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Review Article

The bifacial role of helminths in cancer: Involvement of immune and non-immune mechanisms

, , , , &
Pages 138-148 | Received 15 Aug 2013, Accepted 25 Dec 2013, Published online: 04 Mar 2014

References

  • Rook GA, Dalgleish A. Infection, immunoregulation, and cancer. Immunol Rev 2011;240:141–59
  • Oikonomopoulou K, Brinc D, Kyriacou K, Diamandis EP. Infection and cancer: revaluation of the hygiene hypothesis. Clin Cancer Res 2013;19:2834–41
  • Pisani P, Parkin DM, Munoz N, Ferlay J. Cancer and infection: estimates of the attributable fraction in 1990. Cancer Epidemiol Biomarkers Prev 1997;6:387–400
  • Mayer DA, Fried B. The role of helminth infections in carcinogenesis. Adv Parasitol 2007;65:239–96
  • Fried B, Reddy A, Mayer D. Helminths in human carcinogenesis. Cancer Lett 2011;305:239–49
  • Gouda I, Mokhtar N, Bilal D, et al. Bilharziasis and bladder cancer: a time trend analysis of 9843 patients. J Egypt Natl Canc Inst 2007;19:158–62
  • Stolley PD, Lasky T. Johannes Fibiger and his Nobel Prize for the hypothesis that a worm causes stomach cancer. Ann Intern Med 1992;116:765–9
  • Bach JF. The effect of infections on susceptibility to autoimmune and allergic diseases. N Engl J Med 2002;347:911–20
  • Strachan DP. Hay fever, hygiene, and household size. BMJ 1989;299:1259–60
  • Strachan DP. Family size, infection and atopy: the first decade of the “hygiene hypothesis". Thorax 2000;55:S2–10
  • Rook GA. 99th Dahlem conference on infection, inflammation and chronic inflammatory disorders: darwinian medicine and the ‘hygiene' or ‘old friends' hypothesis. Clin Exp Immunol 2010;160:70–9
  • Wills-Karp M, Santeliz J, Karp CL. The germless theory of allergic disease: revisiting the hygiene hypothesis. Nat Rev Immunol 2001;1:69–75
  • Ngoi SM, Sylvester FA, Vella AT. The role of microbial byproducts in protection against immunological disorders and the hygiene hypothesis. Discov Med 2011;12:405–12
  • Rook GA. Review series on helminths, immune modulation and the hygiene hypothesis: the broader implications of the hygiene hypothesis. Immunology 2009;126:3–11
  • Schistosomes, liver flukes and Helicobacter pylori. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Lyon, 7–14 June 1994. IARC Monogr Eval Carcinog Risks Hum 1994;61:1–241
  • Devaraj S, Hemarajata P, Versalovic J. The human gut microbiome and body metabolism: implications for obesity and diabetes. Clin Chem 2013;59:617–28
  • Dunne DW, Cooke A. A worm's eye view of the immune system: consequences for evolution of human autoimmune disease. Nat Rev Immunol 2005;5:420–6
  • Jackson JA, Friberg IM, Little S, Bradley JE. Review series on helminths, immune modulation and the hygiene hypothesis: immunity against helminths and immunological phenomena in modern human populations: coevolutionary legacies? Immunology 2009;126:18–27
  • Fumagalli M, Pozzoli U, Cagliani R, et al. Parasites represent a major selective force for interleukin genes and shape the genetic predisposition to autoimmune conditions. J Exp Med 2009;206:1395–408
  • Maizels RM, Yazdanbakhsh M. Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat Rev Immunol 2003;3:733–44
  • Anthony RM, Rutitzky LI, Urban Jr JF, et al. Protective immune mechanisms in helminth infection. Nat Rev Immunol 2007;7:975–87
