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| REVIEW ARTICLE |
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| Year : 2011 | Volume
: 57
| Issue : 1 | Page : 65-71 |
Clinical uses of the medicinal leech: A practical review
BS Porshinsky1, S Saha2, MD Grossman3, PR Beery II1, SPA Stawicki1
1 Department of Surgery, Division of Critical Care, Trauma, and Burn, The Ohio State University Medical Center, Columbus, Ohio, USA
2 Department of Plastic Surgery, The Ohio State University Medical Center, Columbus, Ohio, USA
3 St Luke's Regional Level I Trauma Center, Bethlehem, Pennsylvania, USA
| Date of Submission | 29-Apr-2010 |
| Date of Decision | 10-Oct-2010 |
| Date of Acceptance | 04-Nov-2010 |
| Date of Web Publication | 31-Jan-2011 |
Correspondence Address:
SPA Stawicki
Department of Surgery, Division of Critical Care, Trauma, and Burn, The Ohio State University Medical Center, Columbus, Ohio
USA
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/0022-3859.74297
The medicinal leech, Hirudo medicinalis, is an excellent example of the use of invertebrates in the treatment of human disease. Utilized for various medical indications since the ancient times, the medicinal leech is currently being used in a narrow range of well-defined and scientifically-grounded clinical applications. Hirudotherapy is most commonly used in the setting of venous congestion associated with soft tissue replantations and free flap-based reconstructive surgery. This is a comprehensive review of current clinical applications of hirudotherapy, featuring a comprehensive search of all major medical search engines (i.e. PubMed, Google Scholar, ScientificCommons) and other cross-referenced sources. The authors focus on indications, contraindications, practical application/handling of the leech, and therapy-related complications.
Keywords: Complications, contraindications, hirudotherapy, indications, medicinal leech
How to cite this article:
Porshinsky B S, Saha S, Grossman M D, Beery II P, Stawicki S. Clinical uses of the medicinal leech: A practical review. J Postgrad Med 2011;57:65-71 |
How to cite this URL:
Porshinsky B S, Saha S, Grossman M D, Beery II P, Stawicki S. Clinical uses of the medicinal leech: A practical review. J Postgrad Med [serial online] 2011 [cited 2023 Jun 4];57:65-71. Available from: https://www.jpgmonline.com/text.asp?2011/57/1/65/74297 |
| :: Introduction and Historical Perspective | |  |
The medicinal leech, Hirudo medicinalis, is one of the few examples of the use of invertebrates in the treatment of human disease. The word leech is likely derived from the old English word for physician, laece. [1] Leech therapy has been administered since ancient times. A painting in an Egyptian tomb from around 1500 BCE depicts the use of medicinal leeches. [2],[3] Hirudotherapy has also been reported by Themison of Laodicea in the year 50 BCE. [4] Leech therapy played an important role during the seventeenth and eighteenth centuries, at which time it was used for medicinal "blood-letting" and "purification" - a practice believed to cure a variety of ailments from gout to headaches. [3],[5],[6] The use of leeches likely gained popularity among practitioners of phlebotomy due to its ability to achieve more gradual rate of blood loss. According to some, the therapy may have been so popular that leech shortages were reported in Europe during that time. [3] Enthusiasm for leech therapy waned in the late nineteenth and early twentieth century, but scientific interest in Hirudo medicinalis continued. [5],[6] In the early 1880s Haycraft first noted the antithrombotic properties of leech saliva and Jacoby discovered the anticoagulant factor in leech saliva and named it hirudin in 1904. [7] Hirudotherapy re-emerged as an adjunct to plastic, reconstructive, and trauma surgery in the 1970s and 1980s. [3],[5],[6] In the 1980s, French microsurgeons began using leeches to assist with distal digital replantation involving arterial repairs only. [8] Today, the medicinal leech is often used to treat venous congestion in the settings of microvascular replantations, reconstructive surgery, and traumatology. [2],[9],[10] This review focuses on the biology and current therapeutic applications of the medicinal leech.
| :: Methods | | |
A comprehensive search of major medical search engines (i.e. PubMed, Google Scholar, ScientificCommons) was conducted. The following list of search terms was utilized, in various permutations: (a) leech therapy; (b) medicinal leech; (c) hirudotherapy; (d) indications; (e) contraindications; (f) complications; (g) infections. Literature reports most relevant to the focus of the current review were then incorporated into the manuscript as part of the general discussion, topic-specific discussions, or both. Topic-specific references were subsequently tabulated according to the corresponding subject area.
