New irrigation methods sustain malaria control in Sichuan Province, China

Acta Tropica 89 (2004) 241–247

New irrigation methods sustain malaria control in Sichuan Province, China Liu Qunhua a , Kang Xin b , Chao Changzhi a , Feng Shengzheng c , Li Yan a , He Rongzhi d , Zhang Zhihua d , G. Gibson e,∗ , Kang Wenmin a a

e

Sichuan Center for Disease Control and Prevention, Chengdu, Sichuan Province 610041, China b Revenue Bureau for Jinjiang District, Chengdu, Sichuan Province 610016, China c Chengdu Center for Disease Control and Prevention, Wenjiang, Sichuan Province 610030, China d Sichuan Institute of Water Conservancy, Chengdu, Sichuan Province 610071, China Plant, Animal and Human Health Group, Natural Resources Institute, University of Greenwich, Chatham Maritime, Kent ME4 4TB, UK

Abstract Malaria appears to have been all but eradicated from certain areas of Sichuan Province mainly as a consequence of draining a sufficient proportion of rice paddy fields. The two main malaria vectors, both members of the Anopheles hyrcanus group, breed prolifically in rice paddy fields, which farmers have traditionally kept flooded all year round to ensure an adequate water supply. Over the last three decades, the irrigation network has been gradually extended, thus ensuring water security and increasing the area of arable land that could be farmed by intermittent wet/dry irrigation (IWDI). In addition, rice fields that had been left flooded but fallow throughout the winter are now under an annual cycle of wet crop/dry crop rotation (WDCR) to maximise productivity. Accordingly, vector breeding has been greatly reduced. It would appear that vector populations have now fallen below the level required to sustain malaria transmission. © 2003 Elsevier B.V. All rights reserved. Keywords: Malaria control; Irrigation; Agriculture; Anopheles anthropophagous; Anopheles sinensis; Anopheles hyrcanus; Sichuan Province; China

1. Introduction Prior to the mid-1960s, malaria in Sichuan Province was a major public health problem, with the fourth highest level of morbidity in the country. Community participation programmes were established in the 1950s and 1960s, based on an integrated malaria control approach, including case detection and treatment, ∗ Corresponding author. Tel.: +44-1634-883457; fax: +44-1634-883379. E-mail address: [email protected] (G. Gibson).

parasitological surveillance after local outbreaks and vector control by indoor-spraying with residual insecticides (IRS). The severity of epidemics was successfully reduced and incidence rates were stabilised at 10–20 cases/10 000 people. Vector control improved dramatically in 1986 with the introduction of insecticide-treated bed nets (ITN), which eventually covered 2.45 million people in Sichuan by 1993 and malaria dropped to consistently <5 cases/10 000 people. ITN is significantly more popular in the community and more cost-effective than IRS (Cheng et al., 1995; Curtis et al., 1991). This programme

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represented the largest-scale field trial of ITN in the world at the time. Since then more than 10 million people in China are protected by ITN. The success of ITN in China has been acknowledged worldwide and was certainly instrumental in encouraging the WHO and other national and international malaria control agencies to adopt it. ITN is now one of the main instruments of the Roll Back Malaria Campaign in sub-Sahara Africa. In spite of the overall success of ITN, however, malaria transmission continued in Sichuan, albeit at a relatively low level and local epidemics continued to be a problem. The limits to the efficacy of ITN gradually became clear. 1. There is no lasting impact on the density of malaria vectors, so that nets have to be treated indefinitely at regular intervals and at an adequate dose, which requires a significant commitment of financial and operational resources. 2. One of the main vector species (Anopheles sinensis Wiedemann) is less susceptible to house-based control measures, which means that malaria control programmes need to maintain the capability of managing local malaria outbreaks by other measures. Furthermore, for a variety of reasons, including changes in the availability and cost of insecticides, community-wide treatment of bed nets with insecticides was suspended in Sichuan in 1993, although people continue to sleep under bed nets and retreat them with insecticides on an individual basis. 1.1. Malaria vectors The two most important vectors in Sichuan, Anopheles anthropophagous Xu and Feng and A. sinensis, are both members of the Anopheles hyrcanus (Pallas) group (Cheng et al., 1995; Ramsdale, 2001). Although A. sinensis is the most common and widely distributed anopheline mosquito in China, A. anthropophagous is the more efficient vector, due to its close association with humans. It is more anthropophilic (human biting), endophagic (feeds primarily indoors) and endophilic (prefers to rest indoors after feeding), which also means it is more susceptible to IRS and ITN (Curtis et al., 1991; Lu, 1994). On the other hand, A. sinensis obtains only 10% of bloodmeals from humans, and the rest from domestic animals, such

