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Puzzling and ambivalent roles of malarial infections in cancer development and progression

Published online by Cambridge University Press:  13 September 2016

ERIC FAURE
ERIC FAURE*
Affiliation:
Aix-Marseille Université, CNRS, Centrale Marseille, I2M, UMR-7373, 13453 Marseille, France
*
*Corresponding author: Aix-Marseille Université, CNRS, Centrale Marseille, I2M, UMR-7373, 13453 Marseille, France. E-mail: eric.faure@univ-amu.fr
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Summary

Scientific evidence strongly suggests that parasites are directly or indirectly associated with carcinogenesis in humans. However, studies have also indicated that parasites or their products might confer resistance to tumour growth. Plasmodium protozoa, the causative agents of malaria, exemplify the ambivalent link between parasites and cancer. Positive relationships between malaria and virus-associated cancers are relatively well-documented; for example, malaria can reactivate the Epstein-Barr Virus, which is the known cause of endemic Burkitt lymphoma. Nevertheless, possible anti-tumour properties of malaria have also been reported and, interestingly, this disease has long been thought to be beneficial to patients suffering from cancers. Current knowledge of the potential pro- and anti-cancer roles of malaria suggests that, contrary to other eukaryotic parasites affecting humans, Plasmodium-related cancers are principally lymphoproliferative disorders and attributable to virus reactivation, whereas, similar to other eukaryotic parasites, the anti-tumour effects of malaria are primarily associated with carcinomas and certain sarcomas. Moreover, malarial infection significantly suppresses murine cancer growth by inducing both innate and specific adaptive anti-tumour responses. This review aims to present an update regarding the ambivalent association between malaria and cancer, and further studies may open future pathways to develop novel strategies for anti-cancer therapies.

Keywords

MalariaPlasmodiumparasitic infectioncarcinogenesisanti-carcinogenic effectfever therapyBurkitt lymphomaEpstein-Barr virusKaposi sarcoma
Type
Review Article
Information
Parasitology , Volume 143 , Issue 14 , December 2016 , pp. 1811 - 1823
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Copyright © Cambridge University Press 2016 

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References

REFERENCES

Adams, F. (1849). The Genuine Works of Hippocrates. Sydenham Society, London, UK.Google Scholar
Adloye, D. and Grant, L. (2015). A review of cancers in Africa. In Chronic Non-Communicable Diseases in Low and Middle-income Countries (ed. de Graft Aikins, A. and Agyemang, C.), pp. 14–29. CABI, Boston, USA.Google Scholar
Alizadeh, H., Pidherney, M. S., McCulley, J. P. and Niederkorn, J. Y. (1994). Apoptosis as a mechanism of cytolysis of tumour cells by a pathogenic free-living amoeba. Infection and Immunity 62, 1298–1303.Google Scholar
Anonymous. (1991 a). From the centers for disease control. Imported malaria associated with malariotherapy of Lyme disease – New Jersey. Journal of the American Medical Association 265, 317–318.Google Scholar
Anonymous. (1991 b). From the centers for disease control. Self-induced malaria associated with malariotherapy for Lyme disease – Texas. Journal of the American Medical Association 266, 2199.Google Scholar
Barfod, L., Bernasconi, N. L., Dahlback, M., Jarrossay, D., Andersen, P. H., Salanti, A., Ofori, M. F., Turner, L., Resende, M., Nielsen, M. A., Theander, T. G., Sallusto, F., Lanzavecchia, A. and Hviid, L. (2007). Human pregnancy-associated malaria-specific B cells target polymorphic, conformational epitopes in VAR2CSA. Molecular Microbiology 63, 335–347.CrossRefGoogle ScholarPubMed
Benamrouz, S., Guyot, K., Gazzola, S., Mouray, A., Chassat, T., Delaire, B., Chabé, M., Gosset, P., Viscogliosi, E., Dei-Cas, E., Creusy, C., Conseil, V. and Certad, G. (2012). Cryptosporidium parvum infection in SCID mice infected with only one oocyst: qPCR assessment of parasite replication in tissues and development of digestive cancer. PLoS ONE 7, e51232.Google Scholar