| :: Basic Biology of Leeches | | |
First named by Linnaeus in 1758, Hirudo medicinalis is abundant in freshwater systems of North America and Europe. [11],[12] Leeches are usually hermaphroditic, but require a second leech to reproduce. [12] They belong to the phylum Annelida, class Hirudinea. Hirudo medicinalis is the species that inflicts the deepest bite and the most prolonged post-bite extravasation in its class. [1] Being essentially a segmented worm without an exoskeleton, the medicinal leech is a very specialized annelid both anatomically and behaviorally. [2],[13] It consists of 102 annuli (each of which usually consists of five segments). [14] Hirudo medicinalis can grow to approximately 12 cm in length, with its resting length being about one-third of its maximal length. [14] The leech crawls using a large posterior sucker. [12] Posteriorly, the leech has three jaws arranged in a triradiate configuration that attach to and bite through human skin and a smaller anterior sucker that is utilized for feeding. [14]
The feeding behavior of Hirudo medicinalis is controlled predominantly by the neurotransmitter serotonin which is abundant in the largest neuronal cell of the leech, the Retzius cell. [15],[16] The actual act of feeding is stimulated by the proximity of mammalian-range temperature and by the sodium and arginine in blood. [16] Leeches can be very discriminating in their feeding patterns, preferring blood from certain species. [12] Hungry leeches tend to rest at the water's edge and can swim with great accuracy toward objects that produce waves. [15],[17],[18] While some leeches feed on other small invertebrates, others feed exclusively by temporarily attaching to various animals using a very powerful clinging sucker. [2],[12] Certain species use blade-like jaws to incise the skin of the host; other species secrete enzymes that help digest an opening through the skin. [2],[12] The host is frequently unaware of this attack due to the natural anesthetic substance secreted in the leech saliva. The leech also produces one of the most potent anticoagulants known, hirudin, a 65-amino acid peptide that inhibits thrombin-catalyzed conversion of fibrinogen to fibrin and prevents the host blood from clotting. [12],[19] Other important substances secreted by salivary glands of the leech include vasodilators (antihistamines) and hyaluronidases. [20] Of interest, some leeches are capable of ingesting up to nine times their body weight, which may represent an entire year's nourishment. [12] It is important to note that leeches are colonized by endosymbiotic bacteria, mostly Aeromonas spp, that aid in the digestion of blood within their digestive system. [2] The presence of these bacteria, while usually of no consequence to the host, can occasionally contribute to localized (cellulitis/abscess) and/or systemic (gastroenteritis/sepsis) infections. [10],[21] At times, these infections can be very serious, even life-threatening (i.e. myonecrosis, sepsis). [22],[23]
| :: Mechanism and Rationale for Hirudotherapy | | |
Contemporary leech therapy is most often used in the setting of localized venous congestion or hematoma. Venous congestion occurs with native venous thrombosis or with venous outflow thrombosis in a vascular graft or replanted tissue. [6],[10] Reports of hirudotherapy in the setting of soft tissue hematomas include leech applications for large scrotal and lingual hematomas. [24],[25] In this particular setting, the goal of leech application is to avoid the need for surgical intervention. [24],[25]
The actual volume of blood drawn by a single leech is minimal, approximately 2 mL to 20 mL per feeding. [5],[26],[27] Following extraction of this small volume of blood, the leech usually becomes satiated within 10 to 30 min, detaches from the host, and will not re-feed unless purged by incision of the posterior crop. [12],[26],[27],[28] However, due to the presence of hirudin in the leech saliva, continued oozing from the leeching site well after the leech has detached allows therapy sessions to be temporally spaced by up to 6-8 h. [5] Of interest, the secretions from a single leech have been found to prevent in vitro coagulation of 50-100 mL of human blood. [19] Because the leech bite site on the host may continue to ooze blood for as long as 24 to 48 h, the benefit from leech phlebotomy is thought to far exceed the individual meal volume. In cases of hirudotherapy for retained hematomas, continued drainage of dark non-clotted blood from leech attachment sites suggests that resolution of the hematoma may be ongoing for some time after leech detachment. [25] Leeches will detach spontaneously after they are maximally engorged. At this point, they should be removed and disposed of as biohazardous after sacrifice in 70% alcohol. [10] If a leech does not detach, this may indicate arterial insufficiency, and the leech should be removed with 5% topical cocaine, which will paralyze the leech. The leech must not be forcibly detached, and alcohol must not be applied while the leech is still attached. [1] Basic handling of the medicinal leech is described in [Figure 1]. | Figure 1: Pre- and post-application handling of the medicinal leech: (a) Leeches are delivered in a clean container provided by a certified hirudotherapy supplier; (b and c) Leeches are able to move quite quickly on flat surfaces - it is important not to drop or lose a leech when handling it; (d) Satiated leech is visibly distended and moves slower; (e) The leech is being placed into a 70% alcohol solution during the post-application disposal process
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While modern use of leech therapy revolves around providing a temporary substitute/bridge for venous outflow in the setting of critical venous congestion of tissue reconstruction/flaps, one must always differentiate between venous congestion and arterial ischemia within the tissue being considered for hirudotherapy. [10] This is because the use of leeches in tissue with compromised arterial inflow will not only fail to promote tissue healing but may also contribute to introducing bacterial contamination of the ischemic tissue. [10],[21]
The subsequent sections describe details of the most widely reported applications of hirudotherapy, focusing on clinical indications, risks, and benefits of leech therapy. Finally, a section on infectious complications of hirudotherapy follows.
