anopheline vectors and malaria transmission in eastern afghanistan

TRANSACTIONS OF THE ROYAL SOCIETY OF TROPICAL MEDICINE AND HYGIENE (2002) 96,620-626

Anopheline vectors and malaria transmission in eastern Afghanistan

Mark Rowland”‘, Nasir Mohammed’, Hameed Rehman’, Sean Hewitt’, Chandana Mendis’, Mushtaq Ahmad’, Mohammed Kamal’ and Robert Wirtz3 ‘HealthNet International, Peshawar, Pakistan; ‘London School of Hygiene and Tropical Medicine, London WClE 7HT, UK; 3Centers for Disease Control, Atlanta, Georgia, USA

Abstract Anopheline vectors and malaria transmission were studied in 2 river-irrigated, rice-growing districts of eastern Afghanistan from May 1995 to December 1996. Clinical malaria was monitored in 12 rural villages (population 14 538) by passive case detection at local clinics. Adult mosquitoes were collected by space-spraying of living quarters and stables and by cattle bait catches. Mosquito head-thoraces (17 255 specimens) were tested for Plasmodium falciparum and l? vivax circumsporozoite protein (CSP) using enzyme-linked immunosorbent assay. The recorded incidence of l? vivax and I? falciparum was 199 and 41 episodes per 1000 person years, respectively. Twelve species of anopheline were recorded; Anopheles stephensi comprised 82% and A. culicifacies 5%. Eight species tested positive for CSP: A. stephensi, A. culicifacies, A. jluviatilus, A. annularis, A. pulcherrimus, A, maculatus, A. splendidus and A. superpictus. Among infected mosquitoes 46% were positive for P. falciparum, 45% for l? vivax VK-247, and 9% for l? vivax W-2 10. Estimates of the feeding rates of infective vectors on humans indicated that A. stephensi would contribute 76% of infective bites, A. fzuviatilis and A. pulchetimus 7% each, and A. culicifacies and A. superpictus 3% each. The overall infective vector feeding rate correlated with the P. vivax incidence rate in the human population. The conventional view of A. culicifacies being the main rural vector and A. stephensi important only in urban settings needs to be reconsidered in western outreaches of the Indo- Pakistan subcontinent.

Keywords: malaria, mosquitoes, Anopheles stephensi, Anopheles culicijacies, Afghanistan

Introduction The advent of enzyme-linked immunosorbent assay

(ELISA) for detection of sporozoites has transformed the incrimination of vector species in areas of low- moderate malaria transmission (WIRTZ et al., 1987). New species have been implicated and established vectors better understood (BEIER et al., 1990; AMER- ASINGHE et aZ., 1992, 1999; RUBIO-PALIS et al., 1992). In Sri Lanka, for example, the predominance of Ano- pheles culicifacies in transmission has been confirmed, and species once deemed unimportant such as A. subpictus and A. vagus are now implicated (AMERASINGHE et al., 1999). A. culicifacies has a wide geographic distribution from the Persian Gulf to northern southeast Asia, and overlaps with another important vector, A. stephensi, over much of this range (ZAHAR, 1990). It is often asserted that A. culicifacies is the main vector in rural areas whereas A. stephensi is more important in urban or peri-urban settings (REISEN & BOREHAM, 1982; RAO, 1984; MAHMOOD & MACDONALD, 1985; SUBBARAO, et al., 1987).

Traditionally malaria has always been an important problem in Afghanistan (DHIR & RAHIM, 1957). Of the 18 species of anopheline recorded, the principal vectors are purported to be A. superpictus, A. culicifacies, A. hyrcanus, and A. pulcherrimus, all of which have yielded sporozoi;e-posit&e specimens from Afghanistan in the nast (RAo. 1951: IYENGAR, 1954; DHIR & RAHIM, i957j. Changes in environmental 0; demographic facl tars, or in operational control programmes, may have spedies-specific effects which alter-the relative impor- tance of different vectors. This has hannened twice in Afghanistan’s recent past: the first d&g the malaria eradication era, the second during the war with the Soviet Union and its chronic aftermath. When the national programme of malaria eradication based on indoor spraying with DDT expanded coverage in the 1950s the initial results were impressive and previously uninhabitable areas in the north were able to open up for agricultural and industrial exploitation (WHIR 8r RAHIM, 1957). But by 1970 a change in the vector situation had become apparent: the original (at least

