Promising proteins detected by Western blot from Echinococcus granulosus protoscoleces for predicting early post-surgical outcomes in CE-affected Tunisian children.


Journal

Parasites & vectors
ISSN: 1756-3305
Titre abrégé: Parasit Vectors
Pays: England
ID NLM: 101462774

Informations de publication

Date de publication:
30 Mar 2021
Historique:
received: 03 11 2020
accepted: 11 03 2021
entrez: 30 3 2021
pubmed: 31 3 2021
medline: 25 9 2021
Statut: epublish

Résumé

Cystic echinococcosis (CE) affects predominantly young patients in highly endemic areas. Improved serological methods are needed for the follow-up of CE cases, especially given the high rates of post-surgical relapse that require detection as soon as possible. We designed a study to investigate the value of antigenic proteins extracted from Echinococcus granulosus (E. granulosus) protoscoleces, and of recombinant B2t and 2B2t proteins, for assessing the efficacy of surgical treatment carried out on CE-affected children. This study was performed on 278 plasma samples collected from 59 Tunisian children surgically treated for CE and monitored for 3 years post-surgery. The patients were classified according to post-surgical outcomes into a "non-relapsed" (NRCE) and a "relapsed" (RCE) group. We performed in-house ELISAs to measure anti-B2t and anti-2B2t IgG and immunoblotting for the detection of IgG against SDS-PAGE-resolved E. granulosus protoscoleces-specific antigens. The Wilcoxon test was applied to assess anti-B2t and anti-2B2t IgG levels. We applied the Cochran Q test to compare the distribution of immunoblotting antigenic bands between 1-month and 1-year post-surgery. The probability of being "relapse-free" when a decrease in antibody titers occurred between 1 month and 1 year post-surgery was 81% and 75%, respectively, for anti-B2t and anti-2B2t IgG. We identified five protoscolex protein bands of 20, 26/27, 30, 40 and 46 kDa as highly immunoreactive by immunoblot for both RCE and NRCE patients at 1 month post-surgery, and significantly lower immunoreactivity after 1 year (p < 10 The B2t protein could be useful for the prediction of CE early post-surgical outcomes. The proteins of E. granulosus protoscoleces, especially the doublet P26/27 and P40, could be promising predictive biomarkers for the post-surgical follow-up of CE cases as well.

Sections du résumé

BACKGROUND BACKGROUND
Cystic echinococcosis (CE) affects predominantly young patients in highly endemic areas. Improved serological methods are needed for the follow-up of CE cases, especially given the high rates of post-surgical relapse that require detection as soon as possible.
METHODS METHODS
We designed a study to investigate the value of antigenic proteins extracted from Echinococcus granulosus (E. granulosus) protoscoleces, and of recombinant B2t and 2B2t proteins, for assessing the efficacy of surgical treatment carried out on CE-affected children. This study was performed on 278 plasma samples collected from 59 Tunisian children surgically treated for CE and monitored for 3 years post-surgery. The patients were classified according to post-surgical outcomes into a "non-relapsed" (NRCE) and a "relapsed" (RCE) group. We performed in-house ELISAs to measure anti-B2t and anti-2B2t IgG and immunoblotting for the detection of IgG against SDS-PAGE-resolved E. granulosus protoscoleces-specific antigens. The Wilcoxon test was applied to assess anti-B2t and anti-2B2t IgG levels. We applied the Cochran Q test to compare the distribution of immunoblotting antigenic bands between 1-month and 1-year post-surgery.
RESULTS RESULTS
The probability of being "relapse-free" when a decrease in antibody titers occurred between 1 month and 1 year post-surgery was 81% and 75%, respectively, for anti-B2t and anti-2B2t IgG. We identified five protoscolex protein bands of 20, 26/27, 30, 40 and 46 kDa as highly immunoreactive by immunoblot for both RCE and NRCE patients at 1 month post-surgery, and significantly lower immunoreactivity after 1 year (p < 10
CONCLUSIONS CONCLUSIONS
The B2t protein could be useful for the prediction of CE early post-surgical outcomes. The proteins of E. granulosus protoscoleces, especially the doublet P26/27 and P40, could be promising predictive biomarkers for the post-surgical follow-up of CE cases as well.