Benamrouz, S., Conseil, V., Chabé, M., Praet, M., Audebert, C., Blervaque, R., Guyot, K., Gazzola, S., Mouray, A., Chassat, T., Delaire, B., Goetinck, N., Gantois, N., Osman, M., Slomianny, C., Dehennaut, V., Lefebvre, T., Viscogliosi, E., Cuvelier, C., Dei-Cas, E., Creusy, C. and Certad, G. (2014). Cryptosporidium parvum-induced ileo-caecal adenocarcinoma and Wnt signaling in a mouse model. Disease Models & Mechanisms 6, 693–700.Google Scholar
Benelli, G., Lo Iacono, A., Canale, A. and Mehlhorn, H. (2016). Mosquito vectors and the spread of cancer: an overlooked connection? Parasitology Research 115, 2131–2137.CrossRefGoogle ScholarPubMed
Bomford, R. and Wedderburn, N. (1973). Depression of immune response to Moloney leukaemia virus by malarial infection. Nature 242, 471–473.Google Scholar
Braunstein, A. (1929 a). Krebs und Malaria I. Mitteilung. Zeitschrift für Krebsforschung 29, 330–333.CrossRefGoogle Scholar
Braunstein, A. (1929 b). Experimentelle und klinische grundlagen fuer malariabehandlung des krebses. Zeitschrift für Krebsforschung 29, 468–490.CrossRefGoogle Scholar
Braunstein, A. (1931). Über durch malaria bei krebskranken hervorgerufene reaktionen und ihre beziehungen zum reticuloendothelialen System (RES.). Zeitschrift für Krebsforschung 34, 230–233.CrossRefGoogle Scholar
Brown, J., Baisley, K., Kavishe, B., Changalucha, J., Andreasen, A., Mayaud, P., Gumodoka, B., Kapiga, S., Hayes, R. and Watson-Jones, D. (2014). Impact of malaria and helminth infections on immunogenicity of the human papillomavirus-16/18 AS04-adjuvanted vaccine in Tanzania. Vaccine 32, 611–617.Google Scholar
Carmen, J. C. and Sinai, A. P. (2007). Suicide prevention: disruption of apoptotic pathways by protozoan parasites. Molecular Microbiology 64, 904–916.Google Scholar
Chege, D., Higgins, S. J., McDonald, C. R., Shahabi, K., Huibner, S., Kain, T., Kain, D., Kim, C. J., Leung, N., Amin, M., Geddes, K., Serghides, L., Philpott, D. J., Kimani, J., Gray-Owen, S., Kain, K. C. and Kaul, R. (2014). Murine Plasmodium chabaudi malaria increases mucosal immune activation and the expression of putative HIV susceptibility markers in the gut and genital mucosae. Journal of Acquired Immune Deficiency Syndromes 65, 517–525.Google Scholar
Chen, C. J., Liang, K. Y., Chang, Y. S., Wang, Y. F., Hsieh, T., Hsu, M. M., Chen, J. Y. and Liu, M. Y. (1990). Multiple risk factors of nasopharyngeal carcinoma: Epstein-Barr virus, malarial infection, cigarette smoking and familial tendency. Anticancer Research 10, 547–553.Google ScholarPubMed
Chen, L., He, Z., Qin, L., Li, Q., Shi, X., Zhao, S., Zhong, N., and Chen, X. (2011). Antitumour effect of malaria parasite infection in a murine Lewis lung cancer model through induction of innate and adaptive immunity. PLoS ONE 6, e24407.Google Scholar
Chookami, M. B., Sharafi, S. M., Sefiddashti, R. R., Jafari, R., Bahadoran, M., Pestechian, N. and Darani, Y. H. (2015). Effect of two hydatid cyst antigens on the growth of melanoma cancer in C57/black mice. Journal of Parasitic Diseases 39, 1–4.Google Scholar
Chu, E. A., Wu, J. M., Tunkel, D. E. and Ishman, S. L. (2008). Nasopharyngeal carcinoma: the role of the Epstein-Barr virus. Medscape Journal of Medicine 10, 165.Google Scholar
Clemow, F. G. (1903). Medical Geography. Cambridge University Press, Cambridge, UK.Google Scholar
Conant, K. L. and Kaleeba, J. A. R. (2013). Dangerous liaisons: molecular basis for a syndemic relationship between Kaposi's sarcoma and P. falciparum malaria. Frontiers in Microbiology 12, 35.Google Scholar
Cottoni, F., Masala, M. V., Budroni, M., Rosella, M., Satta, R., Locatelli, F., Montesu, M. A. and De Marco, R. (1997). The role of occupation and a past history of malaria in the etiology of classic Kaposi's sarcoma: a case-control study in north-east Sardinia. British Journal of Cancer 76, 1518–1520.Google Scholar
Cottoni, F., Masala, M. V., Pattaro, C., Pirodda, C., Montesu, M. A., Satta, R., Cerimele, D. and de Marco, R. (2006). Classic Kaposi sarcoma in northern Sardinia: a prospective epidemiologic overview (1977–2003) correlated with malaria prevalence (1934). Journal of the American Academy of Dermatology 55, 990–995.Google Scholar
Cunnington, A. J. and Riley, E. M. (2010). Suppression of vaccine responses by malaria: insignificant or overlooked? Expert Review of Vaccines 9, 409–429.Google Scholar
Daneshpour, S., Bahadoran, M., Hejazi, S. H., Eskandarian, A. A., Mahmoudzadeh, M. and Darani, H. Y. (2016). Common antigens between hydatid cyst and cancers. Advanced Biomedical Research 5, 9.Google Scholar
