Trichuris

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Trichuris
Parasite140080-fig3 Gastrointestinal parasites in seven primates of the Tai National Park - Helminths Figure 3i.jpg
Egg of Trichuris sp.
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Animalia
Phylum: Nematoda
Class: Enoplea
Order: Trichocephalida
Family: Trichuridae
Genus: Trichuris
Roederer, 1761
Species

Several, see text

Trichuris (synonym Trichocephalus [1] ), often referred to as whipworms or the silent serpent (which typically refers to T. trichiura only in medicine, and to any other species in veterinary medicine), is a genus of parasitic helminths from the roundworm family Trichuridae. The name whipworm refers to the shape of the worm; they look like whips with wider "handles" at the posterior end.

Contents

Species

The genus Trichuris includes over 70 species, [2] which infect the large intestine of their host, including:

A new species – as yet unnamed – has been identified in François’ leaf monkey ( Trachypithecus francoisi ). [3]

Other species in this genus include Trichuris cynocephalus , Trichuris discolor , Trichuris laevitestis , Trichuris pardinasi , Trichuris navonae , Trichuris ovis , Trichuris rhinopithecus , Trichuris thrichomysi , and Trichuris travassosi .

Trichurias is a soil-transmitted helminthiasis and belongs to the group of neglected tropical diseases, affecting about 604 million people globally. [4]

Researchers are currently facing difficulties completely differentiating the numerous species under the genus Trichuris. When different whipworm species were discovered, the main factor used to differentiate species was the length of the spicule sheath. However, many species were eventually discovered to have similar spicule sheath lengths. [5] Therefore, researchers began to compare other morphologies, such as the structure or orientation surrounding female sex organs of species suspected to be similar, but different. [6] Relatively recently, studies have been conducted to differentiate similar Trichuris species based on mitochondrial DNA differences, a much more accurate method of distinction. [7] However, currently a paucity of research devoted to encoding the DNA of each and every species exists. As a result, Trichuris species distinction is still largely based on morphological differences.

History

Whipworm infections were present in ancient times although no written accounts are available. The evidence is based on several mummies in Europe and Brazil that are found to contain the parasite eggs. [8] [9] [10] One of the oldest known infection of an individual is that of Ötzi, a natural mummy of a man who lived between 3350 and 3105 BCE. [11] [12] The first recorded whipworm, T. trichiura was discovered by Italian pathologist Giovanni Battista Morgagni in 1740 (or 1739 [13] ) from the intestine (the cecum and transverse colon) of an infected man. [14] He reported the novel worm in 1741 in Epistolae Anatomicae (number XIV) , which was published in 1764. However, without proper identification or name, his record was soon forgotten. In 1760-1761 medical course at the University of Göttingen, students dissected out the same parasites from the caecum of a young girl who died of typhoid. Johann Georg Roederer, professor of obstetrics, examined the worms and identified them as roundworms, giving the description and the name Trichuris (Greek θρίξ/thríx, for hair, and οὐρά/ourá, tail). [13] However, Roederer mistook the thread-like head for the tail. [15]

Swedish biologist Carl Linnaeus, dubbed the "father of modern taxonomy", [16] came to learn of the worm from his accomplice Johann Beckmann, former student at Göttingen. Based on Beckman's report, Linnaeus described it as a worm related to the large human roundworm, Ascaris lumbricoides, which he had named in 1758. [17] In 1771, Linnaeus grouped them as teretes, literally roundworms, [18] and gave the first binominal name, Ascaris trichiura. [13] German zoologist Johann August Ephraim Goeze realised that Linnaeus classification was erroneous and created a new genus Trichocephalos (literally hair/thread headed) in 1782, correctly identifying that the hair/thread-like body was the head part. But he did not give the full scientific name. [13] Franz von Paula Schrank described the whipworm of pigs as Trichocephalus suis and that of mice as T. muris in 1788, [19] [20] [21] based on which he was the first to introduce the proper binominal name Trichocephalus hominis for the human parasite. Disagreement emerged as Karl Rudolphi renamed the human parasite as Trichocephalus dispar in 1802, and Johann Georg Heinrich Zeder made a separate genus and name Mastigodes hominines in 1803. [13]

