Response patterns in adventitial layer of Echinococcus granulosus sensu stricto cysts from naturally infected cattle and sheep

Springer Science and Business Media LLC - 2021
Christian Hidalgo1, Caroll Stoore2, María Soledad Baquedano2, Ismael Pereira2, Carmen Franco3, María Eugenia Soto Hernández4, Rodolfo Paredes2
1Instituto de Ciencias Agroalimentarias, Animales y Ambientales (ICA3), Universidad de O’Higgins, San Fernando, Chile
2Laboratorio de Medicina Veterinaria, Escuela de Medicina Veterinaria, Facultad de Ciencias de la Vida, Universidad Andres Bello, Santiago, Chile
3Staff Pathologist, Clinica Santa Maria, Santiago, Chile
4Laboratorio de Biología Periodontal y Departamento de Patología y Medicina Oral, Facultad de Odontología, Universidad de Chile, Santiago, Chile

Tóm tắt

Abstract

Cystic echinococcosis is a zoonotic disease caused by the metacestode of Echinococcus granulosus sensu lato. The disease is characterized by the development of cystic structures inside viscera of the intermediate host, mainly liver and lungs. These cysts are formed by three layers: germinal, laminated, and adventitial layer, the latter being the local host immune response. Metacestodes that develop protoscoleces, the infective stage to the definitive host, are termed fertile, whereas cysts that do not produce protoscoleces are termed non-fertile. Sheep usually harbor fertile cysts while cattle usually harbor non-fertile cysts. Adventitial layers with fibrotic resolution are associated to fertile cysts, whereas a granulomatous reaction is associated with non-fertile cysts. The aim of this study was to analyze cellular distribution in the adventitial layer of fertile and non-fertile E. granulosus sensu stricto cysts found in liver and lungs of cattle and sheep. A total of 418 cysts were analyzed, 203 from cattle (8 fertile and 195 non-fertile) and 215 from sheep (64 fertile and 151 non-fertile). Fertile cysts from cattle showed mixed patterns of response, with fibrotic resolution and presence of granulomatous response in direct contact with the laminated layer, while sheep fertile cysts always displayed fibrotic resolution next to the laminated layer. Cattle non-fertile cysts display a granulomatous reaction in direct contact with the laminated layer, whereas sheep non-fertile cysts display a granulomatous reaction, but in direct contact with the fibrotic resolution. This shows that cattle and sheep cystic echinococcosis cysts have distinct local immune response patterns, which are associated to metacestode fertility.

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Tài liệu tham khảo

Grosso G, Gruttadauria S, Blondi A, Marventano S, Mistretta A (2012) Worldwide epodemiology of liver hydatidosis including the mediterranean area. World J Gastroenterol 18:1425–1437. https://doi.org/10.3748/wjg.v18.i13

Vuitton DA, McManus DP, Rogan MT, Romig T, Gottstein B, Naidich A, Tuxun T, Wen H, Menezes da Silva A (2020) International consensus on terminology to be used in the field of echinococcoses. Parasite 27:41. https://doi.org/10.1051/parasite/2020024

Agudelo Higuita NI, Brunetti E, McCloskey C (2016) Cystic echinococcosis. J Clin Microbiol 54:518–523. https://doi.org/10.1128/JCM.02420-15

Thompson RC (2017) Biology and systematics of echinococcus. Adv Parasitol 95:65–109. https://doi.org/10.1016/bs.apar.2016.07.001

Hidalgo C, Stoore C, Strull K, Franco C, Correa F, Jimenez M, Hernandez M, Lorenzatto K, Ferreira HB, Galanti N, Paredes R (2019) New insights of the local immune response against both fertile and infertile hydatid cysts. PLoS One 14:e0211542. https://doi.org/10.1371/journal.pone.0211542

Diaz A, Casaravilla C, Irigoin F, Lin G, Previato JO, Ferreira F (2011) Understanding the laminated layer of larval Echinococcus I: structure. Trends Parasitol 27:204–213. https://doi.org/10.1016/j.pt.2010.12.012

Jimenez M, Stoore C, Hidalgo C, Correa F, Hernandez M, Benavides J, Ferreras MC, Saenz L, Paredes R (2020) Lymphocyte populations in the adventitial layer of hydatid cysts in cattle: relationship with cyst fertility status and Fasciola hepatica co-infection. Vet Pathol 57:108–114. https://doi.org/10.1177/0300985819875721

