Biology

Management and Control of Nematode Parasites of Small Ruminants

in the Face of Total Anthelmintic Failure

P. J. Waller

Department of Parasitology (SWEPAR), National Veterinary Institute

SE- 751 89 Uppsala, Sweden

Email: Peter.Waller@sva.se

Abstract

Total failure of modern broad spectrum anthelmintics to control nematode parasites of

sheep and goats is a reality, of rapidly increasing dimension, on many farms in the

tropical / subtropical regions of the world. This is primarily associated with the highly

pathogenic, blood sucking parasite, Haemonchus contortus, and where it now cannot

be controlled by chemotherapy, annual mortalities exceeding 20% of the flock can be

expected. Thus sheep and goat enterprises become totally unsustainable, unless major

changes in management are effected. These must include a change away from reliance

on suppressive anthelmintic treatment and to include several non-chemotherapeutic

management options. In situations where livestock numbers need to be preserved and

there is no opportunity to increase the grazing area available, then zero grazing with

cut-and-carry herbage from uncontaminated pasturelands is the only option. In other

circumstances stocking rates need to be substantially reduced, so that short-term

rotational grazing can be effectively practiced. This strategy is improved if it is

combined with the biological control of the free- living stages of the parasites, using

the microfungus Duddingtonia flagrans. Monitoring the parasitological status of the

animals by faecal sampling sentinel sub-flocks for nematode faecal egg counts, or the

use of the FAMACHA procedure, are also valuable tools. Improving overall nutrition of

the flock is an important adjunct to control. As a long-term priority, attempts to

change the genotype of the flocks to those breeds that have been shown to possess

natural resistance to H. contortus are worthwhile.

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INTRODUCTION

Recently, an exhaustive review was commissioned to prioritise animal health

research for poverty reduction in the Developing World, by an international donor

consortium consisting of the WHO, OIE, FAO. This report concluded that gastro

intestinal parasitism had the highest global index as an animal health constraint to the

poor. The highly pathogenic nematode parasite of small ruminants, Haemonchus

contortus, was singled out as being of overwhelming importance (Perry et al. 2002).

This blood-sucking parasite is responsible for acute outbreaks with mortalities,

particularly in young animals. In Kenya alone, it has been estimated that it causes

losses in the order of US$ 26 million each year (Anon. 1999). It is probably the only

nematode parasite of sheep and goats that can be accurately diagnosed without the aid

of laboratory testing. Signs of acute anaemia are obvious, past history (particularly

weather conditions) and discounting other less common conditions that cause anaemia

(eg. fasciolosis, theileriosis etc.), will strongly suggest clinical haemonchosis. This

parasite has very high biotic potential (egg production by female parasites) and at

times when transmission of this parasite is favoured (warm and wet), losses can occur

in all classes of animals. On a “worm- for-worm” basis, H. contortus is generally

considered the most pathogenic parasite of small ruminants (Soulsby, 1986).

Although it occurs in mixed infections with other nematode parasites, it invariably

dominates the faecal worm egg counts and often approaches 90% of worm egg

contamination on pastures under prevailing conditions of high temperature and

humidity, which are the norm in the humid tropics / sub tropics.

However it is now apparent that H. contortus is becoming more important in

the temperate regions of the world, with the apparent change in weather conditions

that favour this parasite (Waller et al. 2004). Thus much of the problems associated

with parasite infections in small ruminants, problems in their control and problems of

anthelmintic resistance, relate specifically to this single species of nematode parasite.

Detailed economic evaluations repeatedly show that the major losses due to parasites

are on animal production, rather than on mortality (Anon. 1991; McLeod 1995). In

many instances, these costs exceed the costs of losses due to the major “killer”

diseases due to viruses and bacteria (Anon. 1991). Recent estimates of the annual

costs of parasites to the sheep industry in Uruguay and South Africa were US$ 41.8

million (Nari et al. 1997) and US$ 45 million (I. K. Horak), respectively.

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WORM CONTROL: PRINCIPLES AND PRACTICES

The severity of nematode parasitic disease is dictated by the degree of larval

pickup, or challenge, from pasture. This is principally determined by the prevailing

weather conditions, namely temperature and rainfall. If either of these environmental

variables is unfavourable (ie. temperature and/or humidity is too low) then

discontinuities in the translation process from egg hatch to infective larval availability

on pasture, can occur (Levine 1963). Thus, both temperature and rainfall are

important parameters controlling this process in the temperate regions of the world,

whereas in the tropics / subtropics, rainfall is the only limiting environmental variable

because temperatures are always high enough to facilitate this process. Consequently,

in the humid tropics / subtropics, the environmental conditions on pasture are

favourable, more-or- less continuously. Whereas in the temperate regions there are

often times when “bottlenecks” occur in the larval translation process, which not only

reduce larval pickup, but also can be exploited in parasite control programmes

(Waller et al. 1995).

In contrast to the livestock systems of the temperate regions, where varying

degrees of winter housing and /or zero grazing are practiced, ruminant livestock

production in the tropics / sub tropics is characterised by all year round grazing on

pasture. Thus larval pickup from pasture is more-or- less continuous and all livestock

are likely to be infected. Whilst livestock owners in many countries of the tropic s /

subtropics, lack the financial resources, knowledge, or the will, to treat their animals

with drugs, there are also many countries in this region where quite the opposite is the

case. In many regions in the tropics / subtropics communal grazing is the norm. Thus

there is little, or no, opportunity of individual farmers to practice any form of parasite

control, unless there is widespread compliance to the same practices by the whole

community.

Anthelmintics: failure and the future?