American parasitologists tried to resolve the confusion in the scientific name by introducing a combination of the names created by Linnaeus and Schrank, making it Trichocephalus trichiura. This became the formal name from 1901 until British parasitologist Robert Thomson Leiper revised the name to incorporate the correct identification by Roederer, giving the name Trichocephalus trichiurus and credited the authorship to Linnaeus. Ignoring the objection to the universal use of Leiper's name, the International Commission on Zoological Nomenclature adopted it, and the full name with authority became Trichocephalus trichiurus (L., 1771) Schrank, 1788. [13] The original name "Trichuris" was rejected as it was general consensus that Roederer did not use it as a proper scientific named, creating a conflict that it could be either the genus or species name. In 1941, the Committee on Nomenclature under the American Society of Parasitologists reanalysed the whipworm taxonomy, with the conclusion:

Since the name Trichuris Roederer, 1761, clearly antedates all other technical names proposed since 1758 for the genus of the whipworms, this name should be employed, providing the requirements laid down in the International Rules of Zoological Nomenclature [sic, International Code of Zoological Nomenclature] are met by the original description. [22]

The 16th meeting of the American Society of Parasitologists approved the conclusion and declared that "Trichuris rather than Trichocephalus is the valid generic name." [23]

Life cycle

In spite of the description of whipworms in the 18th century, the life cycle began to be understood only two centuries later. It was in the 1950s that it was established that whipworms have direct life cycle, required no other animals (vectors or intermediate hosts for their transmission) and rather fragile eggs unlike most other helminths. [15] It is now known that all whipworm species have a similar general life cycle. [2] [24] Whipworm eggs are first ingested by the host. They eventually reach the duodenum of the small intestine, where the eggs ultimately hatch. The larvae from these eggs travel into the large intestine’s cecum. [25] For about four weeks, the whipworms feed on blood vessels located within the cecum. Eventually, the whipworms leave the cecum and begin to lay thousands of eggs. These unembryonated eggs are then released from the host through feces. The process from egg ingestion to release takes around 12 weeks. [26] The released eggs become embryonated in approximately nine to twenty-one days and are eventually ingested by another host. [27]

Whipworm eggs have thick, lemon-shaped, light yellow shells. Located on opposite ends of the shells are plugs that protect the eggs in unfavorable conditions such as rugged soil and the acidic environment of the small intestine. [26] The actual egg is covered by a vitelline membrane. [28] When the eggs first exit the uterus of their mother, they are composed solely of yolk granules. Over a period of 72 hours, the eggs undergo mitotic division into two blastomeres that are separated by a transverse cleavage. Two additional cleavages occur within at least 96 hours, so that the eggs are now composed of four cells each. Cellular division continues in this manner and the morula stage is reached within the next week. After a total of 21–22 days, the larvae become fully developed and will not hatch until ingested by a host. The larvae can live for a total of six months without the assistance of a host. The timeline of egg development can vary depending on the species. [28]

In domestic animals

Whipworms develop when a dog swallows whipworm eggs, passed from an infected dog. Clinical signs may include diarrhea, anemia, and dehydration. The dog whipworm (T. vulpis) is commonly found in the U.S. It is hard to detect at times, because the numbers of eggs shed are low, and they are shed in waves. Centrifugation is the preferred method. Several preventives are available by prescription from a veterinarian to prevent dogs from getting whipworm.

The cat whipworm is a rare parasite. In Europe, it is mostly represented by T. campanula, and in North America it is more often T. serrata. [29] [30] Whipworm eggs found in cats in North America must be differentiated from lungworms, and from mouse whipworm eggs that are just passing through.

