Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-06T02:40:21.184Z Has data issue: false hasContentIssue false
  • English
  • Français

Schistosoma mansoni and endocarditis: from egg to free DNA detection in Egyptian patients and infected BALB/c mice

Published online by Cambridge University Press:  21 January 2018

M.A. Hasby Saad  and
M.M. Watany
M.A. Hasby Saad*
Affiliation:
Medical Parasitology, Tanta University, Faculty of Medicine, Egypt
M.M. Watany
Affiliation:
Clinical Pathology, Tanta University, Faculty of Medicine, Egypt
*
Author for correspondence: M.A. Hasby Saad, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

With the growing incidence of closed schistosomiasis and uncommon presentations, there is a risk of the infection rate being underestimated. A study in Japan reported an unexplained case of endocarditis that was finally diagnosed as a complex Schistosoma japonicum infection; in the absence of advanced techniques, the diagnosis was delayed. We therefore set out to explore the incidence of Schistosoma mansoni in endocarditis patients coming from areas of Egypt where S. mansoni is endemic. We also investigated histopathological changes in the cardiac valves and the presence of cell-free parasite DNA (CFPD) in cardiac tissues of laboratory mice infected with S. mansoni. The study included 186 patients with the manifestations of infective endocarditis. Eggs were detected in the stool samples of 5.91% of patients. Seropositivity was reported in 23.66% of patients and antigen was detected in the urine samples of 10.21%. Using real-time polymerase chain reaction (PCR), CFPD was detected in the blood of 6.98% of the endocarditis patients and 95% of the infected mice, while the cardiac samples of 45% of the mice tested positive for CFPD (means ± SD = 1390.2 ± 283.65, 2158.72 ± 1103.1 and 5.71 ± 2.91, respectively). Histopathological examination revealed abnormal collagen deposition, inflammatory cells and haemorrhagic pigmentation in the heart sections. Despite the low incidence of S. mansoni infection in the studied cohort, the presence of CFPD in the cardiac tissue of infected mice makes it necessary to: (1) investigate the hazards of CFPD deposition in endothelium-rich organs; and (2) test the potential of CFPD to trigger tissue inflammation, abnormal proliferation or genome integration.

Type
Research Paper
Information
Journal of Helminthology , Volume 93 , Issue 2 , March 2019 , pp. 139 - 148
Copyright
Copyright © Cambridge University Press 2018 

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

Abath, FG, Gomes, AL, Melo, FL, Barbosa, CS and Werkhauser, RP (2006) Molecular approaches for the detection of Schistosoma mansoni: possible applications in the detection of snail infection, monitoring of transmission sites, and diagnosis of human infection. Memorias Instituto Oswaldo Cruz 1, 145–148.Google Scholar
Adisa, J, Egbujo, E, Yahaya, B and Echejoh, G (2012) Primary infertility associated with Schistosoma mansoni: a case report from the Jos plateau, north central Nigeria. African Health Sciences 12, 563–565.Google Scholar
Barakat, RM (2013) Epidemiology of schistosomiasis in Egypt: Travel through time: Review. Journal of Advanced Research 4, 425–432.Google Scholar