as cattle and pigs. Although its vectorial efficiency is accordingly much lower than A. anthropophagous, large populations are responsible for maintaining a low level of endemicity in the plains of China and it is the main or sole vector north of 34◦ N. Vectorial efficiency is enhanced during the hottest periods because people often sleep outdoors near their fields, unprotected by bed nets. Local outbreaks of malaria can be sustained by A. sinensis during such periods, especially if the other entomological parameters favouring transmission are also present (e.g., a high sporozoite rate and an aging mosquito population). In common with other species of the A. hyrcanus group, both vectors breed well in marshes, swamps, ponds and ditches, and proliferate in flooded paddy fields. Their breeding habitats are so similar, that their distributions usually overlap, although A. anthropophagous populations are generally more patchy and do not extend as far north (Cheng et al., 1995; Ramsdale, 2001). 1.2. Impact of irrigation on agriculture and malaria Over the last two decades China has established extensive new irrigation schemes to control the availability and conservation of water, as a part of the central government’s ‘West China Development Policy’. International agencies such as the World Bank have provided substantial financial and managerial assistance, which was initiated in part by China’s entry into the global market and new membership of the World Trade Organisation (October 2001). The availability of water, not arable land, is the main limit to agricultural productivity in China generally. The plains of Chengdu in the centre of Sichuan Province are fertile, but historically prone to devastating floods from the watershed of the mountain ranges to the west. Indeed, one of the world’s oldest working irrigation systems was begun in 256 b.c., at the western edge of Sichuan Province, at the mouth of the Minjiang River. The Dujiangyan Dam has been declared a World Heritage Site by UNESCO, and demonstrates the high level of experimental science and engineering skill of the early Chinese. Over the centuries, this water system has been gradually expanded until it is now the largest irrigation system in China, and provides water to 40 counties and 8 cities over an area of 667 000 ha, with an increase of 580 000 ha since 1950. Examples of several

L. Qunhua et al. / Acta Tropica 89 (2004) 241–247

other water supply schemes developed over the last two decades include the Yuxihe System (36 000 ha), the Sheng Zhong Reservoir (92 000 ha) and the Wudu Water System (133 000 ha). These four developments alone account for 1 million ha of increased irrigated fields in the last 50 years, out of the current total irrigated area in Sichuan of 2.3 million ha (Department of Administration of Yuxihe River Irrigation Area, personal communication). Traditionally, farmers in Sichuan kept their fields permanently flooded to ensure an adequate water supply for the spring rice crop. Water security was seen to outweigh the costs of reduced yields caused by continuous flooding. Although the benefits of ‘intermittent wet/dry irrigation’ (IWDI) to rice productivity and mosquito control has been known in China since the 1970s (Lu, 1988; van der Hoek et al., 2001), it has only gradually been introduced in Sichuan, as permitted by the availability of irrigation water. The climate of Sichuan is too cold for a second crop of rice, so flooded rice fields were kept fallow throughout the winter, thus imposing an additional, even more extreme limit on agricultural productivity. The term ‘flooded paddy-fields’ will be used throughout this paper to refer to this system of keeping water in the fields permanently throughout the year to ensure water security.