T. campanula can be found in cats throughout the United States, having a whip-like shape, living in the large intestine and cecum of cats. The cat gets infected with T. campanula by ingesting food or water that is contaminated with the whipworm eggs. Once the cat ingests the infected eggs, they hatch and the larvae mature as adults in the large intestine, where they feed on the blood from the intestinal wall. T. campanula lays eggs that are passed in the feces of the infected cat, remaining alive in soil for years. The infection can be found by examining the feces of the infected cat. Also, blood can be found in the feces that can help in diagnosing of the infected cat. For prevention, cats should visit the veterinarian to get worming, having the feces inspected. [31]

Related Research Articles

<i>Ascaris lumbricoides</i> One of several species of Ascaris

Ascaris lumbricoides is a large parasitic worm that causes ascariasis in humans. A roundworm of genus Ascaris, it is the most common parasitic worm in humans. An estimated 807 million–1.2 billion people are infected with A. lumbricoides worldwide. People living in tropical and subtropical countries are at greater risk of infection.

<i>Trichuris trichiura</i> Parasitic roundworm that causes intestinal infection

Trichuris trichiura, Trichocephalus trichiuris or whipworm, is a parasitic roundworm that causes trichuriasis when it infects a human large intestine. It is commonly known as the whipworm which refers to the shape of the worm; it looks like a whip with wider "handles" at the posterior end.

<span class="mw-page-title-main">Trichuriasis</span> Infection by Trichuris trichiura (whipworm)

Trichuriasis, also known as whipworm infection, is an infection by the parasitic worm Trichuris trichiura (whipworm). If infection is only with a few worms, there are often no symptoms. In those who are infected with many worms, there may be abdominal pain, fatigue and diarrhea. The diarrhea sometimes contains blood. Infections in children may cause poor intellectual and physical development. Low red blood cell levels may occur due to loss of blood.

<i>Baylisascaris</i> Genus of worms

Baylisascaris is a genus of roundworms that infect more than fifty animal species.

<i>Ascaris</i> Genus of roundworms

Ascaris is a nematode genus of parasitic worms known as the "small intestinal roundworms", which is a type of parasitic worm. One species, Ascaris lumbricoides, affects humans and causes the disease ascariasis. Another species, Ascaris suum, typically infects pigs. Other ascarid genera infect other animals, such as Parascaris equorum, the equine roundworm, and Toxocara and Toxascaris, which infect dogs and cats.

Trichuris muris is a nematode parasite of mice. It is very similar to the human roundworm parasite Trichuris trichiura due to its immunological reactivity when crossed, and so is often used in related studies.

<span class="mw-page-title-main">Parasitic worm</span> Large type of parasitic organism

Parasitic worms, also known as helminths, are large macroparasites; adults can generally be seen with the naked eye. Many are intestinal worms that are soil-transmitted and infect the gastrointestinal tract. Other parasitic worms such as schistosomes reside in blood vessels.

<span class="mw-page-title-main">Helminthic therapy</span> Deliberate infestation with parasitic worms

Helminthic therapy, an experimental type of immunotherapy, is the treatment of autoimmune diseases and immune disorders by means of deliberate infestation with a helminth or with the eggs of a helminth. Helminths are parasitic worms such as hookworms, whipworms, and threadworms that have evolved to live within a host organism on which they rely for nutrients. These worms are members of two phyla: nematodes, which are primarily used in human helminthic therapy, and flat worms (trematodes).

The soil-transmitted helminths are a group of intestinal parasites belonging to the phylum Nematoda that are transmitted primarily through contaminated soil. They are so called because they have a direct life cycle which requires no intermediate hosts or vectors, and the parasitic infection occurs through faecal contamination of soil, foodstuffs and water supplies. The adult forms are essentially parasites of humans, causing soil-transmitted helminthiasis (STH), but also infect domesticated mammals. The juveniles are the infective forms and they undergo tissue-migratory stages during which they invade vital organs such as lungs and liver. Thus the disease manifestations can be both local and systemic. The geohelminths together present an enormous infection burden on humanity, amounting to 135,000 deaths every year, and persistent infection of more than two billion people.