Barda, B, Coulibaly, JT, Hatz, C and Keiser, J (2017) Ultrasonographic evaluation of urinary tract morbidity in school-aged and preschool-aged children infected with Schistosoma haematobium and its evolution after praziquantel treatment: a randomized controlled trial. PLoS Neglected Tropical Diseases 11, e0005400. doi: 10.1371/journal.pntd.0005400.Google Scholar
Batal, I, Domsic, RT, Medsger, TA and Bastacky, S (2010) Scleroderma renal crisis: a pathology perspective. International Journal of Rheumatology 2010, 543704. doi:10.1155/2010/543704.Google Scholar
Bettegowda, C, Sausen, M, Leary, RJ, et al. (2014) Detection of circulating tumor DNA in early- and late-stage human malignancies. Science Translational Medicine 6, 224ra24. doi: 10.1126/scitranslmed.3007094.Google Scholar
Bischoff, FZ, Lewis, DE and Simpson, JL (2005) Cell-free fetal DNA in maternal blood: kinetics, source and structure. Human Reproduction Update 11, 59–67.Google Scholar
Camuset, G, Wolff, V, Marescaux, C, Abou-Bacar, A, Candolfi, E, Lefebvre, N, Christmann, D and Hansmann, Y (2012) Cerebral vasculitis associated with Schistosoma mansoni infection. BMC Infectious Diseases 14, 220. doi: 10.1186/1471-2334-12-220.Google Scholar
Chernousova, S and Epple, M (2017) Live-cell imaging to compare the transfection and gene silencing efficiency of calcium phosphate nanoparticles and a liposomal transfection agent. Gene Therapy 24, 282–289.Google Scholar
Chistulo, L, Loverde, P and Engels, D (2004) Schistosomiasis. Nature Reviews of Microbiology 2, 12–13.Google Scholar
Colley, DG and Secor, WE (2014) Immunology of human schistosomiasis. Parasite Immunology 36, 347–357.Google Scholar
Coscas, R, Bensussan, M, Jacob, MP, et al. (2017) Free DNA precipitates calcium phosphate apatite crystals in the arterial wall in vivo. Atherosclerosis 259, 60–67.Google Scholar
Coulibaly, JT, N'Goran, EK, Utzinger, J, Doenhoff, MJ and Dawson, EM (2013) A new rapid diagnostic test for detection of anti-Schistosoma mansoni and anti-Schistosoma haematobium antibodies. Parasites & Vectors 29, 6–29.Google Scholar
de Cleva, R, Herman, P, Pugliese, V, Zilberstein, B, Saad, WA, Rodrigues, JJ and Laudanna, AA (2003) Prevalence of pulmonary hypertension in patients with hepatosplenic Mansonic schistosomiasis – prospective study. Hepato-gastroenterology 50, 2028–2030.Google Scholar
Doenhoff, MJ, Kusel, JR, Coles, GC and Cioli, D (2002) Resistance of Schistosoma mansoni to praziquantel: is there a problem? Transactions of the Royal Society of Tropical Medicine and Hygiene 96, 465–469.Google Scholar
Doenhoff, MJ, El-Faham, M, Liddell, S, Fuller, HR, Stanley, RG and Schramm, JE (2016) Cross-reactivity between Schistosoma mansoni antigens and the latex allergen Hev b 7: putative implication of cross-reactive carbohydrate determinants (CCDs). PLoS One 11, e0159542. doi: 10.1371/journal.pone.0159542.Google Scholar
Edberg, JC, Tosic, L and Taylor, RP (1989) Immune adherence and the processing of soluble complement-fixing antibody/DNA immune complexes in mice. Clinical Immunology and Immunopathology 51, 118–132.Google Scholar
El-Khoby, T, Galal, N, Fenwick, A, et al. (2000) The epidemiology of schistosomiasis in Egypt: summary findings in Nine governorates. American Journal of Tropical Medicine and Hygiene 62, 88–99.Google Scholar
Ferrari, TCA and Moreira, PRR (2011) Neuroschistosomiasis: clinical symptoms and pathogenesis. Lancet Neurology 10, 853–864.Google Scholar
Firth, AL, Mandel, J and Yuan, JX-J (2010) Idiopathic pulmonary arterial hypertension. Disease Models & Mechanisms 3, 268–273.Google Scholar
