Modern Parasitology: A Textbook of Parasitology

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MODERN PARASITOLOGY

Modern Parasitology A TEXTBOOK OF PARASITOLOGY EDITED BY

F. E. G.

cox

Professor of ParQsite Immunology King's College London

SECOND EDITION

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1'82, 1973 by Science Ltd Editorial Offices: OslKy Mead, Oxford OX2 OEL lS John SIr«t, London WCtN 2Bl 23 Ainslie Place, Edinburgh EHJ 6AJ 238 Main Street, Cambridge Musachusctll 02142, USA 54 University Sneer, Culton Victoria 3053, Australia Blackw~lI

OISTllllUTOas

Marllon Book Senica Ltd PO 50" 87 Oxford OX20DT (Orden: Tel: 0186$ 7'1155 Fax: 01865 191m Telex: 8J7515)

USA B1aclc.well Scien~:'~. .

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Malaria parasiles from

human hlood. (al Plasmodium /IIlciparoffl.jbl P. vivlJJC. ( , .- , , , , ,

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.>,',\ , , •...':: .;.'.,.'·L·....;.·__-,.,'.•.• " • '" '. . .. ,

Female

Female

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ventral

sucker

sucker

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....

Female genital

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FiC· 2.6 In copulo pair of adult schistosomes (based on S. mansoni).

for many years in a host who is relatively resistant to new infections. Pairs of adult worms produce eggs which are laid into the lumina of the venules in which they live. There is no direct, non-pathological route by which these eggs can reach the outside world from this location. In fact, most schistosome eggs possess a sharp shell spine which helps to provide a means of escape. Spines lodge in the intima of the venule and impede the movement of eggs by blood flow. Small blood vessels packed with eggs may rupture, enabling them to move into surrounding connective tissue. A proportion of these eggs eventually reach the outside world via the lumen of the gut or bladder in faeces or urine. This necessarily unusual exit route for schistosome eggs is at the heart of their considerable pathogenicity. Many eggs become lodged in the tissues all over the body. In these locations, living and then moribund or dead eggs become immobilized in spherical granulomatous lesions. It is these progressively accumulating lesions in many different organs which give rise to most chronic schistosome-induced pathology. The eggs which do leave an infected person in urine or faeces hatch on contact with freshwater and the emergent miracidia infect a range of aquatic and amphibious snails in which infective cercariae are produced. All human digenean infections other than schistosomiasis are initiated when people eat metacercarial cysts. Schistosome transmission is quite different. Furce-

cercariae emerging from the snails survive on average for about a day at 20"C, swimming tail· first through the water. During this brief, free· swimming and non-feeding existence fuelled by endogenous glycogen reserves, they are directly infective to people entering the water in which they are swimming. Aided by small backwardpointing tegumental spines and cytolytic secretions a cercaria rapidly penetrates bare human skin, often down the side of a hair shaft and sheds its tail in the process. The penetrant cercaria! head can now be considered as an immature adult schistosome or schistosomulum. Schistosomul.a enter the peripheral blood system .and are carried eventu.ally to the lungs, usually within a week of skin penetration. From the lungs the worms migrate to the liver where they p.air up and mature. Pairs of worms then move to their fln.al eggproducing sites. Figure 2.7 illustr.ates the general org.anization of human schistosome life cycles while Table 2.7 oudines specific information on the four major species. Schistosomiasis is very largely a rur.al disease of the tropics. Contact with mud or w.ater c.arrying infective cercariae comes alxmt by children playing in w.ater, w.ater gathering or washing and very import.antly in the course of work. Agricultural practices which involve direct human contact with irrigation w.ater are especially h.az· ardous. One reason for the increasing prev.alence of all rur.al schistosomi.ases is the expanding programme of construction of d.ams for hydroelectric

38

CHAPTER 2

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Fill_ 2.7 Diagramm.atic flow-chart of the main features of the We cycles of human schistosome,.

or Imgatlon purposes in developing countries. Such schemes inevitably produce new waterbodies for snail colonization. The pathological effects of intestinal and urinary schistosomiasis are somewhat different. Those, for instance, of S. mansoni intestinal schistosomiasis are slowly progressive and complex. During the initial invasion stage there may be a transient dermatitis or 'swimmer's itch'. Thereafter most pathology is the direct or indirect result of the host's immunological responses to parasite eggs (see Chapter 8, Section 8.81. In heavy

infections eggs in the lining of the gut cause granulomatous reactions there which can extend into the gut lumen as pseudopapillomas, with or without egg caleification. Extensive change of this sort may cause colonic obstruction and blood loss. The hepatic portal system carries many eggs to the liver and eggs trapped there are the foci of new granulomatous lesions. General damage to the liver induced in this way produces liver enlargement (hepatomegalyl and following portal hypenension, splenomegaly also occurs. Damage to the porul circulation causes collateral