Darani, H. Y., Shirzad, H., Mansoori, F., Zabardast, N. and Mahmoodzadeh, M. (2009). Effects of Toxoplasma gondii and Toxocara canis antigens on WEHI-164 fibrosarcoma growth in a mouse model. Korean Journal of Parasitology 47, 175–177.CrossRefGoogle ScholarPubMed
Darani, H. Y., Yousefi, M., Safari, M. and Jafari, R. (2016). Parasites and immunotherapy: with or against? Journal of Parasitic Diseases 40, 217–226.Google Scholar
Davidson, S. S. (1902). Carcinoma and malaria. British Medical Journal 1, 77.Google Scholar
de Martel, C., Ferlay, J., Franceschi, S., Franceschi, S., Vignat, J., Bray, F., Forman, D. and Plummer, M. (2012). Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncology 13, 607–615.Google Scholar
Deaderick, W. H. (1909). A Practical Study of Malaria. Saunders & Co, London, UK.Google Scholar
Deng, X.-F., Zheng, H., Zhou, D., Liu, Q.-X., Ding, Y., Xu, W.-Y., Chen, Q., Hou, B., Min, J.-X. and Dai, J.-G. (2016). Antitumour effect of intravenous immunization with malaria genetically attenuated sporozoites through induction of innate and adaptive immunity. International Journal of Clinical and Experimental Pathology 9, 978–986. http://www.ijcep.com/files/ijcep0019160.pdf.Google Scholar
Ding, Y., Huang, X., Liu, T., Fu, Y., Tan, Z., Zheng, H., Zhou, T., Dai, J. and Xu, W. (2012). The Plasmodium circumsporozoite protein, a novel NF-kappaB inhibitor, suppresses the growth of SW480. Pathology Oncology Research 18, 895–902.Google Scholar
Duffell, E. (2001). Curative power of fever. Lancet 358, 1276.Google Scholar
Durand-Fardel, M. (1868). Traité Pratique des Maladies Chroniques. Baillière, Paris, France.Google Scholar
Eze, M. O., Hunting, D. J. and Ogan, A. U. (1990). Reactive oxygen production against malaria – a potential cancer risk factor. Medical Hypotheses 32, 121–123.Google Scholar
Faure, E. (2014). Malarial pathocoenosis: beneficial and deleterious interactions between malaria and other human diseases. Frontiers in Physiology 5, 441.CrossRefGoogle ScholarPubMed
Freitas, D. R., Santos, J. B. and Castro, C. N. (2014). Healing with malaria: a brief historical review of malariotherapy for neurosyphilis, mental disorders and other infectious diseases. Revista da Socieda de Brasileira de Medicina Tropical 47, 260–261.Google Scholar
Frevert, U., Galinski, M. R., Hügel, F. U., Allon, N., Schreier, H., Smulevitch, S., Shakibaei, M. and Clavijo, P. (1998). Malaria circumsporozoite protein inhibits protein synthesis in mammalian cells. EMBO Journal 17, 3816–3826.Google Scholar
Geddes, M., Franceschi, S., Balzi, D., Arniani, S., Gafà, L. and Zanetti, R. (1995). Birthplace and classic Kaposi's sarcoma in Italy. Associazione Italiana Registri Tumouri. Journal of the National Cancer Institute 87, 1015–1017.Google Scholar
Gnidehou, S., Doritchamou, J., Arango, E. M., Cabrera, A., Arroyo, M. I., Kain, K. C., Ndam, N. T., Maestre, A. and Yanow, S. K. (2014). Functional antibodies against VAR2CSA in nonpregnant populations from Colombia exposed to Plasmodium falciparum and Plasmodium vivax . Infection and Immunity 82, 2565–2673.Google Scholar
Goonewardene, R., Carter, R., Gamage, C. P., Del Giudice, G., David, P. H., Howie, S. and Mendis, K. N. (1990). Human T cell proliferative responses to Plasmodium vivax antigens: evidence of immunosuppression following prolonged exposure to endemic malaria. European Journal of Immunology 20, 1387–1391.Google Scholar
Gupta, R., Nowakowski, M. and Haseeb, M. A. (2015). Human protozoal infections and their potential for causing neoplasms. In Infection and Cancer: Bi-Directorial Interactions (ed. Shurin, M. R., Thanavala, Y. and Ismail, N.), pp. 75–92. Springer, New-York, USA.Google Scholar
Hargis, B. J. and Malkiel, S. (1979). Sarcomas induced by injection of simian virus 40 into neonatal CFW mice. Journal of the National Cancer Institute 63, 965–968.Google Scholar
Heimlich, H. J. (1990). Should we try malariotherapy for Lyme disease? New England Journal of Medicine 322, 1234–1235.Google ScholarPubMed
Hibbs, J. B. Jr., Lambert, L. H. Jr. and Remington, J. S. (1971). Resistance to murine tumours conferred by chronic infection with intracellular protozoa, Toxoplasma gondii and Besnoitia jellisoni . Journal of Infectious Diseases 124, 587–592.Google Scholar
