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Impact of season on filarial vector density and infection in Raipur City of Chhattisgarh, India.

Introduction

Seasonal fluctuations of climatic conditions appear to influence parasite development and thus vector infection and infectivity rates. Very low or very high tem perature is known to be detrimental not only for the mosquitoes but also to development of filarial larvae in the mosquito. In an experimental study on Culex quinquefasciatus (Diptera : Culicidae), it was noted that both temperature and relative humidity play a very important role in the transmission of Wuchereria bancrofti in man (1). Samarawickrema et al (2) observed that the development of W. bancrofti larvae in Aedes polynesiensis took shorter time (12 days) in warm season than cool season (14 days). No vectorial transmission was observed when the temperature was above 37[degrees]C and relative humidity below 65% in Khurda district of Orissa (3). There is no detailed study on impact of season on vectorial capacity of Cx. quinquefasciatus in Raipur available to date and hence the present study was designed to record monthly prevalence of W. bancrofti larval stages in naturally infected Cx. quinquefasciatus during different seasons of the year and evaluate host efficiency (HE) and transmission intensity index (TII) at Raipur City in central India.

Material & Methods

Study area: The study was conducted in Raipur City of Raipur district in Chhattisgarh state, India which is considered filarial low endemic zone. Raipur City lies between 19[degrees]57' and 21[degrees]55' N latitudes and 81[degrees] 25' and 83[degrees]38' E longitudes. The region has a typical monsoon climate. In general, the region is characterized by hot and dry summer season from March to mid-June, dry and cool winter season from November to February and rainfall is generally concentrated from mid-June to October. The housing pattern in the locality was mainly kutcha, semi pucca and pucca type. The analysis of residential densities at Raipur City has revealed average density of 416 persons per hectare which is rather high in relation to hot climate and the size of the city. The study area is not covered by sewage system. Six localities in Raipur were randomly selected for the present study and no specific control measures were undertaken by any agency during the study period.

Collection of mosquitoes: Indoor resting mosquitoes were collected at regular monthly intervals from selected localities of Raipur City for over a period of 12 months between October 1995 and September 1996. The collections were done regularly between 0600 and 0800 hrs using aspirator tube and torch light by a single person (first author) throughout the study period. All possible resting sites of mosquitoes inside the houses were searched spending 10 min in each of the six houses selected for the study from every locality. The identification of mosquitoes was done using the key of Barraud (4). The mosquito species were scored, tabulated and subjected to detailed analysis, locality-wise. Only Cx. quinquefasciatus was retained and other species were discarded. The resting density was determined by dividing the total number of female mosquitoes collected by the total number of man-hours spent and expressed as number/man hour. Follow-up studies were done in March 1999 and March 2006.

Meteorological conditions: Weekly variations at maximum and minimum temperatures, humidity and rainfall in the region during October 1995-September 1996 were collected with the assistance of the Department of Meteorology at Indira Gandhi Agricultural University, Raipur.

Vector infection, infectivity, host efficiency and transmission intensity index: Each female Cx. quinquefasciatus collected from the field was dissected separately for presence of W. bancrofti larvae. The mosquitoes brought alive from the field were anaesthetized with ethyl ether; wings and legs were removed; head, thorax and abdomen were teased apart in normal saline and were examined carefully for several minutes under microscope for filarial larvae. The larvae recovered were identified and different stages of larvae were enumerated. The vector infection and infectivity rates were worked out at monthly intervals for each locality surveyed. All live Cx. quinque-fasciatus in each collected lot were dissected out. Vector infection and infectivity rates (5), host efficiency (6) and transmission intensity index (7,8) were calculated using the formulae mentioned below.

Infection rate (%) = [No. positive for [L.sub.1], [L.sub.2] & [L.sub.3]/No. of mosquitoes dissected] x 100

Infectivity rate (%) = [No. of mosquitoes + ve for [L.sub.3] stage/No. of mosquitoes dissected] x 100

Host efficiency = Mean No. of [L.sub.3] larvae/Mean No. of microfilariae

Transmission intensity index = Vector density x Vector infectivity rate x Average no. of L3 per infective mosquito

As a follow-up, the vector infection and infectivity rates in all localities were reassessed randomly once after a gap of few years. The statistical analyses (Chi-squared and correlation tests) of the data were carried out using Co-stat software.

