Helminths (nematodes and cestodes) are common GI parasites of commercial poultry. Approximately 100 worm species have been recognized in wild and domestic birds in the USA. Nematodes (roundworms) are the most significant in number of species and in economic impact. Of species found in commercial poultry, the common roundworm (Ascaridia galli) is by far the most common. Field studies show that poultry maintained under free-range conditions may be heavily parasitized; therefore, control measures such as preventing infections or chemotherapy can improve weight gain and egg production. In surveys of poultry raised under nonconfinement conditions throughout the world, an incidence of infection >80% is not uncommon.
Generally, nematodes have separate sexes that have morphologic differences; eg, males of Tetrameres spp are elongated and slender, whereas gravid females are globe-shaped. The size and shape of nematode species vary widely; ascarids are sturdy and long (up to 4.5 in. [116 mm]); capillarids are more delicate, slender, and long (2.3 in. [60 mm]); and other nematodes are much shorter (0.08–0.48 in. [2–12 mm]).
Cestodes (tapeworms) also vary in size. Raillietina spp may be >12 in. (30 cm), whereas Davainea proglottina often is <0.16 in.="" (4="" mm).="" the="" proglottids="" of="" individual="" tapeworms="" are="" hermaphroditic.="" tapeworms="" have="" been="" recovered="" in="" the="" thousands="" from="" individual="" chickens="" and="">0.16>
Modern confinement rearing of poultry has significantly reduced the frequency and variety of endoparasite infections, which are common in ranged birds and in backyard flocks. However, severe parasitism still may be seen in floor-reared layers, breeders, turkeys, or pen-reared game birds where management problems may exist. Contributing factors include the use of poorly managed built-up litter (which fosters the propagation of intermediate hosts and the accumulation of infective eggs) and resistance of the parasites to therapeutic drugs. Range infections of nematodes such as Heterakis gallinarum and Syngamus trachea may increase because of seasonal or climatic abundance of specific invertebrate intermediate hosts, eg, large numbers of earthworms brought to the surface by spring rains. Some species have been associated with large numbers of darkling beetles, which may act as mechanical vectors of infective eggs.
Nematodes have either a species-specific, direct life cycle with bird-to-bird transmission by ingestion of infective eggs or larvae or have an indirect cycle that requires an intermediate host (eg, insects, snails, or slugs). Eggs of many nematode species are resistant to low temperatures and disinfectants but may be more susceptible to heat and desiccation. Eggs of A galli and H gallinarum can survive up to two years in soil.
The life cycle of A galli is simple and direct. Eggs in the droppings become infective in 10–12 days under optimal conditions. The infective eggs are ingested and hatch in the proventriculus, and the larvae live free in the lumen of the duodenum for the first 9 days. They then penetrate the mucosa, causing hemorrhages, return to the lumen by 17–18 days, and reach maturity at 28–30 days. Levels of infection are often underestimated, because early larval stages are barely visible and can remain for long periods within intestinal tissues, whereas adult stages in the lumen are generally fewer in number. Maturation of larval stages can be hampered by adult worm numbers, thereby increasing the time larval stages remain in intestinal tissues and continue to cause damage.
The life cycle of H gallinarum is similar to that of A galli. The greatest production of eggs for each hatched egg ingested occurs in the ring-necked pheasant, followed by the guinea fowl and chicken. The larvae are closely associated with the cecal tissue, but a true tissue phase rarely occurs. Most of the adult worms are found at the blind end of the ceca. Earthworms may ingest the eggs of the cecal worm and serve as a source of infection when ingested by poultry. Darkling beetles may also serve as a mechanical vector.
The life cycle of Capillaria may be direct (C obsignata), require an intermediate host such as earthworms (C annulata and C caudinflata), or be either direct or use earthworms (C contorta). Larval development in the egg takes 8–15 days depending on temperature. Worms reach maturity in 20–26 days after ingestion by the final host.
The gapeworm Syngamus trachea inhabits the trachea and lungs of many domestic and various wild birds. Infection may occur directly by ingestion of infective eggs or larvae; however, severe field infection is associated with ingestion of transport hosts such as earthworms, snails, slugs, and arthropods (eg, flies). Many gapeworm larvae may encyst and survive within a single invertebrate for years. Although gapeworms are not a problem in confinement-reared poultry, they cause serious economic losses in game-farm pens and in range-reared chickens, pheasants, turkeys, and peacocks. Cyathostoma bronchialis is the gapeworm that infects geese and ducks.