  • Sica A, Larghi P, Mancino A, et al. Macrophage polarization in tumour progression. Semin Cancer Biol 2008;18:349–55
  • Girgis NM, Gundra UM, Loke P. Immune regulation during helminth infections. PLoS Pathog [Online] 2013;9:e1003250
  • Mourglia-Ettlin G, Marques JM, Chabalgoity JA, Dematteis S. Early peritoneal immune response during Echinococcus granulosus establishment displays a biphasic behavior. PLoS Negl Trop Dis [Online] 2011;5:e1293
  • Zhang W, Li J, McManus DP. Concepts in immunology and diagnosis of hydatid disease. Clin Microbiol Rev 2003;16:18–36
  • Zhang W, Ross AG, McManus DP. Mechanisms of immunity in hydatid disease: implications for vaccine development. J Immunol 2008;181:6679–85
  • Hemminki K, Liu X, Ji J, et al. Autoimmune disease and subsequent digestive tract cancer by histology. Ann Oncol 2011;23:927–33
  • Hemminki K, Liu X, Ji J, et al. Subsequent COPD and lung cancer in patients with autoimmune disease. Eur Respir J 2011;37:463–5
  • Merrill RM, Isakson RT, Beck RE. The association between allergies and cancer: what is currently known? Ann Allergy Asthma Immunol 2007;99:102–16
  • Prizment AE, Folsom AR, Cerhan JR, et al. History of allergy and reduced incidence of colorectal cancer, Iowa Women's Health Study. Cancer Epidemiol Biomarkers Prev 2007;16:2357–62
  • Maisonneuve P, Lowenfels AB, Bueno-de-Mesquita HB, et al. Past medical history and pancreatic cancer risk: results from a multicenter case-control study. Ann Epidemiol 2010;20:92–8
  • Engkilde K, Thyssen JP, Menne T, Johansen JD. Association between cancer and contact allergy: a linkage study. BMJ Open [Online] 2011;1:e000084
  • Pompei R, Lampis G, Ingianni A, et al. Allergy and tumour outcome after primary cancer therapy. Int Arch Allergy Immunol 2004;133:174–8
  • Rastogi T, Devesa S, Mangtani P, et al. Cancer incidence rates among South Asians in four geographic regions: India, Singapore, UK and US. Int J Epidemiol 2008;37:147–60
  • Gutensohn N, Cole P. Childhood social environment and Hodgkin's disease. N Engl J Med 1981;304:135–40
  • Ma X, Buffler PA, Selvin S, et al. Daycare attendance and risk of childhood acute lymphoblastic leukaemia. Br J Cancer 2002;86:1419–24
  • Gilham C, Peto J, Simpson J, et al. Day care in infancy and risk of childhood acute lymphoblastic leukaemia: findings from UK case-control study. BMJ 2005;330:1294
  • Medzhitov R. Origin and physiological roles of inflammation. Nature 2008;454:428–35
  • Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature 2008;454:436–44
  • Berg M, Soreide K. Prevention: will an aspirin a day keep the colorectal cancer away? Nat Rev Clin Oncol 2011;8:130–1
  • Kaiser J. Will an aspirin a day keep cancer away? Science 2012;337:1471–3
  • Trinchieri G. Cancer and inflammation: an old intuition with rapidly evolving new concepts. Annu Rev Immunol 2012;30:677–706
  • Stevanovic S. Identification of tumour-associated T-cell epitopes for vaccine development. Nat Rev Cancer 2002;2:514–20
  • Hudis CA. Trastuzumab – mechanism of action and use in clinical practice. N Engl J Med 2007;357:39–51
  • Heimburg-Molinaro J, Lum M, Vijay G, et al. Cancer vaccines and carbohydrate epitopes. Vaccine 2011;29:8802–26
  • Mellman I, Coukos G, Dranoff G. Cancer immunotherapy comes of age. Nature 2011;480:480–9
  • Palucka K, Banchereau J. Cancer immunotherapy via dendritic cells. Nat Rev Cancer 2012;12:265–77
