The occurrence of nematode parasites in domestic animals in developing countries is reviewed in this chapter. In addition some references from developed countries were included when indication of economic impact of nematode infections was given. The data presented have been selected from a a database covering the last 15 years complemented by a search of the Helminthological Abstracts (1981–1990).
The nematode parasites consists of a large diversity of species and in order to simplify the presentation has they have been organized in four main paragraphs based in principle on their location in the host: lungworms, gastro-intestinal worms, filaroids, miscellaneous nematodes.
The main arrangement within paragraphs is according to the host/parasite combination.
5.1.1. Lungworms in cattle
The strongyloid species Mammomonogamus laryngeus and M. nasicola are found in the trachea and nasal cavities. Their pathogenicity is considered to be low. Though it is stated that these nematodes may occur in America as well as in Africa and Asia, this review only include references from Central America, the Caribbean and the northern part of South America (Mexico, 01003, 04407; Costa Rica, 03753; Cuba, 04560; Martinique, 06458; Colombia, 00337; Guyana, 02286; Brasil, 03079).
More important is the trichostrongyloid lungworm Dictyocaulus viviparus which may cause severe clinical disease. It is mainly an infection and disease of young animals. Adult cattle, however, may occasionally become affected if no previous exposure has taken place. Some papers indicate percentages of infected animals but these data may not be indicative of the real impact as important epidemiological factors have ben ignored. The overall picture seems to indicate that D. viviparus infections are of minor importance in developing countries. One has to bear in mind, however, that management of cattle may influence the occurrence and importance of D. viviparus infections considerably. Calves from dairy cattle which are raised by hand and are grazed separated from the adult animals are far more at risk than suckling calves running with their dams.
The following references on D. viviparus is the result of the literature search: Mexico (01003, 0447); Costa Rica (02457); Cuba (02827, 05875, 06520); Jamaica (05994); Ecuador (02461); Brasil (01375): Argentine (03782); Tanzania (02738); Congo (05816); Pakistan (03159); India (07783, 00989); Korea (05915); Malaysia (05915).
D. viviparus is also described in buffaloes (04027)
5.1.2. Lungworms in sheep and goats
It seems that the large lungworm of sheep and goats, Dictyocaulus filaria, only has a limited geographical distribution. The same holds for the small lungworms of the Protostrongylidae, Muellerius capillaris and Protostrongylus rufescens which are the most common species. One has to bear in mind, however, that the geographical distribution of the Protostrongylidae is mainly determined by the distribution of the snail intermediate hosts.
Where the lungworms occur they may have an impact on the performance of sheep and goats but probably significantly less than the trichostrongylid infections.
D. filaria has been described from Mexico (02691); Peru (03681); Argentine (00584);
Morocco (Dakkak & Ouhelli, 1988); Sudan (00585); Turkey (01395, 03965); Syria (00894); Iraq (02910, 01367, 00564); Iran (02621); Afghanistan (03723); Pakistan (01364); India (03132, 03973, 05371, 00859, 03784, 06450).
Protostrongylidae were recorded in Mexico (00246, 03313); Peru (03681), Brasil (03284, 05524); Morocco (Cabaret 1986, Cabaret et al. 1980, Dakkak & Ouhelli 1988); Tunesia (00060, 00520); Congo (01462, 01994); Turkey (01395); Iraq (00564, 01367); Iran (02621) also in wild sheep (06337); Pakistan (01364); India (03132, 03973, 05371, 00859).
The possible use of vaccination against lungworm infections has been mentioned (Iraq, 01367; India, 03132).
5.1.3. Lungworms in other ruminants
Though lungworms, Dictyocaulus cameli, of camels are well known, the survey only lists one reference: Mongolia (03824).
2.1.4. Lungworms in horses and donkeys
The lungworms Dictyocaulus arnfieldi has the donkey as its normal host. While the pathogenicity is limited in the donkey the parasite may provoke severe clinical lungworm disease in the horse.
D. arnfieldia in horses was mentioned from Mexico (05743); Colombia (06340); Brasil (05681); Chile (07026); Zambia (01348); Israel (01152, 01326) It has been described in donkeys from Argentine (05614); Mozambique (01165).