Necatoriasis is the condition of infection by Necator hookworms, such as Necator americanus. This hookworm infection is a type of helminthiasis (infection) which is a type of neglected tropical disease.

<i>Toxocara canis</i> Species of roundworm

Toxocara canis is a worldwide-distributed helminth parasite that primarily infects dogs and other canids, but can also infect other animals including humans. The name is derived from the Greek word "toxon," meaning bow or quiver, and the Latin word "caro," meaning flesh. T. canis live in the small intestine of the definitive host. This parasite is very common in puppies and somewhat less common in adult dogs. In adult dogs, infection is usually asymptomatic but may be characterized by diarrhea. By contrast, untreated infection with Toxocara canis can be fatal in puppies, causing diarrhea, vomiting, pneumonia, enlarged abdomen, flatulence, poor growth rate, and other complications.

Capillaria philippinensis is a parasitic nematode which causes intestinal capillariasis. This sometimes fatal disease was first discovered in Northern Luzon, Philippines, in 1964. Cases have also been reported from China, Egypt, Indonesia, Iran, Japan, Korea, Lao PDR, Taiwan and Thailand. Cases diagnosed in Italy and Spain were believed to be acquired abroad, with one case possibly contracted in Colombia. The natural life cycle of C. philippinensis is believed to involve fish as intermediate hosts, and fish-eating birds as definitive hosts. Humans acquire C. philippinensis by eating small species of infested fish whole and raw.

<i>Trichuris suis</i> Species of roundworm

Trichuris suis is a whipworm; the variations in thickness of the anterior and posterior segments give the parasite the characteristic "whip-like" appearance. Adult females measure 6 to 8 cm and adult males 3 to 4 cm. T. suis eggs are oval and yellow-brown with bipolar plugs. T. suis is also used in helminthic therapy studies.

<i>Toxascaris leonina</i> Species of roundworm

Toxascaris leonina is a common parasitic roundworm found in dogs, cats, foxes, and related host species. T. leonina is an ascarid nematode, a worldwide distributed helminth parasite which is in a division of eukaryotic parasites that, unlike external parasites such as lice and fleas, live inside their host. The definitive hosts of T. leonina include canids and felines (cats), while the intermediate hosts are usually rodents, such as mice or rats. Infection occurs in the definitive host when the animal eats an infected rodent. While T. leonina can occur in either dogs or cats, it is far more frequent in cats.

Trichuris vulpis is a whipworm that lives in the large intestine of canines in its adult stages. Out of different types of worms, Trichuris vulpis is one of the smaller worms with a size ranging from 30–50 mm in length. As the name suggests, the worm has a whip-like shape with distinct features including a small, narrow anterior head, which is the digestive part of the worm, and a larger posterior tail, which is the reproductive part of the worm. Eggs from T. vulpis are oval shaped with bipolar plugs and contain a thick outer shell. Their sizes range from 72–90 μm in length and 32–40 μm in width. Because of their thick outer shell, T. vulpis eggs are very resistant to environmental extremes such as freezing or hot temperatures, thus allowing for their long viability in the outside world.

<span class="mw-page-title-main">Soil-transmitted helminthiasis</span> Roundworm infection contracted from contaminated soil

Soil-transmitted helminthiasis is a type of worm infection (helminthiasis) caused by different species of roundworms. It is caused specifically by those worms which are transmitted through soil contaminated with faecal matter and are therefore called soil-transmitted helminths. Three types of soil-transmitted helminthiasis can be distinguished: ascariasis, hookworm infection and whipworm infection. These three types of infection are therefore caused by the large roundworm A. lumbricoides, the hookworms Necator americanus or Ancylostoma duodenale and by the whipworm Trichuris trichiura.

Trichuris serrata, commonly known as a whipworm, is a nematode of the genus Trichuris first discovered in domestic Brazilian cats by Dr. Otto Friedrich Bernhard von Linstow in 1879. Since then, there have been reports of this species in North and South America, Australia, and the Caribbean islands. Information regarding the species' general life cycle and egg development can be seen in the Trichuris page.

