Prevention of malaria in Afghanistan through social marketing of insecticide-treated nets: evaluation of coverage and effectiveness by cross-sectional surveys and passive surveillance

Prevention of malaria in Afghanistan through social marketing

of insecticide-treated nets: evaluation of coverage

and effectiveness by cross-sectional surveys

and passive surveillance

Mark Rowland1,2, Jayne Webster1,2, Padshah Saleh1, Daniel Chandramohan2, Tim Freeman1, Barbara Pearcy1,

Naeem Durrani1, Abdur Rab1 and Nasir Mohammed1

1 HealthNet International, Peshawar, Pakistan2 London School of Hygiene & Tropical Medicine, London, UK

Summary Malaria is often a major health problem in countries undergoing war or conflict owing to breakdown of

health systems, displacement of vulnerable populations, and the increased risk of epidemics. After

23 years of conflict, malaria has become prevalent in many rural areas of Afghanistan. From 1993 to the

present, a network of non-governmental organizations, co-ordinated by HealthNet International, has

operated a programme of bednet sales and re-treatment in lowland areas. To examine whether a strategy

based on insecticide-treated nets (ITN) is a viable public health solution to malaria, communities were

given the opportunity to buy nets and then monitored to determine population coverage and disease

control impact. This was carried out using two contrasting methods: cross-sectional surveys and passive

surveillance from clinics using a case–control design. Nets were purchased by 59% of families. Cross-

sectional surveys demonstrated a 59% reduction in the risk of Plasmodium falciparum infection among

ITN users compared with non-users (OR 0.41; 95% CI 0.25–0.66). The passive surveillance method

showed a comparable reduction in the risk of symptomatic P. falciparum malaria among ITN users

(OR 0.31; 95% CI 0.21–0.47). The cross-sectional method showed a 50% reduction in risk of P. vivax

infection in ITN users compared with non-users (OR 0.50; 95% CI 0.17–1.49) but this effect was not

statistically significant. The passive surveillance method showed a 25% reduction in the risk of

symptomatic P. vivax malaria (OR 0.75; 95% CI 0.66–0.85). ITN appeared to be less effective against

P. vivax because of relapsing infections; hence an effect took more than one season to become apparent.

Passive surveillance was cheaper to perform and gave results consistent with cross-sectional surveys.

Untreated nets provided some protection. Data on socioeconomic status, a potential confounding factor,

was not collected. However, at the time of net sales, there was no difference in malaria prevalence

between buyers and non-buyers. The abundance of Anopheles stephensi, the main vector, did not appear

to be affected by ITN. ITN constitute one of the few feasible options for protection against malaria in

chronic emergencies.

keywords insecticide-treated bednets, malaria, Plasmodium falciparum, Plasmodium vivax, Pakistan

correspondence Mark Rowland, London School of Hygiene & Tropical Medicine, Keppel Street,

London WC1E 7HT, UK. Fax: 00 44 7299 4720; E-mail: [email protected]

Introduction

Controlled trials have demonstrated that insecticide-treated

nets (ITN) can prevent malaria morbidity and mortality

under a variety of epidemiological conditions (Choi et al.

1995; Lengeler 1998). This has stimulated many govern-

ments, UN agencies and non-governmental organizations

(NGOs) to embark upon programmes of net distribution and

treatment (Chavasse et al. 1999). While the utility of ITN

is no longer in doubt, it is far from certain whether delivery

and sales through the less controlled conditions that exist

within development projects, or through the private

sector, can approach the same coverage and impact as

carefully executed trials (D’Alessandro et al. 1995; Lengeler

Tropical Medicine and International Health

volume 7 no 10 pp 813–822 october 2002

ª 2002 Blackwell Science Ltd 813

& Snow 1996). The degree of uncertainty is still greater

when the country being targeted is undergoing civil conflict

or just emerging from conflict. Such places are increasingly

the subject of internationally aided ITN distribution

projects, yet no evidence has been gathered to indicate that

such distributions have any impact on malaria (Rowland &

Nosten 2001). As ITN projects continue to grow in size and

number in both politically stable and unstable environments,

methods for monitoring effectiveness and coverage become

paramount to monitor progress and as a means for

improving strategy.