Stoore C, Andrade C, Hidalgo C, Correa F, Jimenez M, Hernandez M, Paredes R (2018) Echinococcus granulosus hydatid cyst location is modified by Fasciola hepatica infection in cattle. Parasit Vectors 11:542. https://doi.org/10.1186/s13071-018-3128-6

Diaz A (2017) Immunology of cystic echinococcosis (hydatid disease). Br Med Bull 124:121–133. https://doi.org/10.1093/bmb/ldx033

Rogan MT, Bodell AJ, Craig PS (2015) Post-encystment/established immunity in cystic echinococcosis: is it really that simple? Parasite Immunol 37:1–9. https://doi.org/10.1111/pim.12149

Hidalgo C, Stoore C, Pereira I, Paredes R, Alvarez Rojas CA (2020) Multiple haplotypes of Echinococcus granulosus sensu stricto in single naturally infected intermediate hosts. Parasitol Res 119:763–770. https://doi.org/10.1007/s00436-019-06578-2

Lewall DB (1998) Hydatid disease biology, pathology, imaging and classification. Clin Radiol 53:863–874

Paredes R, Godoy P, Rodriguez B, Garcia MP, Cabezon C, Cabrera G, Jimenez V, Hellman U, Saenz L, Ferreira A, Galanti N (2011) Bovine (Bos taurus) humoral immune response against Echinococcus granulosus and hydatid cyst infertility. J Cell Biochem 112:189–199. https://doi.org/10.1002/jcb.22916

Riesle S, Garcia MP, Hidalgo C, Galanti N, Saenz L, Paredes R (2014) Bovine IgG subclasses and fertility of Echinococcus granulosus hydatid cysts. Vet Parasitol 205:125–133. https://doi.org/10.1016/j.vetpar.2014.06.003

Vismarra A, Mangia C, Passeri B, Brundu D, Masala G, Ledda S, Mariconti M, Brindani F, Kramer L, Bacci C (2015) Immuno-histochemical study of ovine cystic echinococcosis (Echinococcus granulosus) shows predominant T cell infiltration in established cysts. Vet Parasitol 209:285–288. https://doi.org/10.1016/j.vetpar.2015.02.027

Barnes TS, Hinds LA, Jenkins DJ, Bielefeldt-Ohmann H, Lightowlers MW, Coleman GT (2011) Comparative pathology of pulmonary hydatid cysts in macropods and sheep. J Comp Pathol 144:113–122. https://doi.org/10.1016/j.jcpa.2010.07.003

Cengiz G, Gonenc B (2020) Comparison of molecular and morphological characterization and haplotype analysis of cattle and sheep isolates of cystic echinococcosis. Vet Parasitol 282:109132. https://doi.org/10.1016/j.vetpar.2020.109132

Mehmood N, Arshad M, Ahmed H, Simsek S, Muqaddas H (2020) Comprehensive account on prevalence and characteristics of hydatid cysts in livestock from Pakistan. Korean J Parasitol 58:121–127. https://doi.org/10.3347/kjp.2020.58.2.121

Varcasia A, Dessi G, Lattanzio S, Marongiu D, Cuccuru C, Carta S, Meloni MP, Tamponi C, Scala A (2020) Cystic echinococcosis in the endemic island of Sardinia (Italy): has something changed? Parasitol Res 119:2207–2215. https://doi.org/10.1007/s00436-020-06717-0

Bonelli P, Loi F, Cancedda MG, Peruzzu A, Antuofermo E, Pintore E, Piseddu T, Garippa G, Masala G (2020) Bayesian analysis of three methods for diagnosis of cystic echinococcosis in sheep. Pathogens 9:796. https://doi.org/10.3390/pathogens9100796

Yanagida T, Mohammadzadeh T, Kamhawi S, Nakao M, Sadjjadi SM, Hijjawi N, Abdel-Hafez SK, Sako Y, Okamoto M, Ito A (2012) Genetic polymorphisms of Echinococcus granulosus sensu stricto in the Middle East. Parasitol Int 61:599–603. https://doi.org/10.1016/j.parint.2012.05.014

Blanton RE, Wachira TM, Zeyhle EE, Njoroge EM, Magambo JK, Schantz PM (1998) Oxfendazole treatment for cystic hydatid disease in naturally infected animals. Antimicrob Agents Chemother 42:601–605. https://doi.org/10.1128/AAC.42.3.601