  • Scott AM, Wolchok JD, Old LJ. Antibody therapy of cancer. Nat Rev Cancer 2012;12:278–87
  • Takahashi N, Ohkuri T, Homma S, et al. First clinical trial of cancer vaccine therapy with artificially synthesized helper/killer-hybrid epitope long peptide of MAGE-A4 cancer antigen. Cancer Sci 2012;103:150–3
  • Zamarron BF, Chen W. Dual roles of immune cells and their factors in cancer development and progression. Int J Biol Sci 2011;7:651–8
  • Brandau S, Suttmann H. Thirty years of BCG immunotherapy for non-muscle invasive bladder cancer: a success story with room for improvement. Biomed Pharmacother 2007;61:299–305
  • Alexandroff AB, Nicholson S, Patel PM, Jackson AM. Recent advances in bacillus Calmette-Guerin immunotherapy in bladder cancer. Immunotherapy 2010;2:551–60
  • Osinaga E. Expression of cancer-associated simple mucin-type O-glycosylated antigens in parasites. IUBMB Life 2007;59:269–73
  • Pfister M, Gottstein B, Cerny T, Cerny A. Immunodiagnosis of echinococcosis in cancer patients. Clin Microbiol Inf 1999;5:693–7
  • Akgul H, Tez M, Unal AE, et al. Echinococcus against cancer: why not? Cancer 2003;98:1999–2000
  • Darani HY, Soozanger N, Khorami S, et al. Hydatid cyst protoscolices induce cell death in WEHI-164 fibrosarcoma cells and inhibit the proliferation of baby hamster kidney fibroblasts in vitro. J Parasitol Res 2012;2012:304183
  • Zhang W, McManus DP. Recent advances in the immunology and diagnosis of echinococcosis. FEMS Immunol Med Microbiol 2006;47:24–41
  • Springer GF. Immunoreactive T and Tn epitopes in cancer diagnosis, prognosis, and immunotherapy. J Mol Med (Berl) 1997;75:594–602
  • Alvarez ED, Medeiros A, Miguez M, et al. O-glycosylation in Echinococcus granulosus: identification and characterization of the carcinoma-associated Tn antigen. Exp Parasitol 2001;98:100–9
  • van Knapen F. Echinococcus granulosus infection and malignancy. BMJ 1980;281:195–6
  • Springer GF, Desai PR, Spencer BD, et al. T/Tn antigen vaccine is effective and safe in preventing recurrence of advanced breast carcinoma. Cancer Detect Prev 1995;19:374–80
  • Gorelik E, Segal S, Feldman M. On the mechanism of tumor “concomitant immunity". Int J Cancer 1981;27:847–56
  • Cox FE. Concomitant infections, parasites and immune responses. Parasitology 2001;122:S23–38
  • Fisher B, Saffer EA, Fisher ER. Comparison of concomitant and sinecomitant tumor immunity. Proc Soc Exp Biol Med 1970;135:68–71
  • Dunn GP, Bruce AT, Ikeda H, et al. Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol 2002;3:991–8
  • Nakachi K, Hayashi T, Imai K, Kusunoki Y. Perspectives on cancer immuno-epidemiology. Cancer Sci 2004;95:921–9
  • Koebel CM, Vermi W, Swann JB, et al. Adaptive immunity maintains occult cancer in an equilibrium state. Nature 2007;450:903–7
  • Boshoff C, Weiss R. AIDS-related malignancies. Nat Rev Cancer 2002;2:373–82
  • Haliotis T, Ball JK, Dexter D, Roder JC. Spontaneous and induced primary oncogenesis in natural killer (NK)-cell-deficient beige mutant mice. Int J Cancer 1985;35:505–13
  • Shankaran V, Ikeda H, Bruce AT, et al. IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 2001;410:1107–11
  • Draghiciu O, Nijman HW, Daemen T. From tumor immunosuppression to eradication: targeting homing and activity of immune effector cells to tumors. Clin Dev Immunol 2011;2011:439053
