Acta Tropica, 52(1992)149 153 c~('~ 1992 Elsevier Science Publishers B.V. All rights reserved 0001-706X/92/$05.00

149

ACTROP 00246

Non-involvement of nulliparous females in the transmission of bancroftian filariasis K.D. Ramaiah and P.K. Das Vector Control Research Centre (Indian Council ~/' Medical Research), lndira Nagar, Medical Complex, Pondieher O' 605 006, India (Received 19 June 1992; accepted 31 August 1992)

The possible involvement of nulliparous females of Culex qu&queJasciatus in the transmission of bancroftian filariasis under field conditions was examined in Pondicherry, South India. Biting nulliparous females that had previously ingested partial blood meals were found infected with microfilariae/Ll stage larvae. None of them harboured infective-stage larvae. These findings suggest that nulliparous females are not involved in the transmission of filariasis. Therefore, their inclusion for estimating the transmission parameters is questionable. However, nulliparous females should also be dissected in order to determine the vector infection rates accurately. Infective larvae were encountered in females of all other age groups. Key words: Culex quinqu~/~tseiatus; Wuchereria haner~/~i; Transmission; Nulliparous females

Introduction

For the transmission of lymphatic filariasis caused by Wuchereria bancrofti, a vector mosquito must take at least two blood meals in order to ingest microfilariae and then transmit the infective stage larvae. In gonotrophically concordant mosquitoes, a full blood meal sustains vitellogenesis and the oogenesis and subsequent deposition of eggs is indicated by dilatation of the pedicel of the ovariole (Detinova, 1962). Partial blood meals may not be adequate to support the process of vitellogenesis (Woke et al., 1956) because of the inadequacy of the blood meals, which may result from the defensive behaviour of the vertebrate host (Edman et al., 1972; Klowden and Lea, 1978, 1979). Thus, although presence of a dilatation is evidence to show that a mosquito has fed at least once and completed a gonotrophic cycle, absence of a dilatation need not necessarily be an indication that a female has not fed on blood. Klowden and Lea (1981), using the Brugia pahangi-Aedes aegypti-Meriones unguiculatus laboratory system, proved that nulliparous mosquitoes, which have taken small quantities of infective blood that are not sufficient to sustain vitellogenesis, can ingest microfilariae and develop and transmit infective stage larvae. The role of nulliparous females in the natural transmission of filariasis is not known. In this paper, we examine the role of nulliparous females and also those of other parity groups of Culex quinquefasciatus, the principal vector of lymphatic filariasis in India. Correspondence to: P.K. Das, Deputy Director, Vector Control Research Centre (ICMR), lndira Nagar, Medical Complex, Pondicherry 605 006, India.

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Study area

Two endemic localities, Muthialpet and Mudaliarpet, in Pondicherry urban agglomeration formed the study area. A detailed description of the study area has been given in a previous publication (Ramaiah and Das, 1992).

Material and Methods

Night biting catches on human volunteers, who acted as baits, were carried out in Muthialpet and Mudaliarpet. It was ensured during the catches that the mosquitoes did not bite the catchers. The details on frequency, duration, time and methods of collection were as described by Ramaiah and Das (1992). The collections were brought to the laboratory and all the females of C. quinquefasciatus were separated according to Sella's classification, based on the stages of blood digestion and ovarian development, into unfed, freshly fed, semi-gravid and gravid (from Detinova, 1962). The females were then dissected to determine their age and occurrence of infection. Methods of dissection, age determination and differentiation of various filarial stages were similar to those described earlier (Ramaiah and Das, 1992). The chi-square test was used to examine the variation in the proportion infected between unfed and partially fed females.

Results

The nulliparous females formed the largest single age class, with 45.4% (Table 1). The number of females with larger number of dilatations decreased progressively. However, the frequency of 4-parous biting females was only 0.2% and insufficient to allow any meaningful interpretation of their epidemiological significance. The biting population was composed of unfed, partially fed (freshly fed) as well as semigravid and gravid females (Table 2). We have not quantified the amount of blood in individual partially fed females, but the vast majority of them had only traces of blood. Though unfed females predominated, the partially fed individuals accounted for a considerable proportion (range 18.3-33.3%, mean 23.5 + 2.1) of different age groups as well as the total biting catch and only few semigravid and TABLE 1 Age specific filarial infection rates of Culex quinqu~/hsciatus Parity grade

NP a l-parous 2-parous 3-parous 4-parous

Number

2549 2226 732 97 12

~NP, nulliparous.

