Abstract
Human bocavirus (HBoV) is a prevalent virus worldwide and is mainly associated with respiratory disorders. Recently, it was detected in several disease conditions, including cancers. Colorectal cancer (CRC) is the third main cause of cancers worldwide. Risk factors that initiate cell transformation include nutritional, hereditary and infectious causes. The aim of the current study was to screen for the presence of HBoV in solid tumors of colorectal cancer and to determine the genotypes of the detected strains. Surgically excised and paraffin-embedded colorectal cancer tissue specimens from 101 male and female patients with and without metastasis were collected over the last four years. Pathological analysis and tumor stages were determined. The presence of HBoV was screened by polymerase chain reaction, and the genotype of the detected HBoV was determined by direct gene sequencing. Most of the examined specimens were adenocarcinoma with mucinous activity in many of them. Twenty-four out of 101 (23.8 %) CRC tissue specimens were found to contain HBoV-1. Low sequence diversity was recorded in the detected strains. The virus was detected in both male and female patients with an age range of 30-75 years. It is proposed that HBoV-1 could play a potential role in the induction of CRC.
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References
Cancer Facts and Figures 2016 (2016) American Cancer Society, 2016. http://www.cancer.org/acs/groups/content/@research/documents/document/acspc-047079.pdf
Lynch HT, de la Chapelle A (2003) Hereditary colorectal cancer. N Engl J Med 348(10):919–932. doi:10.1056/NEJMra012242
Chan DS, Lau R, Aune D, Vieira R, Greenwood DC, Kampman E, Norat T (2011) Red and processed meat and colorectal cancer incidence: meta-analysis of prospective studies. PloS One 6(6):e20456. doi:10.1371/journal.pone.0020456
Liang PS, Chen TY, Giovannucci E (2009) Cigarette smoking and colorectal cancer incidence and mortality: systematic review and meta-analysis. Int J Cancer 124(10):2406–2415. doi:10.1002/ijc.24191
Brenner H, Kloor M, Pox CP (2014) Colorectal cancer. Lancet (London, England) 383(9927):1490–1502. doi:10.1016/s0140-6736(13)61649-9
Coelho TR, Almeida L, Lazo PA (2010) JC virus in the pathogenesis of colorectal cancer, an etiological agent or another component in a multistep process? Virol J 7:42. doi:10.1186/1743-422x-7-42
Munoz N (2000) Human papillomavirus and cancer: the epidemiological evidence. J Clin Virol 19(1–2):1–5
Chen H, Chen XZ, Waterboer T, Castro FA, Brenner H (2015) Viral infections and colorectal cancer: a systematic review of epidemiological studies. Int J Cancer 137(1):12–24. doi:10.1002/ijc.29180
ICTV (2014) International Committee of Virus Taxonomy. http://www.ictvonline.org/virusTaxonomy.asp.
Kapoor A, Slikas E, Simmonds P, Chieochansin T, Naeem A, Shaukat S, Alam MM, Sharif S, Angez M, Zaidi S, Delwart E (2009) A newly identified bocavirus species in human stool. J Infect Dis 199(2):196–200
Kapoor A, Simmonds P, Slikas E, Li L, Bodhidatta L, Sethabutr O, Triki H, Bahri O, Oderinde BS, Baba MM, Bukbuk DN, Besser J, Bartkus J, Delwart E (2010) Human bocaviruses are highly diverse, dispersed, recombination prone, and prevalent in enteric infections. J Infect Dis 201(11):1633–1643
Allander T, Tammi MT, Eriksson M, Bjerkner A, Tiveljung-Lindell A, Andersson B (2005) Cloning of a human parvovirus by molecular screening of respiratory tract samples. Proc Natl Acad Sci USA 102(36):12891–12896