The fact that the lungworm of horses and donkeys was mentioned only a few times in quite different countries may indicate that geographical distribution of the parasite has not yet been fully established.
5.1.5. Lungworms of pigs
The lungworms of pigs belong to the metastrongylid genus Metastrongylus. The main species are M. apri, M. salmi and M. pudendotectus. They may be important as the cause of lungworm disease.
The geographical distribution of Metastrongylus species depends largely on the occurrence of pigs. Therefore, these lungworms as could be expected are only mentioned from some countries in America and from some in east and south-east Asia traditionally known as pig rearing countries.
Moreover the occurrence of Metastrongylus depends on the occurrence of earthworms, the intermediate hosts.
These lungworms were mentioned from Mexico (02424, 02952); Cuba (02739, 02914); Ecuador (02437); Brasil (00607, 03937, 04229); India, (07103); India (02499); Korea (02394, 03644); Taiwan (05945); Malaysia (04210); Philippines (03823); Papua New Guinea (03060).
5.2.1. Toxocara vitulorum in cattle and buffaloes
The ascaroid Toxocara vitulorum seems to have a rather cosmopolitan distribution in the sense that this parasite occurs in the whole of tropical and subtropical regions and in regions with a moderate, continental climate. Patent infection seems only to occur in young calves following the transmission of infective larvae of T. vitulorum via the galactogenic route which is the major route of infection. The life-cycle is therefore theoretically largely independent from the climate and more dependent on the management of cattle. So one may argue that everywhere calves are permitted to suckle their mothers changes for infections with T. vitulorum are present.
It is reported from several countries in south east Asia that these infections may cause clinical disease with high mortality in buffalo calves with a consequent impact on production.
T. vitulorum is mentioned in cattle from Mexico (04307, 05610, 5680); Cuba (04102); British Gyana (02286); Peru (06361);
Chad (08995); Sierra Leone (00889); Togo (00773); Benin (03415); Central African Republic (02335); Congo (06075); Kenya (07199); Zimbabwe (00545); Turkey (01303; Syria (06065); Iraq (01333); Pakistan (03508); India (00754, 01355); Bangla Desh (00173); Korea (03644); Thailand (00057); Malaysia (03222, 06018); Philippines (03825); Indonesia (00908).
It is recorded in buffaloes from Thailand (07046); Vietnam (03129); Malaysia (07260); Philippines (03825); China (01130); Iran (03916); Pakistan (03508); India (01259, 00754, 03459, 04027, 02981); Sri Lanka (00994); Egypt (07135); Ethiopia (01014).
5.2.2. Gastro-intestinal nematodes in cattle and buffaloes
Generally speaking the gastro-intestinal nematode fauna of cattle does not differ significantly between regions. The animals are usually infected with a range of different species. This survey do not give any detailed information on the composition of the parasite fauna in different countries.
When surveys have been conducted the following parasites seems to be representative for the mixed infection of cattle and buffaloes. The trichostrongyloid Haemonchus spp., H. contortus, H. placei and H. similis, are found unless the climate is too dry. The ostertagia species are not very common due to tha fact that most species prefer a temperate climate. Of the other trichostrongylids Trichostrongylus axei is common as are the Cooperia spp., C. oncophora, C. punctata and C. pectinata. Other common nematodes are the strongylid Oesophagostomum radiatum, the hookworm Bunostomum phlebotomum, the rhabditoid Strongyloides papillosus and the trichuroids Trichuris spp. Other nematodes are mentioned in the searched literature only once or twice.
Gastro-intestinal nematode infections are of considerable economic importance causing clinical disease with mortalities but more importantly by causing chronic production losses as a result of reduced weight gain, weight loss and reduced milk production.
The knowledge of gastro-intestinal nematode infections vary considerably between regions as is apparent from the present survey.
In region 1., Central America and the Carribean, only limited information exists from Mexico and Cuba. In region 2., Equatorial America, and region 3., Southern Latin America, considerably more references are available.