Trichuris ovis, commonly known as a whipworm, is a nematode belonging to the genus Trichuris. This whipworm species was first discovered in 1795 and is known to infect sheep and goats. These organisms are capable of inhabiting any region that has the aforementioned hosts, as can be attested by the numerous reports of T. ovis findings throughout North and South America, Australia, Europe, and Asia. Information regarding the species' general life cycle and egg development can be seen in the Trichuris page.

Trichuris discolor, commonly known as a whipworm, is a nematode belonging to the genus Trichuris. The species was discovered by Otto Friedrich Bernhard von Linstow in 1906 and primarily infects cows. However, they can also infect sheep and goats. Like Trichuris ovis, T. discolor is known to be located in any region that their hosts are located. There have been specific reports of this species being found in Japan, Indo-Pakistan, and North America. Information regarding the species' general life cycle and egg development can be seen in the Trichuris page.

<span class="mw-page-title-main">Nematode infection in dogs</span> Threadworm infections of dogs are frequent

Nematode infection in dogs - the infection of dogs with parasitic nemamotodes - are, along with tapeworm infections and infections with protozoa, frequent parasitoses in veterinary practice. Nematodes, as so-called endoparasites, colonize various internal organs - most of them the digestive tract - and the skin. To date, about 30 different species of nematode have been identified in domestic dogs; they are essentially also found in wild dog species. However, the majority of them often cause no or only minor symptoms of disease in adult animals. The infection therefore does not necessarily have to manifest itself in a worm disease (helminthosis). For most nematodes, an infection can be detected by examining the feces for eggs or larvae. Roundworm infection in dogs and the hookworm in dogs is of particular health significance in Central Europe, as they can also be transmitted to humans (zoonosis). Regular deworming can significantly reduce the frequency of infection and thus the risk of infection for humans and dogs.

