Neglected rare human parasitic infections: Part IV: Hirudiniasis Review Article Wael M Lotfy

Department of Community Health Nursing, Faculty of Nursing, Matrouh University, Egypt ABSTRACT Among all species of leeches, only true leeches especially jawed leeches are known to attack humans. These species are either freshwater or land dwellers. Freshwater leeches of medical importance may be divided into two groups: leeches which attack the mucous membranes (endoparasites), and those that attack the skin (ectoparasites). Some species of the former group have been incriminated in causing halazoun, while many species of the latter group were used in bloodletting. Leeches may be potential transmitters of human pathogens. The land leeches are much less fearsome than the aquatic leeches. However, the harm which land leeches cause to man and his domestic animals may be such that some infested foci become true leeches as human parasites and their medical uses, and the recommended methods of prevention almostand control. uninhabitable. This review summarizes current knowledge on the public health significance of Keywords: Annelida, leech, man, public health, segmented worms. Received: 17 January, 2021, Accepted: 22 February, 2021. Corresponding Author: Wael M Lotfy, Tel.: +20 1008154959, E-mail: [email protected] Print ISSN: 1687-7942, Online ISSN: 2090-2646, Vol. 14, No. 1, April, 2021.

True leeches (Hirudinea: Euhirudinea) are They colonise freshwater (Hirudidae or Hirudinidae) segmented worms belonging to the phylum Annelida. and terrestrial (Haemadipsidae and Xerobdellidae) Some species are marine, others are terrestrial, and environments[1,3,5,7]. The hematophagous leeches are the majority are freshwater dwellers[1]. They are usually not particular about their victims. Animals dorsoventrally compressed; the dorsal side is convex, are the primary hosts of such leeches and man is only accidently affected. Bites of jawed leeches are painless are characterized by a very elastic body capable of and result in a tri-radiate lesion which remains open contractionand the ventral and side extension. flattened Each or concave. individual True leech leeches has for a long period and heals slowly due to the hirudin two suckers for attachment: a small anterior one that anticoagulant peptide secreted by the salivary gland surrounds the oral opening, and a larger posterior of the leech. Leeches are temporary parasites because one. True leeches are hermaphrodites, but cross they attack victims only for feeding and drop off when fertilization between two individuals usually occurs they are engorged. They withdraw for prolonged to produce eggs that are deposited in groups, often in periods to sheltered places and slowly digest the a capsule called cocoon[2]. accumulated food[8,9]. systematics and taxonomy of euhirudins, thus it is infections with true leeches are available in the in needThere ofare reviewing several difficulties[3-5]. Euhirudins associated are generallywith the literature,Rare reportsbut only documenting fragmentary accidental information human is available. A literature search was carried out using leeches) and Arhynchobdellida (proboscisless Google Scholar. Textbooks were also searched online leeches).classified intoNoteworthy, two groups: Rhynchobdellidaall rhynchobdellids (proboscis are using Google Books. jawless, and many arhynchobdellids have jaws. Arhynchobdellids may be either predaceous Fresh water leeches carnivores or hematophagous and are divided into Aquatic leeches that threaten humans are divided two orders Pharyngobdellae (worm-leeches) and into endoparastites attacking the mucous membranes Gnathobdellae (jawed leeches). Members of the and ectoparasites attacking the skin. Members of the Pharyngobdellae do not have the ability to penetrate former group have weak jaws adapted for feeding a host’s tissue and suck blood. They are carnivorous on soft tissues such as the mucosa of the upper and equipped with a relatively large, toothless, mouth aerodigestive tracts. Members of the latter group have to ingest the prey. Members of the Gnathobdellae relatively powerful jaws that can penetrate the skin and attach anywhere on the external surface of the They are to a considerable degree sanguivorous body[10]. adaptedhave a jaw for filledthe engorgement with hundreds with of tinyrelatively sharp teeth.large amounts of blood[6]. Almost all species of medically Leeches which attack mucous membranes: The important leeches are found in the Gnathobdellae. jawed leeches that are adapted to cutting human (or