Until the last decade, the use of bednets in Afghanistan

was uncommon (Rowland et al. 1996). But with the

country racked by 20 years of war, the public health

system in disarray, and malaria becoming a major national

problem, a strategy based on ITN for personal protection

seemed the only feasible solution (Rowland et al. 1997).

An efficacy trial in the secure environment of an Afghan

refugee camp just over the border in Pakistan demonstrated

that Afghans were ready to adopt the habit and stood to

gain up to 70% protection against Plasmodium falciparum

and 56% protection against P. vivax infection (Rowland

et al. 1996). In 1992, HealthNet International (HNI)

initiated social marketing of ITN through a network of

district clinics run by several international and local NGOs

in the eastern region of the country.

Within 2 years, the programme’s initial objective of

seeding demand across the region had been achieved, and

the sales revenue generated was contributing towards

restocking of nets. Popularity and progress was such that the

network began to consider whether a malaria control

strategy based on sale of ITN could achieve a coverage and

epidemiological impact significant enough to replace the old

strategy of indoor residual spraying with DDT that existed

before the war. Groups of villages were given the oppor-

tunity to buy nets over a 2-year period. To measure impact,

two methods were compared: the first involved repeated

cross-sectional malaria parasite surveys among net-using

and non-using families, the second involved passive sur-

veillance of malaria cases at district clinics. A variant on the

first method has recently been applied in Tanzania to

evaluate the effectiveness of community-based ITN social

marketing (Abdulla et al. 2001). The second method has

been applied in Afghan refugee camps to evaluate the long-

term effectiveness of ITN (Rowland et al. 1997).

Methods

Study area

The study was conducted in the rural districts of Behsud

and Chaprahar in Nangarhar province, eastern Afghanistan

(Figure 1). By the early 1990s the focus of the war had

shifted to the centre and north of the country and the east

had become secure. Most villages in Nangarhar had been

partly destroyed during fighting but by 1995, the first year

of the study, many inhabitants had returned from refugee

camps in Pakistan, their homes rebuilt, the area de-mined,

irrigation systems repaired, and agriculture stepped up.

Agriculture was the main livelihood. The main crops grown

were wheat from March to May, rice from June to

November, and vegetables. Some farmers grew opium

poppy.

Nangarhar marks the western edge of the monsoon

rains, which fall in July and August. Rivers are also snow-

fed. The main malaria vectors in eastern Afghanistan are

Anopheles stephensi, A. fluviatilis, A. culicifacies, and

A. pulcherrimus (Rowland et al. 2002). In Behsud and

Chaprahar, these species breed in or around rice fields from

June onwards. Malaria is both seasonal and unstable in

Afghanistan, and outbreaks often occur in areas lacking

clinical services. P. vivax accounts for 85% and

P. falciparum for 15% of malaria infections. Incidence of

P. vivax reaches a peak in August, P. falciparum in

October – November, with transmission of both species

continuing until the end of the year (Rowland et al. 2002).

Chloroquine resistant P. falciparum is widespread (Rab

et al. 2001), and is partly responsible for its resurgence in

the last decade (Shah et al. 1997).

The interventions

The sequence of activities is summarized in the flow chart

(Figure 2). Criteria for selecting the two study areas were

presence of extensive rice culture and thus vector breeding,

reputable NGO clinics able to diagnose malaria using

microscopy, and little or no previous targeting with nets.

Nets were introduced in a stepped manner in six villages

from Behsud and in six villages from Chaprahar districts.

Three of six villages from each district were randomly

selected to receive nets in June 1995 and the other three

received nets in June 1996. The purchase price per net was

8000 afghanis (US$2.9) in 1995, increasing to 35 000

afghanis (US$3.3) in 1996 as a result of inflation. This

constituted a 25% subsidy on the manufacturer’s price.

A village was given a day’s advance notice of the arrival of

a mobile sales team, with the news being broadcast from

the mosques’ minarets. On arrival, the team gave a public

health education session about malaria and the use of ITN

using illustrated silk screen flip charts, registered the

families who wanted to buy, and treated the nets in full

public view. This mode of implementation was the

standard approach used by HNI during day-to-day sales

operations. The 12 villages were randomized with eight

Tropical Medicine and International Health volume 7 no 10 pp 813–822 october 2002

M. Rowland et al. Prevention of malaria through social marketing of insecticide-treated nets

814 ª 2002 Blackwell Science Ltd

being offered ITN (polyester nets treated with either

permethrin 500 mg/m2 or lambdacyhalothrin 25 mg/m2)

and four being offered untreated nets (UTN). Treatment

was free at the time of sales, but re-treatment was offered

for US$0.05 per net in both 1996 and 1997.

