Effects of Irrigated Rice Fields and Seasonality on Plasmodium Transmission in West Africa, Particularly in Central Côte d’Ivoire (Tropical Diseases Due to Protozoa and Helminths) Part 2

Effects of seasonality on Plasmodium Transmission

Tables 2 and 3 summarize the mean biting rate, infection rate and the entomological inoculation rate (EIR) of An. gambiae and An. funestus in the two study villages in 2002, 2003 and 2005.

Relationship between season and biting and infection rates

In Zatta, significantly higher An. gambiae s. s. biting rates were recorded in the dry seasons of 2002 and 2005 when irrigated rice farming was practiced, compared to the dry season of 2003 when irrigated rice farming was interrupted (LRT comparing 2002 with 2003: 13.79, LRT comparing 2005 with 2003: 20.50; both P <0.001). In 2003, there was no seasonal difference in the biting rate of An. gambiae s. s. (LRT = 0.13; P = 0.900) and An. funestus s. s. (LRT = 0.17, P = 0.879). In Tiémélékro, in 2002 (LRT = 1.84; P = 0.069) and 2005 (LRT = 0.56; P = 0.455), there were no significant differences in An. gambiae s. s. biting rates between the dry and the rainy season. In 2003, the biting rate was significantly higher in the long rainy season (LRT = 3.87, P <0.001). Regarding An. funestus s. s. biting rates, those recorded in the dry season of 2002 (LRT = 6.15) and 2003 (LRT = 4.50) were significantly higher than those recorded in the rainy season (both P <0.001). The difference in the biting rates between the dry and rainy season in 2005 also showed statistical significance (LRT = 3.26; P = 0.031).

Relationship between season and Plasmodium transmission

In both villages, higher EIRs of An. gambiae s. s. were usually recorded in the rainy season. For example, in Zatta, the EIR of An. gambiae s. s. recorded in the rainy seasons of 2002 and 2005 were 458 and 365 infective bites per person per season (ib/p/s), respectively. In 2003, when irrigated rice farming was interrupted in Zatta, P. falciparum transmission by An. gambiae s. s. and An. funestus s. s. only occurred during the rainy season. In Tiémélékro, in the rainy seasons of 2003 and 2005, the number of infective bites recorded for An. gambiae s. s. (357 and 208 ib/p/s, respectively) were 3-14 times higher than in the dry seasons (25 and 77 ib/p/ s in the respective years). In 2002, in contrast, the EIR of An. gambiae s. s. recorded in the dry season was 2.5 times higher than the one recorded in the rainy season.

The highest EIRs of An. funestus s. s. were usually noted during the dry season. In Tiémélékro, this species was the primary P. falciparum transmitter during the dry season of 2005 when 207 ib/p/s were recorded. With regard to infection rates, with the exception of the 2005 infection rate of An. funestus s. s. recorded in Tiémélékro (χ2 = 4.47, P = 0.035), no significant differences were observed between seasons, neither for An. gambiae s. s. nor for An. funestus s. s. in any village.

In brackets are the number of malaria vectors analyzed; LRT (likelihood ratio test)

^aIrrigated rice farming performed in a synchronized manner

^bInterruption of rice cultivation

^cIrrigated rice farming performed in a synchronized manner

Table 2. Monthly average biting rate, infection rate, parity rate and entomological inoculation rate (EIR) of An. gambiae and An. funestus during the dry season and the rainy season in 2002, 2003 and 2005 in Zatta, central Côte d’Ivoire

In brackets are the number of malaria vectors analyzed; LRT (likelihood ratio test) *Vegetable farming is performed intensively with 2 production cycles per year **Vegetable farming is performed intensively with 1 production cycle per year

Table 3. Monthly average biting rate, infection rate, parity rate and entomological inoculation rate (EIR) of An. gambiae and An. funestus during the dry season and the rainy season in 2002, 2003 and 2005 in Tiémélékro, central Côte d’Ivoire

Discussion

The interruption of irrigated rice farming due to a farmers’ dispute over land property rights, coupled with an unstable socio-political situation in the face of the 2002-2004 armed conflict (Betsi et al., 2006; Fürst et al., 2009) offered a unique opportunity to study the dynamics of malaria transmission. Our analyses complement previous publications (Girardin et al., 2004; Koudou et al., 2005, 2007, 2009), now with an explicit focus on the effect of seasonality on malaria transmission under changing agro-ecological conditions. The following points are offered for discussion.

Firstly, biting rates of An. gambiae in both villages were usually significantly higher in the rainy season than in the dry season. When irrigated rice farming was interrupted in Zatta in 2003, much lower biting rates were observed than in the preceding year and in 2005, but there were no seasonal differences. Hence, the interruption of irrigated rice farming appeared to have hidden the effect of season on An. gambiae biting rate. These findings are in agreement with previous investigations in the humid savannah of Côte d’Ivoire: in an area characterised by intensive agriculture, the biting rate of An. gambiae increased significantly a few weeks after the beginning of the rainy season, whereas it decreased and became lowest towards the end of the dry season (Doannio et al., 2006). Moreover, the blunting of seasonal differences in biting rates due to changing patterns in irrigated rice farming has been documented previously for the savannahs of Senegal (Faye et al., 1993) and Mali (Dolo et al., 2004). In contrast to An. gambiae with the highest biting rates usually observed in the rainy season, the highest biting rates of An. funestus were consistently recorded in the dry season regardless of the prevailing agricultural activity. Moreover, interruption of irrigated rice farming in Zatta showed no effect.