Personal non-commercial use only. PUJ copyright © 2021. All rights reserved DOI: 10.21608/PUJ.2021.58465.1104

15 PARASITOLOGISTS UNITED JOURNAL animal) thin mucous membranes instinctively locate to digest the accumulated blood meal. The digestive and reach these membranes. These leeches have been organs of L. nilotica are empty three to four weeks described in many sites as the oesophagus, conjunctiva, after the meal. However, the leech may survive long mouth, pharynx, larynx, nose, trachea/bronchi, vagina, periods of starvation[10,18,19]. bladder, and rectum. Human infections occur by acquiring the leech through drinking or bathing in Human hirudiniasis due to L. nilotica was described infested water[11-15]. by Savigny, who accompanied Napoleon’s Army to Egypt. In 1799 when the army marched from Egypt to The best-known species of this group is the Nile Syria across the Sinai, the soldiers drank water from leech, Limnatis nilotica,, found in the Middle East, leech-infested ponds. The leeches attached themselves North Africa, and southern Europe. It extends as a to the mucous membranes of their oral cavity and far as Iran, Tajikistan in the east and Azores in the throats. The soldiers suffered great torment by these west[16,17]. It is the most common species of leech in leeches which in some cases caused death from Egypt and Lebanon[16]. Limnatis nilotica inhabits lakes either suffocation or bleeding. A similar condition and streams, and rarely marshes. They usually crawl was experienced by British soldiers in the Sinai in on the bottom or attach themselves to stones or plants. World War I, and by American troops in Vietnam[34]. They swiftly swim in a snake-like fashion towards Infection is not common in humans, and sporadic the prospective animal or human victim. This species reports are available in the literature especially from rarely bites the skin; it usually reaches the mouth or the Middle East and adjoining countries[21]. Due to nostrils of the victim while drinking, then attaches the popularization of tap-water usage in endemic itself to the mucosa. It normally attacks mammals countries, cases of this kind of leech infection have and may attack the skin of frogs. However, it would rarely been reported in recent years[35]. eventually be swallowed and digested by frogs. On attachment, L. nilotica adheres its anterior sucker to In addition to L. nilotica, several other species the soft parts of the mouth or to the bucco-pharyngeal were reported to attack humans. Limnatis paluda [18,19]. In heavy infections, especially in animal hosts, leeches attach Eastern countries where it sometimes coexists with L. themselvescavities, leaving to the its bodygums, flopping under freelythe tongue or the wasnilotica identified[36-38]. In addition, in Central Dinobdella Asia and ferox in somewas reported Middle upper parts of the respiratory tracts as well[20-27]. In in Southeast Asia[39-41], and Myxobdella africana in sub- the human body, usually, a single leech settles in the Saharan Africa[42,43]. In the USA, Macrobdella decora[44], pharynx or in the upper part of the respiratory tract. M. sestertii[45], and M. diplotertia[46] may attack humans. The leech remains in the host for periods varying from Tyrannobdella rex attacks humans in Peru[47]. several days to several weeks[28], causing mechanical injury and anaemia[25-27]. The mechanical injury may Different approaches were applied for the safe result in swelling of the invaded organs, interfering removal of this group of leeches from an infected host. with swallowing or breathing[29]. Leeches can ingest These attempts vary from using forceps for immediate an amount of blood equivalent to 890% of their body extraction to the use of various tranquilizing agents weight[25]. for the leech and to relieve pain as the parasite is being removed[48,49]. Leech extraction from the larynx In some instances, a leech may remain in the may be performed by direct laryngoscopy, with the throat for days without provoking any symptoms. If patient under general or topical/local anesthesia. A swallowed to