Cross-sectional parasite surveys were conducted in June

and November of 1995 and 1996. Villages were census-

surveyed and 25 households from each village were

randomly selected from the enumeration lists. Blood

smears were taken from all household members present on

the day of survey, and each individual was asked whether

they had been using a bednet recently (during the last

fortnight). Individuals were classified as bednet users or

non-users according to their response. About 15% of all

households were sampled at each survey. Households were

randomly selected anew from the enumeration list before

each new survey. Individuals positive for malaria parasites

were treated with chloroquine (25 mg per kg body weight

in divided doses).

Passive surveillance of malaria was carried out from July

1995 to December 1997 through two clinics in Behsud and

two clinics in Chaprahar. Microscopy was performed

routinely on all patients presenting with a history of fever

suspected of being malaria. Patients were asked whether

they had been using a bednet recently. Positive cases were

treated with chloroquine. Ideally, each patient would have

been questioned about socio-economic status, in order to

adjust for this potential confounder later on. But this

would have placed an extra workload on the clinic staff

and difficult to monitor. To raise diagnosis of malaria to a

consistent standard, all microscopists received refresher

training at the start of the study. Their performance was

monitored monthly by taking samples of slides for

re-examination and quality control.

For entomological surveillance, 15 sentinel houses were

randomly selected from the enumeration list of each

village, and collections of mosquitoes were made once a

month by space-spray pyrethroid aerosol in a sleeping

room and animal shed of each house. Collections were

identified to species and scored. The same houses were

monitored throughout.

Statistical analysis

We grouped the villages according to intervention received:

(1) ITN from June 1995 onwards; (2) UTN from June 1995

AFGHANISTAN BY PROVINCE

PAKISTAN

Figure 1 Map of eastern Afghanistan andbednet trial area.




onwards; (3) ITN from June 1996 onwards, and (4) UTN

from 1996 onwards. We compared the odds of parasita-

emia in bednet users vs. non-users within these groups. For

the analysis of passive data, individuals presenting with

symptoms of malaria and a smear positive for malaria

parasites were classified as cases, distinguishing between

falciparum and vivax. Patients presenting with possible

symptoms of malaria at the same health centres during the

same period, but with a negative smear, were classified as

controls. We fitted logistic regression models adjusting for

the effect of age, sex, village and district, and estimated the

odds ratio (OR) of bednet use among cases compared with

controls.

With entomological data, the monthly totals of each

village were log transformed and analysed using Poisson

regression.

Results

Net sales and coverage

In total, 1680 households and 14 538 people from 12

villages were involved in the study. Population character-

istics of the four village groups are shown in Table 1.

Twelve per cent of families (209/1680) had bought

nets prior to the study. Within the six villages offered

nets in year 1, 56% (530/954) of families took up the

offer (range between villages 46%)83%) (Table 2). The

following year 108 families bought nets a second time,

but only 36 families were first time buyers, indicating a

rapid penetration and saturation of the households

willing or able to buy. Among the six villages offered

nets in year 2 for the first time, a similar proportion

took up the offer (54%, range 35%)72%). Seventy-one

per cent (95% CI: 61%)79%) of families that took up

the offer had purchased sufficient nets to cover their

entire family. Re-treatment rates among village groups

buying ITN were 64% (193/302) in year 2 and 47%

(154/329) in year 3, despite only a nominal charge being

levied (Table 2).

Cross-sectional surveys

The prevalence of malaria at admission in June 1995 is

shown in Table 1. The commoner species in mid summer

was P. vivax. Both species were more prevalent in the

10–14-year age group and less prevalent in adults. Malaria

was three to four times more prevalent in Behsud than in

Chaprahar, and approximately 1.5 times more prevalent in

village groups 2 and 3 than in groups 1 and 4. At the time

of the second survey, nets had been in use for 5 months in

village groups 1 and 2. In neither group was a significant

effect of nets observed against either species of malaria

(Table 3).