Hoption Cann, S. A., van Netten, J. P., and van Netten, C. (2006). Acute infections as a means of cancer prevention: opposing effects to chronic infections? Cancer Detection and Prevention 30, 83–93.Google Scholar
Hu, J., Wang, C., Ye, L., Yang, W., Huang, H., Meng, F., Shi, S. and Ding, Z. (2015). Anti-tumour immune effect of oral administration of Lactobacillus plantarum to CT26 tumour-bearing mice. Journal of Biosciences 40, 269–279.Google Scholar
IARC (International Agency for Research on Cancer), author. (2014). Malaria and some polyomaviruses (SV40, BK, JC and Merkel Cell Viruses). IARC Monograph on the Evaluation of Carcinogenic Risks to Humans 104, 9–350.Google Scholar
Igweh, J. C. (2012). Biology of malaria parasites. In Malaria Parasites (ed. Okwa, O. O.), pp. 17–36. InTech, Rijeka, Croatia.Google Scholar
Illingworth, J., Butler, N. S. and Roetynck, S., Mwacharo, J., Pierce, S. K., Bejon, P., Crompton, P. D., Marsh, K. and Ndungu, F. M. (2013). Chronic exposure to Plasmodium falciparum is associated with phenotypic evidence of B and T cell exhaustion. Journal of Immunology 190, 1038–1047.CrossRefGoogle ScholarPubMed
Iruela-Arispe, M. L., Lombardo, M., Krutzsch, H. C., Lawler, J. and Roberts, D. D. (1999). Inhibition of angiogenesis by thrombospondin-1 is mediated by 2 independent regions within the type 1 repeats. Circulation 100, 1423–1431.Google Scholar
Jerusalem, C. (1968). Relationship between malaria infection (Plasmodium berghei) and malignant lymphoma in mice. Zeitschrift fur Tropenmedizin und Parasitologie 19, 94–108.Google Scholar
Jung, B. K., Song, H., Kim, M. J., Cho, J., Shin, E. H. and Chai, J. Y. (2016). High Toxoplasma gondii seropositivity among brain tumour patients in Korea. Korean Journal of Parasitology 54, 201–204.CrossRefGoogle ScholarPubMed
Kienley, G. S. (2012). Fever in cancer treatment: Coley's therapy and epidemiologic observations. Global Advances in Health and Medicine 1, 92–100.Google Scholar
Kim, J. O., Jung, S. S., Kim, S. Y., Kim, T. Y., Shin, D. W., Lee, J. H. and Lee, Y. H. (2007). Inhibition of Lewis lung carcinoma growth by Toxoplasma gondii through induction of Th1 immune responses and inhibition of angiogenesis. Journal of Korean Medical Science 22(Suppl.), S38–S46.Google Scholar
Kruse, W. (1901). Krebs und malaria. Munchener Medizinische Wochenschrift 48, 1920–1923.Google Scholar
Kucerova, P. and Cervinkova, M. (2016). Spontaneous regression of tumour and the role of microbial infection – possibilities for cancer treatment. Anti-Cancer Drugs 27, 269–277.Google Scholar
Kusi, S. (2013). Detecting and quantifying Plasmodium falciparum in blood and tonsils: towards an understanding of malaria-related oncogenesis. Thesis of Biological Sciences, Kwame Nkrumah University of Science and Technology, Ghana.Google Scholar
Lawler, J. (2002). Thrombospondin-1 as an endogenous inhibitor of angiogenesis and tumour growth. Journal of Cellular and Molecular Medicine 6, 1–12.Google Scholar
Lawler, J., and Detmar, M. (2004). Tumour progression: the effects of thrombospondin-1 and -2. International Journal of Biochemistry & Cell Biology 36, 1038–1045.Google Scholar
Lehrer, S. (2010 a). Anopheles mosquito transmission of brain tumour. Medical Hypotheses 74, 167–168.Google Scholar
Lehrer, S. (2010 b). Association between malaria incidence and all cancer mortality in fifty US States and the district of Columbia. Anticancer Research 30, 1371–1373.Google Scholar
Liu, Y.-J., Zhu, X.-T., Ma, S. H. and Li, J. (2006). Effect of malariotherapy on the growth of S180 tumour cells. Chinese Journal of Zoonoses [in Chinese] 10, 1001–1003.Google Scholar
Loeffler, F. (1901). Einer neue Behandlungsmethode des Karzinoms. Deutsche Medizinische Wochenschrift 27, 725–726.Google Scholar
Longley, R. J., Sattabongkot, J. and Mueller, I. (2016). Insights into the naturally acquired immune response to Plasmodium vivax malaria. Parasitology 143, 154–170.Google Scholar
Lu, S. N., Lin, T. M., Chen, C. J., Chen, J. S., Liaw, Y. F., Chang, W. Y. and Hsu, S. T. (1988). A case-control study of primary hepatocellular carcinoma in Taiwan. Cancer 62, 2051–2055.Google Scholar
Lun, Z. R., Lai, D. H., Wen, Y. Z., Zheng, L. L., Shen, J. L., Yang, T. B., Zhou, W. L., Qu, L. H., Hide, G. and Ayala, F. J. (2015). Cancer in the parasitic protozoans Trypanosoma brucei and Toxoplasma gondii . Proceedings of the National Academy of Sciences of the United States of America 112, 8835–8842.Google Scholar
