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Estimation of the Infectious Reservoir of Plasmodium Falciparum in Natural Vector Populations Based on Oocyst Size

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Estimation of the Infectious Reservoir of Plasmodium Falciparum in Natural Vector Populations Based on Oocyst Size TRANSACTIONSOF THE ROYALSOCIETY OF TROPICAL MEDICINE AND HYGIENE (1996) 90,494-497 Estimation of the infectious reservoir of Plasmodium falciparum in natural vector populations based on oocyst size H. Hajilp 2, T. Smith3, J. Th. Meuwissen 4, R. Sauerwein4 and J. D. Charlwood’ ‘Ifakara Centre, P.O. Box 53, Ifakara, Tanzania; 2Ministy of Health, P.O. Box 236, Zanzibar, Tanzania; 3Swiss Tropical Institute, P.O. Box, CH-4002 Basel, Switzerland; 4Department of Medical Microbiology, University of Nijmegen, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands Abstract A method for determining the infectious reservoir of malaria (K) and vector survival rate (P) by measuring oocyst size and discriminating between the most recent and other infections is described. In the laboratory the mean diameter of 3 d oocysts in Anopheles gambiae, kept at 26°C was 115 pm and the mean diameter at day 5 was 245 Km. Oocyst sizes in wild caught mosquitoes from southern Tanzania, that had fed on the oc- cupants of bed nets with holes in the sides, were more variable. 2060 A. gambiae s.1. and 1982A. funestus were examined for oocysts 3 d after feeding; 796 and 654 oocysts from the 153 and 170 infected females, re- spectively, were measured. Becauseof misclassification errors, the use of a simple cut-off model, in which all oocysts less than 17.5 pm in diameter were considered to have arisen from the most recent feed, was thought to overestimate K and underestimate P. A statistical model which allows for overlap in the oocyst size distributions is described. Estimates of the infectious reservoir derived from this model were 2.8% for A. gambiae s.Z.and 4.2% for A. funestus, and the estimated survival rates per gonotrophic cycle were 65.5% and 52.9%, respectively. The utility of measuring oocyst size in naturally infected mosquitoes is discussed. Keywords: malaria,Plasmodium falcipamm, reservoirin vector,Anopheles gambiae s.l., Anopheles funestus, oocyst size Introduction tial contamination of recent oocysts with pre-existing in- Epidemiological studies of transmission of malaria fections. This makes it possible both to estimate K di- from humans to mosquitoes have been carried out both rectly and to study the infectiousness of individual to assessthe infectious reservoir in humans for mosqui- hosts. The method relies on the detection of the oocysts toes (MUIRHEAD-THOMSON& MERCIER,1952; DRAPER. shortly after the blood meal disappears from the stom- 19531MUIRHEAD-THOMSON, 1954, 1957; GRAVESet al.; ach of the mosquito. At this stage the oocysts are much 1988, 1990; GITHEKOet al., 1992; THUIKAM et al., 1993; smaller than those aged 5 d or more, and can be distin- CHARLWOODet al., 1995; J. D. Charlwood et al., in guished by their size from previously acquired infections preparation) and to identify factors which modify the in- (SHUTE& MARYON,1952; MUIRHEAD-THOMSON,1957). fectiousness of individual hosts (HAD et al., in press). Infectivity can be studied in feeding experiments us- Materials and methods ing local vectors, raised from wild-caught larvae or pu- Experiments using bed nets with holes pae (MUIRHEAD-THOMAS& MERCIER,l-952; MUIRHEAD- From February to December 1994 mosquitoes were THOMSON. 1954. 1957; GRAVES et al.. 1990) or collected from volunteers in the village of Kisegese, colony-adapted mosquitoes (GITHEKOet aZ.,‘1992;THUI- southern Tanzania (described by HAJI et al., in press) by KAM et al., 1993). In either casemosquitoes that have fed the use of traps consisting of a cone-shapedbed net with on known hosts are generally kept alive for 5-7 d, long 2-4 juxtaposed holes about 6 cm in diameter halfway up enough for oocyst infections to be apparent by micro- the sides. scopical examination of their midguts. The proportion Mosquitoes were collected each morning into paper with infections (D; the delayed oocyst rate) then gives cups and transported to the field laboratory where they an estimate of infectivity. On the other hand, laboratory- were kept until digestion of the blood meal had been adapted insects may differ from the local population in completed (which took 2-3 d, depending on the tem- their susceptibility to infection. perature). In contrast, the use of bed nets with holes in them to Midguts were dissected in 2% mebromine solution catch mosquitoes does not require the establishment of and transferred into 4% phosphate-buffered formalde- mosquito colonies, estimates infectivity using local vec- hyde in 2 mL plastic vials for preservation. Up to 40 tors, and allows the mosquitoes to feed naturally. De- midguts were stored per vial. They