the stomach, the leech immediately dies. leech attached to the nostrils or the upper pharynx, The clinical presentations are laryngopharyngitis and is detached by application of 1:10,000 adrenalin, a crawling sensation in the throat called halazoun or 30% cocaine, or dimethyl phthalate. An alternative marrara[30,31]. The word halazoun in Arabic means technique is by irrigation with strong alcohol, saline, snail, but here it means that the causative organism turpentine, or vinegar to disconnect the leech. It is has a coiled appearance. Limnatis nilotica is one of the advisable not to grasp a leech with forceps because reported parasitic causes of halazoun in the Middle it has a soft slippery skin that may rupture easily[50]. East[27,30,32]. The leech can enter very narrow ducts, such as the human and animal urethra or cattle teat the leech so as not to leave parts of its mouth behind, canals[10,16,33] leadingIt is important to continuation to avoid firm of bleedingtraction whileand secondarypulling off the eye are available in the literature[12]. infection[51]. . Reports on cases of leech attachment to Species of L. imnatis can always attack victims Leeches that attack the skin: The ectoparasitic hematophagous leeches prefer to live in still or slowly one feed, as does Hirudo medicinalis, but does this atduring intervals its life. while It does attached. not fill When its digestive fully engorged, tract in the leeches detach themselves as the animal starts byflowing sudden freshwaters, swirling of water, although when specimens people and have animals been drinking again and thus escape to the outer water enteringcollected thefrom water fast flowing presumably streams. attract They leeches are activated by the source, where they hide in crevices or under stones impact produced. Then, the leeches attach themselves

16 Hirudiniasis Lotfy to the human or animal skin with whom they come in localities[74,75]. Nowadays, this species is protected contact and actively suck blood[8,9]. by international conventions and regulations[76]. The genus Poecilohdella (syn. Hirudinaria) includes ~ nine This group of leeches was used for medical species that may be indicated for bleeding of patients. purposes for centuries. Although its origin remains They can pierce the thickest skin and viciously attack depletion of blood dates far back to ancient Egypt workers in endemic foci suffer much from these obscure, the first recorded use of leeches for local species.animals andProbably man underthe most natural important conditions. species Rice are field P. of leeches in getting rid of bad blood became popular granulosa in the upper plains of India, P. manilensis in with(1567–1308 European BC). and During Arabian the Medieval physicians. period, Medicinal the use the lowlands of the whole tropical South-West of Asia, leeches were sold to physicians and patients while P. javanica is found in the Sunda Islands and by apothecaries[52-54]. During this period, leech Burma[77]. The medicinal leech H. medicinalis is found bloodletting was preferred to the painful mechanical in its natural habitats in Egypt, where all records of methods. The medical use of leeches reached its peak L. nilotica th century[53]. During the latter half of the same century, the medicinal use of leeches did thatthis speciesL. nilotica from thewhich Nile Rivernaturally refer toattacks it as mucous notin the conform first half with of 19 modern medicine concepts and it membranesand therefore has can been be misidentified.used for bloodletting It is noteworthy in Egypt was almost completely neglected[54]. However, there since ancient times[78]. Another leech that naturally attacks mucous membranes is the North American certain cases of thrombosis or phlebitis, and possibly medical leech Macrobdella decora. It is considered inremained selected some types justification of hypertension for the without use of theanaemia leech[55] in. H. medicinalis. In addition to jawed leeches, some proboscis leeches (rhynchobdellids) of using leeches was conducted to avoid thrombosis[56]. theless genusefficient Haementeria than have been used for medical In 1960, the first treatment of venous congested flaps purposes. These species are Haementeria officinalis in During the last few decades, medicinal leech Haementeria depressa and Haementeria