Machicado, C. and Marcos, L. A. (2016). Carcinogenesis associated with parasites other than Schistosoma, Opisthorchis and Clonorchis: a systematic review. International Journal of Cancer 138, 2915–2921.Google Scholar
McBride, J. S., Micklem, H. S. and Ure, J. M. (1977). Immunosuppression in murine malaria. I. Response to type III pneumococcal polysaccharide. Immunology 32, 635–644.Google Scholar
Mori, A. (1902). Carcinosi e malaria. La Clinica Moderna (Pisa) 8, 158–162.Google Scholar
Nakalembe, M., Banura, C., Namujju, P. B. and Mirembe, F. M. (2015). Immunogenicity to the bivalent HPV-16/18 vaccine among adolescent African students exposed to helminths and malaria. Journal of Infection in Developing Countries 9, 197–205.Google Scholar
Nalwoga, A., Cose, S., Wakeham, K., Miley, W., Ndibazza, J., Drakeley, C., Elliott, A., Whitby, D. and Newton, R. (2015). Association between malaria exposure and Kaposi's sarcoma-associated herpes virus seropositivity in Uganda. Tropical Medicine & International Health 20, 665–672.CrossRefGoogle ScholarPubMed
Nascimento, M. C. (2014). Malaria may influence the transmission of Kaposi sarcoma associated herpesvirus in endemic areas. Journal of Acquired Immune Deficiency Syndromes 67, e41–e43.CrossRefGoogle ScholarPubMed
National Toxicology Program. (2016). Report on carcinogens monograph on Epstein-Barr virus. Report on Carcinogens Monograph. https://ntp.niehs.nih.gov/ntp/about_ntp/monopeerrvw/2015/december/ebv_revised_draft_monograph20160513.pdf.Google Scholar
Neghina, R., Neghina, A. M., Marincu, I. and Iacobiciu, I. (2010). Malaria, a journey in time: in search of the lost Myths and forgotten stories. American Journal of the Medical Sciences 340, 492–498.Google Scholar
Nickell, S. P., Freeman, R. R. and Cole, G. A. (1987). Depression of virus-specific cytotoxic T-cell responses during murine malaria. Parasite Immunology 9, 161–174.Google Scholar
Nishimura, T., Nakui, M., Sato, M., Iwakabe, K., Kitamura, H., Sekimoto, M., Ohta, A., Koda, T. and Nishimura, S. (2000). The critical role of Th1-dominant immunity in tumour immunology. Cancer Chemotherapy and Pharmacology 46(Suppl.), S52–S61.Google Scholar
Odida, M., Schmauz, R. and Lwanga, S. K. (2002). Grade of malignancy of cervical cancer in regions of Uganda with varying malarial endemicity. International Journal of Cancer 99, 737–741.Google Scholar
Oikonomopoulou, K., Brinc, D., Kyriacou, K. and Diamandis, E. P. (2013). Infection and cancer: revaluation of the hygiene hypothesis. Clinical Cancer Research 19, 2834–2841.Google Scholar
Oikonomopoulou, K., Brinc, D., Hadjisavvas, A., Christofi, G., Kyriacou, K. and Diamandis, E. P. (2014). The bifacial role of helminths in cancer: involvement of immune and non-immune mechanisms. Critical Reviews in Clinical Laboratory Sciences 51, 138–148.Google Scholar
Orta, F. (1902). Carcinoma e malaria. Studio clinic e sperimentale Milano 23, 1340–1342.Google Scholar
Parkin, D. M., Sitas, F., Chirenje, M., Stein, L., Abratt, R. and Wabinga, H. (2008). Part I: cancer in Indigenous Africans – burden, distribution, and trends. Lancet Oncology 9, 683–692.Google Scholar
Patrikidou, A., Vahtsevanos, K., Charalambidou, M., Valeri, R. M., Xirou, P. and Antoniades, K. (2009). Non-AIDS Kaposi's sarcoma in the head and neck area. Head & Neck 31, 260–268.Google Scholar
Pinessi, D., Ostano, P., Borsotti, P., Bello, E., Guffanti, F., Bizzaro, F., Frapolli, R., Bani, M. R., Chiorino, G., Taraboletti, G. and Resovi, A. (2015). Expression of thrombospondin-1 by tumour cells in patient-derived ovarian carcinoma xenografts. Connective Tissue Research 56, 355–363.Google Scholar
Pradhan, V. and Ghosh, K. (2013). Immunological disturbances associated with malarial infection. Journal of Parasitic Diseases 37, 11–15.Google Scholar
Purtilo, D. T., Manolov, G., Manolova, Y., Harada, S. and Lipscomb, H. (1984). Squamous cell carcinoma, Kaposi's sarcoma and Burkitt's lymphoma are consequences of impaired immune surveillance of ubiquitous viruses in acquired immune deficiency syndrome, allograft recipients and tropical African patients. IARC Scientific Publications 63, 749–770.Google Scholar