It appears that very little has been published with regard to gastrointestinal nematodes in the African regions 4., 5. and 6.
The number of references from the Asian regions 7., 8. and 9., is higher than for Africa but lower than for America. In general, however, the knowledge of gastro-intestinal infections is practically never extended beyond surveys listing the nematode fauna and the assessment of losses in weight gains. Due to lack of information on gastro-intestinal nematodes some countries do not appear in the data base. Surveys should be promoted in these countries. For most countries information is needed on epidemiology and the economic impact of these parasites. The implementation of adequate control measures is only possible when based on this information.
Studies on gastro-intestinal nematodes or infections by these nematodes in cattle were mentioned from Mexico (04307, 05610, 05680); Costa Rica (05853); Cuba ( 02827, 03342, 05554); Jamaica (05994); Puerto Rico (Frame & Bendezú 1987); Colombia (01352); Venezuela (01126, 05536, 05886); British Gyana (02286); Ecuador (01175); Bolivia (06132); Brasil (01276, 07216); Oaraguay (03498); Uruguay (00583); Chili (05781); Argentine (00584, 02199, 02728); Egypt (07135); Sudan (00634); Ethiopia (01014); Niger (05920); Chad (08995); Senegal (02822); Gambia (Murray et al. 1979); Sierra Leone (00889, 05836); Ghana (03149); Togo (00773); Benin (03415); Nigeria (03165, 03405); Central African Republic (02335, 07187); Congo (02731, 06075); Uganda (03033, 06006); Kenya (01011, 07199); Madagascar (01137); Zimbabwe.
Turkey (02159, 03294); Syria (06065); Iraq (01333); Pakistan (03159); India (00629, 03315); Bangla Desh ( 00063, 00694, 00757, 02291, 02586); Korea (00614, 04455); Taiwan (05698); Thailand (00057); Malaysia (03222, 06018); Philippines (03015, 03825); Indonesia (01103, 00578); Papua New Guinea (03913); Solomon Islands (07953).
Some studies on gastro-intestinal nematodes were conducted on buffaloes, mainly in South-east Asia.
Egypt (00061, 07135); Côte-d'Ivoire (00680); Benin (03415); Pakistan (07111); India (04012); Thailand (00074, 00919, 07046); Vietnam (03129); Malaysia (07260); Philippines (03825).
5.2.3. Gastro-intestinal nematodes in sheep and goats
The situation with regard to the nematode parasite fauna in sheep and goats is similar to that seen in cattle in the sense that it does not differ much between regions. The most important nematodes found in sheep and goats are the tricho-strongylids Haemonchus contortus, Trichostrongylus axei, T. colubriformis, T. vitrinus, T. capricola, Cooperia curticei, Nematodirus filicollis and N. spathiger, the hookworm Bunostomum trigonocephalum, the strongylids Oesophagostomum columbianum and Chabertia ovina, the trichurids Trichuris spp. and the oxyurid Skrjabinema ovis. It is estimated that H. contortus and Oe. columbianum have the largest clinical and economic impact on sheep and goat production.
In more temperate part of region 1. (Mexico and Cuba) the trichostrongylid Ostertagia circumcincta occurs. In region 4. (Northern Africa) and in region 7. (Syria and Iraq) sometimes the trichostrongylid Marshallagia marshalli is mentioned.
In general there is more information about gastro-intestinal nematodes in sheep and goats available than for cattle. More is also known about the impact of the infections but an acceptable knowledge level about the epidemiology of the infections is still lacking from most countries. Therefore an appropriate control system can not yet be designed in most instances.
