Ascaris suum

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Ascaris suum
Adult Ascaris in hand.jpg
Scientific classification
Kingdom: Animalia
Phylum: Nematoda
Class: Secernentea
Order: Ascaridida
Family: Ascarididae
Genus: Ascaris
Species: A. suum
Binomial name
Ascaris suum
(Goeze, 1782)

Ascaris suum, also known as large roundworm of pigs, is a parasitic nematode that causes ascariasis in pigs. While roundworms in pigs and humans are today considered as two species, A. suum and A. lumbricoides, with different hosts, cross infection between humans and pigs is possible, so researchers have argued they are the same species.[1] Ascariasis is associated with contact to pigs and pig manure in Denmark.[2]

A. suum is distributed worldwide and grows up to 40 cm (16 in) in length. Ascaris infections are treated with ascaricides. A. suum is in the family Ascarididae, and is one of the oldest associations to mankind.

Life cycle[edit]

Pigs get infected with A. suum by ingesting infectious parasite eggs that are present in the environment. The larvae of Ascaris complete two moults within the egg and therefore, the larvae emerging from the egg is not a second stage larva (L2) as was previously presumed, but rather a third stage larva (L3) covered by a loosened L2 cuticle.[3] The larvae hatch from the egg inside the intestines and subsequently start their migration through the body of the pig. First they penetrate the intestinal wall at the level of the caecum/colon [4] and use the mesenterial blood veins to migrate to the liver. After borrowing their way through the liver tissue, they again use the efferent blood stream to carry them to the lungs. There, they get stuck in the capillaries surrounding the lungs and they penetrate the lung alveoli. It takes approximately 7 days to reach the lungs. Once the larvae are inside the lung, they migrate up the respiratory tree and are eventually coughed up and swallowed by the host to reach the small intestine again as soon as 10 days after infection. There, the larvae undergo their first molt inside the host to reach the L4 stage by day 14 post infection. Around day 25 post infection they develop into the L5 stage. Worms reach adulthood 6 weeks after infection and when both female and male worms are present in the same host, fertilized eggs are produced and secreted by the female worm. These eggs are then excreted together with the faeces. After an incubation period, infective stage larvae develop in the eggs and are ready to cause infection in a new host.

Paratenic hosts ingest the eggs and the L3 larvae remain in the tissues of the paratenic host until a pig eats them. These may include beetles and earthworms, as well as large to jumbo chicken eggs from at-risk fowl.

Morphology[edit]

A. suum adult male with typical curled posterior end together with a significantly larger female worm.

Males are about 15–31 cm (6–12 in) long, and 2–4 mm (0.1–0.2 in) wide. The posterior end is curved toward the ventral side with a pointed tail. They have simple spicules that measure 2.0–3.5 mm (0.08–0.14 in) long. Females are larger than males, measuring 20–49 cm (8–19 in) long and 3–6 mm (0.12–0.24 in) in diameter. From the anterior end, the vulva occupies about one-third of the body length. In addition to their large size, these species also have the three prominent lips. Each lip contains a dentigerous ridge, and no interlabia or alae. Females can lay up to 200,000 eggs per day, and their uteri can contain up to 27 million eggs at a time. Fertilized eggs are ovoid, ranging from 45 to 75 µm length and 35 to 50 µm in diameter. The uterine wall contributes to the lumpy and thick outer layer of the egg. The mammillated layer is stained golden-brown by the bile when the eggs are passed in faeces. Females can also deposit unfertilized eggs that are narrower and longer than normal fertilized eggs, ranging from 88 to 94 µm in length, and 44 µm diameter. Only the proteinaceous layer can be seen in unfertilized eggs, because after fertilization, the vitelline, chitinous, and lipid layers form.[5]

Epidemiology[edit]

Embryonated A. suum egg containing a visible, infective L3 stage larva.