Results

Variations in temperature, humidity and rainfall: The mean maximum and minimum temperatures ([degrees]C) for the year 1995-96 were recorded to be 33.31[+ or -]0.73 and 20.33[+ or -]0.76. The mean temperature increased from January and reached peak in May (43.58[+ or -]0.37) with a downward trend from June onwards. The lowest mean temperature recorded was 12.15[+ or -]0.67 in December (Fig. 1). The rainfall started rising from June onwards with a peak in July, accounting for 80% of the total rainfall. The total annual rainfall during 1995-96 was 1091.2 mm. (Fig. 1). The humidity increased from June (63%) onwards and with minor variations it remained constant at about 90% till the end of January. The humidity declined thereafter and was minimum in May (40%) (Fig. 1).

[FIGURE 1 OMITTED]

Variation in vector density: The highest density of 162.67 was recorded in December and the lowest of 14.5 in June during 1995-96 (Table 1). The density was maximum in winter followed by rainy and summer seasons. Locality-wise, locality 1 recorded the highest average resting density as compared to locality 5 (Table 2).

Variation in vector infection rate: Monthly variations in vector infection and infectivity rates from each locality are presented in Tables 1 & 2. The mean vector infection and infectivity rates in indoor resting Cx. quinquefasciatus during 12 months study period were 4.05 and 0.25%, respectively. The highest vector infection rate (22.14%) was recorded in August when mean maximum temperature was 30.38[+ or -]0.52[degrees]C, humidity 93[+ or -]0.82% and rainfall 57.53[+ or -]24.74 mm. The lowest infection (2.38%) was recorded in February when rainfall was as low as 2.75[+ or -]2.49 mm. No vector with filarial infection was detected during December which recorded the highest density of mosquitoes (Table 1). Season specific analysis revealed high vector infection in rainy season followed by summer and winter seasons (Fig. 2). Locality-wise, the highest vector infection was observed in locality 2 (6.36%) followed by locality 1 (4.81%), locality 3 (4.27%), locality 4 (3.44%), locality 6 (2.99%) and locality 5 (2.64%) (Table 2). The infection rates were low during winter season although vector density was at its maximum. Negative correlation was apparent between infection rate and the vector density (Fig. 2). Monthly variation in vector infection rate shows significant relation with rainfall (p <0.01) but not with humidity or minimum temperature. A significant rise in vector infection rate was recorded in subsequent follow-up studies in March 1999 and March 2006 (Table 3).

[FIGURE 2 OMITTED]

[FIGURE 3 OMITTED]

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Variation in vector infectivity rate: Of the 130 Cx. quinquefasciatus recorded with filarial larvae over a 12 months initial phase of study, only eight mosquitoes showed L3 stage larvae giving a mean infectivity rate of 0.25% (Table 1). The highest infectivity rate was observed in June (1.15%) when the mean maximum temperature was 38.03[+ or -]2.06[degrees]C and rainfall was 23.90[+ or -]17.81 mm. The lowest was in March (0.41%) when rainfall was zero and mean maximum temperature was 37.27[+ or -]1.55[degrees]C. The infectivity rate was higher in rainy season followed by summer and winter seasons (Fig. 2). Locality-wise, the infectivity rate was highest in locality 6 and lowest in locality 3. Interestingly, infectivity rate was zero in locality 1 although considerably high vector infection rate (4.81%) and density were recorded from that locality (Table 2). Monthly variation in vector infectivity rate did not show any significant relationship with variations in rainfall, humidity and minimum temperature. Monthly variations in maximum temperature and vector density exhibited negative correlation (p <0.08) with vector infectivity rate.

Frequency distribution of W. bancrofti larvae: A total of 685 W. bancrofti larvae were recovered from 130 naturally infected Cx. quinquefasciatus mosquitoes with a mean density of 5.27. The microfilarial stage dominated all other stages with a mean density of 5.37 (Fig. 3). The frequency of microfilariae in vector population ranged from 1-30. There seems to be a negative correlation between number of microfilariae recovered and mosquito frequency. The density of various other stages of filarial larvae also varied widely in infected vector population. The microfilarial density was in the order of [L.sub.1], [L.sub.2] and [L.sub.3] stages respectively (Fig. 3). The number of [L.sub.1] ranged from 110, while [L.sub.2] and L3 ranged from 1-5 in infected populations of Cx. quinquefasciatus. Locality-wise, variations in infection and infectivity rate could be attributed to variation in microclimatic conditions.

Host efficiency index: The average host efficiency recorded was 0.44 with highest in February and least in March (Table 1). The highest host efficiency was observed in winter season followed by summer and rainy seasons. Locality-wise, the highest host efficiency was recorded from locality 4 (0.71) and the lowest from locality 2 (0.39) (Table 2).