Fouad, YM and Yehia, R (2014) Hepato-cardiac disorders. World Journal of Hepatology 6, 41–54.Google Scholar
Garcia, LSSR and Palmer, JC (1999) Algorithms for detection and identification of parasites. pp. 1336–1354 in Murray, PR (Ed.) Manual of clinical microbiology. Washington DC, American Society for Microbiology Press.Google Scholar
Gasim, GI, Bella, A and Adam, I (2015) Schistosomiasis, hepatitis B and hepatitis C co-infection. Virology Journal 12, 19. doi:10.1186/s12985-015-0251-2.Google Scholar
Gomes, AL, Melo, FL, Werkhauser, RP and Abath, FG (2006) Development of a real time polymerase chain reaction for quantitation of Schistosoma mansoni DNA. Memórias do Instituto Oswaldo Cruz 1, 133–136.Google Scholar
Hamburger, J, Turetske, T, Kapeller, I and Deresiewicz, R (1991) Highly repeated short DNA sequences in the genome of Schistosoma mansoni recognized by a species-specific probe. Molecular and Biochemical Parasitology 44, 73–80.Google Scholar
Hamilton, JV, Klinkert, M and Doenhoff, MJ (1998) Diagnosis of schistosomiasis: antibody detection, with notes on parasitological and antigen detection methods. Parasitology 117, S41–S57.Google Scholar
Hidron, A, Vogenthaler, N, Santos-Preciado, JI, Rodriguez-Morales, AJ, Franco-Paredes, C and Rassi, A (2010) Cardiac involvement with parasitic infections. Clinical Microbiology Reviews 23, 324–349.Google Scholar
Igetei, JE, El-Faham, M, Liddell, S and Doenhoff, MJ (2017) Antigenic cross-reactivity between Schistosoma mansoni and peanut: a role for cross-reactive carbohydrate determinants (CCDs) and implications for the hygiene hypothesis. Immunology 150, 506–517.Google Scholar
Kato-Hayashi, N, Yasuda, M, Yuasa, J, Isaka, S, Haruki, K, Ohmae, H and Chigusa, Y (2013) Use of cell-free circulating schistosome DNA in serum, urine, semen, and saliva to monitor a case of refractory imported schistosomiasis hematobia. Journal of Clinical Microbiology 51, 3435–3438.Google Scholar
Katz, N, Chaves, A and Pellegrino, J (1972) A simple device for quantitative stool thick-smear technique in schistosomiasis mansoni. Journal of the São Paulo Institute of Tropical Medicine 14, 397–400.Google Scholar
Khan, MA, Wu, VM, Ghosh, S and Uskoković, V (2016) Gene delivery using calcium phosphate nanoparticles: optimization of the transfection process and the effects of citrate and poly(l-lysine) as additives. Journal of Colloid and Interface Science 1, 48–58.Google Scholar
Leopold, JA (2012) Cellular mechanisms of aortic valve calcification. Circulation. Cardiovascular Interventions 5, 605–614.Google Scholar
Messias-Reason, IJ, Hayashi, SY, Nisihara, RM and Kirschfink, M (2002) Complement activation in infective endocarditis: correlation with extracardiac manifestations and prognosis. Clinical and Experimental Immunology 127, 310–315.Google Scholar
Morgan, IM, DiNardo, LJ and Windle, B (2017) Integration of human papillomavirus genomes in head and neck cancer: is it time to consider a paradigm shift? Viruses 3, 8. doi: 10.3390/v9080208.Google Scholar
Mutapi, F, Maizels, R, Fenwick, A and Woolhouse, M (2017) Human schistosomiasis in the post mass drug administration era. Lancet. Infectious Diseases 17, e42. doi:10.1016/S1473-3099(16)30475-3.Google Scholar
Newman, AM, Bratman, SV, To, J et al. (2014) An ultrasensitive method for quantitating circulating tumor DNA with broad patient coverage. Nature Medicine 20, 548–554.Google Scholar