Presumably, A. suum infections are present in pig farms all over the world. However, few countries have up-to-date information on its prevalence. In a Swedish study it appeared that the pens of sows and fatteners are the heaviest infected environments.[6] This was shown by the presence of eggs in old faecal deposits collected from the pens. These findings were supported by studies from China and Denmark where the highest prevalence of A. suum was also found in breeding sows and fatteners.[7][8] The prevalence in breeding boars is usually lower than in sows or fatteners. Nevertheless, infected boars could also be an important source of transmission of parasite eggs on the farm since they are often located in more traditional pens than the sows (e.g. with solid floor and/or bedding). Moreover, boars are regularly used for contact stimulation of the sows, which allows them to spread the infection by defecating in areas other than their own pen. Strong evidence exists that under indoor conditions, massive infection of piglets with A. suum usually occurs shortly after arrival in the highly infectious fattening units and not in the farrowing pens.[6][8][9] Several studies have shown that A. suum egg excretion was nearly absent in weaners despite the, sometimes substantial, presence of eggs in the farrowing pens of intensive herds.[7][10] Here, the increased hygienic standards in combination with the low humidity in the farrowing pens may significantly reduce the presence of favourable microenvironments for egg survival. On the other hand, in piglets raised under outdoor conditions, significant transmission is thought to occur soon after birth and pigs are infected before fattening.[8][11]

There are three major reasons why Ascaris is still so prevalent in current high intensity pig farms. First, because it has a direct life cycle, and is therefore not reliant on other organisms for its transmission to new hosts. Second, the female parasitic worms are highly fecund and are capable of producing hundreds of thousands of eggs per day that contaminate the surroundings instantaneously. One study showed that pigs that are naturally exposed to a paddock contaminated with A. suum have the highest egg excretion approximately 17 weeks after being introduced onto the paddock. After this point, egg counts seem to drop again.[12] The lifespan of adult A. suum worms can be over 1 year, which is significantly longer than the average lifespan of a fattening pig these days. Therefore, once adult worms are present in fattening pigs, egg shedding increases with the age of the pigs unless the worms are cleared from the intestine by anthelmintic therapy. Third, the eggs of A. suum are generally considered to be highly resistant to external environmental factors suggesting their possible survival for up to several years in the appropriate conditions. So, even if parasitic worms are flushed from the intestine by anthelmintic drugs (which do not have a remanent effect), the pig keeps on reinfecting itself continuously since it is present in a highly contaminated environment. This ensures the establishment of fresh infections very rapidly after treatment. These factors, together with the seemingly unimportant health consequences of A. suum infections have led to a certain negligent attitude towards roundworm infections on the part of the farmer.

Pathogenesis[edit]

Pigs that are infected with A. suum, sometimes carry numerous adult worms in their intestine. Yet, these pigs do not show any disease specific symptoms and are indistinguishable from uninfected pigs. Clinical signs such as breathing difficulties and wheezing, and indirect signs like decreased growth rate and overall lower food conversion efficiency are not specific and therefore seldom associated with ascariosis by the farmer. Although the presence of adult parasites in the small intestine might affect the pig’s productivity,[13] it does not appear to affect the pig’s health significantly. The larval stages of this parasite on the other hand, do cause significant damage to the internal organs of its host in their attempt to successfully complete their hepatopulmonary migration.

Several "white spots" are visible on the pig liver after recent A. suum infection.

In the liver, the inflammatory reaction to this damage is manifested as the so-called ‘white spots’ that are visible on the surface of the liver. Hepatic white spots are the most characteristic lesions caused by migrating A. suum larvae in pigs. After larvae migrated through the liver, the destroyed liver cells are replaced by interlobular depositions of fibrous tissue and cellular infiltrates, producing the typical white spots.[14][15] Three types of white spots have been described: compact and mesh-worked white spots both produced by eosinophilic interstitial hepatitis and the lymphonodular type spots caused by lymphofollicular hyperplasia. White spots appear as early as 3 days post infection and start to resolve after about 2–3 weeks post infection.[16][17] As a result of this, livers can appear normal about 35 days after primary inoculation with Ascaris eggs.[18] In order to complete their hepatopulmonary migration, larvae need to pass through the lungs as well. As these larvae move into the alveolar and bronchial air spaces they cause direct physical damage to the lungs. This can subsequently promote the development of pneumonia or pleurisy. The damage to the respiratory system can be recorded at the slaughterhouse and has been associated with the presence of Ascaris infection.[19] It is obvious that the severity of the damage will depend on the amount of larvae that migrate through the lung [20] and that increased infection levels can easily cause respiratory distress and coughing. However, even after ingestion of high amounts of eggs, the A. suum infection itself very seldom causes lethal damage to the lung. It is rather the secondary, opportunistic, bacterial or viral infections that increase the chances of severe health problems.

