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- Material and methods
Objectives To assess the impact of intensified malaria control interventions in an ethnic minority community in Betul using existing tools.
Methods Two rounds of indoor residual spraying with synthetic pyrethroid insecticide were applied and larvivorous fish introduced, followed by intensive surveillance for early detection of Plasmodium falciparum with rapid diagnostic tests and prompt treatment with sulphadoxine pyrimethamine.
Results Pre-intervention surveys revealed a very high fever rate in the community in all age groups with a slide positivity rate of >50% with >90%P. falciparum. The post-intervention phase showed a sharp steady decline in number of malaria cases (β 0.972; P < 0.0001, 95% CI 0.35–0.47). Monitoring of entomological results revealed a significant decline in both Anopheles species and An. culicifacies (P < 0.0001).
Conclusion A combination of indoor residual spraying and early detection and prompt treatment complemented by rapid diagnostic tests and larvivorous fishes successfully brought malaria under control. These approaches could be applied in other regions of different endemicity to control malaria in India.
Keywords malaria, tribal , Plasmodium falciparum, forest , Anopheles culicifacies, vector
Objectifs Evaluer l'impact d'interventions intensifiées du contrôle du paludisme dans une communauté ethnique minoritaire à Betul en utilisant les moyens existants.
Méthodes Deux séries de pulvérisations d'insecticide d'intérieur à base de pyréthrine synthétique ont été réalisées et des poissons larvovivores ont été introduits. Ceci a été suivi d'une surveillance intensive avec détection précoce de Plasmodium falciparum grâce à des tests de diagnostics rapides et traitement rapide par sulfadoxine-pyriméthamine.
Résultats Des études pré-interventionelles révélaient un taux élevé de fièvre dans la population tout âge confondu avec un taux de positivité des frottis supérieur à 50% dont plus de 90%àP. falciparum. La phase post-interventionelle montrait une chute nette et stable du nombre de cas de paludisme (β 0.972 ; P < 0.0001 ; IC 95% [0.35 ; 0.47]). Le monitorage des études entomologiques montrait une chute significative aussi bien parmi les Anophelesspp qu’An. culicifacies (P < 0,0001).
Conclusions La combinaison des pulvérisations d'insecticides d'intérieur à la détection précoce des cas et leur traitement rapide, associée à l'utilisation des tests de détection rapide et des poissons larvovivores, permet un bon contrôle du paludisme. Ces approches pourraient être appliquées dans d'autres régions d'endémicité différentes pour contrôler le paludisme en Inde.
Mots clefs paludisme , tribu , Plasmodium falciparum, forêt , Anophelesculicifacies, vecteur
Objetivos Evaluar el impacto de intensificadas intervenciones de control de la malaria en una comunidad de minoría étnica en Betul, utilizando herramientas existentes.
Métodos Se aplicaron dos rondas de pulverización residual interior con insecticida piretroide sintético, y se introdujo el pez larvívoro, seguido de una vigilancia intensiva para la detección prematura de Plasmodium falciparum con pruebas de diagnóstico rápido e inmediato tratamiento con sulfadoxina-pirimetamina.
Resultados Sondeos anteriores a la intervención revelaron una alta tasa de fiebre en la comunidad, en todos los grupos etarios, con una tasa deslizante de positividad de >50% con >90%P.falciparum. La fase posterior a la intervención mostró una pronunciada y permanente caída en el número de casos de malaria (β 0.972; P < 0.0001, 95% CI 0.35–0.47). El monitoreo de los resultados entomológicos revelaron una caída significativa en ambas especies Anofeles y An.culicifacies (P < 0.0001).
Conclusión Una combinación de pulverización residual interior y detección temprana e inmediato tratamiento, complementada por pruebas rápidas de diagnóstico e introducción de peces larvívoros consiguió controlar la malaria. Estas estrategias podrían ser aplicadas en otras regiones con diferentes índices de endemicidad para controlar la malaria en la India.