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The new irrigation systems mentioned above, however, have gradually increased the area of arable land served by a dependable source of water, and accordingly, there has been a marked reduction in the area of flooded paddy fields. Wherever possible, farmers now utilise IWDI, draining their fields intermittently during the rice-growing season, to produce optimal yields of rice and to conserve water. A second, ‘dry crop’, such as wheat or vegetables is grown in the winter, in principle at least doubling annual productivity. This new farming system, based on a ‘wet’ spring crop with IWDI, followed by a ‘dry’ winter crop is called ‘wet/dry crop rotation’ (WDCR). As the area under irrigation has spread, so progressively the area of continuously flooded paddy field in Sichuan Province has been reduced by more than 50% over a period of 14 years: from 967 000 ha (1983) to 400 000 ha (1997). Under WDCR, rice paddies are now flooded only intermittently, for a maximum of 98 days between the end of May and the end of August, as required by local conditions. Fig. 1 shows how the area of flooded paddy in Jiangyou County has continued to decline since 1960. For this county, approximately 10% of the original area is still flooded in the winter. For Sichuan Province as a whole, out of a total of 4.4 million ha of arable land, more than 80% of the 2.3 million ha of irrigated land now uses WDCR.

10

18

9

16

Malaria Incidence

8

14 Flooded paddy area 12

6 10 5 8 4 start ITN

3

6

stop ITN

4

2

2

1 0 1950

0 1960

1970

Year

1980

1990

2000

Fig. 1. Relation between malaria incidence and area of flooded paddy fields Jiangyou County, Sichuan Province.

Flooded paddy (100 ha)

Malaria case (sqrt 1/10,000)

7

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These changes in agricultural practice were not intentionally part of a malaria control campaign, so unfortunately no data were gathered at the time with the aim of measuring the impact on malaria. Over the last decade, however, routine entomological and parasitological monitoring have revealed strong correlations between mosquito densities, malaria incidence and the proportion of paddy fields that were flooded. The data provided here demonstrate some of the correlations between these parameters. Some areas of the province have not yet been irrigated, which provides an ideal opportunity to undertake a suitably designed survey to produce a more definitive test of a causal link. The evidence presented here was first published by Gao et al. (2000) in Chinese. The aim of this paper is to make the information in the original publication more accessible to the English readership, and therefore includes more background information about agricultural developments in China than the original.

2. Materials and methods 2.1. Malaria in Sichuan Sichuan Province lies between the latitudes 28◦ N–33◦ N. The climate is temperate, with an annual rainfall in the lowlands of 1000–1200 mm. The most prevalent parasite is Plasmodium vivax, and most transmission occurs May and October when temperatures are optimal for vector breeding and parasite development (Kang Wenmin, personal communication). As detailed in Table 1, malaria transmission during the three main phases of malaria control can

IRS 1950–1986 ITN 1987–1993 WDCR 1994–present

1. 1950–1986: Mainly drug treatment with an increasing use of IRS; fewer epidemics than previously and incidence rates gradually reduced to 20 cases/10 000 people. 2. 1987–1993: ITN implemented; incidence stabilised and reduced to <5 cases/10 000 people. 3. 1994–present: WDCR; incidence reduced to <1 case/10 000 people, with 0 cases in many areas for more than three consecutive years, in spite of the reduction in the ITN programme. 2.2. Malaria incidence and mosquito densities Data from several sites were chosen to represent the main types of agricultural practice. Malaria incidence data came from the records of the Hygiene and Disease Control Stations of Chengdu City, Xindu County, Ebian County and Sichuan Province. For at least the last three decades, malaria mosquito populations have been monitored periodically in several areas, both within and outside the newly irrigated system. Adult mosquitoes were collected once or twice per month from 50 bed nets and one cowshed during the five main breeding months (May to August). For the house collections, occupants were provided with bed nets that were slightly raised, so mosquitoes could enter, but not leave easily. In the morning, field assistants collected all mosquitoes from the bed nets and as many as possible were collected inside each cowshed during a 30 min sampling period.

3. Results Trends in malaria incidence and the results of mosquito surveys at selected localities are summarized below.

Table 1 Malaria incidence in Sichuan Province Year

be characterised as follows.

Mean annual number of cases

Malaria incidence (1/10 000)

198825

7.40–87.49

28998

1.04–4.26

3692

0.07–0.88

IRS: indoor residual spraying; ITN: insecticide treated nets; WDCR: wet/dry crop rotation (see text).

3.1. Jiangyou County The centre of the county is 150 km NNE of Chengdu (the largest city in the province) and is irrigated by the Wu Du System (see above). Approximately 85% of the rice-fields are now under WDCR and there have been no recorded cases of malaria since 1993 (Fig. 1).