Eggs of Oxyspirura mansoni, Manson eyeworm, are deposited in the eye, reach the pharynx via the nasolacrimal duct, are swallowed, passed in the feces, and ingested by the Surinam cockroach, Pycnoscelus surinamensis. Larvae reach the infective stage in the cockroach. When infected intermediate hosts are eaten, liberated larvae migrate up the esophagus to the mouth and then through the nasolacrimal duct to the eye, where the cycle is completed. Other insect species may also serve as the intermediate host.
Cestodes require an intermediate host (eg, insects, crustaceans, earthworms, or snails). Floor layers, breeders, and broilers are infected with Raillietina cesticillus by ingestion of the intermediate host, small beetles that breed in contaminated litter. Cage layers in unscreened houses may become infected with Choanotaenia infundibulum by eating its intermediate host, the house fly. Darkling beetles in proximity may also serve as intermediate hosts.
More than 3,000 of the microscopic tapeworm Davainea proglottina have been recovered from a single bird. Several species of slugs and snails serve as intermediate hosts, and >1,500 infective parasites have been recovered from a single slug.
Pathogenesis and Clinical Findings
Ascaridia, Heterakis, and Capillaria spp are widely distributed and cause such nonspecific clinical signs such as general unthriftiness, inactivity, depressed appetite, and suppressed growth; in severe cases, death may result. A mere few ascarids may depress weight, and larger numbers may block the intestinal tract. Ascarids may migrate up the oviduct (via the cloaca) to become enshelled later within the egg (an aesthetic, but not a public health, problem, avoidable by careful egg-candling before the release of eggs to market). A dissimilis (turkey roundworm) may also migrate out of the intestine, through the portal system, and into the liver, causing hepatic granulomas.
H gallinarum, a mild pathogen, in large numbers may cause thickening, inflammation, or nodulation in the cecal walls. Infection with H gallinarum has been associated with cecal and hepatic granulomas. Heterakis isolonche, highly pathogenic in pheasants, may cause 50% mortality. H gallinarum carries Histomonas meleagridis, the protozoan that causes histomoniasis Histomoniasis .
C contorta in the mucosae of the crop and esophagus, and C obsignata in the wall of the small intestine, cause marked thickening and inflammation of the organs. Birds harboring large numbers of these threadlike worms become weak and emaciated and may die.
Young birds are the most severely affected by gapeworms. Sudden death and verminous pneumonia characterize early outbreaks. Signs of gasping, choking, shaking of the head, inanition, emaciation, and suffocation may follow. Necropsy reveals adult gapeworms obstructing the lumina of the trachea, bronchi, and lungs. Respiratory inflammation may be present. The blood-red, female gapeworm is usually found in copulation with a much smaller, paler male with its head embedded deep in the host tissue. The joined pair have a “Y”-shaped or forked appearance.
Oxyspirura mansoni is a slender nematode, 12–18 mm long, found beneath the nictitating membrane of chickens and other fowl in tropical and subtropical regions. The parasite causes various degrees of inflammation, lacrimation, corneal opacity, and disturbed vision.
Among other nematodes, Amidostomum anseris attacks the gizzard lining of ducks and geese and causes dark discoloration, necrosis, and sloughing at the parasitic loci. Dispharynx nasuta causes ulceration, thickening, and maceration of the proventriculus; heavily infected birds may die. Tetrameres americana, a bright red worm discernible through the proventricular wall, causes diarrhea, emaciation, and with heavy infection, death. Trichostrongylus tenuis causes inflamed ceca, weight loss, anemia, and death, especially in young birds. Ornithostrongylus quadriradiatus, a blood-sucking parasite, causes pigeons to regurgitate bile-stained fluid mixed with food; greenish mucoid diarrhea from hemorrhagic intestines, emaciation, and death follow.
Most pathogenic tapeworms are found in the small intestine; the scolex, usually buried in the mucosa, generally causes mild lesions. Davainea proglottina may cause weight loss. Raillietina tetragona causes weight loss and decreased egg production; R echinobothrida produces granulomas at its attachment sites (“nodular disease”).