Pyo, K. H., Jung, B. K., Xin, C. F., Lee, Y. W., Chai, J. Y. and Shin, E. H. (2014). Prominent IL-12 production and tumour reduction in athymic nude mice after Toxoplasma gondii lysate antigen treatment. Korean Journal of Parasitology 52, 605–612.Google Scholar
Reddy, A., and Fried, B. (2015). An update on helminths in human carcinogenesis. In Infection and Cancer: Bi-Directorial Interactions (ed. Shurin, M. R., Thanavala, Y. and Ismail, N.), pp. 93–108. Springer, New-York, USA.Google Scholar
Riley, E. M., Hviid, L. and Theander, T. G. (2013). Malaria. In Parasitic Infections and the Immune System (ed. Kierszenbaum, F.), pp. 119–143. Academic Press, San Diego, California, USA.Google Scholar
Robbiani, D. F., Deroubaix, S., Feldhahn, N., Oliveira, T. Y., Callen, E., Wang, Q., Jankovic, M., Silva, I. T., Rommel, P. C., Bosque, D., Eisenreich, T., Nussenzweig, A. and Nussenzweig, M. C. (2015). Plasmodium infection promotes genomic instability and AID-dependent B cell lymphoma. Cell 162, 727–737.Google Scholar
Ross, R., Dworsky, R., Nichols, P., Paganini-Hill, A., Wright, W., Koss, M., Lukes, R. and Henderson, B. (1982). Asbestos exposure and lymphomas of the gastrointestinal tract and oral cavity. Lancet 2, 1118–1120.Google Scholar
Roucaute, E., Pichard, G., Faure, E. and Royer-Carenzi, M. (2014). Analysis of the causes of spawning of large-scale, severe malarial epidemics and their rapid total extinction in western Provence, historically a highly endemic region of France (1745–1850). Malaria Journal 13, 72.Google Scholar
Rovighi, A. (1902). Cancro e malaria. Gazzetta degli ospedali e delle cliniche 23, 1175–1176.Google Scholar
Rovighi, A. (1905). Ueber krebs und malaria. Zeitschrift für Krebsforschung 3, 604.Google Scholar
Russell, S., Duquette, M., Liu, J., Drapkin, R., Lawler, J. and Petrik, J. (2015). Combined therapy with thrombospondin-1 type I repeats (3TSR) and chemotherapy induces regression and significantly improves survival in a preclinical model of advanced stage epithelial ovarian cancer. FASEB Journal 29, 576–588.Google Scholar
Salaman, M. H., Wedderburn, N. and Bruce-Chwatt, L. J. (1969). The immunodepressive effect of a murine plasmodium and its interaction with murine oncogenic viruses. Journal of General Microbiology 3, 383–391.Google Scholar
Salanti, A., Clausen, T. M., Agerbæk, M. Ø., Al Nakouzi, N., Dahlbäck, M., Oo, H. Z., Lee, S., Gustavsson, T., Rich, J. R., Hedberg, B. J., Mao, Y., Barington, L., Pereira, M. A., LoBello, J., Endo, M., Fazli, L., Soden, J., Wang, C. K., Sander, A. F., Dagil, R., Thrane, S., Holst, P. J., Meng, L., Favero, F., Weiss, G. J., Nielsen, M. A., Freeth, J., Nielsen, T. O., Zaia, J., Tran, N. L., Trent, J., Babcook, J. S., Theander, T. G., Sorensen, P. H. and Daugaard, M. (2015). Targeting human cancer by a glycosaminoglycan binding malaria protein. Cancer Cell 28, 500–514.CrossRefGoogle ScholarPubMed
Schmauz, R., Mugerwa, J. W. and Wright, D. H. (1990). The distribution of non-Burkitt, non-Hodgkin's lymphomas in Uganda in relation to malarial endemicity. International Journal of Cancer 45, 650–653.Google Scholar
Serraino, D., Corona, R. M., Giuliani, M., Farchi, F., Sarmati, L. and Uccella, I., Andreoni, M. and Rezza, G. (2003). Infection with human herpesvirus type 8 and kaposi's sarcoma in a central Italian area formerly endemic for malaria. Infection 31, 47–50.Google Scholar
Setti, G. (1904). Cancro e chinino. Del preteso antagonismo fra carcinosi e malaria. In La Nuova Rivista Clinico-terapeutica (ed. de Renzi, E.), pp. 319–321. Jovene, Napoli, Italy.Google Scholar
Singh, A. P., Buscaglia, C. A., Wang, Q., Levay, A., Nussenzweig, D. R., Walker, J. R., Winzeler, E. A., Fujii, H., Fontoura, B. M. and Nussenzweig, V. (2007). Plasmodium circumsporozoite protein promotes the development of the liver stages of the parasite. Cell 131, 492–504.Google Scholar
Snounou, G. and Pérignon, J.-L. (2013). Malariotherapy-insanity at the service of malariology. Advances in Parasitology 81, 223–255.CrossRefGoogle ScholarPubMed
Sofronic-Milosavljevic, L., Ilic, N., Pinelli, E. and Gruden-Movsesijan, A. (2015). Secretory products of Trichinella spiralis muscle larvae and immunomodulation: implication for autoimmune diseases, allergies, and malignancies. Journal of Immunology Research 1, 523875.Google Scholar