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Table 2 WDCR implementation and malaria incidence Region

Ricefield area (ha)

Ricefields using WDCR (%)

Malaria cases

Malaria incidence 1/10 000

Taixin Town, Xindu District Wolong Town, Qionglai County Ebian County, Whole County

1210 1146 1006

99.7 93.4 52

0 4 239

0 0.5 3.4

Data taken from within named counties.

3.2. Wolong Town, Qionglai County

3.3. Taixin Town, Xindu District

A village 70 km SW of Chengdu City. It is supplied with water from the Yuxihe System (see above). More than 90% of the rice-fields had changed to WDCR by the end of the 1990s, and malaria incidence fell to 0.5 cases/10 000 people (Table 2). Table 3 shows a comparison of the mean malaria vector densities before and after WDCR. The mean number of mosquitoes (A. sinensis as well as A. anthropophagous) was reduced by more than 90% from 1982 to 1999, in spite of the fact that IRS and ITN had not been used for the previous 6 years. Table 4 shows that in 1999 malaria mosquito densities in Wolong were also consistently lower than in a ‘control’ area (Shuangten, see below), where WDRC had not yet been implemented.

A village 10 km NE of Chengdu City. More than 99% of the rice-field areas are under WDCR and there have been no reported cases of malaria in recent years (Table 2). Malaria vector mosquito densities, too, have decreased as measured nearby, in Shibantan Town (Table 3).

Table 3 Density of A. sinensis and A. anthropophagous before and after WDCR, in two areas >1000 ha (mosquitoes per net per night, n = 50) A. sinensis 1982

1982

1999

Wolong Town, Qionglai County May 1.88 0.31 June 3.86 0.04 July 2.58 0.02 August 1.48 0.01

1.18 0.72 0.29 0.68

0.24 0.02 0.02 0.02

0.06

0.65

0.05

Shibantan Town, Xindu District May 0 0 June 1.04 0.12 July 0.16 0 August 0.36 0 September 0.36 0

0 0.26 0.18 0.36 0.04

0 0 0 0 0

0.17

0

Mean

2.53

0.38

A village 10 km NE of Chengdu City, near Taixin Town (Table 2). Mosquito samples were collected in 1982, when there were 337 000 ha of flooded paddy field in the winter, and in 2002, when the area of flooded paddy had been reduced to 36 000 ha (Table 3). The mean indoor catch of vector mosquitoes was reduced, accordingly. Table 3 shows that virtually no adult mosquitoes were caught in 2002, although few mosquitoes have been caught there since 1992. 3.5. Ebian County

A. anthropophagous 1999

Mean

3.4. Shibantan Town, Xindu District

0.02

A small county in the hills 250 km SSW of Chengdu, where only 50% of the fields use WDCR and the rest remain flooded. Malaria incidence is still relatively high (Table 2). 3.6. Shuangten Town, Junlian County A village 300 km south of Chengdu City, in the foothills near Junlian City, on the border with Yunnan Province. Irrigation farming has not been extended to this area yet. There was no significant change in vector densities between 1982 and 1999 and vector densities in houses and cow sheds remained consistently higher than in Wolong Town (Table 4).

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L. Qunhua et al. / Acta Tropica 89 (2004) 241–247

Table 4 Density of A. sinensis and A. anthropophagous in houses and cow sheds in areas without (Shuangten) and with (Wolong) WDCR, 1999 (mean no. mosquitoes per net per night or mosquitoes per shed per hour, see text) A. sinensis

A. anthropophagous

Shuangten

Wolong

Houses May June July August

0.67 0.33 0.06 0.04

0.22 0.03 0.01 0.01

Mean

0.28

0.06

Cow sheds May June July August

218 400 108 60

66 69 30 30

Mean

196

49

Difference (%)

79

75

4. Discussion Clearly, malaria has been gradually declining over the last few decades in Sichuan Province. Many initiatives have contributed to this decline, especially the control of vectors through IRS/ITN and the treatment of cases. The virtual eradication of malaria in some areas, however, appears to be due to the elimination of a critical proportion of breeding sites with the implementation of IWDI and WDCR. Although the main aims of the new farming system were to increase food production and to conserve water, drier fields are associated with less malaria and lower mosquito populations. Fig. 1 shows a strong correlation between the reduction in area of flooded paddy fields and a decrease in the incidence of malaria transmission in Jiangyou County, which mirrors data for the province as a whole. There have been no cases reported in Jiangyou County since 1993, when the area of flooded paddy field was reduced to 10% of the original area. Malaria transmission continued until the breeding area was finally reduced below a critical threshold level of about 200 out of 20 000 ha. Whereas, control of adult vectors imposes a temporary reduction in vector populations (e.g., by IRS or ITN) and densities recover quickly if there are sufficient breeding sites, WDCR imposes a sustained reduction in the breeding of potential of vectors. In