  • Adisakwattana P, Saunders SP, Nel HJ, Fallon PG. Helminth-derived immunomodulatory molecules. Adv Exp Med Biol 2009;666:95–107
  • Virginio VG, Monteiro KM, Drumond F, et al. Excretory/secretory products from in vitro-cultured Echinococcus granulosus protoscoleces. Mol Biochem Parasitol 2012;183:15–22
  • MacDonald AS, Araujo MI, Pearce EJ. Immunology of parasitic helminth infections. Infect Immun 2002;70:427–33
  • van Riet E, Hartgers FC, Yazdanbakhsh M. Chronic helminth infections induce immunomodulation: consequences and mechanisms. Immunobiology 2007;212:475–90
  • Weng M, Huntley D, Huang IF, et al. Alternatively activated macrophages in intestinal helminth infection: effects on concurrent bacterial colitis. J Immunol 2007;179:4721–31
  • Luperchio SA, Schauer DB. Molecular pathogenesis of Citrobacter rodentium and transmissible murine colonic hyperplasia. Microbes Infect 2001;3:333–40
  • Moreau E, Chauvin A. Immunity against helminths: interactions with the host and the intercurrent infections. J Biomed Biotechnol 2010;2010:428593
  • Macfarlane GT, Macfarlane S. Fermentation in the human large intestine: its physiologic consequences and the potential contribution of prebiotics. J Clin Gastroenterol 2011;45:S120–7
  • Resta SC. Effects of probiotics and commensals on intestinal epithelial physiology: implications for nutrient handling. J Physiol 2009;587:4169–74
  • Vipperla K, O'Keefe SJ. The microbiota and its metabolites in colonic mucosal health and cancer risk. Nutr Clin Pract 2012;27:624–35
  • Holmes E, Li JV, Athanasiou T, et al. Understanding the role of gut microbiome-host metabolic signal disruption in health and disease. Trends Microbiol 2011;19:349–59
  • Donohoe DR, Garge N, Zhang X, et al. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab 2011;13:517–26
  • Dumas ME. The microbial-mammalian metabolic axis: beyond simple metabolism. Cell Metab 2011;13:489–90
  • Plottel CS, Blaser MJ. Microbiome and malignancy. Cell Host Microbe 2011;10:324–35
  • Clemente JC, Ursell LK, Parfrey LW, Knight R. The impact of the gut microbiota on human health: an integrative view. Cell 2012;148:1258–70
  • Khan AA, Shrivastava A, Khurshid M. Normal to cancer microbiome transformation and its implication in cancer diagnosis. Biochim Biophys Acta 2012;1826:331–7
  • Hajishengallis G, Darveau RP, Curtis MA. The keystone-pathogen hypothesis. Nat Rev Microbiol 2012;10:717–25
  • Arthur JC, Perez-Chanona E, Muhlbauer M, et al. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 2012;338:120–3
  • Yoshimoto S, Loo TM, Atarashi K, et al. Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome. Nature 2013;499:97–101
  • Riley DR, Sieber KB, Robinson KM, et al. Bacteria-human somatic cell lateral gene transfer is enriched in cancer samples. PLoS Comput Biol [Online] 2013;9:e1003107
  • Wu S, Li RW, Li W, et al. Worm burden-dependent disruption of the porcine colon microbiota by Trichuris suis infection. PLoS One [Online] 2012;7:e35470
  • Leung JM, Loke P. A role for IL-22 in the relationship between intestinal helminths, gut microbiota and mucosal immunity. Int J Parasitol 2013;43:253–7
  • Li RW, Wu S, Li W, et al. Alterations in the porcine colon microbiota induced by the gastrointestinal nematode Trichuris suis. Infect Immun 2012;80:2150–7
  • Lai RH, Miller MJ, Jeffery E. Glucoraphanin hydrolysis by microbiota in the rat cecum results in sulforaphane absorption. Food Funct 2010;1:161–6