Starita, N., Annunziata, C., Waddell, K. M., Buonaguro, L., Buonaguro, F. M. and Tornesello, M. L. (2015). Identification of Human Herpesvirus 8 sequences in conjunctiva intraepithelial neoplasia and squamous cell carcinoma of Ugandan patients. BioMed Research International 1, 801353.Google Scholar
Tarzaali, A., Viens, P. and Quevillon, M. (1977). Inhibition of the immune response to whooping cough and tetanus vaccines by malaria infection, and the effect of pertussis adjuvant. American Society of Tropical Medicine and Hygiene 26, 520–524.Google Scholar
Tavani, A., La Vecchia, C., Franceschi, S., Serraino, D. and Carbone, A. (2000). Medical history and risk of Hodgkin's and non-Hodgkin's lymphomas. European Journal of Cancer Prevention 9, 59–64.Google Scholar
Taylor, L. H., Latham, S. M. and Woolhouse, M. E. J. (2001). Risk factors for human disease emergence. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 356, 983–989.Google Scholar
Temkin, O. (1945). The Falling Sickness: A History of Epilepsy from the Greeks to the Beginnings of Modern Neurology. Johns Hopkins Press, Baltimore, USA.Google Scholar
Thakker, S. and Verma, S. C. (2016). Co-infections and pathogenesis of KSHV-associated malignancies. Frontiers in Microbiology 7, 151.Google Scholar
Thorley-Lawson, D., Deitsch, K. W., Duca, K. A. and Torgbor, C. (2016). The link between Plasmodium falciparum malaria and endemic Burkitt's lymphoma-new insight into a 50-year-old Enigma. PLOS Pathogens 12, e1005331.Google Scholar
Tolsma, S. S., Volpert, O. V., Good, D. J., Frazier, W. A., Polverini, P. J. and Bouck, N. (1993). Peptides derived from two separate domains of the matrix protein thrombospondin-1 have anti-angiogenic activity. Journal of Cell Biology 122, 497–511.Google Scholar
Torgbor, C., Awuah, P., Deitsch, K., Kalantari, P. and Duca, K. A. and Thorley-Lawson, D. A. (2014). A multifactorial role for P. falciparum malaria in endemic Burkitt's lymphoma pathogenesis. PLOS Pathogens 10, e1004170.Google Scholar
Toure-Balde, A., Sarthou, J. L., Aribot, G., Michel, P., Trape, J. F., Rogier, C. and Roussilhon, C. (1996). Plasmodium falciparum induces apoptosis in human mononuclear cells. Infection and Immunity 64, 744–750.Google Scholar
Tripathi, R., Jaiswal, N., Sharma, B. and Malhotra, S. K. (2015). Helminth infections mediated DNA damage: Mechanisms and consequences. Single Cell Biology 4, 117.Google Scholar
Trnka von Krzowitz, W. (1775). Historia Febrium Intermittentium, Omnis Aevi Observata et Inventa Illustriora Medica ad has Febres Pertinentia Complectens. Ehelen, Vienna, Autria.Google Scholar
Tsuzynski, G. P., Rothman, V. L., Deutch, A. H., Hamilton, B. K. and Eyal, J. (1992). Biological activities of peptides and peptide analogues derived from common sequences present in thrombospondin, properdin, and malaria proteins. Journal of Cell Biology 116, 209–217.Google Scholar
Turhan, N., Esendagli, G., Ozkayar, O., Tunali, G., Sokmensuer, C. and Abbasoglu, O. (2015). Co-existence of Echinococcus granulosus infection and cancer metastasis in the liver correlates with reduced Th1 immune responses. Parasite Immunology 37, 16–22.Google Scholar
Ubillos, L., Freire, T., Berriel, E., Chiribao, M. L., Chiale, C., Festari, M. F., Medeiros, A., Mazal, D., Rondán, M., Bollati-Fogolín, M., Rabinovich, G. A., Robello, C. and Osinaga, E. (2016). Trypanosoma cruzi extracts elicit protective immune response against chemically induced colon and mammary cancers. International Journal of Cancer 138, 1719–1731.Google Scholar
Urban, B. C. and Todryk, S. (2006). Malaria pigment paralyzes dendritic cells. Journal of Biology 5, 4.Google Scholar
Vasilev, S., Ilic, N., Gruden-Movsesijan, A., Vasilijic, S., Bosic, M. and Sofronic-Milosavljevic, L. (2015). Necrosis and apoptosis in Trichinella spiralis-mediated tumour reduction. Central-European Journal of Immunology 40, 42–53.Google Scholar
Vineis, P., Crosignani, P., Sacerdote, C., Fontana, A., Masala, G., Miligi, L., Nanni, O., Ramazzotti, V., Rodella, S., Stagnaro, E., Tumino, R., Viganò, C., Vindigni, C. and Costantini, A. S. (2000). Haematopoietic cancer and medical history: a multicentre case control study. Journal of Epidemiology and Community Health 54, 431–436.Google Scholar
von Hansemann, D. (1914). Über das Vorkommen von Geschwülsten in den Tropen. Z Krebsforsch Zeitschrift für Krebsforschung 14, 39–45.Google Scholar