Shuangten

Wolong

0.39 0.16 0.00 0.01

0.18 0.02 0.02 0.01

0.14

0.05

54 90 30 8

18 6 6 5

45

9

Difference (%)

64

81

Pujiang County, for example, ITN was suspended, and within 2 years the density of vectors and malaria incidence was already increasing. ITN was initiated in Daxing Township, Pujiang County in 1987. The year before, the number of malaria cases was 182 per year and the mean density of A. anthropophagus was 14.5 mosquitoes per net per night during the main breeding season. By 1989 the number of malaria cases dropped to 3 per year and the mean mosquito density was 0.2 mosquitoes per net per night. The bed net treatment programme was suspended in 1990, and by 1991 malaria cases were 19 per year, with a mean mosquito density of 7.9 mosquitoes per net per night. Where WDCR has been implemented on the other hand, the gradual reduction of breeding sites has apparently reduced the reproductive rate of vector populations to such a degree, that even without adult control, mosquito populations do not return to previous levels. It is likely, however, that mosquito populations would quickly recover should farmers revert to continuously flooded paddy fields. There is a real threat that water resources could become over-stretched in China without adequate resource management, and farmers could revert to traditional methods if there were water shortages in the irrigation network. Therefore, it is crucial that policy makers and land use planners be made aware of the correlation between water security and malaria control.

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As malaria has declined, the human population has become healthier and agricultural productivity has increased. The expansion of the irrigation system and the implementation of WDCR has further contributed to an increase in crop productivity and, therefore, the wealth of the farming community as a whole. The annual income of farmers in Sichuan Province has increased by more that 60%, from 1158 yuan/farmer in 1995 to 1915 yuan/farmer in 2000 (Wenmin, personal communication). These are precisely the interactions that can secure a sustainable reduction in malaria. With increased wealth, people can better afford anti-malaria measures and curative treatment when necessary (Ijumba and Lindsay, 2001). Sustainable agriculture based on WDCR has fundamentally changed the epidemiology of malaria in Sichuan, virtually without cost to the established malaria control programmes. These changes may have implications for similar areas in the temperate/sub-tropical zone of Eurasia, wherever malaria vectors thrive in flooded fields. In southeastern Turkey, for example, there have been several epidemics in recent years, associated with new irrigation schemes where there are still endemic foci of malaria and fieldworkers frequently sleep outdoors near the fields in the hot malaria season (Ramsdale, 2001). The intermittent drying of fields and wet/dry crop rotation could have a significant impact on malaria transmission here and elsewhere.

Acknowledgements We thank the following people and organisations. For providing relevant data: Li Hua, Sichuan Bureau of Agriculture; Liu Yongqing, Sichuan Bureau of Farming Land Water Conservancy; Dr. Miao Lingping, Office of Endemic Disease Control, Jiangyou County; Dr. Yu Junhong, Sichuan Center for Disease Control and Prevention, and the Bureau of Dujiangyan Water Conservancy and Irrigation Management, the Department of Yuxihe Water Conservancy Management, the Bureau of Wudu Diversion Work Management and the Sichuan Bureau of Water Conservancy. For technical guidance on rice culture, pest control and medical entomology: Zheng Jiaguo, Sichuan Academy of

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Agriculture; Peng Yufang, West China University of Medical Sciences and Song Jinzhang, Chengdu Military Area. For participating in field investigations; Dr. Li Huageng, Dongfeng Village, Shibantan Town, Xindu District, Chengdu City. This publication is an output from a research project partly funded by the United Kingdom Department for International Development (DFID) for the benefit of developing countries. The views expressed are not necessarily those of DFID. DFID project code ZV0148, an Advisory Support Services Contract.

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