study; Drs F Lwila and P Mbena (district medical officers) and the health workers in the Kilombero and Ulanga districts.

Contributors: SA contributed to the design and planning of the work and was responsible for the field implementation, the analysis and interpretation of the data, and the writing of the paper. JAS has substantially contributed to the design, implementation, analysis and interpretation of the data, and in the writing of the paper. RN, OM, and TM participated in different ways in the design of the study, participated in the implementation of the field work and in the management and interpretation of the data, and contributed to the editing of the article. TS contributed to the design of the study, to its data management and analysis, and to the writing and finalisation of the paper. MT was involved in the planning and supervision of the work and contributed to the analysis and the writing of the paper. CL had overall responsibility for the work and contributed to all key aspects, including the interpretation of the findings and the writing of the paper. SA, JAS, CL will act as guarantors for the paper.

	Footnotes

Funding: Financial support was provided by the Swiss Agency for Development and Cooperation and by the government of Tanzania. CL is in receipt of the PROSPER grant 32-41632.94 from the Swiss National Science Foundation.

Competing interests: During the past five years CL has received financial support from several manufacturers of insecticide and mosquito nets to attend scientific meetings.

A table showing the impact of net use on anaemia reported by other trials is available on the BMJ's website. This article is part of the BMJ's trial of open peer review, and documentation relating to this also appears on the website

	References

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1.	Kitua AY, Smith TA, Alonso PL, Urassa H, Masanja H, Kimario J, et al. The role of low level Plasmodium falciparum parasitaemia in anaemia among infants living in an area of intense and perennial transmission. Trop Med Int Health 1997; 2: 325-333[Medline].
2.	Menendez C, Kahigwa E, Hirt R, Vounatsou P, Aponte JJ, Font F, et al. Randomised placebo-controlled trial of iron supplementation and malaria chemoprophylaxis for prevention of severe anaemia and malaria in Tanzanian infants. Lancet 1997; 350: 844-850[CrossRef][Medline].
3.	Bloland PB, Lackritz EM, Kazembe PN, Were JB, Steketee R, Campbell CC. Beyond chloroquine: implications of drug resistance for evaluating malaria therapy efficacy and treatment policy in Africa. J Infect Dis 1993; 167: 932-937[Medline].
4.	Lengeler C. Insecticide-treated bednets and curtains for preventing malaria. Cochrane Database Syst Rev 2000;4:CD000363.
5.	Insecticide treated nets in the 21st century. Report of the second international conference on insecticide treated nets, Dar es Salaam, Tanzania, October 1999. London: Malaria Consortium (London School of Hygiene and Tropical Medicine), 2000.
6.	Lengeler C, Snow RW. From efficacy to effectiveness: insecticide-treated bednets in Africa. Bull World Health Organ 1996; 74: 325-332[Medline].
7.	Schellenberg JR, Abdulla S, Minja H, Nathan R, Mukasa O, Marchant T, et al. KINET: a social marketing programme of treated nets and net treatment for malaria control in Tanzania, with evaluation of child health and long-term survival. Trans R Soc Trop Med Hyg 1999; 93: 225-231[CrossRef][Medline].
8.	Tanner M, de Savigny D, Mayombana C, Hatz C, Burnier E, Tayari S, et al. Morbidity and mortality at Kilombero, Tanzania, 1982-88. In: Feachem RG, Jamison DT, eds. Disease and mortality in sub-Saharan Africa. Oxford: Oxford University Press, 1991:286-305.
9.	Schellenberg D, Menendez C, Kahigwa E, Font F, Galindo C, Acosta C, et al. African children with malaria in an area of intense Plasmodium falciparum transmission: features on admission to the hospital and risk factors for death. Am J Trop Med Hyg 1999; 61: 431-438[Abstract].
10.	Hatz C, Abdulla S, Mull R, Schellenberg D, Gathmann I, Kibatala P, et al. Efficacy and safety of CGP 56697 (artemether and benflumetol) compared with chloroquine to treat acute falciparum malaria in Tanzanian children aged 1-5 years. Trop Med Int Health 1998; 3: 498-504[CrossRef][Medline].
11.	Stoltzfus RJ. Rethinking anaemia surveillance. Lancet 1997; 349: 1764-1766[Medline].
12.	STATA statistical software, release 6.0. College Station, TX: Stata Corporation, 1999.
13.	Kitua AY, Smith T, Alonso PL, Masanja H, Urassa H, Menendez C, et al. Plasmodium falciparum malaria in the first year of life in an area of intense and perennial transmission. Trop Med Int Health 1996; 1: 475-484[CrossRef][Medline].
14.	Smith T, Beck HP, Kitua A, Mwankusye S, Felger I, Fraser-Hurt N, et al. Age dependence of the multiplicity of Plasmodium falciparum infections and of other malariological indices in an area of high endemicity. Trans R Soc Trop Med Hyg 1999; 93(suppl 1): 15-20[Medline].
15.	Marsh K, Snow RW. Malaria transmission and morbidity. Parassitologia 1999; 41: 241-246[Medline].

(Accepted 27 October 2000)