Papers dealing with gastro-intestinal nematodes in sheep and goats are e.g. from Mexico (01973, 02531, 04410); Belize (03961); Panama (00243); Cuba (00549); Jamaica (05994); Puerto Rico (Bendezú et al. 1983); Colombia (00237); Venezuela (00284, 01200, 00999); Ecuador (00415); Peru (05534); Brasil (00790, 00733, 03201, 06280, 06315); Uruguay (03199); Chili (01383, 03786); Argentine (02584);
Morocco (Dakkak & Ouhelli 1988, Pandey et al. 1984, Cabaret 1983, 1984); Tunesia (02604); Sudan (00634, 03595, 07240); Ethiopia (00575, 04114, 06196); Mauretania (01065, 02265); Tanzania 00493, 01010, 06123); Sierra Leone (00889, 00945); Cameroon (00736, 00819, 02864); Congo (01462, 03609), Kenya (01293, 02545, 03361); Zambia (00822, 03098); Namibia (03758); Zimbabwe (00540, 00747, 04134);
Turkey (02159, 05989, 01081, 01330, 05913, 05679, 00626); Syria (04440, 06478); Israel (02821, 02762); Yemen (03485); Iraq (00037, 00256, 00564); Iran (07070); Afghanistan (03723); Pakistan (00145, 03229); India (00809, 01272, 02343, 01351, 06334, 00811, 00725, 01272, 02382, 03738, 01412); Bangla Desh (00809, 04084); Mongolia (00721); Korea (02732, 04353); China (07151); Taiwan (00875); Malaysia (07014, 07132); Philippines (00046, 04034, 08975, 06042, 04271); Indonesia (01218, 00996, 03777, 03886); Papua New Guinea (00688, 00882); Samoa (02010).
5.2.4. Gastro-intestinal nematodes in lama's and camels
In this survey only a few papers are dealing with gastro-intestinal nematodes of lama's. Some papers only describe the result of surveys and list a few species, e.g. Haemonchus contortus, Tricho-strongylus axei and Cooperia oncophora.
Papers are from Peru (00121, 02133); Chili (00409); Argentine (03408).
The situation in camels, mainly dromedaries, is better documented. The nematode fauna is comparable with the fauna of sheep with two exceptions: in camels Haemonchus longistipes and Camelostrongylus mentulatus occur. In very dry areas H. longistipes does not occur.
Papers dealing with gastro-intestinal nematodes of camels came from Sudan (00492, 00496, 01134, 03478, 08315); Ethiopia (03006, 06271); Niger ( 00007, 00008, 05947); Chad (02442); Kenya (03481, 03866, 07192); Kuwait (00940); Iran (04452); India (02109, 02149, 04026, 05752, 03012).
5.2.5. Gastro-intestinal nematodes in horses and donkeys
Information on gastro-intestinal nematodes in horses and donkeys is in this survey very scanty and incomplete. From the regions 8. and 9., Central and South East Asia, papers are completely lacking. Altogether there is only some superficial information from twelve countries. Nevertheless, it seems that the nematode parasite fauna of horses does not differ much between regions of the world. Some of the parasites registered are: The ascaroid Parascaris equorum, the trichostrongylid Trichostrongylus axei, the Strongylidae a.o. Strongylus equinus, the Cyathostominae, the oxyurids Oxyuris equi and Probstmayria vivipara, the rhabditoid Strongyloides westeri and the spiruroids Habronema microstoma, H. muscae and Drascheia megastoma. Of these worms P. equorum and Str. westeri can cause clinical disease in foals, whereas the Strongylidae and the Cyathostominae can provoke serious clinical diseases including colic. Of the spiruroids only D. megastoma has some significance.
Infections with gastro-intestinal nematodes in horses are mentioned from Mexico (02399); Cuba (08328); Colombia (06340); Brasil (02408); Chile (03563); Morocco (Pandey et al. 1981), also in the donkey (Pandey 1980); Mozambique (01165); Zambia (01348); Zimbabwe in donkeys (00637); Israel (01326, 01152); Pakistan (03508); India (00699, 06056).
5.2.6. Gastro-intestinal nematodes in pigs
The literature searched in this survey shows probably a rather realistic picture of the parasite fauna of pigs. Nevertheless, the number of countries from where records exist is low, even when one takes into consideration that in a large part of the world pigs are kept in low numbers only because of the food habits of the people in that part (region 4., Northern Africa, and the larger part of region 7., South Western Asia).