Address for correspondence: Dr M. Rowland, Disease Control and Vector Biology Unit, London School of Hygiene and Tropical Medicine, Keppel Street, London WClE 7HT, UK; phone +44 (0)207 927 2333 fax +44 (0)207 580 9075, e-mail [email protected]

putative) main vector, A. superpictus, was virtually eli- minated in the north, and replaced bv the exophagic and exophilic A. hyrcanus a&l A. pulcherrimus, -wh&h were able to maintain transmission desnite DDT snrav- ing (ONORI et al., 1975). A. stephensi and A. culicifaci& the predominant species in the east and south, devel- oped resistance to DDT (CULLEN, 1978; ESHGHY & NUSHIN, 1978a); where necessary a change was made to malathion, with good results (ESHGHY & NUSHIN, 197813). In problematic rice-growing areas in the north, where indoor spraying proved relatively ineffective against the exophilic species, the larvivorous fish, Gam- busia, was deployed in rice fields with alleged success (POLEVOY, 1973; ONORI et al., 1975).

After 1980, the war in Afghanistan led to a progressive breakdown of malaria control activities; eastern rural areas were depleted of population, villages partially destroyed, and irrigation systems damaged. De- struction of the health infrastructure and population displacement resulted in an upsurge of malaria in the region (KAZMI & PANDIT, 2001; ROWLAND et al., 2002a, 2002b). During the last decade - despite con- tinuing political instability - the eastern and southern parts of the country have become safe enough for many refugees to return home. Changes in demography, land quality, and water supply are suspected of affecting mosquito abundance and human-vector contact. As part of the assessment of the malaria problem, the vectors and malaria transmission rates were investi- gated in eastern Afghanistan.

Methods Study area

The study took place from May 1995 to December 1996 in the rural districts of Behsud and Chanrahar, near Jalalabad city, Nangahar province, eastern*Afghal nistan. Twelve villages participated, 6 from each dis- trict. War in the east came to an end in 1992. BY the time the study commenced many refugees had returned from Pakistan, rebuilt their mud and timber houses, and repaired the irrigation systems. Families sleep outdoors during the hot summer nights, moving indoors from mid-October. The main crops are wheat in Feb- ruary-May, rice in June-November, vegetables, and opium poppy. The main sources of mosquito breeding are in and around river-irrigated rice fields. Rivers are snow and rain fed. The weak monsoon rains reach Nangarhar in July. Malaria is seasonal, and local

ANOPHELINE VECTORS AND MALARIA TRANSMISSION 6’21

outbreaks with mortality sometimes occur in areas deficient in health services. Chloroquine-resistant Plas- modiumfalciparum is widespread (RAB et al., 2001), and is partly responsible for the upsurge of I? falciparum in the region (SHAH et al., 1997).

In the absence of stable government, international and local non-governmental organizations (NGOs) have taken responsibility for providing basic health care through clinics and urban hospitals. A return to indoor residual spraying is unfeasible under prevailing conditions. Instead, an insecticide-treated net (ITN) social marketing programme, run by HealthNet International (HNI) and a network of local NGOs, has operated in eastern Afghanistan since 1993. ITN coverage in Beh- sud and Chaprahar in 1996 stood at 34% of the population (ROWLAND et al., 2002b).

Malaria and demographic surveillance Behsud and Chaprahar are each served by 2 NGOi

MoH clinics. Microscopy was performed on out- patients with fever or suspected malaria. Cases positive for l? vivax or P. falciparum malaria were treated with chloroquine (25 mgikg bodyweight). Microsco- pists were given refresher training by HNI at the start of the study to raise skills to a high standard. Patient records included name and village, age, and gender. Technical performance (quality control) was monitored each month by re-examining random samples of slides and smears.

Demographic surveillance was carried out in June 1995. All houses in the 12 study villages around the clinics were census surveyed. There were,1688 houses and 14 538 people present.

Mosquito collections and testing Fifteen houses were randomly selected from the

census list of each village for entomological surveillance. Mosquito collections were made once a month by space-spraying a living room and stable room of each house with a non-persistent pyrethroid. The same houses were monitored throughout. Outdoor cattle- bait collections were made the following night.