Transmission intensity index: The annual TII during the study period was 32.72 with highest during January and February while the lowest in March (Table 1). Season-wise, higher TII was recorded in winter followed by rainy season. Locality-wise, the highest TII was recorded from locality 6 (78.64) and the lowest from locality 3 (18.95). Since locality 1 had no [L.sub.3] stages of W. bancrofti, TII is zero (Table 2).

Follow-up study after a gap of 3 yrs and 10 yrs revealed an average vector infection rate of 11 and 8.6% respectively. The highest figures were from locality 1 followed by 2, 4 and 3. The infection rate was significantly high in these localities as compared to initial figures at all the localities (Table 3).

Discussion

The prevalence and intensity of filariasis in human population is directly related to the entomological parameters such as vector infection, infectivity and biting density of infective vector population in the endemic area which in turn are influenced by variations in climate. Rainy season recorded the highest vector infection and infectivity rates although vector density was maximum in winter months. The June month, which recorded the highest infectivity rate, experienced temperature between 28 and 42[degrees]C, moderate to heavy rainfall and relative humidity of 63[+ or -]15. Rainfall appears to be the main influencing factor of vector infectivity rate when both temperatures and relative humidity were favourable.

Distribution of developing filarial larvae in naturally infected wild caught Cx. quinquefasciatus revealed dominance of microfilarial stage as compared to advanced larval stages. Dash et al (3) observed a high correlation between infectivity rate and per man hour density of mosquitoes, however, no such correlation was recorded in this study.

Host efficiency index was very high in January and February months when mean temperature was 23-25.3[degrees]C; rainfall 3-7 mm and relative humidity of 81 to 90%. The rainy season which showed high vector infectivity rate recorded relatively lower host efficiency. The temperature appears to exert some influence on host efficiency index when relative humidity is >60%. Lower temperatures (23-25[degrees]C) with minimum rainfall appear to favour progression of mf to [L.sub.3].

Rao et al (7) and Rao (8), suggested a comprehensive and practical entomological parameter, the "Transmission Intensity Index" (TII) as an alternative to Annual Transmission Potential for measuring the transmission intensities. Winter months recorded higher TII as compared to rainy season in the present study.

Re-examination of vector infection and infectivity rates once again in March 1999 and March 2006 showed a significant rise in the incidence of filarial infection in vector population from all the localities as compared to those of 1996 (p <0.05), but the infectivity rate was zero. This is probably due to examination only once during 1999 and 2006. A significant decline in vector infection rates was recorded in 2006 as compared to those of 1999 (p <0.05) and this could possibly due to the administration of single annual dose of Di-ethyl-carbamazine (6 mg/kg body wt) to whole population in the year 2005 in Raipur City. However, re-examination of these vector parameters in all seasons is needed in order to make a logical conclusion. Further studies are needed to analyze all exogenous and endogenous factors that contribute to the rapid progress of infection in the endemic community.

Acknowledgement

The authors are grateful to the Head, Meteorological Division of Indira Gandhi Agricultural University, Raipur for providing climatic data. The kind help extended by members of Dixit family of Raipur in conducting the entomological survey is gratefully acknowledged. The help rendered by Dr Rameshwar Parihar and Mr Lakshmikant Sharma in the fieldwork is gratefully acknowledged. Financial support extended to the first author (VD) by Department of Science and Technology, New Delhi under Women Scientist Programme is duly acknowledged.

Received: 7 November 2008

Accepted in revised form: 27 July 2009

References

(1.) Basu BC, Rao SS. Studies on filariasis transmission. Indian J Med Res 1939, 27: 233-49.

(2.) Samarawickrema WA, Spears GFS, Folasone K, Cummings RF. Filariasis transmission in Samoa II. Some factors related to the development of microfilariae in the intermediate host. Ann Trop Med Parasitol 1985; 79: 101-7.

(3.) Dash AP, Mahapatra N, Hazra RK, Acharya AS. Transmission dynamics of filariasis in Khurda district of Orissa, India. Southeast J Trop Med Public Health 1998; 29: 20-5.

(4.) Barraud PJ. The Fauna of British India, including Ceylon and Burma, v. V. (Diptera: Culicidae). Tribes Megarhinini and Culicini. London: Taylor and Francis 1934.

(5.) Expert Committee on Filariasis. WHO Tech Rep Ser 1962; p. 233.

(6.) Kartman L. Suggestions concerning an index of experimental filarial infections in mosquitoes. Am J Trop Med Hyg 1954; 3: 329-37.