Volz S, Schildgen O, Klinkenberg D, Ditt V, Muller A, Tillmann RL, Kupfer B, Bode U, Lentze MJ, Simon A (2007) Prospective study of human bocavirus (HBoV) infection in a pediatric university hospital in Germany 2005/2006. J Clin Virol 40(3):229–235. doi:10.1016/j.jcv.2007.07.017
Ma X, Endo R, Ishiguro N, Ebihara T, Ishiko H, Ariga T, Kikuta H (2006) Detection of human bocavirus in Japanese children with lower respiratory tract infections. J Clin Microbiol 44(3):1132–1134. doi:10.1128/jcm.44.3.1132-1134.2006
Kesebir D, Vazquez M, Weibel C, Shapiro ED, Ferguson D, Landry ML, Kahn JS (2006) Human bocavirus infection in young children in the US: molecular epidemiological profile and clinical characteristics of a newly emerging respiratory virus. J Infect Dis 194(9):1276–1282
Fry AM, Lu X, Chittaganpitch M, Peret T, Fischer J, Dowell SF, Anderson LJ, Erdman D, Olsen SJ (2007) Human bocavirus: a novel parvovirus epidemiologically associated with pneumonia requiring hospitalization in Thailand. J Infect Dis 195(7):1038–1045. doi:10.1086/512163
Bastien N, Brandt K, Dust K, Ward D, Li Y (2006) Human bocavirus infection, Canada. Emerg Infect Dis 12(5):848–850
Arthur JL, Higgins GD, Davidson GP, Givney RC, Ratcliff RM (2009) A novel bocavirus associated with acute gastroenteritis in Australian children. PLoS Pathog 5(4):e1000391
Abdel-Moneim AS, Kamel MM, Al-Ghamdi AS, Al-Malky MI (2013) Detection of bocavirus in children suffering from acute respiratory tract infections in Saudi Arabia. PloS One 8(1):e55500. doi:10.1371/journal.pone.0055500
Abdel-Moneim AS, Kamel M, Hamed DH, Hassan SS, Soliman MS, Al-Quraishy S, El-Kholy A (2016) A novel primer set for improved direct gene sequencing of human bocavirus genotype-1 from clinical samples. J Virol Methods 228:108–113. doi:10.1016/j.jviromet.2015.11.023
Koskenvuo M, Mottonen M, Waris M, Allander T, Salmi TT, Ruuskanen O (2008) Human bocavirus in children with acute lymphoblastic leukemia. Eur J Pediatr 167(9):1011–1015. doi:10.1007/s00431-007-0631-8
Brebion A, Vanlieferinghen P, Dechelotte P, Boutry M, Peigue-Lafeuille H, Henquell C (2014) Fatal subacute myocarditis associated with human bocavirus 2 in a 13-month-old child. J Clin Microbiol 52(3):1006–1008. doi:10.1128/jcm.03013-13
Mitui MT, Tabib SM, Matsumoto T, Khanam W, Ahmed S, Mori D, Akhter N, Yamada K, Kabir L, Nishizono A, Soderlund-Venermo M, Ahmed K (2012) Detection of human bocavirus in the cerebrospinal fluid of children with encephalitis. Clin Infect Dis 54(7):964–967. doi:10.1093/cid/cir957
Bonvicini F, Manaresi E, Gentilomi GA, Di Furio F, Zerbini M, Musiani M, Gallinella G (2011) Evidence of human bocavirus viremia in healthy blood donors. Diagn Microbiol Infect Dis 71(4):460–462. doi:10.1016/j.diagmicrobio.2011.08.019
Schildgen V, Malecki M, Tillmann RL, Brockmann M, Schildgen O (2013) The human bocavirus is associated with some lung and colorectal cancers and persists in solid tumors. PloS One 8(6):e68020. doi:10.1371/journal.pone.0068020
Li Y, Dong Y, Jiang J, Yang Y, Liu K, Li Y (2012) High prevelance of human parvovirus infection in patients with malignant tumors. Oncol Lett 3(3):635–640. doi:10.3892/ol.2012.548
Romani S, Mohebbi SR, Khanyaghma M, Azimzadeh P, Bozorgi SM, Damavand B, Jadali F (2013) Detection of human bocavirus 1, 2 and 3 from patients with acute gastroenteritis. Gastroenterol Hepatol Bed Bench 6(Suppl 1):S77–S81