All anophelines were identified to species and pro- cessed for ELISA. To minimize the risk of false positives caused by contamination with cattle blood, specimens were dried and head-thoraces separated from abdomens (SOMBOON et al., 1993). Head- thoraces of known species, collection site, and date were tested in batches-of 10 for the presence of circum- snorozoite nrotein of P. vivax (210 and 247 variants) and l? .falc~pamm. Batches of laboratory-reared, unin- fected 2. stephensi served as negative- controls. The ELISA reagents were sunnlied bv the Walter Reed Army InstitGte for Medical -Research, Washington DC, USA. Procedures were the same as those described by WIRTZ et al. (1987), with minor modifications. Absor- bance was measured at 414 nm with an ELISA mate

A

reader 30 min after the addition of peroxidase. A test well was considered positive if it gave a visible green colour with ABTS substrate and an absorbance reading at least 3 times greater than the outer 95% confidence interval of the mean of the 5 negative controls. All positive samples were retested to confirm the result.

Results Malaria

2756 cases of malaria were recorded at the 4 clinics over the study period. I? vivax accounted for 83% and I? falciparum for 17% of malaria infections. Transmis- sion occurred mainly from June to late November, and coincided with the growing of rice (the main mosquito breeding site) and pooling at the margins of rivers or ditches. Incidence of P. vivax reached a peak in August and l? faZciparum in October-November (Fig. 1 A). Cases presenting between December 1995 and spring 1996 were due to recrudescent P falciparum infections

(presumably chloroquine-resistant) or to delayed or relapsed infections of P. vivax transmitted during the 1995 season. The incidence rate of I? vivax was 199 per 1000 person years; that of P. falciparum was 41 per 1000 person years. Incidence rate in 1996 was half that of 1995 (rate ratio: 0.49 for l? vivax and 0.47 for P. falciparum) .

Mosquitoes Anophelines were more numerous than culicines:

23 614 anophelines and 4527 culicines were caught during space spraying collections over the 19-month study period. A. stephensi was the most abundant anopheline by far, comprising 82% of all anophelines caught. A. culicijacies comprised only 5.0%, A. fl;*viatilus 4.3%. A. salendidus 2.6%. and A. &cherrinzus 1.7%. with A. subiictus, A. annul&, A. suierpictus, A. turkhul di, and A. maculatus present in small numbers (Fig. 2). A. stephensi and A. pulchetimus were most abundant during July-August, A. supevictus during August-Sep- tember, A. culicifacies and A. .fluviatilus during Septem- ber-October, and A. subpictus somewhat -later. A. steDhensi and A. culicifacies were more abundant in 1996 than in 1995, whereas culicines and A. jluviatilus were less abundant in 1996 than in 1995 (Table 1). Almost 85% of the anophelines and 74% of the culicines collected resting indoors were from domestic animal sheds - the preference for animal shelters held for all species of anopheles (Table 1). Outdoor collections from animal bait yielded one extra species - A. hyrcanus - a species that rests exclusively outdoors (Table 1). A. pulchewimus, a partially exophilic species, was more dominant in outdoor than indoor collections. While all species were partially zoophilic, some were clearly more endophilic than others.

Vector competence and transmission 17255 specimens, 58% of the total collected, were

tested for presence of circumsporozoite protein (CSP). The collections made between June and August 1995 were not tested due to homogenates deteriorating during a prolonged power failure. Overall, 26 specimens tested positive for P. falciparum, 25 specimens tested uositive for P. vivax variant 210. and 5 tested nositive for I? vivax variant 247 (Table 2). Eight of-the 11 species of anopheline tested positive for CSP, and 5 species tested positive for both P. vivax and l? falcipar- urn CSP. No species showed a CSP rate greater than l%, with the possible exception of A. maculatzks, which yielded 1 positive specimen from a small sample:

The trend in CSP rate with time is shown in Fin. 1 B. Specimens of A. stephensi positive for P. vivax and I? falciparum were found during every month from June to November. Positives among other species were too few to discern any trend.

CSP rates were highest in sleeping room collections, intermediate in animal shelter collections, and lowest in animal landing collections (Table 3). Because infected mosquitoes must have contracted their infections sev- eral days earlier the trend is perhaps explained by a higher proportion of the sleeping room collection hav- ing fed on humans on previous occasions and to a higher proportion of the cattle landing collection being comprised of newly-emerged mosquitoes that had not fed before.