(7.) Rao CK, Sundram RM, Venkatanarayana M, Rao SJ, Chandrasekharan A, Rao CK. Epidemiological studies on bancroftian filariasis in East Godavari District (Andhra Pradesh): entomological aspects. J Commun Dis 1981; 14: 138-40.

(8.) Rao CK. Indices for evaluation of filariasis in India: a critique. J Commun Dis 1982; 14: 9-15.

Corresponding author:

Dr G.B.K.S. Prasad, SOS Biochemistry, Jiwaji University, Gwalior-474 011, India.

E-mail: gbksprasad@gmail.com

Vandana Dixit [a], Paramanand Baghel [b], A.K. Gupta [b], P.S. Bisen [c] & G.B.K.S. Prasad [a]

[a] Jiwaji University, Gwalior; [b]School of Life Sciences, Pt. Ravishankar Shukla University, Raipur; [c] Bisen Biotech & Biopharma Pvt. Ltd., Gwalior, India
Table 1. Variations in vector density (No./man hour),
infection and infectivity rate, host efficiency (HE) and
transmission intensity index (TII) of indoor resting Cx.
quinquefasciatus between October 1995 and September 1996

Month Mosquito No. of Average Infection
 density mosquitoes [L.sub.3] rate
 dissected

Oct '95 68.67 209 0 0
Nov 86.83 298 0 0
Dec 162.67 688 0 0
Jan '96 47.50 285 2 2.81
Feb 35 210 4 2.38
Mar 43 245 1 2.45
Apr 51.17 285 0 2.81
May 20.67 118 0 0
Jun 14.50 87 3 4.59
Jul 40.50 239 3 10.50
Aug 40.17 241 2 22.41
Sep '96 52 308 0 6.49
Average 55.22 267.75 2.37 4.05

Month Infectivity Host transmission
 rate efficiency intensity
 index

Oct '95 0 -- 0
Nov 0 -- 0
Dec 0 -- 0
Jan '96 0.70 1.07 67.45
Feb 0.48 2.67 67.20
Mar 0.41 0.21 17.63
Apr 0 -- 0
May 0 -- 0
Jun 1.15 0.69 50.02
Jul 0.42 0.51 51.03
Aug 0.83 0.27 66.66
Sep '96 0 -- 0
Average 0.25 0.44 32.72

Table 2. Locality specific vector density (No./man hour),
infection and infectivity rates, host efficiency (HE) and
transmission intensity index (TII) of indoor resting
Culex quinquefasciatus during 1995-96

 No. of
Locality Mosquito mosquitoes Average Infection
(No.) density dissected rate

Budhapara (1) 77.33 561 0 4.81
Fafadih (2) 39.33 472 3 6.36
Gudhyari (3) 55.75 586 2 4.27
Kankalipara (4) 52.92 524 2 3.44
Rajatalab (5) 49.83 569 1.5 2.64
Tikrapara (6) 56.17 501 3.5 2.99
Average 55.22 267.75 2.37 4.05

 Transmission
Locality Infectivity Host intensity
(No.) rate efficiency index

Budhapara (1) 0 0 0
Fafadih (2) 0.21 0.39 24.78
Gudhyari (3) 0.17 0.53 18.95
Kankalipara (4) 0.38 0.71 40.22
Rajatalab (5) 0.35 0.46 26.20
Tikrapara (6) 0.40 0.49 78.64
Average 0.25 0.44 32.72

Table 3. Follow-up studies * on filarial infection
and infectivity rates of the filaria vector
Cx. quinquefasciatus in March 1999 & March 2006

Locality March 1999
(No.)
 Mosquito Infection Infectivity
 dissected rate rate

Budhapara (1) 63 14.28 0
Fafadih (2) 41 12.19 0
Gudhyari (3) 55 10.90 0
Kankalipara (4) 53 11.32 0
Rajatalab (5) 65 9.23 0
Tikrapara (6) 43 6.98 0
Total 53.33 10.94 0

Locality March 2006
(No.)
 Mosquito Infection Infectivity
 dissected rate rate

Budhapara (1) 39 10.25 0
Fafadih (2) 42 4.76 0
Gudhyari (3) 30 13.33 0
Kankalipara (4) 20 10 0
Rajatalab (5) 35 5.71 0
Tikrapara (6) 54 9.26 0
Total 220 8.64 0

* Follow-up study was done only in the month of March.
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Publication:Journal of Vector Borne Diseases
Article Type:Report
Geographic Code:9INDI
Date:Sep 1, 2009
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