  • Kulkarni N, Reddy BS. Inhibitory effect of Bifidobacterium longum cultures on the azoxymethane-induced aberrant crypt foci formation and fecal bacterial beta-glucuronidase. Proc Soc Exp Biol Med 1994;207:278–83
  • Smith PM, Howitt MR, Panikov N, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 2013;341:569–73
  • Mattson MP. Hormesis defined. Ageing Res Rev 2008;7:1–7
  • Bukowski JA, Lewis RJ. Is the hygiene hypothesis an example of hormesis? Nonlinearity Biol Toxicol Med 2003;1:155–66
  • El-Bolkainy MN, Mokhtar NM, Ghoneim MA, Hussein MH. The impact of schistosomiasis on the pathology of bladder carcinoma. Cancer 1981;48:2643–8
  • Madbouly KM, Senagore AJ, Mukerjee A, et al. Colorectal cancer in a population with endemic Schistosoma mansoni: is this an at-risk population? Int J Colorectal Dis 2007;22:175–81
  • Murata M, Thanan R, Ma N, Kawanishi S. Role of nitrative and oxidative DNA damage in inflammation-related carcinogenesis. J Biomed Biotechnol [Online] 2012;2012:623019
  • Badawi AF, Mostafa MH, Aboul-Azm T, et al. Promutagenic methylation damage in bladder DNA from patients with bladder cancer associated with schistosomiasis and from normal individuals. Carcinogenesis 1992;13:877–81
  • Badawi AF, Cooper DP, Mostafa MH, et al. Promutagenic methylation damage in liver DNA of mice infected with Schistosoma mansoni. Carcinogenesis 1993;14:653–7
  • Badawi AF, Awney HA, Mostafa MH. Formation of promutagenic methylation damage in tissue-DNA of mice treated with antischistosomal agents. Cancer Lett 1993;75:167–73
  • Badawi AF, Mostafa MH, O'Connor PJ. Involvement of alkylating agents in schistosome-associated bladder cancer: the possible basic mechanisms of induction. Cancer Lett 1992;63:171–88
  • Eissa S, Swellam M, El-Khouly IM, et al. Aberrant methylation of RARbeta2 and APC genes in voided urine as molecular markers for early detection of bilharzial and nonbilharzial bladder cancer. Cancer Epidemiol Biomarkers Prev 2011;20:1657–64
  • Herrera LA, Ramirez T, Rodriguez U, et al. Possible association between Taenia solium cysticercosis and cancer: increased frequency of DNA damage in peripheral lymphocytes from neurocysticercosis patients. Trans R Soc Trop Med Hyg 2000;94:61–5
  • Herrera LA, Rodriguez U, Gebhart E, Ostrosky-Wegman P. Increased translocation frequency of chromosomes 7, 11 and 14 in lymphocytes from patients with neurocysticercosis. Mutagenesis 2001;16:495–7
  • Hsu S, Kim M, Hernandez L, et al. IKK-epsilon coordinates invasion and metastasis of ovarian cancer. Cancer Res 2012;72:5494–504
  • DiDonato JA, Mercurio F, Karin M. NF-kappaB and the link between inflammation and cancer. Immunol Rev 2012;246:379–400
  • Bauer J, Namineni S, Reisinger F, et al. Lymphotoxin, NF-kB, and cancer: the dark side of cytokines. Dig Dis 2012;30:453–68
  • Herrera LA, Santiago P, Rojas G, et al. Immune response impairment, genotoxicity and morphological transformation induced by Taenia solium metacestode. Mutat Res 1994;305:223–8
  • Hao L, Cai P, Jiang N, et al. Identification and characterization of microRNAs and endogenous siRNAs in Schistosoma japonicum. BMC Genomics [Online] 2010;11:55
  • Liu Q, Tuo W, Gao H, Zhu XQ. MicroRNAs of parasites: current status and future perspectives. Parasitol Res 2010;107:501–7