The number of infective bites per person per night or entomological inoculation rate (EIR) is usually esti- mated from the product of human landing rate and sporozoite rate. Human landing catches were impracti- cal in the political and social conditions existing in Afghanistan, and thus a direct measure of the number of bites per human per night could not be obtained. An indirect estimate of human landing rate, based on the size of the resting mosquito population and the proportion feeding on humans (human blood index), also could not be obtained because no facility for blood

622 MARK ROWLAND ETAL.

40

8 35 2 8 30

; 25 8 20 a 2 15

- 10

5

0 7 8 9 10 11 12 1 2 3 4 5 6 7 8 9 10 11 12

Month 1995-96

B 1.0, , 6000

0.8 5000

2 0.7 4000 - 0.6

; z

2 0.5 3000 E ; 0.4

9 0.3 2000 -z z

0.2 1000 0.1 0.0 0

9 10 11 12 1 2 3 4 5 6 7 8 9 10 11

Month 1995-96

C 0.014

10’11’12’1’2’3’4 5’6’7 8 Month 1995-96

vivax falciparum

Fig. 1. Study data from the districts of Behsud and Chaprahar, eastern Afghanistan, from May 1995 to December 1996. (A) Incidence of malaria. (B) Monthly circumsporozoite protein (CSP) positivity rates among all anophelines. (C) Predicted number of infective bites per person (advanced by 1 month for PZasmodium vivax and by 2 months for P. falciparum). This predicts the incidence in the human population (on the assumption that clinical/parasitological symptoms occur 1 month after P. &ax and 2 months after I? falcipamm infection).

meal testing was available. However, it may be assumed number of persons per household. The gonotrophic that the proportion feeding on humans is similar to the period y was assumed to be 2 d for every species, and proportion of the overall resting catch found in human sleeping rooms (Table 1). An approximation to EIR

the mean number of persons per household $ was 7.5

might then be calculated for each species from the according to the census. CSP, p and q varied according to individual species. IVFR for each species is shown in

Infective Vector Feeding Rate (IVFR) = (CSP) p q/y 4

formula: Table 4, and indicates that A. steahensi would contribute 76% of infective bite!, ,A. flu&t&s and A. pulcherrimus 7% each, and A. culzcafacies and A. superpictus 3%

Where CSP is the species-specific CSP rate, p is the each. mean abundance of each species per house per night, q The monthly trend in IVFR is shown in Fig. 1 C. is the proportion resting in sleeping rooms, y is the This Figure also serves as a prediction of the trend in period of the gonotrophic cycle, and $ is the mean incidence in the human population advanced by 1 or 2

ANOPHELINE VECTORS AND MALARIA TRANSMISSION 623

6 7 8 9 10 11 12 1 2 3 4 5 6 7 8 9 10 11 :

q A. stephensi q other anophelines culicines

Month 1995-96

e! r=' 2.5

8

6 7 8 9 10 11 12 1 2 3 4 5 6 7 8 9 10 11 12

Month 1995-96

Fig. 2. Mosquito density per house in the districts of (A) Behsud and (B) Chaprahar, eastern Afghanistan from May 1995 to December 1996.

months (assuming the interval between parasite inoculation and clinical presentation in humans takes this length of time). Comparing predicted incidence from IVFR (Fig. 1 C) with actual incidence based on clinic data (Fig. 1 A), the correlation was significant for P. &ax (r = 0.63, P < 0.05) but non-significant for l? fulcipamm, infections of which occurred later than predicted.

Discussion Afghanistan is associated with much of the region’s

malaria problem. Both l? v&x and I? fdciparum are transmitted, though the transmission season is short, being restricted to June-November. Before the war, the number of recorded infections per year varied between 40 000 and 80000 (API 2.5-5 per 1000) of

which only about 1% were I? falciparum (DJELANTIK, 1975). After 1980 the progressive breakdown in health services and malaria control activities led to epidemics breaking out in eastern and northern areas; data be- came less reliable or less readily available (DELFINI, 1987; ZAHAR, 1990). Changes in demography altered the pattern of disease. Depopulation of fertile river valleys and increased population density in towns tended to reduce the incidence of malaria whereas the breakdown of irrigation systems increased the number of breeding sites and outbreaks (SCHAPIRA & ROZEN- DAAL, 1990).

