Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-14T07:07:44.010Z Has data issue: false hasContentIssue false

A possible relationship between Thromboxane B2 and Leukotriene B4 and the encapsulation of Dirofilaria repens worms in human subcutaneous dirofilariasis

Published online by Cambridge University Press:  24 July 2019

R. Morchón*
Affiliation:
Laboratory of Parasitology, Animal and Human Dirofilariosis Group, Faculty of Pharmacy, University of Salamanca, Campus Miguel Unamuno s/n, 37007 Salamanca, Spain
E. Carretón
Affiliation:
Research Institute of Biomedical and Health Sciences (IUIBS), University of Las Palmas de Gran Canaria, 35001 Las Palmas, Spain
R. García
Affiliation:
Laboratory of Parasitology, Animal and Human Dirofilariosis Group, Faculty of Pharmacy, University of Salamanca, Campus Miguel Unamuno s/n, 37007 Salamanca, Spain
T. Zueva
Affiliation:
Laboratory of Parasitology, Animal and Human Dirofilariosis Group, Faculty of Pharmacy, University of Salamanca, Campus Miguel Unamuno s/n, 37007 Salamanca, Spain
V. Kartashev
Affiliation:
Rostov State Medical University, Rostov-na-Donu 344022, Russia
F. Simón
Affiliation:
Laboratory of Parasitology, Animal and Human Dirofilariosis Group, Faculty of Pharmacy, University of Salamanca, Campus Miguel Unamuno s/n, 37007 Salamanca, Spain
*
Author for correspondence: R. Morchón, E-mail: rmorgar@usal.es

Abstract

Human subcutaneous dirofilariosis has several clinical presentations. Many cases present as subcutaneous nodules, as a consequence of a local inflammatory reaction that encapsulates and destroys the worms. In addition, there are cases in which migrating worms located in the ocular area remain unencapsulated. In the present work, the levels of two pro-inflammatory eicosanoids, thromboxane B2 (TxB2) and leukotriene B4 (LTB4) are analysed by commercial Enzime-Linked immunosorbent assay (ELISA) in serum samples from 43 individuals, 28 diagnosed as having subcutaneous dirofilariasis presenting a subcutaneous nodule, five diagnosed as having dirofilariasis, in which the worms remained unencapsulated in the periphery of the eye, and ten healthy individuals living in a non-endemic area, used as controls. The worms were surgically removed, identifying Dirofilaria repens as the causative agent in all cases, by Polymerase Chain Reaction (PCR). Individuals with nodules showed significantly higher levels of TxB2 and LTB4 than healthy controls, whereas significant differences in LTB4 levels were observed between individuals with unencapsulated worms and healthy controls. It is speculated that the absence of LTB4 may contribute to the fact that worms remain unencapsulated as a part of immune evasion mechanisms.