%

45.4 39.6 13.0 1.7 0.2

+ ve for infection

+ ve for L3

Number

%

Number

%

42 229 120 24 0

1.7 10.3 16.4 24.7 0.0

0 13 21 9 0

0.0 0.6 2.9 9.3 0.0

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gravid females were encountered (Table 2). The proportion of unfed and freshly fed females did not show much variation between different parous groups. Increasing infection with at least one stage (Mf/L1/L2/L3) of the parasite and L3 was seen in females of each successive age class up to the 3-parous group (Table 1). No L3 larvae were found in any of the nulliparous females, but, 7.1% of the partially fed nulliparous females were found with Mf/L1 stage larvae (Table 2). None of those without detectable traces of blood was infected. Out of 33 partially fed infected nulliparous females, 31 were found infected with microfilariae and 2 with L1 stage of the parasite. Of all the females infected with filarial larvae, 10.1% were from this age class. Of the biting females with L3, 30.2% belonged to l-parous group and 48.8% and 20.9% to the 2-parous and 3-parous groups, respectively. Variation in the proportion infected was not statistically significant between unfed and partially fed females of I-parous (P= 0.07) and 2-parous (P= 0.94) females. TABLE 2 Filarial infection rates of unfed, fed, semigravid and gravid females of different parous groups of

C. quinquefasciatus AC, abdomen condition; UF, unfed; PF, partially fed (freshly fed); SG, semigravid; G R , gravid. AC

Number

+ v e for inf. No.

Nulliparous UF PF SG GR

+ v e for L3 %

No.

%

1998 468 40 43

0 33 4 5

0.0 7.1 10.0 11.6

0 0 0 0

0.0 0.0 0.0 0.0

1685 488 27 26

156 61 8 4

9.3 12.5 29.6 15.4

9 4 0 0

0.5 0.8 0.0 0.0

2-parous UF PF SG GR

551 167 6 8

78 35 2 5

14.2 21.0 33.3 62.5

15 5 0 1

2.7 3.0 0.0 14.2

3-parous UF PF SG GR

75 20 1 1

15 8 1 0

20.0 40.0 100.0 0.0

7 2 0 0

9.3 10.0 0.0 0.0

4-parous UF PF SG GR

8 4 0 0

0 0 0 0

0.0 0.0 0.0 0.0

0 0 0 0

0.0 0.0 0.0 0.0

l-parous UF PF SG GR

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Discussion

Results of earlier laboratory studies (Klowden and Lea, 1978; Klowden and Lea, 1981) proved that, because of host defensive abilities, a substantial proportion of biting mosquito females do not succeed in engorging on blood to repletion (Edman et al., 1972). This led to multiple feeding within a single gonotrophic cycle (Klowden and Lea, 1978). To this can be added our finding that partial feeding occurs in C. quinquefasciatus under natural conditions also and is evident from the presence of traces of fresh blood in over 20% of the biting females. The amount of infected blood ingested is an important determinant of the magnitude and intensity of infection in mosquitoes (Sasa, 1976). A prevalence of infection of 7.1% of the partially fed nulliparous females and the presence of microfilariae in 31 of the 33 fed infected females of this age group suggests that even small quantities of blood are sufficient to infect a proportion of the biting population under field conditions. Consecutive partial blood meals that are not adequate to trigger vitellogenesis can result in the transmission of filariasis even by nulliparous mosquitoes, as shown in the laboratory by Klowden and Lea (1981). However, absence of L3 in any of the nulliparous females in the present study shows that the possibility of biting C. quinqueJasciatus repeatedly taking such small blood meals, that fail to trigger oogenesis over a period of the time required for the development of microfilariae into L3, is rare under natural conditions. Thus, from the transmission point of view, the role of nulliparous mosquitoes appears to be unimportant. However, the practice of examining only parous mosquitoes to determine the infection of the vectors (Krafsur and Garret-Jones, 1977; Collins, 1979) will underestimate the prevalence of vector infection as shown by the fact that in our sample 1.7% of nulliparous females were infected and 10.1% of the total infected were from this age class. Hence, we consider that nulliparous mosquitoes should be included in the sample for dissection in order to accurately determine the filarial infection rates of the vector population. Some of the filariometric indices such as monthly and annual biting rates, infective biting rates and Annual Transmission Potential (ATP) are estimated from the density of the biting population, including both parous and nulliparous females. Since the latter are not involved in the transmission of disease, the validity of their inclusion for estimating these parameters is debatable. Standardization of calculation of these indices is all the more important because of the anomalies observed between transmission indices and infection or disease parameters in different endemic areas (Southgate, 1992). In Pondicherry, the first gonotrophic cycle in C. quinquefasciatus lasts 5 days and the subsequent ones 3 days (Rajagopalan, 1980). The time required for the development of microfilariae to L3 is 11 days at 30°C (Brunhes, 1969) and 11-12 days at 28°C (Rajagopalan et al., 1977). Therefore, infected females must survive at least two gonotrophic cycles for microfilariae to develop into L3. But, 0.6% of the 1-parous or 30.2% of the total infective (with L3) females, which would be expected to be less than 8 days old if they were gonotrophically concordant, were found with L3 in the present study. Several other workers also reported the presence of L3 in l-parous females (Hitchcock, 1970; Nathan, 1981). Delayed oviposition (Rajagopalan et al., 1977) due to the taking of incomplete blood meals as already described is presumably the reason for this.