With the improvement in security in the east of the country during the 199Os, NGOs were able to support or substitute for government health services. Clinics were established in Behsud and Chaprahar. With the

624 MARK ROWLAND ETAL.

Table 1. Mosquito abundance in eastern Afghanistan, from May 1995 to December 1996

Species

Anophelines Culicines A. superpictus A. fluviatilus A. culicifacies A. srephensi A. subpictus A. maculatus

A. splendidus A. turkhudi A. annular-i> A. pulchetimus A. hyrcanus

Annual abundance” Distribution within housesb Exophagy and endophily’

Ratio Living Ratio Cattle landing Stable resting Ratio 1995 1996 1996:1995 room Stable LR:S catch N (%) catch N (%) SRC:CLC

41.6 60.7 1.P 10.3 56.7 0.18 2743 (23) 9358 (77) 3.4 8.2 5.5 0.7’ 1.6 4.4 0.36 348 (27) 956 (73) 2.7 2.1 2.5 1.2 0.2 0.8 0.22 9 (3) 268 (97) 29.8 5.5 3.4 0.6’ 0.7 2.9 0.23 21 (8) 236 (92) 11.2 4.6 7.3 1.6f 1.0 3%.i . 0.22 65 (10) 579 (90) 8.9

24.4 41.6 1.7’ 6.9 0.21 1480 (17) 7261 (83) 4-9 1.8 2.3 1.3’ 0.2 ;:7 0.30 30 (22) 105 (78) 3.5 ;:: 1.4 A:; 0.0 0.27 6 (23) 20 (77) 3.3

2.1 0.2 0.9 0.19 141 (23) 477 (77) 2.0 1.8 0.9 0.1 0.5 0.10 24 (42) 77 (76) ;:; 1.7 1.8 1.1 0.1 0.3 0.21 56 (42) 77 (58) 1.4 1.8 2.1 1.2 0.2 o-4 0.39 336 (57) 258 (43) O-8

- - - - 575 (100) 0 (0) 0.0

“Annual abundance, geometric mean number of mosquitoes in 1995 and 1996 (per 10 houses). bDistribution within houses, geometric mean number of mosquitoes in animal shelters and living quarters (per 10 houses). ‘Exophagy and endophily, comparison of the total mosquitoes caught biting cattle outdoors and number resting in the animal stable the day before. dP < O-05. ‘P-c 0.01. fP< 0.001.

Table 2. Species of anopheline and number testing positive for circumsporozoite protein in eastern Afghanistan, from May 1995 to December 1996

Species

Number positive Percentage positive Number

tested I? vivax 2 10 I? vivax 247 l? falciparmm CSP rate l? vivax l? falciparum

A. maculatus A. pulcherrimus A. superpictus A. annularis A. jluviatilus A. stephensi A. culicifacies A. splendidus A. hyrcanus A. subpictus A. turkhudi

29 663 277 172 802

12 705 996 618 575 233 185

1 2

1 2

17 1 1 -

T - 3 3.45 0.90

1 1 0.72 -

19 2

0.58

3 0.50 0.31 - 1 0.20 - - 0.16 - - -

-

Total 17255 25 5 26 0.32

3.45 0.45 oi5 0.36 0.36 0.58 0.25 oi5 0.16 0.15 0.10 0.10 0.16 -

- - - - - -

0.17 0.15

CSP, circumsporozoite protein.

Table 3. Circumsporozoite protein rates in different collection sites in eastern Afghanistan, from May 1995 to December 1996

Stable room Living (sleeping) room Cattle landing catch outdoors

Number tested

9027 2539 2743

Percentage positive (no. positive)

Z? vivax 210 l? vivax 247 l? falciparum Total

0.17 (15) 0.03 (3) 0.13 (12) 0.39 (10) z’;; i:g . 0.07 (2) 0.22 (6)

Annual Parasite Index in Behsud and Chaprahar stand- ing at 240 per 1000 in 1995-96, the malaria problem in these districts had clearly become much more serious during the war. However the situation may not have been any worse than the one existing before the malaria eradication era. Cross-sectional surveys in Behsud in 1952, before the onset of the DDT campaigns, indicated a parasite prevalence of 95% (DHIR & RAHIM, 1957); this was very similar to survey results (10.3%) in July 1995 (ROWLAND et al., 2002b). During the war years the frequency of P. falciparum infections (17%) relative to l? vivax infections had certainly increased, and this was probably due to the spread of chloroquine resistant parasites and the limited availability of alter-

native antimalarials (DELFINI, 1989; ROWLAND et aZ., 1997; RAB et al., 200 1). Deficient clinical services, drug shortages, and drug resistance, are the 3 factors regu- larly associated with malaria outbreaks in remote areas of Afghanistan (HNI, unpublished surveys).