Identifiants

pubmed: 33781311
doi: 10.1186/s13071-021-04679-5
pii: 10.1186/s13071-021-04679-5
pmc: PMC8008569
doi:

Substances chimiques

Antibodies, Helminth 0
Antigens, Helminth 0
Helminth Proteins 0
Immunoglobulin G 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

180

Références

Kern P, Menezes da Silva A, Akhan O, Mullhaupt B, Vizcaychipi KA, Budke C, et al. The echinococcoses: diagnosis clinical management and burden of disease. Adv Parasitol. 2017;96:259–369.
pubmed: 28212790
Chahed MK, Bellali H, Touinsi H, Cherif R, Ben Safta Z, Essoussi M, et al. Distribution of surgical hydatidosis in Tunisia, results of 2001–2005 study and trends between 1977 and 2005. Arch Inst Pasteur Tunis. 2010;87:43–52.
pubmed: 21604459
Ammann RW, Eckert J. Cestodes Echinococcus. Gastroenterol Clin North Am. 1996;25:655–89.
pubmed: 8863045
Moro P, Schantz PM. Cystic echinococcosis in the Americas. Parasitol Int. 2006;55(Suppl):S181–6.
pubmed: 16376604
Agudelo Higuita NI, Brunetti E, McCloskey C. Cystic Echinococcosis. J Clin Microbiol. 2016;54:518–23.
pubmed: 26677245 pmcid: 4767951
Siles-Lucas M, Casulli A, Conraths FJ, Muller N. Laboratory diagnosis of Echinococcus spp. in human patients and infected animals. Adv Parasitol. 2017;96:159–257.
pubmed: 28212789
Tamarozzi F, Mariconti M, Covini I, Brunetti E. Rapid diagnostic tests for the serodiagnosis of human cystic echinococcosis. Bull Soc Pathol Exot. 2017;110:20–30.
pubmed: 28275967
Kapan M, Kapan S, Goksoy E, Perek S, Kol E. Postoperative recurrence in hepatic hydatid disease. J Gastrointest Surg. 2006;10:734–9.
pubmed: 16713547
Prousalidis J, Kosmidis C, Anthimidis G, Kapoutzis K, Karamanlis E, Fachantidis E. Postoperative recurrence of cystic hydatidosis. Can J Surg. 2012;55:15–20.
pubmed: 21939605 pmcid: 3270079
Sielaff TD, Taylor B, Langer B. Recurrence of hydatid disease. World J Surg. 2001;25:83–6.
pubmed: 11213160
Little JM, Hollands MJ, Ekberg H. Recurrence of hydatid disease. World J Surg. 1988;12:700–4.
pubmed: 3072778
Alizadeh Z, Mahami-Oskouei M, Spotin A, Kazemi T, Ahmadpour E, Cai P, et al. Parasite-derived microRNAs in plasma as novel promising biomarkers for the early detection of hydatid cyst infection and post-surgery follow-up. Acta Trop. 2020;202:105255.
pubmed: 31682814
Piccoli L, Tamarozzi F, Cattaneo F, Mariconti M, Filice C, Bruno A, et al. Long-term sonographic and serological follow-up of inactive echinococcal cysts of the liver: hints for a “watch-and-wait” approach. PLoS Negl Trop Dis. 2014;8:e3057.
pubmed: 25122222 pmcid: 4133254
Hernandez-Gonzalez A, Muro A, Barrera I, Ramos G, Orduna A, Siles-Lucas M. Usefulness of four different Echinococcus granulosus recombinant antigens for serodiagnosis of unilocular hydatid disease (UHD) and postsurgical follow-up of patients treated for UHD. Clin Vaccine Immunol CVI. 2008;15:147–53.
pubmed: 17989342
Rigano R, Ioppolo S, Ortona E, Margutti P, Profumo E, Ali MD, et al. Long-term serological evaluation of patients with cystic echinococcosis treated with benzimidazole carbamates. Clin Exp Immunol. 2002;129:485–92.
pubmed: 12197890 pmcid: 1906476
Hernandez-Gonzalez A, Sanchez-Ovejero C, Manzano-Roman R, Gonzalez Sanchez M, Delgado JM, Pardo-Garcia T, et al. Evaluation of the recombinant antigens B2t and 2B2t, compared with hydatid fluid, in IgG-ELISA and immunostrips for the diagnosis and follow up of CE patients. PLoS Negl Trop Dis. 2018;12:e0006741.
pubmed: 30188936 pmcid: 6143278
Carmena D, Benito A, Eraso E. Antigens for the immunodiagnosis of Echinococcus granulosus infection: an update. Acta Trop. 2006;98:74–86.
pubmed: 16527225
Monteiro KM, de Carvalho MO, Zaha A, Ferreira HB. Proteomic analysis of the Echinococcus granulosus metacestode during infection of its intermediate host. Proteomics. 2010;10:1985–99.
pubmed: 20217864
Tamarozzi F, Sako Y, Ito A, Piccoli L, Grisolia A, Itoh S, et al. Recombinant AgB8/1 ELISA test vs. commercially available IgG ELISA test in the diagnosis of cystic echinococcosis. Parasite Immunol. 2013;35:433–40.
pubmed: 23834586
Jiang L, Zhang Y-G, Liu M-X, Feng Z. Analysis on the reactivity of five subunits of antigen B family in serodiagnosis of echinococcosis. Exp Parasitol. 2012;131:85–91.
pubmed: 22446351
Monteiro KM, Cardoso MB, Follmer C, da Silveira NP, Vargas DM, Kitajima EW, et al. Echinococcus granulosus antigen B structure: subunit composition and oligomeric states. PLoS Negl Trop Dis. 2012;6:e1551.
pubmed: 22413028 pmcid: 3295803
Sarkari B, Rezaei Z. Immunodiagnosis of human hydatid disease: Where do we stand? World J Methodol. 2015;5:185–95.
pubmed: 26713278 pmcid: 4686415
Hernandez-Gonzalez A, Santivanez S, Garcia HH, Rodriguez S, Munoz S, Ramos G, et al. Improved serodiagnosis of cystic echinococcosis using the new recombinant 2B2t antigen. PLoS Negl Trop Dis. 2012;6:e1714.
pubmed: 22802975 pmcid: 3389031