ghilianii in South America[1,70]. and reconstructive surgery[54,57-62]. This came with the Central America, and both therapy became more acceptable in the field of plastic An easy method for removal of skin leeches is by and proteins in leech saliva: anti-thrombin (hirudin, bufrudin),identification anti-platelet of a variety (calin,of useful saratin), bioactive factor peptides Xa the oral sucker at the anterior end of the leech, then inhibitors (lefaxin), anti-bacterial (theromacin, the fingernail or another suitable object to detach theromyzin) and others[63,64]. In July 2004, the use of along the victim’s skin against the leech, the suction leeches as a medical aid gained approval by the FDA[65]. ofthe the posterior sucker's sucker. seal is As broken, the fingernail and the isjaws pushed are Although the medicinal leech is known as a long-time disconnected[79]. Although medically inadvisable, vector of all types of blood transmitted pathogens, common methods to remove attached leeches are to apparently it does not directly transmit pathogens via the injection of contaminated saliva[66-69]. Thus, it is such as alcohol, lemon juice, vinegar, insect repellent, advisable to discard a leech after it has been used for heatapply rub,a flame, or asome lit cigarette, carbonated salt, soap,drinks. or aBy chemical these a therapeutic purpose[69]. Probably bacterial infection applications the leech quickly detaches, regurgitating is the most common complication associated with its stomach contents into the wound. The leech vomit medicinal leeching and occurs in 2-36% of the patients. may carry some pathogens, and thus increase the risk Several bacterial strains have been encountered of infection[79]. Hydroxycitronellal which has a sweet in these infestations involving Aeromonas spp., Pseudomonas spp. and Vibrio spp.[60,64]. aquatic and land leeches[80]. floral aroma is an effective repellent against both The most common leeches used medically are Land leeches those of the genus Hirudo[70-73]. Among them, H. They are a group of hematophagous terrestrial medicinalis (syn. H. officinalis Savigny, 1822) was species belonging to different genera that are adapted reported in Britain and in southern Norway to the to life in damp forests with high humidity. Most species southern Urals, probably as far as the Altai Mountains. are found in tropical and subtropical areas of the Indo- Hirudo nipponia was used medically in East Asia, land species found in isolated foci in subtropical or Pacific Asia. There are ~10 unusual and lesser-studied Hirudo.including orientalis Far East (Transcaucasian district in Russian, countries, Japan, Iran, Korea, and and Europe[9]. Global warming may be blamed for China, Mongolia,H. Ryukyutroctina Islands (North-Western and Taiwan. Africa Besides, and thetemperate gradual regions extinction of Centralof European and Southland leeches America,[81]. Spain), H. uinquestriata (Australia), and H. verbana Up to now, the taxonomy of land leeches is not fully (SwitzerlandCentral Asia), and Italy to Turkey and Uzbekistan) understood, especially at the species level[4,5,82,83]. Land were recorded[70-73]. Hirudo medicinalis was once leeches are placed in the two families; Haemadipsidae common all over Europe. Leech collection, for about and Xerobdellidae. There are some 60 species of two centuries, resulted in its disappearance from many blood-feeding land leeches, ~50 belong to the family

17 PARASITOLOGISTS UNITED JOURNAL Haemadipsidae, and the rest are placed in the family Xerobdellidae[1]. Many genera of land leeches in the harmful effects on the environment and non-target family Haemadipsidae are found in tropical regions speciesvast forested[94]. Garments, areas involved,however difficulttight, do terrain not offer and