The anopheline fauna does not appear to have chan- ged much over the years. A. stephensi had become more abundant; but with the exception of A. d’thali, all 12 species recorded in our surveys were reported from Nangarhar in the past (RAo, 1951; DHIR & RAHIM, 1957). The status of A. stephensi as a rural vector is controversial. It is important in urban or peri-urban areas of India, Pakistan and Iran, but in rural areas A. culicifacies is considered more significant (RAo, 1984;

ANOPHELINE VECTORS AND MALARIA TRANSMISSION 625

Table 4. Estimates of infective vector feeding rates derived from mosqui- to densities, relative abundance in living rooms, and sporozoite rates in eastern Afghanistan, from May 1995 to December 1996

Species

A. stephensi A. pulchenimus A. jluviatilus A. culicifacies A. superpictus A. maculatus A. splendidus A. annularis A. subpictus A. turkhudi

Total

Infective vector feeding rate Percentage Bites per per person per year contribution person to overall number

per year l? vivax P. falciparum of infective bites

52.8 0.083 1 0.0789 75.6 1.7 0.0079 0.0079 7.4 2.9 0.0073 0.0073 6.8 3.4 0.0034 0.0034 3.2 1.1 0.0033 0.0033 3.1

0.1 0.004 1 0~0000 1.5 0.0025 0~0000 ;:: 0.4 0.002 1 0~0000

;:; 0~0000 0~0000 ;:; 0~0000 0~0000 0.0

65.0 0.1136 0.1008 100

MAHMOOD & MCDONALD, 1985; SUBBARAO et al., 1987). The situation is confused by the existence of 2 forms of A. stephensi - type and rnysorensis (SWEET & RAo, 1937; RAo, 1984; SUBBARAO et al., 1987). Type form is not found in rural situations whereas mysorensis occurs in both urban and rural situations and is purported to be less significant as a vector. SUBBA~~O et al. (1987) considered the 2 forms to be ecological variants and could find no barriers to mating in-the laboratory (the distinction between forms is based on egg morphology). It is not known whether A. stephensi in eastern rural Afghanistan is type, mysorensis or a mixture of both. With vector status of rural A. stephensi confirmed, the subject deserves further study.

Other species now implicated as vectors in Afghani- stan include A. maculatus, A. annular+ A. jluviatilus, and A. splendidus. A. jluviatilis is a known vector in Iran and India in mountain foothills (ZAHAR, 1990). A. annularis is a secondary vector in South Asia; in Sri Lanka, as here, it yielded l? vivax-CSP-positive specimens (AMERASINGHE et al., 1999). A. subpictus, a ditch breeder, also tested CSP-positive in Sri Lanka (AMER- ASINGHE et al., 1992, 1999), but our small collection tested negative. A. pulchetimus and A. superpictus tended to show higher rates of infection than other species and this accords with previous rankings of vector status (E&o, 1951; IYENGAR, 1954; DHIR & F&HIM, 1957).

The infective vector feeding rate - our proxy for entomological inoculation rate - was a useful way to compare the transmission potential of different species. It correlated quite closely with the trend in l? vivax incidence. This was surprising considering the assump- tions and limitations of the method: IVFR makes no allowance for the proportion of mosquitoes that may rest away from human habitations, and assumes the ratio of indoor resting between living quarters and animal shelters corresponds with the human blood index. Some admixing of human-fed and animal-fed mosquitoes would inevitably take place between feeding outdoors and resting indoors. Nevertheless the distribution ratio between human and animal quarters did anmox- imate to human blood indices determined previously in Afghanistan and Pakistan (DHIR & RAHIM. 1957: RE- ISE?N & BOREHAM, 1982; &HMOOD & i~&~btiiE, 1985) and a relationship between the 2 indices would be expected. The association between IVFR and incidence patterns suggests that the CSP rates determined here are close to the true sporozoite rates, and that the species testing positive are indeed the local vectors.

The malaria control strategy in Afghanistan is based increasingly on social marketing of ITNs nets (ROW- LAND et al., 2002b). Encouraging self-reliance seems a

sensible approach at a time when the new government is only gradually beginning to assert itself and factional fighting remains a possibility. ITNs distributed in the 2 entomological survey areas protected against malaria transmitted by the main species of vector described here. It is expected that in any country of the region where these species predominate, ITN should prove effective.

Acknowledgements HealthNet International’s malaria control and research pro-

gramme is supported by the European Commission (DGl), the United Nations High Commissioner for Refugees, and WHOiUNDPKUorld Bank Special Programme for Research and Training in Tropical Diseases. M. R. is 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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Received 15 March 2002; revised 18 April 2002; accepted for publication 29 April 2002

anopheline vectors and malaria transmission in eastern afghanistan

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