| :: Hirudotherapy for Soft Tissue Hematomas | | |
Extensive lingual swelling (macroglossia) represents an acute airway emergency. [25] Most frequently attributed to seizure-related activity, traumatic macroglossia may also arise from blunt or penetrating injuries to the lower face that lead to the development of a large lingual hematoma. [25],[26] In the setting of blunt trauma to the face, macroglossia can be secondary to bleeding from the fracture site at the mandibular symphysis via dissection into the sublingual space. [25] Non-traumatic lingual swelling has also been associated with prone positioning in spinal surgery and cleft palate repair. [27],[29] Although lingual swelling has been traditionally treated expectantly, it is generally agreed that airway management should be performed early in anticipation of increasing swelling to prevent acute airway emergency. [25],[30] Once the tongue becomes massively swollen, a cycle of venous and lymphatic congestion begins, contributing to persistent/worsening swelling. [31] Reported therapeutic alternatives in this setting include head elevation, manual reduction of the tongue, and corticosteroid administration. [25],[27],[29],[31]
Medicinal leech application has been reported to be successful in the management of massive post-traumatic lingual swelling. [25],[26] Clinical results have been satisfactory, with resolution of swelling and only minor post-leeching glossal puncture marks. [25] [Table 1] contains a list of clinical reports describing hirudotherapy in the setting of lingual swelling. | Table 1: Clinical reports describing the use of Hirudo medicinalis in the setting of soft tissue hematomas
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| :: Hirudotherapy in Tissue Flap Reconstructions | | |
Perhaps the best established modern application of leech therapy is in tissue flap reconstructions. Despite our improving understanding of tissue perfusion, flaps continue to fail for a variety of reasons. The most common reason for tissue flap failure is inadequate venous outflow. Most authors agree that the initial step in this setting should be surgical exploration and examination of the venous pedicle to alleviate venous insufficiency. Only when venous compromise is determined to be surgically irreparable of if surgery is contraindicated should hirudotherapy be considered. [1] [Table 2] lists examples of hirudotherapy in this clinical setting. In one paper, hirudotherapy was associated with morbidity, including the need for blood transfusions. [33] In another report, the use of leech therapy was described in the setting of heparin-induced thrombocytopenia associated with lower extremity tissue flap failures. [34] In this case, the patient underwent an initial soleus flap placement, which failed despite an intact Doppler signal throughout the pedicle. Subsequently, a microvascular gracilis flap was constructed but began failing in the immediate postoperative period, despite re-exploration-proven patency of both artery and vein. After stopping all heparin administration, hirudotherapy was started, with flap viability maintained until shortly after discontinuation of leech therapy on Day 7. At that time, muscle necrosis ensued. During subsequent workup, it was shown that the patient had heparin-induced thrombocytopenia. In this case, the observation of flap salvage using hirudotherapy - and thus hirudin, the natural non-heparin anticoagulant present in leech saliva - may have constituted indirect evidence that the initial flap insufficiency was associated with heparin-induced thrombocytopenia, especially in the context of immediate gracilis flap failure following discontinuation of leech therapy. [34] An example of leech therapy in the setting of free-flap reconstruction is shown in [Figure 2].  | Table 2: Clinical reports describing the use of Hirudo medicinalis in the setting of tissue flap reconstructions
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 | Figure 2: Application of hirudotherapy to a facial free flap-based reconstruction complicated by early postoperative venous congestion: (a) The leech is applied directly to the flap; (b) The leech attaches; (c) As feeding continues, the leech grows in size until it becomes satiated
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| :: Hirudotherapy in the Setting of Severe Soft Tissue Injury and Surgical Replantation | | |