References

  1. ↑ Roberts, Larry S.; Janovy, Robert Jr. (2009). Foundations of Parasitology (8th ed.). McGraw Hill. p.  399. ISBN   9780073028279.
  2. 1 2 Else, Kathryn J.; Keiser, Jennifer; Holland, Celia V.; Grencis, Richard K.; Sattelle, David B.; Fujiwara, Ricardo T.; Bueno, Lilian L.; Asaolu, Samuel O.; Sowemimo, Oluyomi A.; Cooper, Philip J. (2020-05-28). "Whipworm and roundworm infections". Nature Reviews. Disease Primers. 6 (1): 44. doi:10.1038/s41572-020-0171-3. ISSN   2056-676X. PMID   32467581.
  3. ↑ Liu GH, Gasser RB, Nejsum P, Wang Y, Chen Q, Song HQ, Zhu XQ (2013). "Mitochondrial and nuclear ribosomal DNA evidence supports the existence of a new Trichuris species in the endangered François' leaf-monkey". PLOS ONE. 8 (6): e66249. Bibcode:2013PLoSO...866249L. doi: 10.1371/journal.pone.0066249 . PMC   3688784 . PMID   23840431.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  4. ↑ Fenwick, A (Mar 2012). "The global burden of neglected tropical diseases". Public Health. 126 (3): 233–6. doi:10.1016/j.puhe.2011.11.015. PMID   22325616.
  5. ↑ Knight, Robert (1984). "Morphological Differences in Trichuris ovis Associated with Different Host Species". The Journal of Parasitology. 70 (5): 842–843. doi:10.2307/3281784. JSTOR   3281784. PMID   6512651.
  6. ↑ Ketzis, Jennifer (2015). "Trichuris spp. infecting domestic cats on St. Kitts: identification based on size or vulvar structure?". SpringerPlus. 4 (115): 115. doi: 10.1186/s40064-015-0892-z . PMC   4355293 . PMID   25789211.
  7. ↑ Liu, Guo-Hua; Wang, Yan; Xu, Min-Jun; Zhou, Dong-Hui; Ye, Yong-Gang; Li, Jia-Yuan; Song, Hui-Qun; Lin, Rui-Qing; Zhu, Xing-Quan (2012). "Characterization of the Complete Mitochondrial Genomes of Two Whipworms Trichuris ovis and Trichuris discolor (Nematoda:Trichuridae)". Infection, Genetics and Evolution. 12 (2012): 1635–1641. doi:10.1016/j.meegid.2012.08.005. PMID   22926017.
  8. ↑ Jaeger, Lauren Hubert; Gijón-Botella, Herminia; del Carmen del Arco-Aguilar, María; Martín-Oval, Mercedes; Rodríguez-Maffiotte, Conrado; del Arco-Aguilar, Mercedes; Araújo, Adauto; Iñiguez, Alena Mayo (2016). "Evidence of Helminth Infection in Guanche Mummies: Integrating Paleoparasitological and Paleogenetic Investigations". Journal of Parasitology. 102 (2): 222–228. doi:10.1645/15-866. ISSN   0022-3395.
  9. ↑ Dufour, Benjamin; Segard, Maxence; Le Bailly, Matthieu (2016). "A First Case of Human Trichuriasis from a Roman Lead Coffin in France". The Korean Journal of Parasitology. 54 (5): 625–629. doi:10.3347/kjp.2016.54.5.625. ISSN   1738-0006. PMC   5127534 . PMID   27853119.
  10. ↑ Bianucci, Rafaella; Torres, Eduardo J Lopes; Santiago, Juliana MF Dutra; Ferreira, Luis Fernando; Nerlich, Andreas G; Souza, Sheila Maria Mendonça de; Giuffra, Valentina; Chieffi, Pedro Paulo; Bastos, Otilio Maria; Travassos, Renata; Souza, Wanderley de; Araújo, Adauto (2015). "Trichuris trichiura in a post-Colonial Brazilian mummy". Memórias do Instituto Oswaldo Cruz. 110 (1): 145–147. doi:10.1590/0074-02760140367. ISSN   0074-0276. PMC   4371230 .
  11. ↑ Zink, Albert; Samadelli, Marco; Gostner, Paul; Piombino-Mascali, Dario (2019). "Possible evidence for care and treatment in the Tyrolean Iceman". International Journal of Paleopathology. 25: 110–117. doi:10.1016/j.ijpp.2018.07.006. ISSN   1879-9825. PMID   30098946.
  12. ↑ Nerlich, Andreas G.; Egarter Vigl, Eduard; Fleckinger, Angelika; Tauber, Martina; Peschel, Oliver (2021). "Der Mann aus dem Eis: Lebensszenario und Pathologische Befunde aus 30 Jahren Forschung an der Gletschermumie „Ötzi"". Der Pathologe (in German). 42 (5): 530–539. doi:10.1007/s00292-021-00961-6. ISSN   0172-8113. PMID   34240239.