April 1995

Selection of 12villages from 2districts withinthe catchmentareas of 4clinics

May 1995

(1) Enumerationof households

(2) Training ofVHWs andmicroscopists

June 1995

(1) X-sectionalmalaria survey -1

(2) Randomizationof villages intofour study groups

June–July1995

November1995

X-sectionalmalariasurvey- 2 inall 12 studyvillages

June–July1996

Oct – Nov1996

Passivesurveillancecommences in 2villages ofBehsud andChaprahar

Group 1(1) Sale ofsubsidised nets(2)Treatment ofnets withinsecticide


Group 2(1) Sale ofsubsidised nets




June– July1996

X-sectionalmalariasurvey-3 inall 12 studyvillages

X-sectionalmalariasurvey-4 inall 12 studyvillages

Figure 2 Key activities flow chart.




At the time of the third survey, a significant effect of ITN

was becoming evident against P. vivax in group 1,

prevalence being almost threefold less among net users

than among non-users. The vivax cases presenting at this

time would have been transmitted in the previous summer–

autumn when nets were already in use. Within groups 3

and 4, where nets had been purchased only a week before,

there was no difference in P. vivax prevalence between

net-using and non-using groups. This was an important

finding because it indicated that within these villages there

appeared to be no inherent difference in malaria risk

between families that chose to buy nets and those that

chose not to. Hence any subsequent difference in malaria

prevalence arising between users and non-users in later

surveys would probably be an effect of net use rather than

unknown socioeconomic or behavioural factors.

At the time of the fourth survey, the prevalence of

P. falciparum was significantly less in net users than in non-

users in three of four groups, and even in the fourth

group the trend was in the same direction as the others.

Overall, there was a 59% reduction in the odds of

P. falciparum parasitaemia in net users compared with

non-users after adjusting for other predictors (OR 0.41,

95% CI 0.25–0.66). The OR for P. vivax in net users vs.

Table 2 Uptake of nets and re-treatment in the four village-intervention groups

IndicatorsGroup 1n (%)

Group 2n (%)

Group 3n (%)

Group 4n (%)

Number of families buying nets in 1995 302 (59%) 228 (52%) 0 0Number of nets sold in 1995 1339 806 0 0Average number of persons per net in net owning families in 1995 2.1 2.5 – –Number of families buying nets for the first time in 1996 25 (5%) 11 (2.5%) 255 (68%) 135 (39%)Number of nets sold in 1996 250 142 730 395Average number of persons per net in net owning families in 1996 2.0 2.2 2.9 2.5Number of families re-treating nets in 1996 193 (64%) – – –Number of nets re-treated in 1996 816 (61%) – – –Number of families re-treating nets in 1997 154 (47%) – 138 (54%) –Number of nets re-treated in 1997 388 (24%) – 326 (45%) –

Table 1 Baseline characteristics

Characteristics Group 1 Group 2 Group 3 Group 4

Number of villages 4 2 4 2Number of households 514 440 378 348Mean household/village (range) 128 (77–176) 110 (46–248) 189 (153–225) 174 (43–305)Total population 4852 3824 3158 2580Mean population/village (range) 1213 (644–1999) 956 (293–1486) 1579 (1288–1990) 1290 (313–2268)Mean household size 9.4 8.7 8.4 7.4

Age distribution (%)0–4 years 549 (21) 448 (22) 268 (21) 287 (21)5–9 years 623 (23) 504 (25) 360 (28) 363 (26)10–14 years 298 (11) 271 (13) 173 (13) 164 (12)14+ years 1197 (45) 817 (40) 497 (38) 576 (41)Mean age 18.3 17.3 16.9 17.3Male:Female ratio 46:54 48:52 50:50 47:53

Baseline parasite prevalenceSample size 2272 1728 1079 1286Positive for P. falciparum (%) 17 (0.7) 16 (0.8) 15 (1.2) 5 (0.4)Positive for P. vivax (%) 170 (6.9) 184 (9.5)* 128 (10.5)* 97 (7.0)

Group 1: Insecticide-treated nets (ITN) from June 1995 onwards.Group 2: Untreated nets (UTN) from June 1995 onwards.Group 3: ITN from June 1996 onwards.Group 4: UTN from June 1996 onwards.* Significantly different compared to group 1 (P < 0.01).




non-users in group 1 had increased from 0.29 to 0.50

during the fourth survey. A significant effect against P.

vivax was evident when groups 1 and 3, which had been

using ITN, were combined (OR 0.38, 95% CI 0.20–0.74),

but not in groups using UTN (Table 3).