Nour, NM (2010) Schistosomiasis: health effects on women. Reviews in Obstetrics & Gynecology 3, 28–32.Google Scholar
Ochodo, EA, Gopalakrishna, G, Spek, B, Reitsma, JB, van Lieshout, L, Polman, K, Lamberton, P, Bossuyt, PM and Leeflang, MM (2015) Circulating antigen tests and urine reagent strips for diagnosis of active schistosomiasis in endemic areas. Cochrane Database for Systemic Reviews 11, CD009579. doi: 10.1002/14651858.CD009579.pub2.Google Scholar
Ortu, G, Ndayishimiye, O, Clements, M, et al. (2017) Countrywide reassessment of Schistosoma mansoni infection in Burundi using a urine-circulating cathodic antigen rapid test: informing the national control program. American Journal of Tropical Medicine and Hygiene 96, 664–673.Google Scholar
Othman, AA and Soliman, RH (2015) Schistosomiasis in Egypt: A never-ending story? Acta Tropica. 148, 179–190.Google Scholar
Pantel, K (2016) Blood-based analysis of circulating cell-free DNA and tumor cells for early cancer detection. PLoS Medicine 13, e1002205.Google Scholar
Papamatheakis, DG, Mocumbi, AOH, Kim, NH and Mandel, J (2014) Schistosomiasis-associated pulmonary hypertension. Pulmonary Circulation. 4, 596–611.Google Scholar
Pérez-Vázquez, A, Fariñas, MC, García-Palomo, JD, Bernal, JM, Revuelta, JM and González-Macías, J (2000) Evaluation of the Duke criteria in 93 episodes of prosthetic valve endocarditis: could sensitivity be improved? Archivos de medicina interna 160, 1185–1191.Google Scholar
Pillay, P, Taylor, M, Zulu, SG, et al. (2014) Real-time polymerase chain reaction for detection of Schistosoma DNA in small-volume urine samples reflects focal distribution of urogenital schistosomiasis in primary school girls in KwaZulu Natal, South Africa. American Journal of Tropical Medicine and Hygiene 90, 546–552.Google Scholar
Pisetsky, DS (2012) Antinuclear antibodies in rheumatic disease: a proposal for a function-based classification. Scandinavian Journal of Immunology 76, 223–228.Google Scholar
Pontes, LA, Dias-Neto, E and Rabello, ALT (2002) Detection by polymerase chain reaction of Schistosoma mansoni DNA in human serum and faeces. American Journal of Tropical Medicine and Hygiene 66, 157–162.Google Scholar
Pontes, LA, Oliveira, MC, Katz, N, Dias-Neto, E and Rabello, A (2003) Comparison of a polymerase chain reaction and the Kato–Katz technique for diagnosis infection with Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 68, 652–656.Google Scholar
Roperch, J-P, Benzekri, K, Mansour, H and Incitti, R (2015) Improved amplification efficiency on stool samples by addition of spermidine and its use for non-invasive detection of colorectal cancer. BMC Biotechnology 15, 41. doi:10.1186/s12896-015-0148-6.Google Scholar
Rose, MF, Zimmerman, EE, Hsu, L, Golby, AJ, Saleh, E, Folkerth, RD, Santagata, SS, Milner, DA Jr and Ramkissoon, SH (2014) Atypical presentation of cerebral schistosomiasis four years after exposure to Schistosoma mansoni. Epilepsy & Behavior Case Reports 2, 80–85.Google Scholar
Sandoval, N, Siles-Lucas, M, Perez-Arellano, JL, Carranza, C, Puente, S, López-Abán, J and Muro, A (2006) A new PCR-based approach for the specific amplification of DNA from different Schistosoma species applicable to human urine samples. Parasitology 133, 581–587.Google Scholar
Schrader, C, Schielke, A, Ellerbroek, L and Johne, R (2012) PCR inhibitors – occurrence, properties and removal. Journal of Applied Microbiology 113, 1014–1026.Google Scholar