Madagascar, Sri Lanka, Malaysia, and Japan). Although recommended to prevent leech bite, either in the form haemadipsidssurrounding the exhibit Indian andhigh Pacific biodiversity, Oceans (especiallythey are ofsufficient an ointment protection applied in on enzootic the exposed foci. body Repellents parts or are by characterised by peculiar anatomical structures which make them distinct from related families[84-87]. cloth sleeves for legs was reported to give protection Members of this family feed on blood, except for a few upimpregnation to 90 days. of The the use clothes. of essential Repellent-impregnated oils and plant species of the genus Idiobdella that are adapted to extracts provided promising results[95] eating small snails[87]. Most of the known haemadipsids plant origin are preferred over synthetic repellents represent the genus Haemadipsa. The best studied as prolonged use of the latter could be harmful. Repellents due toof species are representatives of the genera Haemadipsa their toxicity and chemical nature[96]. and Philaemon. The genus Haemadipsa prevails in Asia and Indonesia, while the genus Philaemon prevails Conclusion: Several species of true leeches, either in Australia and South America[86-89]. Surprisingly, freshwater or land dwellers, can attack the human little is known about their biology, probably because body. Additionally, they may be potential transmitters biologists believe that they do not transmit human of human pathogens. Although medicinal leech therapy pathogens[90]. has been used for centuries, it has recently enjoyed a

In their natural habitats, land leeches are usually surgery. True leeches, especially land leeches, are found wandering along grasses or standing erect on amongcomeback the inmost the fieldneglected of plastic human and parasites. reconstructive More their posterior sucker and waving their bodies. Land studies are needed to be carried out in endemic foci to gain a better understanding regarding their biology passing man (or animal). They climb on to the lower and taxonomy. branchesleeches are of trees exceptionally or shrubs efficientto a height in of attacking about four a feet and wait for the victim on the edges of the leaves. Conflict of interest: To their surprise, people strolling in enzootic foci discover the leeches hanging on to their skin mostly There is no conflict of interest. on the legs or might feel trickling of blood after the REFERENCES leeches have fallen off. Land leeches can crawl on to their host even while moving. They rapidly creep 1. Sket B, Trontelj P. Global diversity of leeches between the tight clothes and even through the holes (Hirudinea) in freshwater. Hydrobiologia 2008; of the shoe laces aiming to reach the skin which they 595(1):129-137. pierce painlessly[91,92]. The genus Haemadipsa was 2. recorded to ingest ~ 1,000 mg of blood in 10 minutes[93]. Animals without backbone. 3rd The land leech sucks blood for 40-120 minutes and Buchsbaum R, Buchsbaum M, Pearse J, Pearse V. then drops off. Hundreds of leeches can attack a man 3. Trontelj P, Sket B, Steinbruck G. Molecular ed. Chicago, phylogeny IL: The within a short time. Blood continues to stream from ofUniversity leeches: ofcongruence Chicago Press; of nuclear 1987. and mitochondrial the wound for ~ 30 minutes washing away the hirudin rDNA data sets and the origin of bloodsucking. J Zool allowing the closure of the wound by a clot. Usually, the wound heals by itself, but, sometimes, if the affected 4. Borda E, Siddall ME. Arhynchobdellida (Annelida: place is not thoroughly cleaned, secondary infection Oligochaeta:Syst Evol Res Hirudinida):1999; 37:141-147. phylogenetic relationships may complicate the condition. In cases of massive and evolution. Mol Phylogenet Evol 2004; 30(1):213- infestation, the loss of blood may be considerable, and 225. it may even cause death, especially in animals. Land 5. Borda E, Oceguera-Figueroa A, Siddall ME. On leeches may attach themselves to the eye causing blindness. Areas dominated by leeches causing harm of terrestrial haemadipsoid leeches (Hirudinida: to man and his domestic animals become almost Arhynchobdellida:the classification, Hirudiniformes). evolution and Mol biogeography Phylogenet uninhabitable. During the World War II, the land Evol 2008; 46(1):142-154. 6. Hirudinea): Their structure, forests of Myanmar (formerly Burma) and Malaysia. Inleeches enzootic posed foci, a land problem leeches to disappear soldiers fightingduring the in dry the PergamonMann KH. Press; Leeches 1962. ( season, burrowing into the soil or creeping under logs, 7. physiology, ecology and embryology. Oxford, UK: to reappear when the damp conditions of the rainy season have returned. The land leeches are much less 2011;Elliott 4(1):21-41.JM, Kutschera U. Medicinal leeches: Historical fearsome than the aquatic ones[8,9,91,92]. 