Perry WB, Connaughton JC (2007) Abdominoperineal resection: how is it done and what are the results? Clin Colon Rectal Surg 20(3):213–220. doi:10.1055/s-2007-984865
Weiser MR, Quah HM, Shia J, Guillem JG, Paty PB, Temple LK, Goodman KA, Minsky BD, Wong WD (2009) Sphincter preservation in low rectal cancer is facilitated by preoperative chemoradiation and intersphincteric dissection. Annals Surg 249(2):236–242. doi:10.1097/SLA.0b013e318195e17c
De Dosso S, Sessa C, Saletti P (2009) Adjuvant therapy for colon cancer: present and perspectives. Cancer Treat Rev 35(2):160–166. doi:10.1016/j.ctrv.2008.10.001
Davis NC, Evans EB, Cohen JR, Theile DE (1984) Staging of colorectal cancer. The Australian clinico-pathological staging (ACPS) system compared with Dukes’ system. Dis Colon Rectum 27(11):707–713
Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: Methods in molecular biology. Humana Press, Totowa, pp 365–386
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
SPSS-Inc. (2007) SPSS for Windows, Version 16.0. SPSS Inc, Chicago
Ting Y, Manos MM (1990) Detection and typing of genital human papillomaviruses. In: Innis M, Gelfand D, Sninsky J, White T (eds) PCR protocols: a guide to methods and applications. Academic Press, Inc., San Diego, Calif, pp 356–367
Lusebrink J, Schildgen V, Tillmann RL, Wittleben F, Bohmer A, Muller A, Schildgen O (2011) Detection of head-to-tail DNA sequences of human bocavirus in clinical samples. PloS One 6(5):e19457. doi:10.1371/journal.pone.0019457
Kapoor A, Hornig M, Asokan A, Williams B, Henriquez JA, Lipkin WI (2011) Bocavirus episome in infected human tissue contains non-identical termini. PloS One 6(6):e21362. doi:10.1371/journal.pone.0021362
Berns KI (1990) Parvovirus replication. Microbiol Rev 54(3):316–329
Hao Y, Gao J, Zhang X, Liu N, Li J, Zheng L, Duan Z (2015) Seroepidemiology of human bocaviruses 1 and 2 in China. PloS One 10(4):e0122751. doi:10.1371/journal.pone.0122751
Oleksiewicz MB, Alexandersen S (1997) S-phase-dependent cell cycle disturbances caused by Aleutian mink disease parvovirus. J Virol 71(2):1386–1396
Op De Beeck A, Caillet-Fauquet P (1997) Viruses and the cell cycle. Progr Cell Cycle Res 3:1–19
Schenk T, Strahm B, Kontny U, Hufnagel M, Neumann-Haefelin D, Falcone V (2007) Disseminated bocavirus infection after stem cell transplant. Emerg Infect Dis 13(9):1425–1427. doi:10.3201/eid1309.070318
Falcone V, Ridder GJ, Panning M, Bierbaum S, Neumann-Haefelin D, Huzly D (2011) Human bocavirus DNA in paranasal sinus mucosa. Emerg Infect Dis 17(8):1564–1565. doi:10.3201/eid1708.101944
Eklund L, Bry M, Alitalo K (2013) Mouse models for studying angiogenesis and lymphangiogenesis in cancer. Mol Oncol 7(2):259–282. doi:10.1016/j.molonc.2013.02.007
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This study was supported by the Taif University, through the Grant project number (3970-436-1).
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SUPPL. 1 Deduced amino acid sequence of the terminal VP1 protein motifs of different HBoV-1 strains detected in CRC cases. a Amino acid numbering based on ST1 (accession number DQ000495) VP1 (TIFF 195 kb)
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Abdel-Moneim, A.S., El-Fol, H.A., Kamel, M.M. et al. Screening of human bocavirus in surgically excised cancer specimens. Arch Virol 161, 2095–2102 (2016). https://doi.org/10.1007/s00705-016-2885-9
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DOI: https://doi.org/10.1007/s00705-016-2885-9