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Universities of Leeds, Sheffield and York promoting access to White Rose research papers Universities of Leeds, Sheffield and York http://eprints.whiterose.ac.uk/ This is the published version of an article in Parasitology, 106 (4) White Rose Research Online URL for this paper: http://eprints.whiterose.ac.uk/id/eprint/77526 Published article: Quinnell, RJ, Slater, AF, Tighe, P, Walsh, EA, Keymer, AE and Pritchard, DI (1993) Reinfection with hookworm after chemotherapy in Papua New Guinea. Parasitology, 106 (4). 379 - 385. ISSN 0031-1820 http://dx.doi.org/10.1017/S0031182000067123 White Rose Research Online [email protected] 379 Reinfection with hookworm after chemotherapy in Papua New Guinea R. J. QUINNELL1*, A. F. G. SLATER1!, P. TIGHE2, E. A. WALSH2, A. E. KEYMER1 andD. I. PRITCHARD2 1 Department of Zoology, South Parks Road, Oxford OX1 3PS 2 Department of Life Science, Nottingham University, Nottingham NG7 2RD (Received 2 June 1992; revised 29 October 1992; accepted 30 October 1992) SUMMARY Reinfection with hookworm (Necator americanus ) following chemotherapy was studied over 2 years in a rural village in Madang Province, Papua New Guinea. The prevalence of hookworm infection had returned to pre-treatment levels after 2 years, and the geometric mean hookworm burden had returned to 58 % of the pre-treatment value. The rate of acquisition of adult worms was independent of host age, and was estimated as a geometric mean of 2-9-3-3 worms/host/year (arithmetic mean 79-8-9 worms/host/year). There was significant predisposition to hookworm infection; the strength of this predisposition did not vary significantly between age or sex classes. Key words: hookworm, Necator americanus, reinfection, predisposition, chemotherapy, Papua New Guinea. 1981). Hookworm is the commonest helminth in- INTRODUCTION fection in Papua New Guinea: in 1919-1923 the Hookworms (Necator americanus and Ancylostoma Australian Hookworm Campaign recorded a preva- duodenale) are among the most prevalent of all lence of 68% from a countrywide survey of more human infections. The distribution of these parasites than 46000 people (Sweet, 1924), while more recent extends throughout the wet tropics and subtropics, estimates give a prevalence of 74—90 % (Vines, 1970). and an estimated 1150 million people are infected Despite its commonness little is known about the (Bundy, 1990). A large number of studies of local population dynamics of the parasite, and hookworm epidemiology have been carried out, estimates of intensity have relied on the use of faecal especially in the 1920s and 1930s, when the Rocke- egg counts. In the only published reinfection study feller Foundation funded studies and control pro- from Papua New Guinea, Ashford & Barnish (1989) grammes in many countries (Ettling, 1990). How- found no predisposition to high or low hookworm ever, since this period the study of hookworm has egg count in children from a highland village. been neglected in comparison to that of other human The present study was carried out in a lowland helminths. In particular, there have been very few village on Karkar Island, Madang Province, Papua studies involving the use of anthelmintic-induced New Guinea. This study is part of a wider investi- worm expulsion to accurately determine worm gation of the epidemiology and immunology of N. burdens (Bundy, 1990). Worm expulsion has been americanus, the only species of hookworm found in used in recent studies in India and Zimbabwe the area; the study design and pre-treatment results (Anderson & Schad, 1985; Schad & Anderson, 1985; have been previously published (Pritchard et al. Bradley et al. 1992), but to date there has been only 1990). The present paper describes the extent and one community-based reinfection study with in- pattern of reinfection 1 and 2 years after treatment. tensity assessed by worm counts, that of Haswell- Elkins et al. (1988). Studies on hookworm in Papua New Guinea have concentrated on assessing its distribution and preva- MATERIALS AND METHODS lence, and its relationship to nutritional status, Fieldwork was carried out in the village of Kebasob, particularly anaemia (Zigas, 1973; Shield et al. Karkar Island, Papua New Guinea. Details of the study area, study design and methods used have * Present address: Department of Medical Parasitology, already been described (Pritchard et al. 1990). London School of Hygiene and Tropical Medicine, Briefly, an initial survey was carried out in July- Keppel St, London WC1E 7HT. f Present address: Picower Institute for Medical Re- August 1988. Faecal samples were obtained from search, 350 Community Drive, Manhasset, New York 202 people, who were then treated with the an- 11030, USA. thelmintic pyrantel pamoate (Combantrin, Pfizer Parasitology (1993), 106, 379-385 Copyright © 1993 Cambridge University Press http://journals.cambridge.org Downloaded: 10 Sep 2009 IP