Vascular congestion poses a significant challenge in reconstructive surgery. Traumatic injury with extensive soft tissue loss and/or the need for replantation constitutes an important indication for medicinal leeching. [40] Clinical signs that should prompt consideration of hirudotherapy in these settings include the development of tissue edema, purple discoloration, and warmth of the reconstructed/replanted tissue - all suggestive of ongoing venous congestion in the presence of preserved arterial inflow. [41],[42] Application of hirudotherapy in the setting of surgical replantation of a digit can be seen in [Figure 3] and [Table 3]. | Table 3: Selected clinical reports describing the use of Hirudo medicinalis in the setting of severe soft tissue injury and surgical replantation
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 | Figure 3: Leech therapy application in a case of digital replantation: (a and b) Application of the leech using non-traumatic forceps - the leech is held until it attaches; (c) Following successful attachment, the leech starts feeding; (d and e) The leech grows in size as it continues to feed
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| :: Hirudotherapy in Penile Replantation | | |
A well-known entity in urologic trauma, penile amputation poses a difficult surgical problem. [10],[45] The current approach to penile replantation involves reapproximation of the urethra and corporal bodies with microsurgical anastomosis of the dorsal vein. Adequacy of postoperative venous outflow is critical to the success of replantation. [45] Prior to the common use of microvascular techniques, non-microsurgical penile replantations were plagued by skin loss, urethral strictures and fistulae, loss of the glans penis, and sensory deficits. [46] Anecdotal evidence suggests that the success of non-microsurgical replantation may be augmented with the adjunctive use of hirudotherapy [Table 4]. [45]  | Table 4: Clinical reports describing the use of Hirudo medicinalis in the setting of penile replantation
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| :: Less Common and Controversial Applications of Hirudotherapy | | |
Among the less common applications of hirudotherapy, Heckmann et al., described the successful use of the medicinal leech for the treatment of forearm compartment syndrome. [32] However, this therapeutic approach is very controversial, and it has to be emphasized that hirudotherapy does not constitute the standard of care for any type of compartment syndrome. [47] The authors of this review concur with the published criticism of the initial report - undertaking the risks associated with nonoperative approach to extremity compartment syndrome is currently not justified. Nevertheless, for the sake of factual completeness, this report was included in the review.
Due to the presence of anti-inflammatory substances in the saliva of medicinal leeches, leech therapy has also been used in recent times to treat localized inflammation and pain. Michalsen et al., recently published a randomized controlled trial that demonstrated significantly better pain relief among patients with osteoarthritis of the knee treated with leech therapy compared with topical diclofenac therapy. [48] This use of hirudotherapy remains experimental [Table 5]. | Table 5: Selected clinical reports describing the use of Hirudo medicinalis in less common and controversial clinical applications
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| :: Special Topics in Hirudotherapy: Infectious Complications | | |
Leeches should be obtained from appropriately regulated commercial sources. [25] They represent a potential vector of blood-borne diseases, including the human immunodeficiency virus (HIV) and hepatitis viruses. [25],[49],[50] The leech bite leads to direct communication between the leech digestive tract and the host soft tissue, The most commonly encountered infectious agent during hirudotherapy is the Gram-negative rod, Aeromonas hydrophila, a prominent component of the leech intestinal flora. [22] However, infections with Pseudomonas spp and Vibrio spp have also been reported. [12],[51] Because of the intimate contact between the leech and the patient, infections associated with hirudotherapy occur in 2.4-20% of patients who do not receive antibiotic prophylaxis. [2],[22] A wide range of clinical infections have been reported including cellulitis, flap necrosis, extensive muscular necrosis, and even septic shock. [2] Ischemia produces local immunosuppression - another reason why hirudotherapy should be reserved for areas with adequate arterial supply.