Economic importance of pig ascariasis[edit]

Infections with A. suum, and especially the larval migration phase, have shown to reduce the economic profitability of a pig farm.[21] The presence of this parasite on a pig farm reduces its productivity in a number of direct or indirect ways. Perhaps the most obvious of which is the condemnation of the livers that are visibly affected by parasite migration. Whether the liver is trimmed or fully condemned evidently depends on the amount of white spots detected on the liver. At the level of the lung, the passage of ascarid larvae is associated with impaired pulmonary bacterial clearance [22] making it easier for secondary bacterial and viral infections to settle. Increased susceptibility to Pasteurella multicoda, Escherichia coli and Salmonella spp. have already been associated with ascariosis.[23][24][25] Moreover, a recent study also observed a significant negative effect of A. suum infection on the seroconversion and antibody levels to a Mycoplasma hyopneumoniae vaccine.[26] Not only the negative effects of these diseases on the productivity but also the costs of their treatment indirectly contributes to the effect of ascariosis.

The decreased health status of pigs, as a consequence of roundworm infection, is reflected in general production parameters like daily weight gain, feed conversion efficiency and meat quality. However, in farms with low infection levels, the effect of infection is expected to be minimal and the economical profitability of active Ascaris control can be questioned.[27] It is difficult to determine the economical losses due to parasites that are not lethal. There are numerous interactions between the worm, the host, the presence of other diseases, the production system and many other factors. Recent evaluations of the economical performance of infected pig farms has indicated that the improved feed conversion, increased daily weight gain, lower mortality and better carcass quality act in a synergetic way. Hence, strategic deworming should result in a win-win effect on economic and environmental performances with gross profit margin increases of 3 to 12 euro per average present finisher per year.[28][29][30] To distinguish between pig populations that suffer significant economical damage and those that are less affected, we depend on the availability of diagnostic tools to provide us with information on the presence and infection pressure of this parasite on a farm. If interpreted correctly, diagnostic tools can be of use to evaluate the applied control strategies and see whether efforts for parasite control need to be increased or changed.

Diagnosis[edit]

Infections with A. suum very seldom cause clinical disease and therefore typically remain unrecognized by farmers and veterinarians. To be able to evaluate the evolution of the infection status and therefore the efficacy of the applied control strategies, the use of correct diagnostic tools is crucial. The presence of A. suum infections on pig farms can be investigated in different ways. First, the presence of adult worms in the faeces and general clinical signs including coughing, rapid shallow breathing, unthriftiness, and weight loss or reduced weight gain could indicate the presence of Ascaris on the farm. In the laboratory, serum or faecal samples can be investigated to detect antibodies or parasite eggs respectively. Finally, at the slaughterhouse, the presence of worms in the intestine and the number of affected livers and lungs also provide information on the ‘Ascaris-status’ of a farm.

Coprological examination[edit]

White spots on the liver[edit]

Serological examination[edit]

The enzyme-linked immunosorbent assay (ELISA) is an able to determine the presence of A. suum as well as the concentration of the parasite. This is possible because A. suum doesn't only live within the lumen of the intestines, but penetrates mucosa to enter the mesenteric veins where the immune system is able to create antibodies to fight against the larval stage.[31] The ELISA test is more practical in finding an infection and the severity of the infection.

Control of A. suum on pig farms[edit]

Although, the aim of control programs against this parasite should be to eliminate the parasite completely, a significant reduction in transmission intensity will readily result in a marked decrease of adverse effects on the health and productivity of the pig herd. Although, anthelmintic treatment alone, without the support of good general farm management and increased hygienic standards will probably not suffice to effectively control parasitic infections on farms, it is, at this moment, the only available method to clear pigs from roundworm infections.

Anthelmintic treatment[edit]

A leading drug in the treatment of Ascaris infection is Ivermectin, a semi-synthetic derivatie of the natural product of a streptomyces species; Avermectin B1a. Broad spectrum treatments in the form of Benzimidazoles are available which act to prevent tubulin polymerization in the nematode cells, however this has a knock on effect to the host as cellular tubulin will also be affected.