A more or less cosmopolitan nematode fauna in pigs consists of the ascaroid Ascaris suum, the trichostrongylid Hyostrongylus rubidus, the strongylids Oesophagostomum dentatum and Oe. quadrispinulatum, the spiruroids Ascarops strongylina and Physocephalus sexalatus, the rhabditoid Strongyloides ransomi, the trichurid Trichuris suis and the acanthocephalan (not a nematode) Macracanthorhynchus hirudinaceus. In the regions 8. and 9., Central and South East Asia, Gnathostoma spp. have been described. Sometimes other nematodes are mentioned as e.g. Bourgelatia diducta in India (00784) and Capillaria papuensis from Papua New Guinea (02374).
The impact of the infections with gastro-intestinal helminths on the production of pigs will be considerable as some of the nematodes and M. hirudinaceus can cause severe problems including clinical diseases. A. suum occurring in percentage's of 5–85% and Str. ransomi, 4–21% are mainly of importance in piglets and young pigs. The Oesophagostomum spp., occurring in high percentage's (10–97%), have a negative influence on weight gains and on fertility.
One has to bear in mind that the percentage's of occurrence are very much influenced by the management of the pigs, the intensiveness of the keeping and the hygienic measures taken.
Gnathostoma spp. are also of importance as cause of visceral larva migrans in man.
Improved management and hygienic measures adapted to the local circumstances could probably ameliorate the production of pigs by controlling the nematode infections.
Infections with gastro-intestinal nematodes were recorded from Mexico (00282, 04108, 04539); Belize (01554); Cuba (02739, 02914); Ecuador (02437), Brasil (00607, 05587); Chile (06275); Argentine (07159, 04001); Nigeria (03634); Mozambique (01167, 02294); Zimbabwe (00858); India (00784, 01415, 12160); China (01404, 08391); Korea (02394, 03644, 03689, 04109); Taiwan (00868, 02162, 02350); Thailand (03568, 04591, 06928); Malaysia (00732); Singapore (01228); Philippines (00047, 00119, 03823); Papua New Guinea (02374, 03805, 04244, 06789).
5.3.1. Filaroids in cattle and buffaloes
Quite a number of filaroid nematodes are mentioned from developing countries. This is not surprising because the intermediate hosts, mainly bloodsucking insects, are present in abundance in these regions.
Some of the filaroids such as Thelazia spp., Onchocerca spp. and Parafilaria bovicola seem to occur in all regions, whereas Elaeophora poeli is absent from regions 1., 2. and 3., America, and Stephanofilaria spp. seem to be restricted to the regions 7., 8. and 9, Asia.
The clinical disturbances brought about by these filaroids are very different. The lazia spp. cause keratitis and Stephanofilaria spp, are the cause of skin ulcerations. The microfilariae of Elaeophora poeli give raise to dermatitis and the adults of Parafilaria bovicola damage the skin and the underlying muscles wich results in of lesser quality and condemnation of meat. Onchocerca spp, are of minor importance while Setaria labiato-papillata is seen by chance mostly at post mortem.
Because of the life-cycles using mainly bloodsucking insects control of the infections will be very difficult.
References on Filaroids in cattle included in this data base are from Mexico
(05843); Guatemala (04382); Colombia (00071, 06429); British Gyana (02286);
Brasil (00740, 01071, 01336, 03314, 03418, 05633); Argentine (01419);
Sudan (02808, 03329, 03826, 06227) (also the parasite of camels Dipetalonema
evansi, 07173); Ethiopia (06197); Tanzania (00515, 08998) Onchocerca gutturosa
(06059); Mali (00049, 03076); Senegal (03020, 03859, 08377); Gambia (Murray
et al. 1979); Sierra Leone (00598, 00599, 05836); Togo (02815, 06097, 07088);
Nigeria (02583, 03706); Congo (01637, 02731) Thelazia spp. (00803); Mozambique
(01169); Zambia Onchocerca spp. (06398, 07433) Thelazia rhodesi (07243);
Zimbabwe (07142);
Oman (07057); Iraq (03855) Onchocerca sp. (04341); Iran Onchocerca spp. 27%
(06150); India (00985, 02113, 02155, 03017, 03112, 03171, 03527, 03691, 06256)
Stephanofilaria assamensis (00629); Bangla Desh (00453, 01398, 05645, 05728,
05834, 07189, 07204); Mongolia in insects (02180); China (01069, 02493, 04289,
05668); Korea (02314, 03828); Taiwan (00761); Malaysia (02653, 06213, 07044);
Philippines (00125); Indonesia (01227, 03885) Onchocerca sp. in Bos indicus
(04363);
Filaroids in buffaloes are recorded in Mozambique (01169);
India Onch. armillata, Stephanofilaria spp. Thelazia spp. S. labiatopapillata,
Elaeophora spp., P. bovicola (01145, 02486, 03396, 03940, 06302,
06374, 06379, 07165); China (01069, 02493, 04289, 05668); Thailand (07796);
Philippines (00125).