Aeromonas spp. produce beta-lactamase, so penicillins and first-generation cephalosporins are ineffective. The organisms most often involved in hirudotherapy-associated bacterial infections are usually sensitive to second and third-generation cephalosporins, aminoglycosides, chloramphenicol, fluoroquinolones, and trimethoprim. [1]
| :: Conclusions | | |
Modern leech therapy utilizing Hirudo medicinalis is based on sound scientific principles and has resulted in important patient care enhancements. Leech therapy is most often used in the settings of localized venous congestion associated with flap reconstructions and surgical replantations. Hirudotherapy has also been used to treat soft tissue swelling and hematomas in trauma. Infectious complications can be minimized by obtaining leeches from appropriate commercial sources and utilizing effective antibiotic prophylaxis against Aeromonas.
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[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]
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Hirudotherapy (medicinal leeches) for treatment of upper airway obstruction in a dog |
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| H. Nicole Trenholme, Isabelle Masseau, Carol R. Reinero | | Journal of Veterinary Emergency and Critical Care. 2021; 31(5): 661 | | [Pubmed] | [DOI] | | | 7 |
Justification of the effectiveness of hirudotherapy in dentistry |
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| A. I. Abdullaeva, Elena P. Pustovaya, V. M. Slonova, A. S. Karnaeva, O. V. Pilshchikova, A. A. Gevorkyan | | Russian Journal of Dentistry. 2020; 24(5): 328 | | [Pubmed] | [DOI] | | | 8 |
Tibbi Sülük Terapisi (Hirudoterapi) |
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| M.öner KÜÇÜK, Ozan YAMAN | | Journal of Biotechnology and Strategic Health Research. 2019; 3: 29 | | [Pubmed] | [DOI] | | | 9 |
Evaluation of the effects of Leech Salivary Extract (LSE) on Haematological parameters in Rats |
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| Babayi H | | Journal of Hematology and Clinical Research. 2017; 2(1): 006 | | [Pubmed] | [DOI] | | | 10 |
Medicinal leech therapy—an overall perspective |
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| Ali K. Sig, Mustafa Guney, Aylin Uskudar Guclu, Erkan Ozmen | | Integrative Medicine Research. 2017; 6(4): 337 | | [Pubmed] | [DOI] | | | 11 |
The Effect of External Apple Vinegar Application on Varicosity Symptoms, Pain, and Social Appearance Anxiety: A Randomized Controlled Trial |
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| Derya Atik,Cem Atik,Celalettin Karatepe | | Evidence-Based Complementary and Alternative Medicine. 2016; 2016: 1 | | [Pubmed] | [DOI] | | | 12 |
Leech Therapy in Iranian Traditional Medicine |
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| Alireza Barzegar, Amir Azizi, Pouya Faridi, Abdolali Mohagheghzadeh | | Complementary Medicine Research. 2015; 22(1): 50 | | [Pubmed] | [DOI] | | | 13 |
LEECH THERAPY IN TREATMENT OF CARDIOVASCULAR DISEASES |
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| N N Konyrtaeva, A M Grjibovski, G K Kausova, V A Zhernov, Zh A Kalmataeva | | Ekologiya cheloveka (Human Ecology). 2015; 22(6): 57 | | [Pubmed] | [DOI] | | | 14 |
Medicinal leech therapy |
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| Celina Liu,Thomas W. Barkley | | Nursing. 2015; 45(11): 25 | | [Pubmed] | [DOI] | | | 15 |
Medical leech therapy in plastic reconstructive surgery |
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| Khosrow S. Houschyar,Arash Momeni,Zeshaan N. Maan,Malcolm N. Pyles,Olivia S. Jew,Marion Strathe,Andreas Michalsen | | Wiener Medizinische Wochenschrift. 2015; 165(19-20): 419 | | [Pubmed] | [DOI] | | | 16 |
Preventing Infective Complications following Leech Therapy: Elimination of SymbioticAeromonasspp. from the Intestine ofHirudo verbanaUsing Antibiotic Feeding |
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| Agata Litwinowicz,Joanna Blaszkowska | | Surgical Infections. 2014; 15(6): 757 | | [Pubmed] | [DOI] | | | 17 |
To suck or not to suck: medicinal leech therapy for lower extremity wounds in patients with peripheral arterial disease |
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| Gunalp Uzun,Adem Ozdemir,Senol Yildiz,Mehmet Tanyuksel | | International Wound Journal. 2014; : n/a | | [Pubmed] | [DOI] | | | 18 |
Coleridge, Nitric Acid and the Spectre of Syphilis |