Overall, the prevalence of P. vivax reduced from 4.4%

(52/1143) in the second survey to 2.6% (21/1313) in the

fourth survey among net users while it remained relatively

stable from 3.4% (61/1811) to 3.2% (78/2527) among

non-users. The prevalence of P. falciparum remained stable

from 1.9% (25/1143) to 2.2% (25/1313) among net users

while it increased from 3.8% (68/1811) to 4.7% (78/2527)

among non-users.

Passive surveillance

Figure 3 shows the relationship between the monthly

variation in bednet use, mean temperature, and mosquito

density during 1995 and 1996. During the winter months

net users comprised less than 5% of clinic attenders. Peak

attendance by users was in August 1996 (36.0%). Net use

rates correlated both with monthly changes in mosquito

abundance (r ¼ 0.78) and with ambient temperature

(r ¼ 0.87). Despite the hot, stuffy summer nights, net

owners were presumably making use of nets to protect

themselves against the greater discomfort caused by

mosquito biting.

The passive surveillance study confirmed that the

differences in the distribution of age and sex between net

users and non-users were negligible. Net use grew from

24% (1429/6023) in 1995 to 34% (1470/4300) in 1997.

The odds of malaria infection was greater for the 5–14-

year age groups than for the 0–4-year and >15-year age

groups, and greater for females than for males. The odds of

infection were lower for village group 1 that had used ITN

for 3 years, and was lower for year 3 than for years 2 and 1

(Table 4). There was a negative association between use of

bednets and malaria (OR 0.34 for P. falciparum and 0.89

for P. vivax). There was a significant protective effect of

nets against P. falciparum in all village groups except for

group 4 that had received UTN only in year 2 (Table 5).

A significant protective effect against P. vivax was only

apparent in the village group 1 that had used ITN since

1995.

Table 3 Cross-sectional study: comparison of parasitaemia between net users and non-users in the four village-intervention groups

Parasite negative inP. falciparum positives(% positive) in

P. vivax positives(% positive) in OR� of P. falciparum

in net users vs.non-users

OR� of P. vivaxin net users vs.non-usersIntervention groups Users Non-users Users Non-users Users Non-users

Survey 2Group 1 (ITN)� 707 499 12 1.7 14 (2.7) 29 (3.9) 22 (4.2) 0.59 (0.27–1.30) 0.95 (0.54–1.99)Group 2 (UTN)§ 207 261 5 (2.4) 8 (3.0) 13 (5.9) 10 (3.7) 0.78 (0.25–2.45) 1.64 (0.69–3.91)

Survey 3Group 1 (ITN)– 1147 366 1 (0.1) 1 (0.3) 17 (1.5) 16 (4.2) 0.34 (0.02–5.6) 0.29 (0.14–0.59)**Group 2 (UTN)�� 462 206 0 (0) 0 (0) 32 (6.5) 5 (2.4) – 2.79 (1.06–7.38)*Group 3 (ITN)�� 784 415 5 (0.6) 1 (0.2) 52 (6.2) 21 (4.8) 2.74 (0.30–60.1) 1.24 (0.74–2.13)Group 4 (UTN)§§ 206 308 1 (0.5) 0 (0) 6 (2.8) 9 (2.8) – 1.01 (0.35–2.90)

Survey 4Group 1 (ITN)–– 591 812 6 (1.0) 20 (2.4) 4 (0.7) 11 (1.3) 0.41 (0.17–1.00)* 0.50 (0.17–1.49)Group 2 (UTN)�� 143 422 4 (2.7) 19 (4.3) 5 (3.4) 10 (2.3) 0.65 (0.23–1.86) 1.54 (0.54–4.39)Group 3 (ITN)�� 366 757 10 (2.7) 42 (5.3) 7 (1.9) 36 (4.5) 0.49 (0.25–0.98)* 0.40 (0.18–0.89)*Group 4 (UTN)§§§ 172 352 0 (0) 18 (4.9) 5 (2.8) 8 (.2.2) 0.00 (0.00–0.44)** 1.27 (0.43–3.77)