Schwarzenbach, H, Nishida, N, Calin, GA and Pantel, K (2014) Clinical relevance of circulating cell-free microRNAs in cancer. Nature Reviews. Clinical Oncology 11, 145–156.Google Scholar
Shaker, Y, Samy, N and Ashour, E (2014) Hepatobiliary schistosomiasis. Journal of Clinical and Translational Hepatology 2, 212–216.Google Scholar
Sozzi, G, Conte, D, Leon, M, et al. (2003) Quantification of free circulating DNA as a diagnostic marker in lung cancer. Journal of Clinical Oncology 21, 3902–3908.Google Scholar
ten Hove, RJ, Verweij, JJ, Vereecken, K, Polman, K, Dieye, L and van Lieshout, L (2008) Multiplex real-time PCR for the detection and quantification of Schistosoma mansoni and S. haematobium infection in stool samples collected in northern Senegal. Transactions of the Royal Society of Tropical Medicine and Hygiene 102, 179–185.Google Scholar
Tucker, MS, Karunaratne, LB, Lewis, FA, Freitas, TC and Liang, Y (2001) Schistosomiasis. Current Protocols in Immunology 103, 19. doi:10.1002/0471142735.im1901s28.Google Scholar
Vahedi, F, Nazari, N, Arbabi, S and Peymanfar, Y (2012) Investigation of DNA integration into reproductive organs following intramuscular injection of DNA in mice. Reports of Biochemistry & Molecular Biology 1, 21–24.Google Scholar
Victor, EG, Lira, V, Arruda, A, Monteiro, I and Lima, R (1996) Cardiac granulomas due to Schistosoma eggs and endomyocardial fibrosis. Arquivos brasileiros de cardiologia 67, 259–61.Google Scholar
Vinkeles Melchers, NVS, van Dam, GJ, Shaproski, D, Kahama, AI, Brienen, EAT, Vennervald, BJ and van Lieshout, L (2014) Diagnostic performance of Schistosoma real-time PCR in urine samples from Kenyan children infected with Schistosoma haematobium: day-to-day variation and follow-up after praziquantel treatment. PLoS Neglected Tropical Diseases 8, e2807. doi: 10.1371/journal.pntd.0002807.Google Scholar
Weerakoon, KGAD, Gobert, GN, Cai, P and McManus, DP (2015) Advances in the diagnosis of human schistosomiasis. Clinical Microbiology Reviews 28, 939–967.Google Scholar
Wichmann, D, Panning, M, Quack, T, Kramme, S, Burchard, G-D, Grevelding, C and Drosten, C (2009) Diagnosing schistosomiasis by detection of cell-free parasite DNA in human plasma. PLoS Neglected Tropical Diseases 3, e422. doi: 10.1371/journal.pntd.0000422.Google Scholar
World Health Organization (WHO) (2014) Schistosomiasis fact sheet. Available at http://www.who.int/mediacentre/factsheets/fs115/en (accessed 27 October 2017).Google Scholar
Wu, L, Wu, M, Tian, D, et al. (2012) Clinical and imaging characteristics of cerebral schistosomiasis. Cell Biochemistry and Biophysics 62, 289–295.Google Scholar
Xie, Y, Chen, Y, Sun, M and Ping, Q (2013) A mini review of biodegradable calcium phosphate nanoparticles for gene delivery. Current Pharmacology and Biotechnology 14, 918e925.Google Scholar
Yanagisawa, S, Yuasa, T and Tanaka, T (2010) Clinical diagnosis of Schistosoma japonicum infection complicating infective endocarditis and liver cirrhosis. Internal Medicine 49, 1001–1005.Google Scholar
Yu, Y, Keller, SH, Remillard, CV, et al. (2009) A functional single-nucleotide polymorphism in the TRPC6 gene promoter associated with idiopathic pulmonary arterial hypertension. Circulation 119, 2313–2322.Google Scholar
Zimmermann, B, Zhong, XY, Holzgreve, W and Hahn, S (2007) Real-time quantitative polymerase chain reaction measurement of male fetal DNA in maternal plasma. Methods of Molecular Medicine 132, 43–50.Google Scholar