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| Thomas Owens | | Romanticism. 2014; 20(3): 282 | | [Pubmed] | [DOI] | | | 19 |
The use of medical leeches for venous congestion |
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| N. J. Buote | | Veterinary and Comparative Orthopaedics and Traumatology. 2014; 27(3): 173 | | [Pubmed] | [DOI] | | | 20 |
In vivo anti-hyperglycemic activity of saliva extract from the tropical leech Hirudinaria manillensis |
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| Abdualkader Abdualrahman Mohammed,Ghawi Abbas Mohammad,Alaama Mohamed,Awang Mohamed,Merzouk Ahmed | | Chinese Journal of Natural Medicines. 2013; 11(5): 488 | | [Pubmed] | [DOI] | | | 21 |
Leech therapeutic applications |
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| Abdualkader, A.M. and Ghawi, A.M. and Alaama, M. and Awang, M. and Merzouk, A. | | Indian Journal of Pharmaceutical Sciences. 2013; 75(2): 127-137 | | [Pubmed] | | | 22 |
Diversity and selective pressures of anticoagulants in three medicinal leeches (Hirudinida: Hirudinidae, Macrobdellidae) |
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| Sebastian Kvist,Gi-Sik Min,Mark E Siddall | | Ecology and Evolution. 2013; 3(4): 918 | | [Pubmed] | [DOI] | | | 23 |
Medicinal leech therapy in pain syndromes: a narrative review |
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| Detlev Koeppen,Michael Aurich,Thomas Rampp | | Wiener Medizinische Wochenschrift. 2013; | | [Pubmed] | [DOI] | | | 24 |
Nasal ala reconstruction with a crus helix composite graft: A stepladder approach |
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| Zilinsky, I., Farber, N., Haik, J., Weissman, O., Israeli, H., Winkler, E. | | Journal of Drugs in Dermatology. 2012; 11(3): 376-381 | | [Pubmed] | | | 25 |
Cutaneous complications of improper leech application |
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| Pietrzak, A. and Kanitakis, J. and Tomasiewicz, K. and Wawrzycki, B. and KozŁowska-Łój, J. and Dybiec, E. and Chodorowska, G. | | Annals of Agricultural and Environmental Medicine. 2012; 19(4): 790-792 | | [Pubmed] | | | 26 |
Functional characterisation of Vizottin, the first factor Xa inhibitor purified from the leech Haementeria vizottoi |
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| Lourenço Oliveira, D.G. and Alvarez-Flores, M.P. and Lopes, A.R. and Chudzinski-Tavassi, A.M. | | Thrombosis and Haemostasis. 2012; 108(3): 570-578 | | [Pubmed] | | | 27 |
New perspectives on complementary and alternative medicine: An overview and alternative therapy |
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| Pan, S.-Y. and Gao, S.-H. and Zhou, S.-F. and Tang, M.-K. and Yu, Z.-L. and Ko, K.-M. | | Alternative Therapies in Health and Medicine. 2012; 18(4): 20-36 | | [Pubmed] | | | 28 |
Biotechnological production of recombinant analogues of hirudin-1 from Hirudo medicinalis |
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| Kostromina, M.A. and Esipov, R.S. and Miroshnikov, A.I. | | Russian Journal of Bioorganic Chemistry. 2012; 38(2): 142-151 | | [Pubmed] | | | 29 |
Biotechnological production of recombinant analogues of hirudin-1 from Hirudo medicinalis |
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| M. A. Kostromina,R. S. Esipov,A. I. Miroshnikov | | Russian Journal of Bioorganic Chemistry. 2012; 38(2): 142 | | [Pubmed] | [DOI] | | | 30 |
Functional characterisation of Vizottin, the first factor Xa inhibitor purified from the leech Haementeria vizottoi |
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| D. G. L. Oliveira,M. P. Alvarez-Flores,A. R. Lopes,A. M. Chudzinski-Tavassi | | Thrombosis and Haemostasis. 2012; 108(3): 570 | | [Pubmed] | [DOI] | | | 31 |
Complications of tissue ischemia in dermatologic surgery |
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| AMY DELANEY,STEPHANIE DIAMANTIS,VICTOR J. MARKS | | Dermatologic Therapy. 2011; 24(6): 551 | | [Pubmed] | [DOI] | | | 32 |
Complications of tissue ischemia in dermatologic surgery |
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| Delaney, A. and Diamantis, S. and Marks, V.J. | | Dermatologic Therapy. 2011; 24(6): 551-557 | | [Pubmed] | | | 33 |
Bloodletting - An ayurvedic perspective |
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| Sathish, H.S., Vaghela, D.B. | | Journal of Postgraduate Medicine. 2011; 57(3): 253 | | [Pubmed] | |
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