remained in good layed oocyst rates from bed nets with holes have been condition for more than a vear. which facilitated batch used to estimate the infectious reservoir (K> processing. Preserved midguts were mounted in 4% (CHARLWOODet al., in press), but when the study re- phosphate-buffered formaldehyde, covered with a cover- quires the identification of the source of the mosquito glass, and examined at x40 with a compound micro- infections it is less than ideal becauseoocysts may be de- scope.The presenceof very small oocysts was sometimes rived from more than one feed (HAJI et al., in press); confirmed using an oil immersion objective. Oocysts l-K/D then gives an estimate of the proportion of the from preserved midguts were measured to an accuracy of detected infections that were acquired before the last 0.3 nm using an ocular graticule. feed. Estimates of K derived from parous rates together with values of D from collections using bed nets with Laboratory determination of oocyst growth rate holes in Namawala (J. D. Charlwood et al., in prepara- The rate of development of oocysts was determined tion) indicated that about 60% of oocysts may have been using a colony of A. gambiae S.S.in the laboratory, fed on derived from previous feeds. Using mark-recapture cultured aametocvtes of the Pf54 strain of PZasmodium methods, BABIKERet al. (1995) estimated that about one- falciparui After feeding, mosquitoes were kept at 26°C quarter of the infected Anophelesgambiae s.1. and one- for 3-5 d when they were processedas described above. eighth of the infected A. funestus caught in bed nets with holes had obtained their infections elsewhere. In this study we report on a modification of the bed Data analysis nets with holes technique that seeksto avoid the poten- Let K be the probability that an anthropophagic mos- auito acauired an infection at the latest feed. R the nrob- Address for correspondence: Tom Smith, Department of Public ability that it was already infected (equivalent to thk im- Health and Epidemiology,Swiss Tropical Institute, P.O. Box, mediate oocyst rate in mosquitoes coming to feed), and CH-4002 Base& Switzerland; fax + 41 61 271 7951. D the overall probability that a mosquito is infected (the RESERVOIROF PLASMODIUM FALCIPARUM 495 delayed oocyst rate). The ratio R/D can be used as an es- 30 timate of P, the survival per gonotrophic cycle (SERVICE, A 1993; J. D. Charlwood et al., in preparation). D is esti- Laboratory 25 mated directly as the overall infection prevalence, whilst -I m the estimation of K and R is more problematical. In order to estimate K, it was necessary to estimate the g20 proportion of mosquitoes infected at the most recent i?i 5 days feed, and therefore to determine the proportion of oo- 5 a 15 n 3 days cysts that were derived from that feed. Let x denote the 0 1 size of an oocyst, 8(x) the distribution of oocyst sizes 2! when the infection was acquired at the most recent feed, u 10 and o(x) the distribution of oocyst sizes from previous infections. The overall distribution of oocyst sizes is 5 then: f(x) -(l-h) 0(x) + Q(x) 0 5 30 55 80 where the mixing proportionz h, is the proportion of oo- 300 cysts that resulted from previous feeds. Note that this is B different from the distribution of oocyst sizes in mosqui- toes with infections derived from both the latest and 250- A. gambiae $.I. previous feed(s), which has a mixing proportion p and is w consequently z200 5 f’(x) - (1-P)86) + PW) 3 150 (i) The simplest approach was to consider all oocysts 4 with diameters below a given cut-off size as those from t 100 the most recent feed, and all others to be from earlier feeds: This allowed classification of individual mosqui- 50 toes and therefore provided direct estimates of h, D and R. It did not allow for overlap between the 2 distribu- i tions, 13(x) and Q(x), and therefore presumably resulted 0 in some misclassification of mosquitoes. 10 20 30 40 50 60 70 80 90 (ii) The second method estimated the extent of over- 300 lap between the distributions. The distribution of oo- cysts in laboratory mosquitoes kept for 3 d can be con- 250 sidered as an estimate of O(x). By comparing the A, funestus observed f(x) with this distribution, estimates of h and a(x) were obtained, using the method of VOUNATSOU et $200 (in press). hi. ii Using these estimates of D, h, 8(x) and Q(x), estimates 3 150 of I< were obtained bv maximum likelihood (see the AD- z pendix). The estimation procedure assumed that all mosquitoes were equally susceptible, and that the prob- t 100 abilities of acquiring an infection at successive feeds were independent. It follows that 50 D=R+K-RK 0 and hence R =(D-K)/( 1-K) 10 20 30 40 50 60 70 60 90 Considering all infections, the expected number of oo- Size (pm) cysts from the most recent feed per infected mosquito is N(l-p)K/D and from previous feed(s) it is NPR/D; the Figure.
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