Ben Nouir N, Gianinazzi C, Gorcii M, Muller N, Nouri A, Babba H, et al. Isolation and molecular characterization of recombinant Echinococcus granulosus P29 protein (recP29) and its assessment for the post-surgical serological follow-up of human cystic echinococcosis in young patients. Trans R Soc Trop Med Hyg. 2009;103:355–64.
pubmed: 19027129
Nouir NB, Nuñez S, Frei E, Gorcii M, Müller N, Gianinazzi C, et al. Post-surgical follow-up (by ELISA and immunoblotting) of cured versus non-cured cystic echinococcosis in young patients. Parasitology. 2008;135:105–14.
pubmed: 17767795
Ben Nouir N, Nunez S, Gianinazzi C, Gorcii M, Muller N, Nouri A, et al. Assessment of Echinococcus granulosus somatic protoscolex antigens for serological follow-up of young patients surgically treated for cystic echinococcosis. J Clin Microbiol. 2008;46:1631–40.
pubmed: 18367566
Kittelberger R, Reichel MP, Jenner J, Heath DD, Lightowlers MW, Moro P, et al. Evaluation of three enzyme-linked immunosorbent assays (ELISAs) for the detection of serum antibodies in sheep infected with Echinococcus granulosus. Vet Parasitol. 2002;110:57–76.
pubmed: 12446090
Craig PS, Gasser RB, Parada L, Cabrera P, Parietti S, Borgues C, et al. Diagnosis of canine echinococcosis: comparison of coproantigen and serum antibody tests with arecoline purgation in Uruguay. Vet Parasitol. 1995;56:293–301.
pubmed: 7754606
Gasser RB, Lightowlers MW, Obendorf DL, Jenkins DJ, Rickard MD. Evaluation of a serological test system for the diagnosis of natural Echinococcus granulosus infection in dogs using E granulosus protoscolex and oncosphere antigens. Aust Vet J. 1988;65:369–73.
pubmed: 3223848
Stojkovic M, Adt HM, Rosenberger K, Boubaker G, Hernandez-Gonzalez A, Junghanss T, et al. Follow-up of surgically treated patients with cystic echinococcosis: can novel recombinant antigens compete with imaging? Analysis of a patient cohort. Trop Med Int Health. 2017;22:614–21.
pubmed: 28218991
Ben Salah E, Sakly W, Barrera C, Mosbahi S, Bellanger AP, Farhani R, et al. Soluble programmed death-1 (sPD-1) as predictor of early surgical outcomes of pediatric cystic echinococcosis. Parasite Immunol. 2020;43(3):e12809.
pubmed: 33207012
WHO Informal Working Group. International classification of ultrasound images in cystic echinococcosis for application in clinical and field epidemiological settings. Acta tropica. 2003;85:253–61.
Hosch W, Junghanss T, Stojkovic M, Brunetti E, Heye T, Kauffmann GW, et al. Metabolic viability assessment of cystic echinococcosis using high-field 1H MRS of cyst contents. NMR Biomed. 2008;21:734–54.
pubmed: 18384178
Brunetti E, Kern P, Vuitton DA. Expert consensus for the diagnosis and treatment of cystic and alveolar echinococcosis in humans. Acta Trop. 2010;114:1–16.
pubmed: 19931502
Muller J, Wastling J, Sanderson S, Muller N, Hemphill A. A novel Giardia lamblia nitroreductase, GlNR1, interacts with nitazoxanide and other thiazolides. Antimicrob Agents Chemother. 2007;51:1979–86.
pubmed: 17438059 pmcid: 1891416
Poretti D, Felleisen E, Grimm F, Pfister M, Teuscher F, Zuercher C, et al. Differential immunodiagnosis between cystic hydatid disease and other cross-reactive pathologies. Am J Trop Med Hyg. 1999;60:193–8.
pubmed: 10072135
Manzano-Roman R, Sanchez-Ovejero C, Hernandez-Gonzalez A, Casulli A, Siles-Lucas M. Serological diagnosis and follow-up of human cystic echinococcosis: a new hope for the future? Biomed Res Int. 2015;2015:428205.
pubmed: 26504805 pmcid: 4609352
Dehkordi AB, Sanei B, Yousefi M, Sharafi SM, Safarnezhad F, Jafari R, et al. Albendazole and treatment of hydatid cyst: review of the literature. Infect Disord Drug Targets. 2019;19:101–4.
pubmed: 29956639
Ma J, Benz C, Grimaldi R, Stockdale C, Wyatt P, Frearson J, et al. Nuclear DBF-2-related kinases are essential regulators of cytokinesis in bloodstream stage Trypanosoma brucei. J Biol Chem. 2010;285:15356–68.
pubmed: 20231285 pmcid: 2865264
Hidalgo C, Garcia MP, Stoore C, Ramirez JP, Monteiro KM, Hellman U, et al. Proteomics analysis of Echinococcus granulosus protoscolex stage. Vet Parasitol. 2016;218:43–5.
pubmed: 26872926
Chen L, Chen H, Yao C, Chang C, Xia H, Zhang C, et al. The toxicity of NaF on BmN cells and a comparative proteomics approach to identify protein expression changes in cells under NaF-stress: impact of NaF on BmN cells. J Hazard Mater. 2015;286:624–31.
pubmed: 25661258
Li ZJ, Zhao W. Analysis of protoscoleces-specific antigens from Echinococcus granulosus with proteomics combined with Western blot. Biomed Environ Sci. 2012;25:718–23.
pubmed: 23228843
Hou Q-L, Wang H, Zhang Z-Z, Cao W-Y, Zhang F-C, Zhang W-B. Immunolocalization of the antioxidant protein TPx of Echinococcus granulosus. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi. 2007;23:998–1000.
pubmed: 17988575
Li J, Zhang W-B, Loukas A, Lin R-Y, Ito A, Zhang L-H, et al. Functional expression and characterization of Echinococcus granulosus thioredoxin peroxidase suggests a role in protection against oxidative damage. Gene. 2004;326:157–65.
pubmed: 14729274