8. use, ecology, genetics and conservation. Freshw Rev leeches of families Hirudinidae and Haemadipsidae: Field control of land leeches with chemicals Keegan HL, Toshioka S, Suzuki H. Blood sucking Asian and insecticides was unsuccessful because of the Biomedical Reports of the 406 Medical Laboratory No. 16. US Army Medical Commend, Japan; 1968. 18 Hirudiniasis Lotfy 9. 29. Solomon E. Leech: An unusual cause of (laryngo- tracheal) obstruction. Ethiop Med J 1991; 29(3):141- 10. WitenbergSawyer RT. G.Leech Hirudiniases. biology and In: behaviour. van Hoeden Oxford, J, editor. UK: 142. Clarendon Press; 1986. 30. Witenberg G. What is the cause of the parasitic 1964; pp 710-719. laryngo-pharyngitis in the Near East ("Halzoun")? 11. Zoonoses. New York, NY: Elsevier Publishing Company Acta Med Orient 1944; 3:191-192. to leech in the vagina. Ann Trop Paediatr 1981; 1:189- 31. 190.Lepage P, Serufilira A, Bossuyt M. Severe anaemia due Clinostomum complanatum 12. Chung DI, Moon CH, Kong HH, Choi DW, Lim DK. child. Am J Ophthalmol 1997; 124(1):110-112. The first human case of 13. Alcelik T, Cekic O, Totan Y. Ocular leech infestation in a 32. (Trematoda: Clinostomidae) infection in Korea. Eur Arch Otorhinolaryngol 2001; 258(9):455-457. parasiticKorean J Parasitolpharyngitis 1995; known 33(3):219-223. as halzoun in the Middle 14. IdrisKaygusuz MA. I, YalcinVaginal S, Keleshirudiniasis E. Leeches from in theDhaherah larynx. East.Watson J Trop JM, Med Kerim Hyg RA.1956; Observations 59(7):147-154. on forms of Province, Oman: With a note on internal hirudiniasis. 33. Swanson LE. Leeches (Hirudineans) in the teat canals Sultan Qaboos Univ Med J 2006; 6(2):83-86. or udders of cattle. J Am Vet Med Assoc 1959; 135:278. 15. Sapmaz E, Toplu Y. Unusual cause of epistaxis; leech 34. Dillon Press; 1989. Med Sci 2014; 1(1):1-3. 35. Halton CM. Those amazing leeches. Minneapolis, MN: 16. infestation in the nose. Interlink Continental J Med effective method. Otolaryngol Head Neck Surg 2005 the blood-sucking leeches, Hirudinea Limnatis nilotica 132(5):Tseng CC, 814-815. Ho CY. Removal of a nasal leech: A safe and Oreviand Hirudo M, Eldor medicinalis A, Giguzin, and I, Rigbi its relationship M. Jaw anatomy to their of 36. feeding habits. J Zool 2000; 250(1):121-127. leeches taken by the U.S. Naval Medical Mission 17. Kuntz RE, Myers BJ. Helminths of vertebrates and (Annelida: Hirudinea). Arch Biol Sci 2006;58(1):21- 46(5):1071-1075. 24.Grosser C, Pesic V. On the diversity of Iranian leeches 37. to Yemen, Southwest Arabia. Can J Zool 1968; 18. Hirudinea). Senckenb Biol 1985; 66:135-152. of Limnatis nilotica (Savigny, 1820). Med Parazitol 38. Ruckert F. Egel aus den Levante-Ländern (Clitellata:Limnatis (Mosk)Shevkunova 1955; EA. 24(4):346-351. Certain data on biology of feeding paluda as a respiratory parasite in man: case report 19. Negm-Eldin MM, Abdraba MA, Benamer HE. First fromBoye SaudiES, Joshi Arabia. DC. JOccurrence Trop Med Hyg of 1994;the leech 97(1):18-20. record, population ecology and biology of the leech 39. Desilva PH, Anderson AA. A record of Dinobdella Ferox Limnatis nilotica in the Green Mountain, Libya. (Blanchard) (Hirudidae, Hirudinea) taken from the nasal cavity of man. Ann Trop Med Parasitol 1964; Zoologie) 2013; 49:37-42. 58:1-2. 20. Travaux de l’Institut Scientifique, Rabat (Série 40. Süsswasserblutegel als Parasiten im Menschen. Zbl infestation of man. Trop Geogr Med 1987; 39(1):94- BaktSeyfarth Hyg 1 Abt C. Orig Tropische 1917; 79:89-96. und subtropische 95.Campbell JR, Hart FL, Purnomo L. Nasal leech 21. Marschak A. Parasitological aspects of ENT practice in 41. Israel. Harefuah 1958; 54(2):47-48. report of nasal infestation by the leech, Dinobdella 22. Almallah Z. Internal hirudiniasis in man with Limnatis feroxMakiya. J UOEH K, Tsukamoto 1988; 10(2):203-209. M, Horio M, Kuroda Y. A case nilotica, in Iraq. J Parasitol 1968; 54(3):637-638. 42. 23. Al Safadi MM, El-Shimy NA. Freshwater leeches from anaemia and death due to the pharyngeal leech Yemen. Hydrobiologia 1993; 263:185-190. MyxobdellaCundall DB, africana Whitehead SM, Hechtel FO. Severe 24. Limnatis 80(6):940-944. nilotica from Oman (Hirudinea: Hirudinidae). Miscnea 43. . Trans R Soc Trop Med Hyg 1986; ZoolNesemann Hung 1997; H, Forster 11:11-14. R. First record of severe anaemia due to a pharyngeal leech (Myxobdella 25. africanaEstambale BB, Knight R, Chunge R. Haematemesis and Hoarseness due to leech ingestion. J Laryngol Otol Trop Med Hyg 1992; 86(4):458. 