For livestock produc ers that can afford it, control of nematode parasites has

been based on the use of anthelmintic drugs. However, since the early 1960’s there

have been only three major classes of broad-spectrum anthelmintics commercially

released for the control of nematode parasites of ruminant livestock, namely: the

benzimidazoles / probenzimidazoles (BZs), the tetrahydropyrimidines /

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imidazothiazoles (most important drug being levamisole: LEV), and the macrocyclic

lactones (MLs), or avermectins /mylbemycins. Although the re are novel classes of

anthelmintic drugs that have been discovered (eg parahequamide,

cyclooctadepsipeptides), possibly the greatest constraint in their commercial

development are the enormous costs involved (Waller 1997). The international

pharmaceutical industry is undergoing unprecedented re-structuring with resultant

company mergers and the reorganisation of product portfolios. Apart from the

lucrative companion animal and horse market, it is evident that veterinary drugs have

been a victim of these “down- sizing” activities. Simply it is a matter of economics.

There is more money to be made in human pharmaceuticals – even the cosmetic

industry – than providing new drugs for the grazing livestock industries. Therefore, it

seems to me to be unlikely tha t a new anthelmintic drug (class) for use against

nematode parasites of food producing domestic livestock will be released onto the

market place in the foreseeable future.

Because of the clinical importance of H. contortus, and the very high

efficiency of the broad spectrum anthelmintics against this parasite (at least in

initially), the concept of suppressive drenching of sheep and goats became firmly

entrenched in many countries of the tropics / subtropics where this parasite is

endemic. Frequent (every 4 – 6 weeks), and often haphazard treatment became

commonplace. This has become much more the case since patent protection of all the

currently available broad-spectrum anthelmintics has lapsed, resulting in a burgeoning

in the marketing of generic anthelmintic products. Quality assurance was an absolute

pre-requisite for the parent companies, but now they have to compete on the

deregulated market against companies with these “look alike” products. On the face

of it, this outcome for the farmers seems to be favourable, with not only a greater

range, but also much cheaper products, becoming available. However, many instances

of poorly manufactured, or counterfeit, generic products have been reported. This is

particularly so in the developing countries, which cannot provide the resources to

monitor product quality and to prosecute offenders (Wanyangu et al. 1994; Waller et

al. 1996). Also, as a result of this unfair competition, there are instances of highly

reputable companies marketing substandard products in this region of the world (van

Wyk et al. 1995). Thus in most instances, freeing-up the anthelmintic market in the

tropics / subtropics has not been in the farmers best interests. As poor quality products

assume a significant market share, then not only do the farmers waste their money, by

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failing to control parasites in their animals, but they hasten the selection process for

anthelmintic resistance.

Recently, the World Organisation for Animal Health (Office International des

Epizooties: OIE) commissioned a survey to determine the status of parasiticide

resistance in pests of livestock worldwide (Nari and Hansen 1999). Of the 151

member countries, responses were obtained from 77 (55% response). The parasites

considered to be of greatest importance to the livestock in each country were in rank

order – worms (73% of respondent countries), ticks, mange mites, flies and lice.

Control of these pests was almost entirely by the use of chemicals. Resistance had

been diagnosed in 55% of the responding countries. Of these, 86% had diagnosed

anthelmintic resistance, 50% ixodicide resistance and 31% insecticide resistance. An

important note was that these estimates were considered conservative, as 27% of

countries mentioned a lack of capabilities, infrastructure, and/or interest in assessing

the significance of these problems.

The examples of anthelmintic resistance in nematode parasites of ruminant

production systems would form, more-or-less, a uniform gradation along the spectrum

from no problem to total failure, which is continuously changing for the worse. The

first reports of total chemotherapeutic failure across the entire range of broad-

spectrum anthelmintics, was made in 1983 (pre – marketing of MLs) on goat farms in

north coastal NSW, Australia, which experienced high levels of summer rainfall

(Anon. 1983). Subsequently, van Wyk (1990) cited a number of instances in the high

rainfall, or irrigated areas, of South Africa where farmers had to abandon sheep

farming because of failure to control worms using chemothe rapy. Total failure of the

BZs and LEV, plus 70% resistance to ivermectin (IVM), the first of the MLs, was

reported in a survey of anthelmintic resistance of sheep farms in the humid Oriental

region of Paraguay (Maciel et al. 1996). Most recently it has been found that total

chemotherapeutic failure to all the three broad-spectrum anthelmintic groups (also to

the narrow spectrum, salicylanilide drugs) exist on all the large government managed

small ruminant breeding farms in the eastern Malaysian state of Sabah

(Chandrawathani et al. 2004). Coupled with a similar result on a large government

breeding farm on Peninsula Malaysia (Chandrawathani et al. 2003b), it seems as

though Malaysia has the dubious distinction of being able to declare itself the first

country where virtually total anthelmintic failure to control internal parasites of small

ruminants is present – at least in the large breeding farms, whose main purpose is to

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supply sheep and goats to small- holder farmers. Thus in the space of approximately

20 years, the situation of virtually total anthelmintic failure has moved from the

individual farm, to district, to region, to state and finally to a country problem.

All the above situations share three important features. Namely, they are all

located in the humid tropics / subtropics, where conditions are more-or-less

continuously wet throughout the entire year, secondly the major nematode pathogen,

H. contortus, completely dominates the parasite profile, and thirdly sheep and goat

raising was/is attempte d to be the sole production system. The experience on Sabah,

where total anthelmintic failure has likely to have been present for some years, is that

annual mortalities exceeding 20% of the flock can be expected (Chandrawathani et al.

2004) – totally unsustainable livestock systems by any assessment!

SOLUTIONS IN THE FACE OF FAILURE