� Odds ratios adjusted for the effect of age, sex and district.� Treated net was in use for 5 months.§ Untreated net was in use for 5 months.– Treated net was in use for 12 months.�� Untreated net was in use for 12 months.�� Treated net was in use for < 1 month.§§ Untreated net was in use for < 1 month.–– Treated net was in use for 17 months.�� Untreated net was in use for 17 months.�� Treated net was in use for 5 months.§§§ Untreated net was in use for 5 months.*P < 0.05; **P < 0.01.




Individual protective effectiveness [IPE ¼ (1 ) OR)%]

of ITN against P. falciparum infection from the cross-

sectional surveys and the passive surveillance case–control

study were 59% and 69%, respectively, and against

P. vivax 50% and 25%, respectively. Community

protective effect (CPE) is defined as the product of

Table 4 Case–control study based on passive surveillance at district clinics

Predictors ControlsCases P. falciparum(% positive)

Cases P. vivax(% positive) OR� P. falciparum OR� P. vivax

Age group0–4 4259 71 (1.6) 682 (14) 1.0 1.05–9 3400 159 (4.5) 812 (19) 2.7 (2.0–3.6)*** 1.6 (1.4–1.7)***10–14 2094 90 (4.1) 450 (18) 2.4 (1.8–3.4)*** 1.4 (1.2–1.6)***15+ 7963 233 (2.8) 1186 (13) 1.8 (1.4–2.4)** 1.0 (0.9–1.1)

SexMale 10351 273 (2.6) 1634 (14) 1.0 1.0Female 7429 280 (3.6) 1506 (17) 1.4 (1.2–1.7)*** 1.2 (1.1–1.3)

DistrictBehsud 13804 343 (2.4) 1614 (11) 1.0 1.0Chaprahar 3988 210 (5.0) 1526 (28) 0.49 (0.41–0.59)*** 0.33 (0.30–0.35)***

Village group1 12074 212 (1.7) 1507 (11) 1.0 1.02 3325 202 (5.8) 863 (21) 3.0 (2.5–3.7)*** 1.9 (1.7–2.0)***3 1094 93 (7.8) 304 (22) 4.2 (3.2–5.4)*** 2.0 (1.7–2.3)***4 1211 40 (3.2) 456 (27) 1.5 (1.0–2.1)* 2.6 (2.3–3.0)***

Period1995 4175 336 (7.4) 1519 (27) 1.0 1.01996 3869 150 (3.7) 751 (16) 0.67 (0.54–0.83)*** 0.69 (0.63–0.77)***1997 4293 28 (0.6) 241 (5) 0.10 (0.07–0.15)*** 0.18 (0.15–0.21)***

BednetNon-users 11263 479 (4.1) 2335 (17) 1.0 1.0Users 4537 55 (1.2) 723 (14) 0.34 (0.26–0.46)*** 0.89 (0.81–0.97)**

�All the predictors shown in the table were included in the logistic model.* P < 0.05; ** P < 0.01; *** P < 0.001.

40

35

30

25

20

15

10

5

0Jul Oct Jan Apr Jul Oct

1995–1996

% using nets Mosquito density (% of total caught) Mean temperature (˚C)Figure 3 Relationship between net usage,mosquito density and temperature.




IPE · net coverage (Lengeler & Snow 1996). Net coverage

estimates obtained from the cross-sectional survey and

passive surveillance were 57% and 34%, respectively.

Thus the CPE of ITN was 20.1% against P. falciparum and

17.0% against P. vivax from cross-sectional surveys and

23.5% against P. falciparum and 8.5% against P. vivax

from passive surveillance.

Entomology

Mosquitoes were more numerous in animal sheds than

in sleeping rooms (Table 6). Mosquitoes were 3.4 times

more abundant in animal sheds in 1996 than in 1995

(P < 0.001), but were not significantly more abundant in

sleeping rooms in 1996 than in 1995. There was no

significant effect on mosquito density of ITN over UTN or

of ITN over no-nets in sleeping rooms or animal sheds

in 1995. However, in 1996, there was a significant effect

of ITN over UTN in sleeping rooms (rate ratio 0.55,

95% CI: 0.33–0.92, P ¼ 0.03). This effect of ITN was not

apparent in animal rooms (P ¼ 0.45) and thus ITN did

not appear to reduce mosquito densities overall.