2000;25.Al-Hadrani 114:145-146. A, Debry C, Faucon F, Fingerhut A. 44. ) in a Kenyan child: a case report. Trans R Soc 26. hirudiniasis. J Parasitol 1959; 45(4):59. Ayadi A. Limnatis nilotica causing severe anaemia in 45. SmithMeyer DG. MC. The Another rediscovery unusual of Macrobdella case of sestertia erratic anCheikh-Rouhou infant. Med Trop F, Besbes (Mars) M, 2000; Makni 60(1):100-101. F, Chaabouni M, Whitman (Hirudinea: Hirudinidae). J Parasitol 1977; 27. 63(4):759-760. Severe anemia due to the pharyngeal leech Limnatis 46. niloticaAgin H, in Ayhan a child. FY, Türkiye Gulfidan Parazitoloji G, Cevik D, Dergisi Derebasi 2008; H. feeding response by the leech Macrobdella diplotertia 32:247-248. (Annelida:Trauth SE, NealHirudinea RG. Geographic) to wood range frog expansion and spotted and 28. salamander egg masses. J Ark Acad Sci 2004; 58:139- 141. literatureChen WC, Chienreview. CY, Eur Yang Arch CH, Otorhinolaryngol Li JH, Hwang CF. 2010;Nasal 47. 267(8):1225-1229.leech infestation: Report of seven leeches and Gomez GP, Beltran M, Lai YT, et al. Tyrannobdella rex Phillips AJ, Arauco-Brown R, Oceguera-Figueroa A,

19 PARASITOLOGISTS UNITED JOURNAL

n. gen. n. sp. and the evolutionary origins of mucosal 66. leech infestations. PLoS ONE 2010; 5(4):e10057. Exp Med 1957; 105:373-382. 48. 67. Shope RE. The leech as a potential virus reservoir. J the leech as a live foreign body: detection, precaution medical leech, Hirudo medicinalis andSaki N,treatment. Rahim F, NikaghlaghPak J Biol S,Sci Saki 2009; G. Meta 12(24):1556- analysis of [A]Dickinson 1984; 154:449-455. MH, Leut CM. Feeding behavior of the 1563. 68. Adams SL. The medical leech. , AL. pageJ Comp from Physiol the 49. annelids of internal medicine. Ann Intern Med 1988; Abdel-Salam NM. Leech infestation of man in Al-Taif, 109:399-405. SaudiEl-Dib Arabia. NA, El-Rahimy J Egypt SocHH, ParasitolEl-Matarawy 1987; OM, 17(2): Omar 615- SH, 69. 618. M. Experiments on the possible role of leeches as 50. vectorsNehili M, of Ilk animalC, Mehlhorn and H,human Ruhnau pathogens: K, Dick W, aNjayou light An unusual cause of respiratory distress: Live leech inPandey the larynx. CK, Sharma Anesth R, Analg. Baronia 2000; A, Agarwal 90(5):1227-1228. A, Singh N. 80(4):277-290. 51. 70. and electron microscopy study. Parasitol Res 1994; laryngeal leech: A safe and effective method. Am J OtolaryngolUygur K, Yasan 2003; H, 24(5):338-340. Yavuz L, Dogru H. Removal of a 209.Eldor A, Orevi M, Rigbi M. The role of the leech in 52. Davis A, Appel T. Bloodletting instruments in the 71. Utevskymedical SY, therapeutics. Trontelj P. A Blood new species Rev 1996; of the 10(4):201- medicinal National Museum of History and Technology. leech (Oligochaeta, Hirudinida, Hirudo) from Trans- Arlington, MA: The Printers’ Devil; 1993. 53. Thear MJ. Leeches in medicine. Aust N Z J Surg 1998; Hirudo 68:292-295. 72. UtevskyCaucasia S, and Zagmajster an identification M, Atemasov key forA, Zinenko the genus O, 54. Whitaker IS, Izadi D, Oliver DW, Monteath G, Butler Utevska. Parasitol O, Utevsky Res A,2005; Trontelj, 98(1):61-66. P. Distribution and PE. Hirudo medicinalis and the plastic surgeon. Br J status of medicinal leeches (genus Hirudo) in the Plast Surg 2004; 57(4):348-353. Western Palaearctic: anthropogenic, ecological, or 55. Physicians, Sanitarians and Medical Zoologists. 3rd ed. 2010; 20(2):198-210. FaustPhiladelphia, EC. Human PA: Lea Helminthology:& Febiger; 1949. A Manual for 73. Tronteljhistorical P, effects? Utevsky Aquat SY. Phylogeny Conserv andMar phylogeography Freshw Ecosyst 56. of medicinal leeches (genus Hirudo): fast dispersal treated by application of leeches. Br J Plast Surg 1960; and shallow genetic structure. Mol Phylogenet Evol 13:187-192.Deganc M, Zdravic F. Venous congestion of flaps 2012; 63(2):475-485. 57. 74. of leeches in plastic and reconstructive surgery. J Oryx 1981; 16(02):165-168. Kraemer BA, Korber KE, Aquino TI, Engleman A. Use 75. ElliottSawyer JM, RT. Tullett Why we PA. need The status to save of the the medicinal medicinal leech. leech 58. Hirudo medicinalis in Europe and especially in the TheReconstr use of Microsurg the medicinal 1988; leech, 4(5):381-386. Hirudo medicinalis, in theMumcuoglu reconstructive KY, Pidhorz plastic C, Cohen surgery. R, Ofek Internet A, Lipton J Plast HA. 76. Surg 2007;4(2). taxonomy:British Isles. Molecular Biol Conserv systematics 1984; 29:15-26. of the medicinal 59. leechTrontelj (genus P, Utevsky Hirudo SY.). Mol Celebrity Phylogenet with aEvol neglected 2005; therapy. New York, NY: Georg Thieme; 2007. 34(3):616-624. 60. GreenMichalsen PA, A,Shafritz Roth M,AB. Dobos Medicinal G. Medicinal leech use leech in 77. Tan E. A new species of the genus Poecilobdella microsurgery. J Hand Surg Am 2010; 35(6):1019- Hirudinea, 1021. Hirudinidae). Acta Zootaxonomica Sinica 2006; 61. 4:790-793.from Guangdong and Hainan, China ( 78. El-Shimy N. Distribution of the medicinal leech, practicalPorshinsky review. BS, SahaJ Postgrad S, Grossman Med 2011; MD, 57(1):65-71. Beery Ii PR, Hirudo medicinalis, in the Middle East. Zool Middle 62. Stawicki SP. Clinical uses of the medicinal leech: a East 1986; 1(1):154-155. leeches in reconstructive plastic surgery. Evidence- 79. Wittke-Michalsen E. The technique of leech therapy. basedMumcuoglu complementary KY. Recommendations and alternative for themedicine. use of leech therapy. New York, NY: Thieme Medical 63. Publishers;In: Michalsen 2007. A, Roth M, Dobos G (Editors). Medicinal histochemistryeCAM 2014; 2014:205929. of the salivary complex of the 80. Murdock JW. State-of-the-art study on leech repellents. giantSawyer leech RT, DamasHaementeria D, Tomic ghilianii MT. Anatomy (Hirudinea and, 81. 425. landColumbus, leech: OH: biology Battelle and Memorial DNA-based Institute; taxonomy 1963. of a 64. AbdualkaderRhynchobdellida). AM, ArchGhawi Zool AM, Exp Alaama Gen 1982; M, Awang 122:411- M, rareKutschera species U, that Pfeiffer is threatened I, Ebermann by climate E. The Europeanwarming. Merzouk A. Leech therapeutic applications. Indian J Naturwissenschaften 2007; 94(12):967-974. Pharm Sci 2013; 75(2):127-137. 82. 65. leeches from Taiwan, Haemadipsa rjukjuana comb. n.,Lai a YT,new Nakano record for T, ChenHaemadipsa JH. Three picta species Moore, ofand land an Rados C. Beyond bloodletting: FDA gives leeches a medical makeover. FDA Consum 2004; 38(5):9.

20 Hirudiniasis Lotfy

updated description of Tritetrabdella taiwana (Oka). 89. Zookeys 2011; 139:1-22. ME. Pyrosequencing the salivary transcriptome 83. et ofKvist Haemadipsa S, Brugler interrupta MR, Goh TG, Giribet G, Siddall al Haemadipsa rjukjuana Haemadipsidae): anticoagulant diversity and insight Won(Hirudiniformes: S, Park BK, Kim Haemadipsidae) BJ, Kim HW, Kang in GageoJG, Park Island, TS, into the evolution of anticoagulation (Annelida: capabilities Clitellata: in . Molecular identification of leeches. Invert Biol 2014; 133(1):74-98. 84. Moore JP. Leeches (Hirudinea) from the Hawaiian 90. Smythies BE. Leeches of Borneo. Sarawak Mus J 1959; Korea. Korean J Parasitol 2014; 52(2):169-175. 13:279-294. in the Bishop Museum collection. Occas Pap Bernice P 91. Moore JP. Arhynchobdellae. In: Harding WA, Moore BishopIslands, Mus and 1946;two new 18:171-191. species from the Pacific region JP (Editors). The Fauna of British India: Hirudinea. 85. 92. Moore JP. Leeches from Borneo with descriptions of Ringuelet RA. Nuevos taxia de hirudineos neotropicos newLondon, species. UK: Taylor Proc Acadand Francis; Nat Sci 1927. Philadelphia p. 97-295. 1929; Nov.con la Physis redefinicion 1972; 31:193-201. de Semiscolecidae y la descripcion 81:267-295. 86. de Cylicobdellidae fam. Nov. y Mesobdellidae fam. 93. Harrison JL. Leeches. Med J Malaya 1953; 8(2):180- of the land leeches (Hirudinoidea: Haemadipsoidea 185. superfam.Richardson nov).LR. A contributionActa Zool Acad to the Sci general Hung zoology 1975; 94. 21:119-152. leeches. Def Sci J 2002; 52(1):73-76. 87. 95. Nath DR, Das NG, Das SC. Bio-repellents for land leeches in the Seychelle Islands, and a consequential revisionRichardson of the LR. status On the of zoologicallandleeches nature in Madagascar of land- 131.Nath DR, Das NG, Das SC. Persistence of leech (Hirudinea 96. Skinnerrepellents WA, on cloth. Johnson Indian HL. J Med The Res design 1993; 97(A):128-of insect 92:837-866. repellents. New York, NY: Academic Press; 1980. 88. Nybelin O.: Haemadipsoidea).Nesophilaemon n. Rev g. Zoolfur Philaemon Afr 1978; skottsbergi L. Johansson aus den Juan Fernandez Inseln. Zool Anz 1943; 142:249-250.

21