Identification of individual parasites by morphology or molecular biological tests
A reliable diagnosis of helminthiasis can be made by accurate identification of the individually recovered parasites by their morphology or increasingly by molecular biological methods. Only specific recognition of the parasite allows meaningful recommendations for flock therapy and management. To determine the species by morphology, worms detected during necropsy should be carefully removed, put into a saline solution, and examined under a microscope. However, identification of the often fragile worms can be difficult for nonexperts and is complicated by intraspecies variation.
Detection of worm eggs by fecal flotation allows for the reliable confirmation of the presence of worms. The infecting species cannot usually be differentiated this way, however. And because eggs are shed intermittently and in varying numbers, the absence of eggs in one sample does not necessarily mean that worms are absent.
ELISA systems to detect antibodies against A galli have been described. However, they are not commercially available, and the detected antibodies are not species-specific.
PCR for species identification uses universal primers that amplify the partial cytochrome c oxidase subunit II (cox2) gene, a fragment of the rDNA gene comprising the internal transcribed spacers, and the partial nicotinamide adenine dinucleotide dehydrogenase subunit 1 gene. This is followed by sequencing of the PCR products used to characterize different worms. However, there are few published reference sequences, and these are necessary to validate the tests for routine diagnosis.
Treatment and Control
Few drugs are available for treatment of chickens and other poultry.
Birds should only be treated in cases of severe infection that show clinical signs.
There are decreasing numbers of medications approved for treatment of helminthiasis in poultry. There are also reports of resistance developing against the remaining drugs. To reduce the potential spread of resistance, treatment should be limited to birds with severe infection that show clinical signs of disease. Such targeted treatment also seems to more effectively decrease worm burden and cumulative environmental parasite egg numbers than untargeted routine treatment. Worm loads have been reported to rebound quickly following deworming, however.
Improvement of management and sanitation in confined operations will generally lower the parasite levels in birds. In range birds, the only option is to move to new pasture, although the benefit that may result will be of short duration. Application of approved insecticides to soil and litter when premises are unoccupied may interrupt the life cycle of the parasite by destroying its intermediate host. When the premises are restocked, groups of birds of different species or ages should be separated to avoid spread of parasites. Migration of darkling beetles or other insects may infect new or widely separated housing.
Approved compounds are very limited in the USA. Because of frequently changing regulations, the status of any medication should be checked before its administration. Approved drugs for use in the USA are listed online in the FDA’s Green Book and in the commercially available Feed Additive Compendium .
Only approved drugs may be used in birds producing eggs or meat for the commercial market. Label directions and recommended doses should be followed precisely, with scrupulous adherence to withdrawal times.
Several compounds are reported to be effective against nematode infections but are not approved for use in poultry or other avian species in the USA.
Fenbendazole is approved for chickens and turkeys in the USA against Ascaridia galli and Heterakis gallinarum when administered in the drinking water at a dosage of 1 mg/kg for 5 consecutive days. It is has also been shown to be effective against Ascaris spp. when administered once at 10–50 mg/kg; if needed the treatment can be repeated after 10 days. At 10–50 mg/kg, fenbendazole when administered daily over 5 days is effective against Capillaria. Fenbendazole is also effective against other nematodes when administered at 10–50 mg/kg/day for 3–5 days or as a single dosage of 20–100 mg/kg, or when added to the drinking water at 125 mg/L for 5 days or to the feed at 100 mg/kg. At 20 mg/kg for 3–4 days, it effectively removes gapeworms in pheasants. Toxicity has been reported in pigeons that received fenbendazole at the rate of 30 mg/kg for 5 days. Fenbendazole should not be administered during molt, because it may interfere with feather regrowth.
Flubendazole (1.43 mg/kg) is used widely in Europe against Ascaridia spp and H gallinarum.
Mebendazole fed prophylactically at 64 ppm or curatively at 125 ppm is effective against Ascaridia spp in turkey poults. At 10 mg/kg for 3 days, mebendazole has been reported to be effective against Amidostomum anseris and Trichostrongylus tenuis.At recommended levels for chickens, mebendazole has some reported effect against Dispharynx nasuta, tetramisole against Subulura brumpti and Strongyloides avium, and piperazine against Tetrameres.