Discussion

Repeated cross-sectional surveys and case–control methods

based on passive surveillance demonstrated that bednets

were less protective against P. vivax than against

P. falciparum. An effect against P. vivax infection was not

evident in every cross-sectional survey, and may take a few

seasons to become apparent probably because of relapses

from earlier infections masking the effect. An effect of nets

against P. falciparum infection was more immediately

apparent. UTN conferred some protection against malaria,

and this conforms with recent evidence from Africa

(Abdulla et al. 2001; Armstrong-Schellenberg et al. 2001;

Clarke et al. 2001).

Cross-sectional surveys were a more expensive method

of monitoring. Passive surveillance is more efficient

because the only additional task is to ask questions about

net usage in addition to the routine clinical history. Thus,

passive surveillance would be preferable if the two methods

were able to give similar results.

There were two important differences between the two

study designs. Whereas cross-sectional surveys directly

assessed a representative sample of the target population,

passive surveillance monitored a more restricted source

population, i.e. one that had fever and which chose to seek

treatment at one of the clinics involved in the study.

Secondly, whereas passive surveillance measured sympto-

matic parasitaemia, cross-sectional surveys measured both

symptomatic and asymptomatic parasitaemia. Despite this,

the fact that the IPE of ITN derived from the final survey

and from the passive surveillance case–control study were

similar (59% and 69%, respectively) seems to indicate that

the clinic attender study population was representative of

the target population.

If there were any reason why net users should be more or

less prone to episodes of fever, not related to malaria, than

non-users, selection bias would be introduced. It is

conceivable that a family bednet used by several people

would provide a better environment for the spread of

infectious agents such as respiratory viruses. If this were so,

net users might experience more episodes of fever unrelated

to malaria, and this would lead to an overestimation of the

protective effect of bednets. To our knowledge this has

never been studied.

Table 5 Passive surveillance case–control study: effect of use of bednets on clinical malaria in the four village-intervention groups

Controls P. falciparum cases P. vivax casesOR� of net use inP. falciparum cases

OR� of net use inP. vivax casesIntervention groups Users Non-users Users Non-users Users Non-users

Group 1 (ITN)� 3467 6810 26 169 395 1042 0.31 (0.21–0.47)** 0.75 (0.66–0.85)**Group 2 (UTN)� 267 813 9 84 88 216 0.33 (0.16–0.67)* 1.22 (0.92–1.64)Group 3 (ITN)§ 661 2499 16 184 192 661 0.34 (0.21–0.58)** 1.11 (0.92–1.33)Group 4 (UTN)§ 127 1073 4 36 45 409 1.15 (0.40–3.31) 1.01 (0.70–1.45)

� Adjusted for the effect of age, sex, district and study period.� Most nets were in use for 30 months from July 1995 to December 1997.§ Nets were in use for 18 months from July 1996 to December 1997.*P < 0.01; **P < 0.001.

Table 6 Mosquito density per room: Anopheles stephensigeometric means (95% confidence interval)

Villagegroup

Bedroom Animal shed

1995 1996 1995 1996

1 0.6 (0.5–0.8) 0.8 (0.7–1.0) 1.3 (1.0–1.6) 4.5 (3.7–5.3)2 0.7 (0.5–1.0) 1.2 (0.9–1.5) 1.5 (1.1–2.0) 7.4 (6.0–9.1)3 0.6 (0.4–0.7) 0.6 (0.5–0.7) 1.5 (1.2–1.9) 4.3 (3.6–5.2)4 1.3 (0.9–1.6) 1.4 (1.0–1.8) 3.5 (2.7–4.6) 6.7 (5.0–8.9)




The study population was divided into cases and

controls purely on the basis of presence or absence of

malaria parasites. Any false positives or false negatives

from the tests would bias the interpretation of the

protective effect of bednets. If people were pre-treated with

chloroquine before attending the clinic for diagnosis, some

cases would be misclassified as controls. Selection bias

would be introduced if the rate of pre-treatment with

chloroquine was different between net users and non-users.