Wahman, A., Melnick, S. L. and Rhame, F. S. (1991). The epidemiology of classic, African and immunosuppressed Kaposi's sarcoma. Epidemiologic Reviews 13, 178–199.Google Scholar
Wakeham, K., Webb, E. L., Sebina, I., Muhangi, L., Miley, W., Johnson, W. T., Ndibazza, J., Elliott, A. M., Whitby, D. and Newton, R. (2011). Parasite infection is associated with Kaposi's sarcoma associated herpesvirus (KSHV) in Ugandan women. Infectious Agents and Cancer 6, 15.Google Scholar
Wakeham, K., Webb, E. L., Sebina, I., Nalwoga, A., Muhangi, L., Miley, W., Johnston, W. T., Ndibazza, J., Whitby, D., Newton, R. and Elliott, A. M. (2013). Risk factors for seropositivity to Kaposi sarcoma-associated herpesvirus among children in Uganda. Journal of Acquired Immune Deficiency Syndromes 63, 228–233.Google Scholar
Wang, G. and Gao, M. (2016). Influence of Toxoplasma gondii on in vitro proliferation and apoptosis of hepatoma carcinoma H7402 cell. Asian Pacific Journal of Tropical Medicine 9, 63–66.Google Scholar
Ward, M., Ward, A. and Johansson, O. (2016). Does the mosquito have more of a role in certain cancers than is currently appreciated? – The mosquito cocktail hypothesis. Medical Hypotheses 86, 85–91.Google Scholar
Wassmer, S. C., Taylor, T. E., Rathod, P. K., Mishra, S. K., Mohanty, S., Arevalo-Herrera, M., Duraisingh, M. T. and Smith, J. D. (2015). Investigating the pathogenesis of severe malaria: a multidisciplinary and cross-geographical approach. American Society of Tropical Medicine and Hygiene 93(Suppl.), S42–S56.Google Scholar
Wedderburn, N. (1970). Effect of concurrent malarial infection on development of virus-induced lymphoma in Balb-c mice. Lancet 296, 1114–1116.Google Scholar
Wedderburn, N. (1974). Immunodepression produced by malarial infection in mice. In Parasites in the Immunized Host: Mechanisms of Survival. (ed. Porter, R. and Knight, J.), pp. 123–135. Ciba Foundation Symposium n°25 (new series), Elsevier, Amsterdam, The Netherlands.Google Scholar
Wedderburn, N., Campa, M., Tosta, C. E. and Henderson, D. C. (1981). The effect of malaria on the growth of two syngeneic transplantable murine tumours. Annals of Tropical Medicine and Parasitology 75, 597–605.Google Scholar
Weinstat-Saslow, D. L., Zabrenetzky, V. S., VanHoutte, K., Frazier, W. A., Roberts, D. D. and Steeg, P. S. (1994). Transfection of thrombospondin 1 complementary DNA into a human breast carcinoma cell line reduces primary tumour growth, metastatic potential, and angiogenesis. Cancer Research 54, 6504–6511.Google Scholar
Weiss, G. E., Traore, B. and Kayentao, K., Ongoiba, A., Doumbo, S., Doumtabe, D., Kone, Y., Dia, S., Guindo, A., Traore, A., Huang, C. Y., Miura, K., Mircetic, M., Li, S., Baughman, A., Narum, D. L., Miller, L. H., Doumbo, O. K., Pierce, S. K. and Crompton, P. D. (2010). The Plasmodium falciparum-specific human memory B cell compartment expands gradually with repeated malaria infections. PLoS Pathogens 6, e1000912.Google Scholar
Welsh, J. D., Brown, J. D., Arnold, K., Mathews, H. M. and Prince, A. M. (1976). Hepatitis BS antigen, malaria titers, and primary liver cancer in South Vietnam. Gastroenterology 70, 392–326.Google Scholar
Whitrow, M. (1990). Wagner-Jauregg and fever therapy. Medical History 34, 294–310.Google Scholar
WHO (World Health Organization). (2015). World Malaria Report 2015. World Health Organization, Geneva, Switzerland. http://www.who.int/malaria/media/world-malaria-report-2015/en/.Google Scholar
Wykes, M. N. and Good, M. F. (2008). What really happens to dendritic cells during malaria? Nature Reviews. Microbiology 6, 864–870.CrossRefGoogle ScholarPubMed
Xiaoping, C., Heimlich, H. J. and Binquan, X. (1999). Preliminary report of malariotherapy for advanced tumours. [in Chinese] Zhejiang Cancer Journal 3, 15.Google Scholar
Yadav, M. and Prasad, U. (1984). Malaria antibody levels in patients with nasopharyngeal carcinoma. Southeast Asian Journal of Tropical Medicine and Public Health 15, 234–237.Google Scholar
Zabel, W. (1970). Die Malariatherapie beim karzinom und die technik der malariablutkonservierung. In Die Zusätzliche Therapie der Geschwulsterkrankungen (ed. Zabel, W.), pp. 99–116. Haug, Heidelberg, Germany.Google Scholar
Zeng, G. and Zhong, N. (2011). Translational medicine: what is in a name from the perspective of Chinese clinicians? Science China Life Sciences 54, 1077–1080.Google Scholar