  • Simoes MC, Lee J, Djikeng A, et al. Identification of Schistosoma mansoni microRNAs. BMC Genomics [Online] 2011;12:47
  • Cheng G, Jin Y. MicroRNAs: potentially important regulators for schistosome development and therapeutic targets against schistosomiasis. Parasitology 2012;139:669–79
  • Manzano-Roman R, Siles-Lucas M. MicroRNAs in parasitic diseases: potential for diagnosis and targeting. Mol Biochem Parasitol 2012;186:81–6
  • Hu G, Zhou R, Liu J, et al. MicroRNA-98 and let-7 regulate expression of suppressor of cytokine signaling 4 in biliary epithelial cells in response to Cryptosporidium parvum infection. J Infect Dis 2010;202:125–35
  • Blomme B, Van SC, Callewaert N, Van VH. Alteration of protein glycosylation in liver diseases. J Hepatol 2009;50:592–603
  • Chandler K, Goldman R. Glycoprotein disease markers and single protein-omics. Mol Cell Proteomics 2013;12:836–45
  • Balog CI, Mayboroda OA, Wuhrer M, et al. Mass spectrometric identification of aberrantly glycosylated human apolipoprotein C-III peptides in urine from Schistosoma mansoni-infected individuals. Mol Cell Proteomics 2010;9:667–81
  • Aji T, Matsuoka H, Ishii A, et al. Retention of a mutagen, 3-amino-1-methyl-5H-pyrido[4,3-b]indole (Trp-P-2), in the liver of mice infected with Schistosoma japonicum. Mutat Res 1994;305:265–72
  • Wang Y, Holmes E, Nicholson JK, et al. Metabonomic investigations in mice infected with Schistosoma mansoni: an approach for biomarker identification. Proc Natl Acad Sci USA 2004;101:12676–81
  • Beckage NE. Endocrine and neuroendocrine host-parasite relationships. Receptor 1993;3:233–45
  • Hernandez-Bello R, Escobedo G, Guzman C, et al. Immunoendocrine host-parasite interactions during helminth infections: from the basic knowledge to its possible therapeutic applications. Parasite Immunol 2010;32:633–43
  • Phares K. An unusual host-parasite relationship: the growth hormone-like factor from plerocercoids of spirometrid tapeworms. Int J Parasitol 1996;26:575–88
  • Smout MJ, Laha T, Mulvenna J, et al. A granulin-like growth factor secreted by the carcinogenic liver fluke, Opisthorchis viverrini, promotes proliferation of host cells. PLoS Pathog 2009;5:e1000611
  • Thuwajit C, Thuwajit P, Kaewkes S, et al. Increased cell proliferation of mouse fibroblast NIH-3T3 in vitro induced by excretory/secretory product(s) from Opisthorchis viverrini. Parasitology 2004;129:455–64
  • Cataisson C, Salcedo R, Hakim S, et al. IL-1R-MyD88 signaling in keratinocyte transformation and carcinogenesis. J Exp Med 2012;209:1689–702
  • Iliopoulos D, Hirsch HA, Struhl K. An epigenetic switch involving NF-kappaB, Lin28, Let-7 MicroRNA, and IL6 links inflammation to cell transformation. Cell 2009;139:693–706
  • Guerra C, Collado M, Navas C, et al. Pancreatitis-induced inflammation contributes to pancreatic cancer by inhibiting oncogene-induced senescence. Cancer Cell 2011;19:728–39
  • Zeng S, Yang Y, Tan Y, et al. ERBB2-induced inflammation in lung carcinogenesis. Mol Biol Rep 2012;39:7911–17
  • Ray KC, Moss ME, Franklin JL, et al. Heparin-binding epidermal growth factor-like growth factor eliminates constraints on activated Kras to promote rapid onset of pancreatic neoplasia. Oncogene 2013 . [Epub ahead of print]. doi: 10.1038/onc.2013.3
  • Tye H, Kennedy CL, Najdovska M, et al. STAT3-driven upregulation of TLR2 promotes gastric tumorigenesis independent of tumor inflammation. Cancer Cell 2012;22:466–78