Management practices[edit]

It has been presented that fenbendazole causes decreased embryonation rates in eggs that are released from the adult female.[32] The recommended time to treat with fenbendazole is 2 weeks prior to moving infected pigs into a new clean facility.

Vaccination[edit]

Incidents and outbreaks[edit]

In Canada in 1970, a postgraduate student tainted his roommates' food with A. suum. Four of the victims became seriously ill; two of these suffered acute respiratory failure.[33][34]

Genetics[edit]

A 273-megabase draft genome for A. suum was published in 2011.[35]

References[edit]

  1. ^ http://www.parasitesandvectors.com/content/5/1/42
  2. ^ http://jcm.asm.org/content/43/3/1142.full
  3. ^ Fagerholm et al., 2000, Differentiation of cuticular structures during the growth of the third-stage larva of A suum after emerging from the egg. J Parasitol 86, 421-427.
  4. ^ Murrel et al., 1997, J Parasitol 83, 255-260.
  5. ^ Larry S. Roberts & John Janovy, Jr. (2008). Foundations of Parasitology (8th ed.). McGraw-Hill. ISBN 978-0-07-131103-8. 
  6. ^ a b Nilsson, 1982; Acta Vet Scan Suppl. 79,1-108.
  7. ^ a b Lai et al., 2011; Res Vet Sci 91, e121-124.
  8. ^ a b c Roepstorff and Nansen, 1994; Vet Parasitol 54,69-85.
  9. ^ Beloeil et al., 2003; Livest Prod Sci 81, 99-104.
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  12. ^ Mejer and Roepstorff, 2006; Parasitol 133, 305-312.
  13. ^ Andersen, 1976, The influence of A. suum infection upon growth rates in pigs; Nord Vet Med 28, 322-330
  14. ^ Nakagawa et al., 1983. Pathological studies on white spots of the liver in fattening pigs. Natl Inst Anim Health Q 23, 138-49.
  15. ^ Perez et al., 2001. Immunohistochemical characterization of hepatic lesions associated with migrating larvae of A. suum in pigs. J comp Pathol 124, 200-206.
  16. ^ Eriksen et al., 1980, Nord Vet Med 32, 233-242.
  17. ^ Roepstorff et al., 1997, Parasitol 115, 443-452.
  18. ^ Copeman and Gafaar, 1972; Sequential development of hepatic lesions of ascaridosis in colostrum-derived pigs. Aust Vet J 48, 263-68.
  19. ^ Bernardo et al., 1990, Ascariasis, respiratory diseases and production indices in selected Prince Edward Island swine herds. Can J Vet Res 54, 267-273
  20. ^ Miskimins et al., 1994. The serious effects of Ascarid larval migration on a group of market-weight swine. Vet Med 89,247-253.
  21. ^ Holland, Celia. Ascaris the Neglected parasite. Elsevier. pp. 363–381. ISBN 978-0-12-396978-1. 
  22. ^ Curtis et al., 1987. Can J Vet Res 51, 525-527.
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  31. ^ Roepstorff, A. (1998-07-01). "Natural Ascaris suum infections in swine diagnosed by coprological and serological (ELISA) methods". Parasitology Research 84 (7): 537–543. doi:10.1007/s004360050444. ISSN 0932-0113. PMID 9694368. 
  32. ^ "Abstract: Pittman JS. 2015;23(5):252-263 Effect of fenbendazole on shedding and embryonation of Asca". www.aasv.org. Retrieved 2016-05-06. 
  33. ^ James A. Phills; A. John Harrold; Gabriel V. Whiteman; Lewis Perelmutter (1972). "Pulmonary infiltrates, asthma and eosinophilia due to Ascaris suum infestation in man" (PDF). New England Journal of Medicine 286: 965–970. doi:10.1056/NEJM197205042861802. PMID 5062734. 
  34. ^ "Risk Assessment for Food Terrorism and Other Food Safety Concerns". Food and Drug Administration Center for Food Safety and Applied Nutrition. October 13, 2003. Archived from the original on May 27, 2009. Retrieved February 15, 2012. 
  35. ^ Aaron R. Jex; Shiping Liu; Bo Li; Neil D. Young; Ross S. Hall; et al. (2011). "Ascaris suum draft genome" (PDF). Nature 479 (7374): 529–533. doi:10.1038/nature10553. PMID 22031327.