  13. 1 2 3 4 5 6 Skryabin, K.I. (1992-01-01), Skryabin (ed.), "Superfamily Trichocephaloidea Spassky, 1954", Key to Parasitic Nematodes, BRILL, pp. 382–471, doi:10.1163/9789004630437_018, ISBN   978-90-04-09137-5 , retrieved 2024-05-08
  14. ↑ Horton, J. (2024), "Trichuris trichiura (Human Whipworm)", Encyclopedia of Food Safety, Elsevier, pp. 699–703, doi:10.1016/b978-0-12-822521-9.00067-8, ISBN   978-0-12-822520-2 , retrieved 2024-05-08
  15. 1 2 Hurst, Rebecca J. M.; Else, Kathryn J. (2013). "Trichuris muris research revisited: a journey through time". Parasitology. 140 (11): 1325–1339. doi:10.1017/S0031182013001054. ISSN   1469-8161. PMC   3761323 . PMID   23965819.
  16. ↑ Calisher, CH (2007). "Taxonomy: what's in a name? Doesn't a rose by any other name smell as sweet?". Croatian Medical Journal. 48 (2): 268–270. PMC   2080517 . PMID   17436393.
  17. ↑ Grove, David I (1986). "Who discovered that intestinal worm infections could be diagnosed by finding eggs in the faeces?". Journal of the Royal Society of Medicine. 79 (11): 670–673. doi:10.1177/014107688607901118. PMC   1290536 . PMID   3540299.
  18. ↑ Katz, Michael; Despommier, Dickson D.; Gwadz, Robert W. (1989), "The Nematodes", Parasitic Diseases, New York, NY: Springer US, pp. 6–10, doi:10.1007/978-1-4684-0327-5_1, ISBN   978-1-4684-0329-9 , retrieved 2024-05-08
  19. ↑ Beer, R. J. S. (1973). "Studies on the biology of the life-cycle of Trichuris suis Schrank, 1788". Parasitology. 67 (3): 253–262. doi:10.1017/S0031182000046497. ISSN   0031-1820. PMID   4761766.
  20. ↑ Beer, R. J. (1976). "The relationship between Trichuris trichiura (Linnaeus 1758) of man and Trichuris suis (Schrank 1788) of the pig". Research in Veterinary Science. 20 (1): 47–54. ISSN   0034-5288. PMID   1257627.
  21. ↑ Feliu, Carlos; Spakulová, Marta; Casanova, Juan Carlos; Renaud, François; Morand, Serge; Hugot, Jean Pierre; Santalla, Francis; Durand, Patrick; Spakulova, Marta; Renaud, Francois (2000). "Genetic and Morphological Heterogeneity in Small Rodent Whipworms in Southwestern Europe: Characterization of Trichuris muris and Description of Trichuris arvicolae n. sp. (Nematoda: Trichuridae)". The Journal of Parasitology. 86 (3): 442. doi:10.2307/3284855.
  22. ↑ "Supplement to the Report of the Sixteenth Annual Meeting of the American Society of Parasitologists". The Journal of Parasitology. 27 (3): 279–282. 1941. ISSN   0022-3395.
  23. ↑ "American Society of Parasitologists: Sixteenth Annual Meeting, Philadelphia, Pa". The Journal of Parasitology. 27 (3): 276–279. 1941. ISSN   0022-3395.
  24. ↑ Olsen, Oliver (1974). Animal Parasites. New York: Dover Publications, Inc. pp. 497–502. ISBN   0486651266 . Retrieved 23 November 2015.
  25. ↑ Ransom, Brayton (1911). The Nematodes Parasitic in the Alimentary Tract of Cattle, Sheep, and Other Ruminants. Washington D.C.: US Department of Agriculture. pp. 111–117.
  26. 1 2 "The Biology of the Goat". GoatBiology.com. Karin Christensen. Retrieved 23 November 2015.
  27. ↑ "Intestinal Parasites - Whipworms". CAPCVet.org. CAPC. Archived from the original on 8 December 2015. Retrieved 23 November 2015.
  28. 1 2 Thapar, Gobind Singh; Singh, Suresh (1954). "Studies on the Life-History of Trichuris ovis (Abildgaard, 1795) (Fam. trichuridae: Nematoda)". Proceedings of the Indian Academy of Sciences, Section B. 40 (3): 69–88. doi:10.1007/BF03050426. S2CID   82067217.
  29. ↑ "Whipworms". VeterinaryPartner.com. 24 September 2007. Retrieved 2009-05-19.
  30. ↑ Hendrix CM, Blagburn BL, Lindsay DS (1987). "Whipworms and intestinal threadworms". Vet. Clin. North Am. Small Anim. Pract. 17 (6): 1355–75. doi:10.1016/s0195-5616(87)50006-7. PMID   3328393.
  31. ↑ Nash, Holly. "Whipworms (Trichuris serrata) in Cats". Veterinary Services Department. Retrieved 8 December 2011.
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