Webster et al. (unpublished) showed that people from

Behsud who used a bednet were less likely to pre-treat with

chloroquine before attending clinic for malaria tests

(OR ¼ 0.26, P < 0.001). This pattern of behaviour

underestimated the effectiveness of bednets.

The assessment of protective effect is liable to confound-

ing if potential predictors of malaria risk such as economic

status or access to education differ between net users and

non-users. Socioeconomic status was not assessed, and this

was a weakness in our study designs. Recent evidence shows

that buyers of nets in Afghanistan are economically better off

(Howard & Rowland, unpublished). Yet, a difference in

wealth does not necessarily mean that net buyers and non-

buyers will differ in their risk of contracting malaria. Parasite

rate among buyers was similar to that among non-buyers at

the time of buying. Yet, by the end of the year, prevalence

was significantly lower among those who had been using

ITN during the course of the year.

The use of ITN can, in regions where vectors are

anthropophilic (e.g. East Africa), reduce survival of vectors

which would be shown by a decreased sporozoite rate and

a decreased vector density (Magesa et al. 1991). This

should have a beneficial effect on non-users as well as on

ITN users (Curtis et al. 1998). In Afghanistan, where the

vectors are zoophilic, mosquito density did not appear to

be reduced by ITN, and sporozoite rates were too low to

show the possibility of an indirect protective effect on non-

users (Rowland et al. 2002). Had there been such a

reduction, the effectiveness of bednets would have been

underestimated using the case–control methodology.

The local vector species are capable of transmitting both

species of malaria parasites (Rowland et al. 2002). It may

therefore be assumed that nets were equally protective

against P. falciparum and P. vivax transmission. Because an

effect against P. falciparum is immediate, the effect may be

measured through either cross-sectional methods or passive

data collection using a case–control design. But until it is

possible to distinguish new infections from relapsed infec-

tions, neither the cross-sectional nor passive surveillance

methods are adequate to show the real effect on P. vivax.

The effect is only demonstrable as a trend over time.

As Behsud and Chaprahar are considered to be typical

of rural Afghanistan, the study indicates that social

marketing of ITN is a viable malaria control strategy for

the country. Under the present uncertain conditions, it is

more appropriate to help people to protect themselves

than to return to the pre-war, centralized programmes of

DDT spraying that are too easily disrupted by crisis. For

families that are unwilling or unable to buy nets, an

alternative strategy must be found. Achieving high

coverage seems more a question of affordability than of

desirability. In a recent study, 90% coverage was

achieved when the price was set at US$1 per net

(T. Freeman, unpublished). This suggests that a dual

marketing strategy may offer the best prospect: After the

first wave of sales has swept over rural districts, it

should be possible to target the most endemic foci with

highly subsidized nets. Alternatively, the second phase

might target the most at risk by offering a highly

subsidized net to anyone who is diagnosed with malaria

at a public clinic. After the defeat of the Taliban and the

promise of the West to help rebuild Afghanistan, what

better use of aid than to provide the inhabitants with a

form of protection against malaria they so clearly want.

With the rural population at risk amounting to just a

few million (Anon 1998), and with double nets costing

about US$4 each (even less with cost-recovery), the aim

seems eminently achievable with the resources promised.

Acknowledgements

We would like to express our appreciation of microscopy

trainers Fazle Rahim, Aminullah and Sakhi Jan, entomol-

ogists Hamid Rahman, Mushtaq Faran and M. Kamal, and

logistician Noorullah. Clive Davies kindly advised us on

the analysis of entomological data. HealthNet Interna-

tional’s malaria control and research programme is sup-

ported by the European Commission (DG1), the United

Nations High Commissioner for Refugees, and WHO/

UNDP/World Bank Special Programme for Research and

Training in Tropical Diseases (project no. 960662). M.R.

and D.C. are supported by the UK Department for

International Development and the Gates Foundation.

However, none of these donors can accept responsibility

for any information provided or views expressed.

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Prevention of malaria in Afghanistan through social marketing of insecticide-treated nets: evaluation of coverage and effectiveness by cross-sectional surveys and passive surveillance