5.3.2. Filaroids in sheep and goats
Only a few references are found in the survey. Of the worms mentioned below Gongylonema pulchrum belongs systematically to the spiruroids and Setaria labiato-papillata may in sheep and goats be the cause of lumbar paralysis by occurring in the spinal cord.
Records come from Mexico G. pulchrum (00683);
Kenya Onchocerca gutturosa (06485);
Oman S. labiato-papillosa (07075); Iran S. labiato-papillosa (02482); India
Onchocerca spp. 0.9% (00624); China S. labiato-papillosa (05668); Malaysia
Stephanofilaria kaeti (07044).
5.3.3. Filaroids in camels
Onchocerca gutturosa from Sudan (04129) and Onch. armillata from Niger (02443) are the two filaroids mentioned from camels in this review.
5.3.4. Filaroids in horses and donkeys
Only a few filaroids are mentioned in horses and donkeys. Onch. raillieti is recorded in Egypt from a donkey (03826) and Onch. reticulata in Iran (06083) from a horse. Parafilaria multipapillosa, a possible cause of bleeding, nodular lesions in the skin, was sporadically seen in horses in Iran (06083). In Iran (02258) Elaeophora bohmi was found in a donkey. In the same host Gongylonema sp. was found in Tunesia.
Setaria spp. may cause disturbances of the central nervous system as the worms can invade the spinal cord. S. equina is recorded from a donkey, Setaria sp. from a mule and S. digitata from a horse in China (01060, 05240, 05668). Other records of S. digitata from horses are from India (01269, 04195); Malaysia (06213) and Philippines (02614).
5.3.5. Filaroids in pigs
Only Suofilaria suis from China (03569) and Onch. dewittei from Malaysia are recorded in this survey.
5.4.1. Trichinella spiralis
Trichinella spiralis is an important nematode because it is a zoonosis and may invade practically all mammals including man. In man it may lead to severe clinical disease and even death. Therefore much attention has been and should be paid to Trichinella infections in slaughter animals. Because of its importance there are regular, international conferences on trichinellosis.
While the geographical distribution of T. spiralis may be regarded as more or
less cosmopolitan the references in the literature of this survey are recorded
from pigs in Mexico (00643, 05589); Ecuador (00404); Chile (002205, 04208);
Argentine (04161);
Egypt (00793); Kenya (03911);
Turkey in wild boar (01250); Iran in wild boar (02182, 06543); India (05828);
China (00700); Thailand (01880, 05958); Indonesia (03791).
5.4.2. Stephanurus dentatus
The stephanurid, related to hookworms and strongylids, Stephanurus dentatus occurs in pigs in the kidney and surrounding tissue. Most of the damage is done by the migrating larvae to the liver and other organs. Control of the infections is difficult.
The infection is recorded in the survey from Mexico (00263); Cuba (03437,
04264); Bolivia (00147); Brasil (02423);
Mozambique (01167);
China also in cattle ((03031, 03157); Philippines (00045); Solomon Islands
(06775); New Caledonia (00005, 03128).
5.4.3. Rhabditis spp.
Some Rhabditis spp., rhabditoids, are the cause of severe external otitis in cattle. The infection is brought about by polluted diptanks for tick control.
The infection is mentioned from Brasil (07064) and Tanzania (03206, 03207, 07061).