Palabras clave malaria , tribal , Plasmodium falciparum, selva , Anofeles culicifacies, vector
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- Material and methods
Despite 50 years of control efforts, malaria remains a major public health problem in central India. Large scale developmental activities in the tribal belt of Madhya Pradesh (MP) due to several multipurpose projects resulted in the movement of people from one area to another. This, coupled with nomadism practiced by tribal populations of the state, has posed a sizable problem (Singh et al. 2004a) as P. falciparum is on the increase in tribal districts of MP (Singh et al. 2003, 2004a,b). In Betul, a tribal district (pop. 1.4 m, 45% ethnic tribe) the reported annual incidence of malaria as per National Vector Borne Disease Control Programme (NVBDCP) has increased gradually from 0.43 in 1990 to 1.4 in 1995 to 11.37 per 1000 population in 2000 (Anon 2000). In Betul, the persistence of endemic foci coupled with the influx of migrants working on the Sukhtava hydro-electrical project site in Hosangabad 20 km from Betul, harbouring various strains of falciparum parasites, gave rise to a sharp increasing trend of malaria transmission. The malaria in Betul is not responsive to control measures by NVBDCP. The two powerful tools, i.e. indoor residual spraying (IRS) and chemotherapy, on which the programme relied, are no longer effective (Sharma 1996). IRS requires large amount of DDT for adequate coverage. Resistance to DDT is increasing and the risks of DDT on human health and the environment (Roberts et al. 2000) have resulted in a reduction in spraying with DDT and an increase in the use of chemotherapy using chloroquine (CQ). But resistance to CQ is also rising (Singh et al. 2003), indicating the need for change in control strategies and better intervention tools. On the request of Government of MP, we investigated the malaria situation and recommended specialized intervention approaches i.e. enhanced surveillance activities and intensified antivector intervention. The objective was to develop a programme to prevent and control malaria using existing tools.
A programme of malaria control was started in Betul in Jan 2001 in accordance with national guidelines on the recommendation of Malaria Research Centre (MRC) field station at Jabalpur, Indian Council of Medical Research (ICMR). The district malaria officer and his staff directed the local malaria intervention activities. Repeated cross-sectional surveys were undertaken by MRC throughout the 5 year period following the introduction of specialized intervention measures. This present paper reports the results of an assessment of the effectiveness of this combined intervention approach.
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- Material and methods
Age specific (10 and >10 years) and species specific parasite rates before and during the intervention period are presented in Table 2. In 2000, before the initiation of special intervention measures, the prevalence of malaria was very high even in infants (data not shown separately). Analysis revealed that significantly more malaria cases were recorded in children 10 years than in older age groups (β−0.286, SE 0.055, P < 0.0001, 95% CI 0.674–0.836). P. falciparum was accounting for more than 90% of the infection in both the age groups. P. falciparum gametocytes were detected in both age groups. Post-intervention results revealed that there was a highly significant reduction in malaria cases after initiation of intervention (P < 0.0001). The estimated malaria parasitaemic cases decrease in log odds for each year (β−0.972, SE 0.037, P < 0.0001, 95% CI 0.352–0.407). From 2002 onward, parasitaemia was not detected among infants. The prevalence of gametocytes of P. falciparum was relatively higher in the post-intervention phase (2001–2002) and the differences in the prevalence of gametocyte carriage before and after the intervention was significant (χ2 = 12.33, P < 0.0005). However, only one gametocyte was recorded between 2003 and 2005.
Table 2. Age wise malaria situation in study villages of district Betul before intervention and after intervention (2000–2005)
|10 years||>10 years|
| BSE*||Positive/ P.falciparum†|| SPR‡|| PfG%§||BSE||Positive/ P.falciparum||SPR|| PfG%|
The data collected on the distribution of malaria cases by species of parasite and season are summarized in Table 3. In 2000, the overall parasite prevalence among subjects screened during the autumn was 51%, when 93% of infection were caused by P. falciparum and 7% by P. vivax. In 2001 among the subjects screened during the dry hot season, the malaria prevalence was 20% of which only 43% were P. falciparum. In autumn and monsoon the overall malaria prevalences were 20 and 28.7% respectively, of which 85.5% and 79% respectively were P. falciparum. These results indicated that malaria infection due to P. falciparum was more common in autumn than the dry hot and monsoon season (χ2 = 353, df 2, P < 0.0001) and P. vivax is the dominant infection during summer (χ2 = 398, df 2, P < 0.0001). Only gametocytes of P. falciparum were seen in all the seasons however significantly more gametocytes were seen in summer (χ2 = 10.76, df 2, P < 0.005).
Table 3. Malaria cases in study villages of district Betul (2000–2005), by season
|Year & Season||BSE*||+ve†||P. vivax||P. falciparum||PfG‡||SPR§||Pf%¶|
The spleen rate was >70% before intervention (Table 4), with AES indices around 1.92. After initiation of intervention measures the spleen rate dropped steadily to 4% in 2005 [χ2 (for trend) = 1495.34, P < 0.00001]. Similarly, the number of malaria infections in enlarged spleen cases declined steadily from 64% in 2000 to 4% in 2005 [χ2 (for trend) = 223.41, P < 0.00001].