Cambendazole provided control of Ascaridia spp when given in three treatments of 50 mg/kg for chickens and 20 mg/kg for turkeys. At 60 mg/kg for 3 days, cambendazole has been reported to be effective against A anseris and at 30 mg/kg against T tenuis.
Albendazole administered as a single oral suspension (5 mg/kg bird weight) was reported effective against A galli, H gallinarum, and C obsignata. The drug also has been reported effective against cestodes if administered at 20 mg/kg. There are no published withdrawal times.
Nitarsone at 170 g/ton (0.01875%) of feed has been reported to reduce A dissimilis fecundity and worm burden in chickens and turkeys.
Tetramisole at 40 mg/kg, flubendazole at 30 ppm in feed, and ivermectin 1% at 10 mg/mL in water were effective in removing A galli, H gallinarum, and Capillaria spp in chickens. Tetramisole at 3.6 mg/kg for 3 consecutive days in the drinking water removes gapeworms. Poultry treated while larvae are migrating in the body develop immunity to gapeworms, even though therapy may abort larval migration.
Pyrantel tartrate was more effective then pyrantel pamoate against the adult stage of A galli, and it was somewhat effective against Capillaria spp when administered at 15–25 mg/kg.
Levamisole administered at 25–30 mg/kg appears to be effective against A dissimilis, H gallinarum, and C obsignata; it can also be given in the drinking water at 0.03%–0.06%. Levamisole fed at a level of 0.04% for 2 days or at 2 g/gal. drinking water for 1 day each month has proved to be an effective control in game birds. Kiwis are reported to be acutely sensitive to levamisole at doses well within the safe range for domesticated poultry.
Phenothiazine has been used to treat cecal worms in chickens at 0.5 g/bird and in turkeys at 1 g/bird, given in 1 day. Combined in drinking water as a 1-day treatment, phenothiazine (0.5%–0.56%) and piperazine (0.11%) have been used to treat heterakids and ascarids; this drug combination is no longer approved for poultry in the USA.
Methyridine injected subcutaneously at a dose of 25–45 mg/bird is effective in clearing C obsignata. In pigeons, a subcutaneous injection of 1 mL of 10% methyridine in the pectoral region or leg of pigeons removed Capillaria spp, but the drug must be handled with care because contact with skin may produce lesions.
Coumaphos removes Capillaria spp in quail.
Haloxon at 25 and 50 mg/kg, or at 750 ppm in the feed for 5–7 days, has good activity against Capillaria spp in chickens and quail.
Pyrantel (100 mg/kg) and citarin (40 mg/kg) have been reported to be effective against A anseris and T tenuis.
Thiabendazole at 75 mg/kg controls T tenuis infections.
Poultry producers wanting to treat for tapeworms should be aware that expulsion of the parasite will be a short-term remedy if the scolex is not removed or if the intermediate host is not eliminated as a source of reinfection. Butynorate in combination with piperazine and phenothiazine as a feed additive or individual tablets has shown some efficacy. Other promising experimental drugs include chlorophene, niclosamide, and praziquantel, none of which are approved in the USA.
As a treatment for Manson eyeworm, a local anesthetic can be applied to the eye, and the worms in the lacrimal sac exposed by lifting the nictitating membrane. A 5% cresol solution (1–2 drops) placed in the lacrimal sac kills the worms immediately. The eye should be irrigated with sterile water immediately to wash out the debris and excess solution. The eyes improve within 48–72 hours and gradually become clear if the destructive process caused by the parasite is not too far advanced.
The use of diatomaceous earth supplemented at 2% in feed and fed continuously lowers numbers of Heterakis and Capillaria in chickens. The efficacy of several essential oils and plant extracts have been measured, with inconsistent results.
Helminthiasis is an infection with members of the phylum Nematoda (roundworms) or the class Cestoda (tapeworms, flatworms). It usually does not cause clinical signs.
Reliable diagnosis of the infecting species is done by the morphology of the adult worms. Detection of egg in the feces proves infection but does not always help to differentiate species.
Control relies on improvement of management and sanitation. Very few compounds are approved for use in chickens and turkeys and should only be used against severe infections.