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Aeknowledgment The authors wish to thank Dr. Vijai Dhanda, Director, Vector Control C e n t r e ( I C M R ) P o n d i c h e r r y , f o r his c r i t i c a l c o m m e n t s o n t h e p a p e r .

Research

References Brunhes (1969) Nouvelles donnees sur les vecteurs de Wuchereria bancrofti a Madagascar. Influence de la temperature sur la vitesse de developpement du parasite et le taux d'infection du vecteur. Bull. Org. Mond. Sant6 40, 763 769. Collins, R.C. (1979) Onchocerciasis transmission potentials of four species of Guatemalan Simuliidae. Am. J. Trop. Med. Hyg. 28, 72 75. Detinova, T.S. (1962) Age-grouping methods in Diptera of medical importance. WHO Monogr. Ser. 47, 1-216. Edman, J.D., Webber, L.A. and Kale II, H.W. (1972) Effect of mosquito density on the interrelationship of host behavior and mosquito feeding success. Am. J. Trop. Med. Hyg. 21,487-491. Hitchcock, J.C.Jr. (1970) Evaluation of filariasis mosquito surveys based on the physiological age of the vector. J. Parasitol. 56, 149 153. Klowden, M.J. and Lea, A.O. (1978) Blood meal size as a factor affecting continued host-seeking by Aedes aegypti (L). Am. J. Trop. Med. Hyg. 27, 827 831. Klowden, M.J. and Lea, O.A. (1979) Effect of defensive host behavior on the blood meal size and feeding success of natural populations of mosquitoes (Diptera: Culicidae). J. Med. Entomol. 15, 514-517. Klowden, M.J. and Lea, O.A. (198l) Laboratory transmission of Brugia pahangi by nulliparous Aedes aegypti (Diptera: Culicidae). J. Med. Entomol. 18, 383-385. Krafsur, E.S. and Garrett-Jones (1977) The survival in nature of Wuchereria-infected Anophelesfunestus Giles in Northeastern Tanzania Trans. R. Soc. Trop. Med. Hyg. 71, 155-160. Nathan, M.B. (1981) Bancroftian filariasis in coastal north Trinidad, West Indies: intensity of transmission by Culex quinquefasciatus. Trans. R. Soc. Trop. Med. Hyg. 75, 721-730. Rajagopalan, P.K., Kazmi, S.J. and Mani, T.R. (1977) Some aspects of transmission of Wuchereria bancrofti and ecology of Culex pipiens fatigans in Pondicherry. Indian J. Med. Res. 66, 200-207. Rajagopalan, P.K. (1980) Population dynamics of Culex pipiensfatigans, the filariasis vector, in Pondicherry-Influence of climate and environment. Proc. Indian Natl. Sci. Acad. B 46, 745 751. Ramaiah, K.D. and Das, P.K. (1992) Seasonality of adult Culex quinquefasciatus and transmission of bancroftian filariasis in Pondicherry. Acta. Trop. 50, 275 283. Sasa, M. (1976) Human Filariasis. University of Tokyo Press. Tokyo. Southgate, B.A. (1992) Intensity and efficiency of transmission and the development of microfilaraemia and disease: their relationship in lymphatic filariasis. J. Trop. Med. Hyg. 95, 1-12. Woke, P.A., Ally, M.S. and Rosenberger , C.R. (1956) The number of eggs developed related to the quantities of human blood ingested in Aedes aegypti (L.). Ann. Entomol. Soc. Am. 49, 435-441.

Non-involvement of nulliparous females in the transmission of bancroftian filariasis.

The possible involvement of nulliparous females of Culex quinquefasciatus in the transmission of bancroftian filariasis under field conditions was exa...
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