Secondly, with the only exception of a significantly higher infection rate of An. funesuts in Tiémélékro in the rainy season compared to te dry season of 2005, infection rates of both An. gambiae and An. funestus showed no clear seasonal patterns. Different results were reported from Dielmo, a holoendemic area in Senegal, where the infection rate of malaria vectors showed considerable seasonal variation (Fontenille et al., 1997). The observations made in Senegal corroborated previous findings obtained in the savannah area in the north of Côte d’Ivoire (Dossou-Yovo et al., 1995), and other findings documenting a high infection rate of An. funestus at the beginning of the dry season in an irrigated rice area compared to a non-irrigated rice farming area (Dossou-Yovo, 2000). It should be noted, however that the mean annual infection rate of An. gambiae in Zatta was significantly higher when irrigated rice farming was in place (in 2002 and 2005) compared to a year with interrupted irrigated rice farming (Koudou et al., 2005).

Thirdly, the influence of changing patterns of irrigated rice farming on the An. gambiae-specific EIR in Zatta has been discussed elsewhere (Koudou et al., 2005, 2007). In brief, interruption of irrigated rice farming resulted in several-fold lower EIRs compared to normal years. Here, we now document that seasonal patterns of transmission remained. Indeed, considerably higher EIRs were observed for An. gambiae in the rainy season compared to the dry season. Of note, the EIR of An. gambia in the dry season of 2003 in Zatta dropped to zero. In Tiémélékro, high EIRs were recorded throughout the study period for An. gambiae and, in general, EIRs were higher in the rainy season compared to the dry season. An. funestus seemed to play an important role in the transmission of malaria, particularly in the dry season. Our results therefore confirm previous observations made elsewhere in the northern savannah of Côte d’Ivoire (Dossou-Yovo, 2000) and in southern Cameroon (Bonnet et al., 2002). Whilst An. gambiae was the key P. falciparum transmitter mainly during the rainy season, An. funestus was the main vector species during the dry season. It is interesting to note that a previous study focusing on climatic models for suitable malaria transmission in Africa, based on monthly rainfall and temperature data, concluded that an average of 80 mm rainfall per month, for at least 3-5 months, is a minimum to ascertain stable malaria transmission (Craig et al., 1999). Usually, a rapid rise in the An. gambiae population at the beginning of the short rainy season was followed by an increase in the EIR (Bonnet et al., 2002).

With regard to An. funestus, the highest EIRs were usually observed during the dry season. Indeed, An. funestus is often abundant and has high EIR during dry season compared to the rainy season (Fontenille et al., 1997; Manga et al., 1997). An. funestus was identified as the main malaria vector in the Guinean climatic region, in East Africa and Madagascar (Robert et al., 1985; Severini et al., 1990). As shown in our study, despite the presence of irrigated rice field, there is a great variability in the annual EIR values and seasonality would seem to play a key role (Mabaso et al., 2007).

Finally, an important finding of our study is that in Zatta, where irrigated rice farming was interrupted in 2003/2004, Plasmodium prevalence rates and the number of presumptive malaria cases decreased. This observation is corroborated by a significant decrease in the EIR from 2002 to 2003 (Koudou et al., 2005) and a significant increase from 2003 to 2005 (Koudou et al., 2007). This study demonstrated also that irrigated rice cultivation is associated with elevated malaria prevalence rates, as well as high numbers of presumptive malaria cases, as seen in Burundi (Coosemans, 1985), Kenya (Githeko et al. , 1993) and Madagascar (Marrama et al., 1995). However, research carried out in Tanzania showed that irrigated rice farming was not associated with a higher risk of malaria. One important reason for this observation is that farmers engaged in irrigated rice have the opportunity to gain some extra money, part of which is spent for protective measures against malaria. A reduced risk of malaria despite enhanced rice production has been termed ‘paddies paradox’ (Ijumba & Lindsay, 2001).

Conclusion

In conclusion, analyses of our entomological data revealed that malaria transmission in two different agro-ecological settings of central Côte d’Ivoire is very high, but there are clear seasonal patterns. Whilst the interruption of irrigated rice farming in one of the two study villages resulted in a highly significant reduction in the EIR, seasonal patterns of transmission remained. Hence, even in intensive agriculture areas, the effect of season on malaria transmission must be taken into consideration for the design of integrated interventions and their monitoring.

Additionally, in Zatta, from 2002 to 2003, the highly significant reduction in the annual EIR was paralleled by a significant reduction in the Plasmodium prevalence rate, and the proportions of presumptive and clinically-confirmed malaria cases. Once irrigated rice farming was resumed, there was an increase in entomological and parasitological parameters of malaria. In Tiémélékro, despite the significant increase in the EIR from the year 2002 to 2005 (Koudou et al., 2005, 2007), malaria prevalence rates, and the presumptive and clinical malaria cases decreased. Hence, the reduction of malaria transmission in endemic areas does not necessary reduce the incidence of clinical malaria episodes (Charlwood et al., 1998), highlighting the complex relationship between these parameters.