Auteurs

Eya Ben Salah (EB)

Département de Biologie Clinique B, Faculté de Pharmacie, Laboratoire de Parasitologie-Mycologie Médicale Et Moléculaire, LR12ES08, Université de Monastir, 1 Rue Avicenne, 5000, Monastir, Tunisie.

Coralie Barrera (C)

Department of Parasitology Mycology, University Hospital of Besançon, UMR/CNRS 6249 Chrono-Environnement Research Team, University of Bourgogne- Franche-Comté, Besançon, France.

Sana Mosbahi (S)

Pediatric Surgery Department, Fattouma Bourguiba Hospital, Medical School , Monastir, Tunisia.

Bruno Gottstein (B)

Institute for Infectious Diseases, Faculty of Medicine, University of Bern, 3001, Bern, Switzerland.

Mar Siles-Lucas (M)

Instituto de Recursos Naturales Y Agrobiología de Salamanca (IRNASA-CSIC), 37008, Salamanca, España.

Samia Belhassen (S)

Pediatric Surgery Department, Fattouma Bourguiba Hospital, Medical School , Monastir, Tunisia.

Abdellatif Nouri (A)

Pediatric Surgery Department, Fattouma Bourguiba Hospital, Medical School , Monastir, Tunisia.

Hamouda Babba (H)

Département de Biologie Clinique B, Faculté de Pharmacie, Laboratoire de Parasitologie-Mycologie Médicale Et Moléculaire, LR12ES08, Université de Monastir, 1 Rue Avicenne, 5000, Monastir, Tunisie.

Laurence Millon (L)

Department of Parasitology Mycology, University Hospital of Besançon, UMR/CNRS 6249 Chrono-Environnement Research Team, University of Bourgogne- Franche-Comté, Besançon, France.

Wahiba Sakly (W)

Département de Biologie Clinique B, Faculté de Pharmacie, Laboratoire de Parasitologie-Mycologie Médicale Et Moléculaire, LR12ES08, Université de Monastir, 1 Rue Avicenne, 5000, Monastir, Tunisie. wsaklya@gmail.com.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH