Acanthocheilonema

Acanthocheilonema is a genus within the family Onchocercidae which comprises mainly tropical parasitic worms.[1] Cobbold created the genus Acanthocheilonema with only one species, Acanthocheilonema dracunculoides, which was collected from aardwolf (Proteles cristatus: Hyaenidae) in the region of South Africa in nineteenth century.[2] These parasites has a wide range of mammalian species, namely Carnivora, Macroscelidea, Rodentia, Pholidota, Edentata, and Marsupialia. Although many species among several genera of filarioids exhibit high degree of endemecity in studies done on mammalian species in Japan region. [3] [4] However, no concrete evidence has confirmed any endemic species in the genus Acanthocheilonema.

Acanthocheilonema
Scientific classification
Kingdom: Animalia
Phylum: Nematoda
Class: Chromadorea
Order: Rhabditida
Family: Onchocercidae
Genus: Acanthocheilonema

There are about fifteen well characterized parasitic species found in genus Acanthocheilonema. A. delicata n. sp. (2013), A. dracunculoides (Cobbold 1870), A. filaria (Kou, 1958), A. mansonbahri (Nelson, 1961), A. mephitis (Webster and Beauregard, 1964), A. odendhali (Perry, 1967), A. pachycephalum (Ortlepp, 1961), A. pricei (Vaz and Pereira, 1934), A. procyonis (Price, 1955), A. reconditum (Grassi, 1889), A. sabanicolae (Eberhard and Campo-Aasen, 1986), A. setariosa (Mönnig, 1926), A. spirocauda (Leidy, 1858), A. viteae (Krepkogorskaja, 1933), and A. weissi (Seurat, 1914) are the well characterized parasitic species found all around the world in variety of hosts.[5] Some of the crucial parasites that affect a wide range of host species are discussed below.

Acanthocheilonema delicata

Acanthocheilonema delicata was discovered and characterized from an endemic badger species (Meles anakuma) in Japan. [5] The researchers identified the DNA sequences of [[mitochondrial cytochrome c oxidase subunit 1 (cox1) gene in the Japanese badgers. Morphologically, filarioids analyzed were identified as thin, small and delicate and in females the length was longer (twice as in males). Anterior of the filarioids is slightly bulbous having two sets of four papilla (worms) and amphids. They possess distinct buccal cavity with buccal capsule consisting of a thick buccal ring. The esophagus is divided into short anterior muscular portion and long, posterior glandular portion.[5] Caudal extremity in both males and females consists of three conical lappets. The location of the parasitic adult worms in the host species (Meles anakuma) was found to be the subcutaneous connective tissue. Whereas, the microfilaria was found in the skin. Data taken from the Genbank of fourteen species of genus Acanthocheilonema compared to the newly found species for possible similarities and distinctions shown in the table below:

comparison of morphological characteristics of Acanthocheilonema parasites
Species →A. delicataA. dracunculoidesA. odendhaliA. reconditumA. spirocaudaA. viteae
Body LengthFemale-22–38; Male-10–16μmFemale-38.5–45.2; Male-21.7–24μmFemale-100-150; Male-46-64μmFemale-20.7-25.5; Male-9.3-17.1μmFemale-155; Male-87μmFemale-49μm; Male-38μm
Body width at mid-bodyFemale-85-140;Male-60-85μmFemale-220-280;Male-140-160μmFemale-348-415;Male-228-281μmFemale-146-168;Male-92-100μmFemale-660;Male-400μmFemale-230-350;Male-155-165μm
Total esophagus lengthFemale-3000–4125;Male-2520–3350μmFemale-1940–2500;Male-1960–2170μmFemale-1782–2197;Male-1890–2251μmFemale-2040–2340;Male-1860–2040μmFemale-1300–1800;Male-1900–2000μmFemale-1370-1570;Male-1600-1660μm
TailFemale-167–250;Male-113–162μmFemale-240–395;Male-140–180μmFemale-214–322;Male-147–245μmFemale-180–300;Male-80–145μmFemale-260;Male-230μmFemale-320–470;Male-280μm
No. of terminal lappets3333Female-3; Male-43
Microfilariae width7-9μm4.5-5.2μm3.5μm4.5μm4-4.5μm4.5μm
Microfilariae body length153–180μm121-218μm231-249μm270μm266-302μm180-200μm
Host animalMeles anakumaProteles cristatus and spotted hyaenaZalophus californianusCrocuta crocuta and Hyaena hyaenaPhoca vitulina concolorMeriones libycus
Parasitic location of adult wormsSubcutaneous connective tissuePeritoneal cavityIntermuscular fasciaSubcutaneous connective tissuePulmonary artery and right ventricleSubcutaneous tissue
Parasitic location of microfilariaeSkinBloodbloodbloodbloodblood
localityJapanKenyaCalifornia, USAItaly, India, USA, Kenya, JapanThe coast of Maine, USAIran
Reference[5][6] [7][[8]] [[9]][[10]][[11]] [[12]][[13]] [[14]] [[15]]

Acanthocheilonema dracunculoides

Acanthocheilonema dracunculoides Cobbold, a species discovered in 1870, is a nematode parasitic worm particularly found in domestic dogs and other carnivores like aardwolf, spotted hyaena and red fox.[16] These parasites can be located on various continents like Europe, Asia and Africa.[17] it is known to be endemic in Morocco, Algeria, Tunisia, Mali, Niger, Democratic Republic of Congo, Sudan, Somalia1, Kenya, Tanzania and South Africa.[18][19][20][21] [22][23][24] This parasite follows an indirect life cycle. In the carnivore species, the male and female parasite tend to be biased to exist mainly in the peritoneal cavity. [25] Males are typically shorter and are 15–32 mm long and 0.1–0.2 mm wide, whereas females are almost double, standing at 30–60 mm long and 0.1–0.3 mm wide in diameter. [26][27] Sexually mature female parasites of A. dracunculoides are viviparous, they produce L1-stages, known as microfilariae, which eventually appear in the peripheral blood. Microfilariae are unsheathed and measure 185–276 µm (length) by 4.2–6 µm (width)[28] [29] Although, the final host is the carnivores for A. dracunculoides there are some other intermediate hosts that are involved in the parasite life cycle. Louse fly Hippobosca longipennis and the hard tick Rhipicephalus sanguineus, also known as dog tick, have been identified as intermediate hosts that helps the parasite to complete its life cycle.[30] Although, Acanthocheilonema dracunculoides has prior reputation of not being endemic parasite in the domestic dogs, recent evidences of the presence of parasite in the domestic animals and show some signs of pathogenicity. As mostly these parasites are considered innocuous in the dogs, recent studies and evidence from Spain suggests that the parasite is not completely harmless and innocuous in the domestic dogs as believed earlier. [31] [32]

The discovery of Acanthocheilonema parasites in the non-endemic species has triggered more research in this field. Dirofilaria immitis, D. repens, Acanthocheilonema dracunculoides and A. reconditum are the common species that have been known to be found in canine filarial nematodes. These nematodes present blood circulating microfilariae which are differentiated to the species level using the techniques like PCR and by acid phosphatase activity patterns.[33] A. reconditum and A. dracunculoides live in the peritoneal cavity and adipose tissue of the host species and are less pathogenic,[34] however D. immitis and D. repens are considered to be the emerging agents of parasitic zoonoses and are continuously expanding their ranges in the European. areas.[35]

Acanthocheilonema odendhali

The filarial worm Acanthocheilonema odendhali was first discovered in 1967 from the California California sea lion Zalophus californianus. [36] This species was found inhabiting the intermuscular fascia and thoracic and the abdominal cavities. Initially this species was described in the Dipetalonema genus as Dipetalonema odendhali, however due to later evidences it was transferred to the genus Acanthocheilonema. [37] A. odendhali was subsequently found in other marine species like Steller sea lion (Eumetopias jubatus) and northern fur seal (Callorhinus ursinus).[38] [39] Besides the A. odendhali, other filarioidean species such as A. spirocauda, commonly known as heart-worm has also been identified as parasitic in phocids.[40][41]