Table 4. Results of spleen examination in children (2–9 years) in study villages in Betul (2000–2005)
|Month||Children examined||Enlarged spleen||Spleen rate (%)||Odd ratio|| AES*|| BSE†|| Pv|| Pf|| Mix‡|| SPR§||Odd ratio|
| Autumn 2000||696||504||72||1.00||1.92||504||23||295||5||64.09||1.00|
| Summer 2001||399||230||58||0.52||2.08||230||35||53||2||39.13||0.61|
| Autumn 2002||945||237||25||0.13||1.72||237||28||50||5||35.02||0.55|
| Summer 2003||1107||133||12||0.05||1.65||133||3||9||0||9.02||0.14|
| Autumn 2004||1533||94||6||0.02||1.08||94||1||3||0||4.26||0.07|
| Summer 2005||680||28||4||0.02||1.8||28||0||1||0||3.57||0.06|
Monitoring of entomological data during pre-intervention phase revealed that seven species were prevalent in indoor resting collection (Mean MHD 21.23 ± 8.01), of which An. culicifacies was the most dominant species (16.77 ± 7.02). The other species found in small numbers were An. subpictus, An. annularis, An. fluviatilis, An. vagus, An. splendidus and An. theobaldi. Out of seven, only An. culicifacies and An. fluviatilis are vectors. After initiation of intervention measures, both Anopheles and An. culicifacies (Table 5) mean density declined significantly (4.17 ± 3.09 and 3.31 ± 2.82 respectively) when compared with pre-intervention period (P < 0.0001), though the number fluctuate between the surveys depending on the availability of breeding sites and climatic conditions therefore the data was transformed by log x+1.
Table 5. Indoor resting density (MHD) of total Anopheles species and Anopheles culicifacies in study villages before intervention and after intervention in Betul (2000–2005)
|Month||Anopheles (mean ± SD)||An. culicifacies (mean ± SD)|
| Oct 2000||32.17 ± 4.5||25.83 ± 2.02|
| Dec 2000||17.12 ± 3.9||13.38 ± 4.57|
| Mar 2001||10.6 ± 1.8||4.3 ± 1.2|
| May 2001*||0.5 ± 0.9||0.3 ± 0.45|
| Jun 2001||9.14 ± 9.7||5.27 ± 6.9|
| Sep 2001||11.1 ± 3.7||9.4 ± 3.1|
| Dec 2001||2.0 ± 3.4||2.0 ± 3.4|
| Apr 2002||2.5 ± 2.5||2.07 ± 2.1|
| Jul 2002||11.5 ± 3.3||10.5 ± 3.1|
| Oct 2002||13.8 ± 8.25||11.7 ± 6.29|
| Mar 2003||0.0||0.0|
| Sep 2003||18.0 ± 11.8||12.0 ± 6.56|
| May 2004||0.0||0.0|
| Dec 2004||0.0||0.0|
| May 2005||0.17 ± 0.29||0.0|
Fish of the Gambusia sp. were introduced into several An. culicifacies breeding sites in 2001 (1 280 000), 2002 (1 534 000), 2003 (1 777 000), 2004 (1 677 000) and 2005 (817 200) by the NVBDCP. For the past 5 years we have monitored these sites at least once a year and confirmed that the fish have become established. Insecticide susceptibility tests showed that mortality of An. culicifacies to DDT was 10% and to malathion 41.8%. One hundred percent mortality was recorded with Deltamethrin. Consequently, this synthetic pyrethroid was chosen for indoor residual spray in place of DDT.
Further investigations revealed that while compliance with SP was very good, with CQ some villagers complained that the tablets per dose were too many [10 tablets for an adult (1500 mg) for 3 days and six tablets (45 mg) PQ for single dose]. In response to these complaints, blister packs were introduced by the NVBDCP in the year 2003–2005, consisting of only three tablets of CQ for 3 days and one tablet of PQ (adult dose). This change was well received by both the health staff and the community.
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- Material and methods
In 2000, Betul is accounted for 10% of all malaria cases in MP, although it harbored less than 1% of the state population (Anon 2000). Between 1990 and 2000, the population of Betul increased by 28%; the number of reported malaria cases as per NVBDCP rose by >3000% and corresponding figures for P. falciparum rose to >7000% with 27 deaths (Anon 2000). The PHC system was weak and supply of antimalarial drugs and DDT for IRS was irregular. Malaria transmission is intense due to An. culicifacies and An. fluviatilis complex occurring in extensive areas of Betul, as in other parts of MP (Subbarao et al. 1992; Singh et al. 1999, 2004b) However, precise data on the sporozoite rate were not available. To estimate accurately how many die from malaria per year is difficult to achieve. Most deaths from malaria occur at home; hence malaria deaths are grossly underestimated (Greenwood et al. 2005). During October–November 2000, the district hospital was visited by hundreds of people more than its capacity. Drug stocks became depleted. In-patient capacity was quickly exceeded as trained staff became strained and supplies low. The quality of care decreased and case reporting became a lower priority, often resulting in an underestimation of the true situation.