Type
Short Communication
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bogatcheva, NV, Sergeeva, MG, Dudek, SM and Verin, AD (2005) Arachidonic acid cascade in endothelial pathobiology. Microvascular Research 69, 107127.Google Scholar
Brattig, NW (2004) Pathogenesis and host responses in human onchocerciasis: impact of Onchocerca filariae and Wolbachia endobacteria. Microbes and Infection 6, 113128.Google Scholar
Brattig, NW, Schwohl, A, Hoerauf, A and Büttner, DW (2009) Identification of the lipid mediator prostaglandin E2 in tissue immune cells of humans infected with the filaria Onchocerca volvulus. Acta Tropica 112, 231235.Google Scholar
Capelli, G, Genchi, C, Baneth, G, et al. (2018) Recent advances on Dirofilaria repens in dogs and humans in Europe. Parasite & Vectors 11, 663.Google Scholar
Cook-Mills, JM and Deem, TL (2005) Active participation of endothelial cells in inflammation. Journal of Leukocyte Biology 77, 487495.Google Scholar
European Academies Science Advisory Council (EASAC) (2010) Climate change and infectious diseases in Europe. Available at https://www.easac.eu/fileadmin/PDF_s/reports_statements/Climate_change_and_infectious_diseases_in_Europe.pdf (accessed 27 May 2019).Google Scholar
Genchi, C, Kramer, LH and Rivasi, F (2011) Dirofilarial infections in Europe. Vector Borne and Zoonotic Diseases 11, 13071317.Google Scholar
Gioia, G, Lecová, L, Genchi, M, Ferri, E, Genchi, C and Mortarino, M (2010) Highly sensitive multiplex PCR for simultaneous detection and discrimination of Dirofilaria immitis and Dirofilaria repens in canine peripheral blood. Veterinary Parasitology 172, 160163.Google Scholar
González-Miguel, J, Rosario, L, Rota-Nodari, E, Morchón, R and Simón, F (2010a) Identification of immunoreactive proteins of Dirofilaria immitis and D. repens recognized by sera from patient with pulmonary and subcutaneous dirofilariosis. Parasitology Internatational 59, 248256.Google Scholar
González-Miguel, J, Morchón, R, Siles-Lucas, M, Oleaga, A and Simón, F (2010b) Identification of Dirofilaria immitis immunreactive proteins recognized by sera from infected cats using two-dimensional electrophoresis and mass spectrometry. Molecular and Biochemical Parasitology 174, 7882.Google Scholar
Grandi, G, Morchón, R, Kramer, L, Kartashev, V and Simón, F (2008) Wolbachia in Dirofilaria repens, an agent causing human subcutaneous dirofilariasis. Journal of Parasitology 94, 14211423.Google Scholar
Kartashev, V and Simón, F (2018) Migrating Dirofilaria repens. The New England Journal of Medicine 378, e35.Google Scholar
Kartashev, V, Tverdokhlebova, T, Korzan, A, Vedenkov, A, Simón, L, González-Miguel, J, Morchón, R, Siles-Lucas, M and Simón, F (2015) Human subcutaneous/ocular dirofilariosis in Russian Federation and Belarus, 1997-2013. International Journal of Infectious Diseases 33, 209211.Google Scholar
Kramer, LH, Kartashev, VV, Grandi, G, Morchón, R, Nagorni, SA, Karanis, P and Simón, F (2007) Human subcutaneous dirofilariasis, Russia. Emerging Infectious Diseases 13, 150152.Google Scholar
Liu, LX and Weller, PF (1992) Intravascular filarial parasites inhibit platelet aggregation. Role of parasite-derived prostanoids. The Journal of Clinical Investigation 89, 11131120.Google Scholar
Liu, LX, Buhlmann, JE and Weller, PF (1992) Release of prostaglandin E2 by microfilariae of Wuchereria bancrofti and Brugia malayi. The American Journal of Tropical Medicine and Hygiene 46, 520523.Google Scholar
Moore, J, McDermott, L, Price, NC, Kelly, SN and Cooper, A (1999) Sequence-divergent units of the ABA-1 polyprotein array of the nematode Ascaris suum have similar fatty-acid- and retinol-binding properties but different binding-site environments. Biochemical Journal 340, 337343.Google Scholar
Morchón, R, López-Belmonte, J, Rodríguez-Barbero, A and Simón, F (2006) High levels of serum thromboxane B2 are generated during human pulmonary dirofilariasis. Clinical Vaccine Immunology 13, 11751176.Google Scholar
Morchón, R, Rodríguez-Barbero, A, Velasco, S, López-Belmonte, J and Simón, F (2008) Vascular endothelial cell activation by adult Dirofilaria immitis antigens. Parasitology International 57, 441446.Google Scholar
Morchón, R, González-Miguel, J, Carretón, E, Kramer, LH, Velero, L, Montoya-Alonso, JA, Simón, F and Siles-Lucas, M (2014) Proteomic analysis of the somatic and surface compartments from Dirofilaria immitis adult worms. Veterinary Parasitology 203, 144152.Google Scholar
Pampiglione, S, Canestri Trotti, G and Rivasi, F (1995) Human dirofilariasis due to Dirofilaria (Nochtiella) repens: a review of world literature. Parassitologia 37, 149193.Google Scholar
Rogerio, AP and Anibal, FF (2012) Role of leukotrienes on protozoan and helminth infections. Mediators of Inflammation 2012, 595694.Google Scholar
Rola-Pleszcynski, M, Gagnon, L and Sirois, P (1983) Leukotriene B4 augments human natural cytotoxic cell activity. Biochemical and Biophysical Research Communications 113, 531537.Google Scholar
Sankari, T, Hoti, SL, Das, L, Govindaraj, V and Das, PK (2013) Effect of Diethylcarbamazine (DEC) on prostaglandin levels in Wuchereria bancrofti infected microfilaraemics. Parasitology Research 112, 23532359.Google Scholar
Simón, F, Siles-Lucas, M, Morchón, R, González-Miguel, J, Mellado, I, Carretón, E and Montoya-Alonso, JA (2012) Human and animal dirofilariasis: the emergence of a zoonotic mosaic. Clinical Microbiology Reviews 25, 507544.Google Scholar
Tezuka, H, Imai, S, Muto, R, Furuhashi, Y and Fujita, K (2002) Recombinant Dirofilaria immitis polyprotein that stimulates murine B cells to produce nonspecific polyclonal immunoglobulin E antibody. Infection and Immunity 70, 12351244.Google Scholar
Yaqoob, P (2004) Fatty acids and the immune system: from basic science to clinical applications. Proceedings of the Nutrition Society 63, 89104.Google Scholar