A. odendhali was primarily reported in the northern fur seals on the island of Pribilof Archipelago in 1967.[42] Prior to that two scientists Mark C. Keyes and Eugene T. Lyons had discovered the microfilariae in the blood of subadult male seals and adult filarioids and microfilariae in the samples collected from the blubber, fur, and the skin from these male seals.[43] In these studies, the prevalence and the intensity of these species were not examined. The life cycle of A. odendhali is still unknown. However, according to the National Marine Mammal Laboratory, Northwest and Alaska Fisheries Center (NWAFC) repots, some blood sucking flies or insects that infests the wounds are some potential intermediate hosts (vectors) in their life cycle.[44] Pathogenicity of A. odendhali was however not studied in these experiments and research but this parasite is considered as non-pathogenic.[45] In 2011 and 2012, a studied that investigated helminths of northern fur seals on Saint Paul Island in Alaska discovered thatA. odendhali was a parasite on the northern fur seals.[46] Another research done by the same researchers investigated the intensity and prevalence of the parasite and discovered that prevalence of adultA. odendhali parasites in the fur seals was 18 percent, whereas the intensity depends on the individual host species and the seven parasite specimens found in the parasite. Average intensity of infection was approximately 1.32 ±0.83 SD, whereas the abundance was found 0.24 SD.[46]

Acanthocheilonema reconditum

Acanthocheilonema reconditum is a non-pathogenic canine helminth parasite of the specialized connective tissue. It is distributed in the same endemic areas as D. immitis, which is also known as heart-worm.[47][48] Although it is endemic to some areas mentioned earlier, but the parasite is widely distributed as it has been identified in other species and around different continents. Dogs are frequently parasitized by the filarids. This transmission is usually carried out by the flea species and lice species. Flea vectors include species such as Ctenocephalides canis, Pulex irritans, Pulex simulans, and Echidnophaga gallinacea, whereas the lice species include Linognathus setosus and Heterodoxus spiniger. These vectors are infected with the A. reconditum parasite with the microfilariae during the blood repast in a parasitized dog. These species acts as intermediate hosts in completing the life cycle of this parasite.[49]

These microfilariae develop onto a infectious stage during the L3 (larvae stage 3) stage in the digestive tract of these vectors from where they can be inoculated into the new host. The third stage larvae could be found as soon as 7 days after the appearance of the vectors on the donor host species.[50] (L3) Once it enters the new host species, the microfilariae develops into the adult stage. Most of these adult stage parasites are located in the subcutaneous tissue. [51] Although the infection by A. reconditum does not exhibit any clinical signs, a treatment to limit dissemination is primarily recommended. Recent studies of A. reconditum occurrence in the southern regions of Italy has shown prevalence of this parasite as high as 13.3% with an annual incidence rate of 5.9%, which was observed in naturally exposed dogs. [52] Recent experiments has enhanced the scientific knowledge and the biology and ecology of this parasite. The full development of microfilariae occurs in the experimental infected cat flea Ctenocephalides felis felis in about 15 days. localization and size of this parasite in this infected flea suggests the possibility that this might act as an intermediate host throughout the ingestion of the infected fleas rather than inoculation of the blood meal on dogs.[52][49] Moreover, Ivermectin (0.25 mg/kg) is a drug that is preferred to treat infection by this parasite.[53] As Microfilariae of this parasite are mainly found in the blood, they are often mistaken for other parasites like Dirofilaria immitis. It is therefore crucial to identify and distinguish between them using modified knott procedure. [54]