From 2001 an array of different control strategies have been applied, ranging from treatment to reduction of transmission and reduction of vector density. Their effect on the number of new malaria cases was carefully monitored. Both active surveillance and spleen examination demonstrated a sharply diminishing trend from 2001 to 2005. The EDPT is important to prevent development of severe malaria and death and has the additional advantage of checking the spread of transmission (Hung Le et al. 2002; Singh et al. 2004a). It is unlikely that we missed many persons with malaria parasites during cross-sectional surveys. People attended because of the medical care available and because otherwise the nearest health facility would be at least 10–25 km away. Private medical care is non-existent. Further, the transmission of malaria parasites from human to mosquitoes depend on the availability of mature infectious gametocytes in the peripheral blood (Akim et al. 2000). Gametocyte carriage can be used as an estimate of transmission potential of malaria parasite from human to mosquitoes. The almost complete absence of P. falciparum gametocyte in 2003, 2004 and 2005 was most likely the result of intensive intervention measures. This is further supported by the data collected by the Ministry of Health in MP. The records revealed that malaria incidence declined from 11.37 per thousand in 2000 to 0.22 per thousand in 2005 (Anon 2005).
From 2001 to 2003, SP was used but its use gradually reduced as P. falciparum was no longer considered a serious problem. The efficacy of SP has been demonstrated in many endemic areas in the world especially in Africa (Bloland et al. 1993). However, resistance to SP has occurred in most countries where the drug has been introduced to replace CQ (EANMAT 2003). SP has been very effective in most part of India and some form of combination treatment is now clearly needed to extend its effectiveness. Combination therapy with drugs with different modes of action is now the preferred approach to malaria treatment to inhibit the emergence and spread of parasites resistant to one component of the combination (White & Olliaro 1996; Greenwood et al. 2005). The combination of amodiaquine and SP will be efficacious and feasible for the programme, but will remain so only if these drugs are not used for monotherapy (Dorsay et al. 2002).
Antivector intervention was mainly focused on IRS as this is a more efficient method to reduce the number of infectious mosquitoes as well as to reduce the longevity of those that might otherwise become infectious as the goal of IRS was to decrease transmission. However, the stage at which spraying with pyrethroid could have omitted and the further control left to surveillance and treatment of those found parasitaemic is not clear. Since the start of this study it has become very clear that spray reduce the number of vectors in the houses very efficiently. However, over the long-term recurrent IRS campaigns are an expensive preventive strategy because costs do not decrease with time. If the IRS with pyrethroid insecticide continue for many years, it is likely that the protective efficacy declines. Fish can decrease the abundance of An. culicifacies by feeding on the aquatic larval stages in identified breeding places (Ghosh et al. 2005). Because of the presence of unidentified numerous breeding sites and the incompleteness of predation in small pools and pits, the consideration of larvivorous fish in malaria control is probably marginal as recorded earlier in Mandla (Singh et al. 1989) and worldwide in a variety of settings (Polevoy 1973; Kaneko et al. 2000; WHO 2003). Yet, the introduction of larvivorous fish is a safe and inexpensive malaria control option (Kolaczinski et al. 2005) that can be easily done in defined breeding sites (Sharma & Ghosh 1989). Further investigations are necessary to clarify the epidemiological effectiveness of Gambusia spp. in different ecological settings.
Although the interventions have jointly contributed to the control of malaria, it is hard to quantify which is the most efficient tool and similarly, hard to presume which should be given priority for resource allocation. EDPT is important to prevent severe and potentially fatal malaria (Kilama et al. 1994). However, it is not easy to simultaneously cover a large population with EDPT and proper surveillance for a sufficient period of time. IRS with pyrethroid insecticide have shown benefits but logistics, high costs and the need of recurrent spraying are disadvantages. The efficacy of this combined approach is demonstrated in Betul but question about costs, sustainability and possible increases in disease and mortality after withdrawal of specialized intervention measure remain to be seen. A number of previous control operation in MP have failed in the long-term because of incomplete interruption and subsequent reintroduction of malaria have resulted in severe malaria outbreaks with increased morbidity and mortality due to reduced immunity of the population (Hung Le et al. 2002; Singh et al. 2003). In Betul also in the remaining four PHCs the diagnosis and treatment were less regulated by the state health authorities because of resource crunch.
In conclusion, we can find no reference to compare our results of malaria control. The lack of published documentation about what has been tried, what has worked and what has failed leaves a significant gap in our knowledge of malaria control. It is not known whether the combination of IRS and EDPT can be replicated under programme conditions in other parts of MP as human migration to and from the endemic foci in the forested regions remains a challenge for malaria control and a permanent pressure on resources put for adequate malaria control (Hung Le et al. 2002).