address: 129.11.77.198 R. J. Quinnell and others 380 Ltd) at a dose of 10 mg/kg. All faecal output was were carried out according to Sokal & Rohlf (1981). collected for 48 h and expelled worms counted. Negative binomial distributions were fitted by an Later, anthelmintic treatment was offered to all iterative maximum-likelihood method (Elliott, villagers who had not been included in the study 1977). group: in total, an estimated 60% of the village population received treatment. In August 1989 faecal samples were collected from RESULTS as many as possible of the original sample. Five Prevalence of hookworm infection people were found to be infected with Ascaris lumbricoides and were treated with Combantrin; the The prevalence of hookworm infection before rest of the population was not treated. In July- chemotherapy, assessed by faecal egg counts, was August 1990 faecal samples were collected again, all 92-9%, which was reduced to an estimated 37% by people treated and counts of expelled worms per- chemotherapy. Prevalence had increased to 65-0% formed as in 1988. and then 80-7 % after 1 and 2 years reinfection (Fig. Only data from people who provided samples in 1). The prevalence assessed by worm recovery was all years are analysed: 140 people provided faecal 81-3% in 1988 and 82-7% in 1990. samples in all 3 years, and 75 people provided full The age-prevalence profiles of infection in all 3 post-treatment faecal output in both 1988 and 1990. years are shown in Fig. 2. After reinfection preva- The efficacy of anthelmintic treatment was as- lence did not increase with host age, and had sessed in a subsample of 25 people in 1988: the cure returned to pre-treatment levels in the younger age rate was 60 % and the reduction in arithmetic mean classes in 1990. Prevalence was very similar in male 2 faecal egg count 94% (Pritchard et al. 1990). and female hosts in all three years (Fig. 1; x — 1*17, Seventy-two h faecal collections were made from a 0-387and0053 in 1988,1989and 1990, D.F. = l.N.s. total of 20 worm-positive individuals in 1988 and in all cases). 1990. These people expelled a mean of 88 % of their worms during the first 48 h. Intensity of hookworm infection Faecal egg counts were performed according to a modified formalin—ether concentration technique After 2 years reinfection the geometric mean (95 % (Hall, 1981); results are presented as eggs per gram c.l.) worm burden was 4-8 (33-6-8) worms/host, of faeces (eggs/g). Worms were counted after 58% of the pre-treatment value of 8-3 (5-5-12-3) washing post-treatment faeces through two grades of worms/host. Corresponding arithmetic means were sieve (1 mm and 300 /u,m). The sediment was pre- 13-0 worms/host in 1990 and 25"3 worms/host in served in 10% formalin and worms were recovered 1988. Worm burden differed significantly between after careful searching by eye, counted and sexed. years, but there was no significant effect of host sex During the 3 years village meetings were held on worm burden. Although the percentage mean when the pathology of hookworm infection and its reinfection was lower in female than male hosts, 40 mode of transmission were explained to interested compared to 78%, there was no significant effect of villagers (in Melanesian pidgin). Leaflets were also host sex on the degree of reinfection (ANOVA: year, distributed advising people on latrine use and the F173 = 7-12, P<001; host sex, F1 73 = 2-01, N.S.; safe disposal of faeces. Ethical clearance for the study interaction, Fx 73 = 2-17, N.S.). was obtained from the Medical Advisory Committee The age-intensity profiles of infection were very of the Department of Health, Government of Papua different pre-treatment and after reinfection: mono- New Guinea. tonic pre-treatment and flat after reinfection (Fig. 3 and Pritchard et al. 1990). There was a highly significant correlation between worm burden and Statistical analysis host age in 1988 (r = 0-453, n = 75, P < 0-001) but The distributions of egg counts, worm burdens and not in 1990 (r = 0-090, n = 75, N.S.); these cor- host ages were positively skewed: these data were relation coefficients differed significantly (t = 2-39, analysed after logarithmic transformation. Predis- P < 005). position was analysed by non-parametric methods The geometric mean faecal egg counts in 1988, on untransformed data. Age and sex standardization 1989 and 1990 were 93, 23 and 45 eggs/g respectively of data (where indicated) was performed by z- (Fig. 4). The per capita egg production of female transformation within sex and age classes (3-8 years, worms was similar before treatment and after 2 years 9-13 years, 14-30 years and 31-60 years old in 1988). reinfection, geometric means (95 % c.l.) being 20 As there are problems in testing the homogeneity of (14-30) and 17 (11-27) eggs/g/female respectively rank correlation coefficients, the predisposition an- (paired i-test: D.F.
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