  • Erb KJ. Can helminths or helminth-derived products be used in humans to prevent or treat allergic diseases? Trends Immunol 2009;30:75–82
  • El-Malky M, Nabih N, Heder M, et al. Helminth infections: therapeutic potential in autoimmune disorders. Parasite Immunol 2011;33:589–93
  • Reddy MVR. Immunomodulators of helminthes: promising therapeutics for autoimmune disorders and allergic diseases. Indian J Clin Biochem 2010;25:109–10
  • Jouvin MH, Kinet JP. Trichuris suis ova: testing a helminth-based therapy as an extension of the hygiene hypothesis. J Allergy Clin Immunol 2012;130:3–10
  • Summers RW, Elliott DE, Urban Jr JF, et al. Trichuris suis therapy for active ulcerative colitis: a randomized controlled trial. Gastroenterology 2005;128:825–32
  • Bager P, Kapel C, Roepstorff A, et al. Symptoms after ingestion of pig whipworm Trichuris suis eggs in a randomized placebo-controlled double-blind clinical trial. PLoS One 2011;6:e22346
  • Bager P, Arnved J, Ronborg S, et al. Trichuris suis ova therapy for allergic rhinitis: a randomized, double-blind, placebo-controlled clinical trial. J Allergy Clin Immunol 2010;125:123–30
  • Fleming JO, Isaak A, Lee JE, et al. Probiotic helminth administration in relapsing-remitting multiple sclerosis: a phase 1 study. Mult Scler 2011;17:743–54
  • Lack G. Clinical practice. Food allergy. N Engl J Med 2008;359:1252–60
  • Summers RW, Elliott DE, Urban Jr JF, et al. Trichuris suis therapy in Crohn's disease. Gut 2005;54:87–90
  • Summers RW, Elliott DE, Qadir K, et al. Trichuris suis seems to be safe and possibly effective in the treatment of inflammatory bowel disease. Am J Gastroenterol 2003;98:2034–41
  • Cao Y, Stosiek P, Springer GF, Karsten U. Thomsen-Friedenreich-related carbohydrate antigens in normal adult human tissues: a systematic and comparative study. Histochem Cell Biol 1996;106:197–207
  • Schmitt FC, Figueiredo P, Lacerda M. Simple mucin-type carbohydrate antigens (T, sialosyl-T, Tn and sialosyl-Tn) in breast carcinogenesis. Virchows Arch 1995;427:251–258
  • Li Q, Anver MR, Butcher DO, Gildersleeve JC. Resolving conflicting data on expression of the Tn antigen and implications for clinical trials with cancer vaccines. Mol Cancer Ther 2009;8:971–9
  • Liu WM, Fowler DW, Gravett AM, et al. Supernatants from lymphocytes stimulated with Bacillus Calmette-Guerin can modify the antigenicity of tumours and stimulate allogeneic T-cell responses. Br J Cancer 2011;105:687–93
  • Ahirwar DK, Manchanda PK, Mittal RD, Bid HK. BCG response prediction with cytokine gene variants and bladder cancer: where we are? J Cancer Res Clin Oncol 2011;137:1729–38
  • Coley WB. The treatment of malignant tumors by repeated inoculations of erysipelas. With a report of ten original cases. 1893. Clin Orthop Relat Res 1991:3–11
  • Wiemann B, Starnes CO. Coley's toxins, tumor necrosis factor and cancer research: a historical perspective. Pharmacol Ther 1994;64:529–64
  • Ferlay J, Shin HR, Bray F, et al. GLOBOCAN 2008, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 10. Lyon, France: International Agency for Research on Cancer 2010
  • Bray F, Ren JS, Masuyer E, Ferlay J. Global estimates of cancer prevalence for 27 sites in the adult population in 2008. Int J Cancer 2013;132:1133–45

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