Sakamoto T, Cabrera PA (2003) Immunohistochemical observations on cellular response in unilocular hydatid lesions and lymph nodes of cattle. Acta Trop 85:271–279

Basika T, Munoz N, Casaravilla C, Irigoin F, Batthyany C, Bonilla M, Salinas G, Pacheco JP, Roth J, Duran R, Diaz A (2012) Phagocyte-specific S100 proteins in the local response to the Echinococcus granulosus larva. Parasitology 139:271–283. https://doi.org/10.1017/S003118201100179X

Hadavi E, de Vries RHW, Smink AM, de Haan B, Leijten J, Schwab LW, Karperien M, de Vos P, Dijkstra PJ, van Apeldoorn AA (2021) In vitro degradation profiles and in vivo biomaterial-tissue interactions of microwell array delivery devices. J Biomed Mater Res B Appl Biomater 109:117–127. https://doi.org/10.1002/jbm.b.34686

Morais JM, Papadimitrakopoulos F, Burgess DJ (2010) Biomaterials/tissue interactions: possible solutions to overcome foreign body response. AAPS J 12:188–196. https://doi.org/10.1208/s12248-010-9175-3

Onuki Y, Bhardwaj U, Papadimitrakopoulos F, Burgess DJ (2008) A review of the biocompatibility of implantable devices: current challenges to overcome foreign body response. J Diabetes Sci Technol 2:1003–1015. https://doi.org/10.1177/193229680800200610

Amri M, Touil-Boukoffa C (2015) A protective effect of the laminated layer on Echinococcus granulosus survival dependent on upregulation of host arginase. Acta Trop 149:186–194. https://doi.org/10.1016/j.actatropica.2015.05.027

Barrios AA, Grezzi L, Miles S, Mariconti M, Mourglia-Ettlin G, Seoane PI, Diaz A (2019) Inefficient and abortive classical complement pathway activation by the calcium inositol hexakisphosphate component of the Echinococcus granulosus laminated layer. Immunobiology 224:710–719. https://doi.org/10.1016/j.imbio.2019.05.009

Casaravilla C, Pittini A, Ruckerl D, Seoane PI, Jenkins SJ, MacDonald AS, Ferreira AM, Allen JE, Diaz A (2014) Unconventional maturation of dendritic cells induced by particles from the laminated layer of larval Echinococcus granulosus. Infect Immun 82:3164–3176. https://doi.org/10.1128/IAI.01959-14

Pittini A, Martinez-Acosta YE, Casaravilla C, Seoane PI, Ruckerl D, Quijano C, Allen JE, Diaz A (2019) Particles from the Echinococcus granulosus laminated layer inhibit CD40 upregulation in dendritic cells by interfering with Akt activation. Infect Immun 87:e00641-e719. https://doi.org/10.1128/IAI.00641-19

Seoane PI, Ruckerl D, Casaravilla C, Barrios AA, Pittini A, MacDonald AS, Allen JE, Diaz A (2016) Particles from the Echinococcus granulosus laminated layer inhibit IL-4 and growth factor-driven Akt phosphorylation and proliferative responses in macrophages. Sci Rep 6:39204. https://doi.org/10.1038/srep39204

Hachim D, LoPresti ST, Yates CC, Brown BN (2017) Shifts in macrophage phenotype at the biomaterial interface via IL-4 eluting coatings are associated with improved implant integration. Biomaterials 112:95–107. https://doi.org/10.1016/j.biomaterials.2016.10.019

Hou J, Shi J, Chen L, Lv Z, Chen X, Cao H, Xiang Z, Han X (2018) M2 macrophages promote myofibroblast differentiation of LR-MSCs and are associated with pulmonary fibrogenesis. Cell Commun Signal 16:89. https://doi.org/10.1186/s12964-018-0300-8

Hidalgo C, Stoore C, Hernandez M, Paredes R (2020) Fasciola hepatica coinfection modifies the morphological and immunological features of Echinococcus granulosus cysts in cattle. Vet Res 51:76. https://doi.org/10.1186/s13567-020-00799-5

Pai CH, Lin SR, Liu CH, Pan SY, Hsu H, Chen YT, Yen CT, Yu IS, Wu HL, Lin SL, Lin SW (2020) Targeting fibroblast CD248 attenuates CCL17-expressing macrophages and tissue fibrosis. Sci Rep 10:16772. https://doi.org/10.1038/s41598-020-73194-x

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