Table 2.7 Some features of human schistosomes

N=
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FIe- 4.17 The relationship between the probability that a female worm is mated jl(l' and the mean p,arasice burden per host [MO) for various leX\Ial habiu and distributed p,attems of worm numbers per host (Poisson and negative binomial with parameter l< • O.34I.IAfter May, 1977.1

scnt in the parasite's life cycle, either between the arrival of an infective stage in the bost and its attainment of sexual maturity lsee Table 4.2), or between the production of a transmission stage and its development to the infective stage, R is reduced by a factor fill. wbere/i is the proportion of worms that attain sexual maturity in the host and 11 is the proportion of transmission stages that survive to become infective. 4 Many helminth parasites of humans, such as hookworms and schistosomes, have separate sexes. The production of transmission stages is therefore only achieved by female worms who have mated and R is reduced by a factor rrfJ, where [is the proponion of female worms within the total parasite population (many helminths of humans appear to have sex ratios of approximately I : II and q, is the probability that a mature female worm is mated. The mating probability is dependent on a variety of factors, in particular whether the parasite is monogamous or polygamous {bookworms are thought to be polygamous while scbistosomes appear to be monogamous} and the frequency distribution of parasite numbers per host IFig. 4.27). The mating probability is of some significance to the dynamics of helminth

infections and will be discussed funher in conm~(tion with breakpointll in disease transmission. S The mean worm burden per host lthe intensity of infectionl is linearly related to the value of R, while the prevalence of infection is detennined by the mean and the frequency distribution of parasite numbers per host (Fig. 4.281. High mean burdens ltesulting from high R values) may result in low prevalences if the distribution of parasites is highly aggregated within the host population lsee Figs 4.27 &. 4.28). The negative binomial probability distribution is a good empirical model of aggregated distributions of parasite numbers per host IFig. 4.4), and a rough guide to the degree of worm clumping within the host population may be obtained from the following equation: p=

1- Ikllk + MIl'.

1321

This expression equates the mean parasite burden per host, M, and the prevalence of infection, p, with the parameter k of the negative binomW model which varies inversely with the degre~ of parasite aggregation lvalues ofk. in excess of ten imply that the worms are effectively randomly distributed within the host popUlationl values close to zero imply a high degree of aggregation,

CHAPTER 4

104

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with the majority of parasites being haboured by a few hosts). Surprisingly, for some infections of humans, such as the intestinal nematode Ascaris

lumbricoides, the degree of parasite aggregation (as measured by kl appeArs to be relatively inde-

pendent of the human population sampled [e.g. its geographical location). An illustration of this point is presented in Fig. 4.29 where the relations.hip between mean worm burden of A. Jumbricoides (determined by worm expulsion) and the prevalence of infection is recorded for various

a-Ol}

3

Fig.4.18 laJ The relationship between R and the mean plIrasite burden per host at equilibrium (M'j. (hj The relationship between the equilibrium prevalence of infection and R for various distribution patterns of wonn numbers per host (Poisson k ..... "", negative binomial k "" 0.34, negative binomial k :0 0.01).

epidemiological studies carried out in different parts of the world. The solid line denotes the fit predicted by equation (321 with a k value of 0.543. Note how tightly the observed values cluster around the predictions of the negative binomial model. These data hint at a positive association between the value of k and mean wonn burden, which may suggest the influence of densitydependent constraints on parasite population size at high densities (causing a decline in aggregation and a concomitant increase in the value of kl.

EPIDEMIOLOGY 100

..

90 80 ~

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70 60

j: 20 10

O~O-~--~--~---, 10 20 30 Mean WOfm burden Fie. 4.29 The relationship between prcValCDCC of

infcctionlPl and the mean worm burden lMl for A.scDOJ 1umbri~du. The squares arc observed values and the solid line il the 8t of cquationl311 in the text with Ir. - O.543.ICuym £t01., 1990.)

The degree of clumping often varies in different age-