Acanthocheilonema spirocauda

Acanthocheilonema spirocauda, also known as seal heartworm, is a filarial parasite that primarily infects the phocid seals, including Phoca vitulina (Harbor seal). The Heartworm was originally described as Filaria spirocauda by Leidy.[55] Eventually Acanthocheilonema was raised to generic level and this species settled under this genus, and a researcher Anderson presented its current name.[56] A. spirocauda is found in the heart of the seals, and that is why is got its name 'Heartworm'. [56] While there is no significant threat to the seal populations due to this parasite as of now, however the infection with this parasite can result in pathological consequences like in the case of D. immitis, which includes the characteristics such as anorexia, fatigue, heart and lung complications, and potentially death. [57] Researchers suggest that these parasites share strong evolutionary basis with its phocid hosts about some 45 million years ago[57] It is believed to be transmitted via the seal louse (Echinophthirius horridus). [58] The prevalence of the parasite in the host species is approximately 8.8%, and intensity ranges up to 44 specimens per heart.[59]

Additional researchers have investigated its additional potential hosts and global distribution patters of this parasite. Studies discovered some additional hosts of this parasite that include ribbon seal P. fasciata, harp seal P. groenlandica, ringed seal P. hispida, Baltic ringed seal P. h. botnica, Ladoga seal P.h. ladogensis, spotted seal P. largha, hooded seal Cystophora cristata, and bearded seal Erignathus barbatus.[60] The primary sites of infection in the hosts are Right and left ventricle of the heart, pulmonary vein, pulmonary artery, and vena cava.[59] These parasites are widely distributed around the globe. They can be found in Northern Hemisphere, and Holarctic distribution. [60][61] The present localities of A. spirocauda includes Danish North Sea (Agger Tange), Limfjord (Thy), Skagerrak (Lysekil) and Kattegat (Rungsted, Lille Vrøj) and the Baltic Sea (Lunds høje, Falster).[59]

Acanthocheilonema viteae

A. viteae is a filarial nematode that infects the rodents species.[62] A. Viteaeis also used as a model species in the research experiments in order to study Human filarial infections.[63] The natural host for this parasite are gerbils, whereas the experimental hosts include hamsters, jirds (Meriones unguiculatus, also known as Mongolian gerbils), and Mastomys species.[64] The vector that aids to finish its life cycle is a soft tick named, Ornithodoros tartakovskyi (natural) andOrnithodoros moubata(experimental vector).[65] The adults of A. Viteae resides in the deep Subcutaneous tissue, where as the microfilariae circulates in the blood.[66] These worms are known to modulate the host immunological systems, however they do not prohibit the immunological pathways entirely. It renders them the increased survival. Excretory product called ES-62 is secreted by A. Viteae that is homologous to the one produced by the humans but not parasitic. ES-62 molecules tend to exhibit anti-inflammatory actions using Phosphorycholine moiety to affect the intracellular pathways that are associated with the antigen receptors and TLR dependent cell responses.[67]

In nature, during the 3rd larvae infected stage, A. Viteae parasites are transferred to their mammalian hosts with the aid of vector Ornithodoros tartakovskyi. In the mammalian host, the L3 stage develops to mature adults and generates the microfilariae, which are again ingested by ticks. After reaching L3 parasites transfers to mammalian hosts via arthropods mouth parts.[68] [69] Various stages of A. Viteae has two Chitinase protein bands, one of 205 kDa and 68 Kda. Studies reveal that the 205 kDa band of stage L3 was an oligomer formed of 68kDa monomers.[70] Chitin has been reported as a component of the eggshells of these nematodes[71] Chitinase plays a vital role in 3rd larvae stage (L3) and female worms, as its inhibition during these stages leads to have increased mortality. There are no safe and efficient drugs to eliminate these infections so far but Chitin is seen as a potential target for the development of anthelmintic drugs and vaccines.[72] Intracellular bacteria Wolbachia are prevalent among the different species of nematodes. However, Wolbachia is absent in Acanthocheilonema viteae. Since, the A. Viteae lacks the Wolbachia, it is widely used as the negative control for the experiments investigating the bacterium.[73] Their role in the pathology of filarial infections and symbiotic nature with host makes it potential target to intervene in filarial infections in the humans. [74]

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