Skip to main content

Mosquitoes, Plasmodium Parasites, and Cancer: Where from, Where to?

  • Chapter
  • First Online:
Mosquito-borne Diseases

Part of the book series: Parasitology Research Monographs ((Parasitology Res. Monogr.,volume 10))

  • 1079 Accesses

Abstract

Plasmodium spp. are among the principal parasites carried by mosquitoes (Diptera: Culicidae), and mosquitoes are probably man’s worst enemy. Over thousands of years and across the globe, mosquito-borne diseases have killed, or maimed, humans, other mammals, birds, and reptiles. Plasmodium parasites are not exclusive to mosquitoes. It has been reported that Culicoides (Diptera: Ceratopogonidae) are susceptible to Plasmodium infection, with some of their abdomens containing human blood and infected with avian Plasmodium, illustrating how little we know about numerous vectors affecting humans. Furthermore, it has been also outlined that an avian parasite (Plasmodium lophurae) can be experimentally adapted to a human host. Mosquitoes also carry other parasites, for example, Dirofilaria and hookworms. This chapter, however, will remain focused on the interrelationship between Plasmodium spp. parasites and mosquitoes and looks to the future. Will we, as some are beginning to suggest, find that mosquitoes have an involvement in the development of some cancers, and will we find that mosquitoes play a greater role in Lyme disease than hitherto imagined? The chapter is broken into eight sections, the first being an overview of the history of Plasmodium and some key facts about mosquitoes, the second looks at the role of mosquito saliva in immunosuppression and the IARC group 1 carcinogens carried by mosquitoes, the third looks at other infectious agents linked to cancer, the fourth looks at current beliefs on cancer causation, the fifth considers how the immune system reacts to these carcinogens, the sixth why the possible role of mosquitoes in cancer development has not been uncovered so far, and the seventh casts a critical eye on developments in mosquito control. Finally, we provide outlooks for future research.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abedi Kiasari B, Vallely PJ, Klapper PE (2011) Merkel cell polyomavirus DNA in immunocompetent and immunocompromised patients with respiratory disease. J Med Virol 83(12):2220–2224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Akpata R, Neumayr A, Holtfreter MC, Kranz I, Singh DD, Mota R et al (2015) The WHO- ultrasonography proptocol for assessing morbidity due to Schistosoma haematobium. Acceptance and evolution over 14 years. Systematic review. Parasitol Res 114:1279–1289

    Article  PubMed  Google Scholar 

  • Alavi Y, Arai M, Mendoza M, Tufet-Bayona M, Sinha R, Fowler K et al (2003) The dynamics of interactions between Plasmodium and the mosquito: a study of the infectivity of Plasmodium berghei and Plasmodium gallinaceum and their transmission by Anopheles stephensi, A. gambiae, and A. aegypti. Int J Parasitol 33:933–943

    Article  CAS  PubMed  Google Scholar 

  • Alibek K, Vakpenove A, Baiken Y (2013) Role of infectious agents in the carcinogenesis of brain and head and neck cancers. Infect Agent Cancer 8:7

    Article  PubMed  PubMed Central  Google Scholar 

  • Allain J-P, Stramer SL, Carneiro-Proietti ABF, Martins ML, Lopes da Silva SN, Ribeiro M et al (2009) Transfusion-transmitted infectious diseases. Biologicals 37:71–77

    Article  PubMed  Google Scholar 

  • Allander T, Andreasson K, Gupta S, Bjerkner A, Bogdanovic G, Persson MA et al (2007) Identification of a third human polyomavirus. J Virol 81:4130–4136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anargyrou K, Petrikkos GL, Suller MT, Skiarda A, Siakantaris MP, Ostuntoyinbo RT et al (2003) Pulmonary Balantidium coli infection in a leukemic patient. Am J Hematol 73(3):180–183

    Article  CAS  PubMed  Google Scholar 

  • Anderson JF, Andreadis TG, Main AJ, Ferrandino FJ, Vossbrink CR (2006) West Nile virus from female and male mosquitoes (Diptera: Culicidae) in subterranean, ground, and canopy habitats in Connecticut. J Med Entomol 43:1010–1019

    Article  PubMed  Google Scholar 

  • Anderson SL, Richards SL, Smartt CT (2010) A simple method for determining arbovirus transmission in mosquitoes. J Am Mosq Control Assoc 26(1):108–111

    Article  PubMed  PubMed Central  Google Scholar 

  • Babakir-Mina M, Ciccozzi M, Perno CF, Ciotti M (2011) The novel KI, WU, MC polyomaviruses: possible human pathogens? New Microbiol 34(1):1–8

    PubMed  Google Scholar 

  • Banfield WG, Woke PA, Mackay CM (1966) Mosquito transmission of lymphomas. Cancer 19:1333–1336

    Article  CAS  PubMed  Google Scholar 

  • Becnel JJ, White SE (2007) Mosquito pathogenic viruses – the last 20 years. J Am Mosq Control Assoc 23(S2):36–49

    Article  PubMed  Google Scholar 

  • Beier JC, Müller GC, Gu W, Arheart KL, Schlein Y (2012) Attractive toxic sugar bait (ATSB) methods decimate populations of Anopheles malaria vectors in arid environments regardless of the local availability of favored sugar-source blossoms. Malar J 11:31

    Article  PubMed  PubMed Central  Google Scholar 

  • Benelli G (2016a) Plant-mediated biosynthesis of nanoparticles as an emerging tool against mosquitoes of medical and veterinary importance: a review. Parasitol Res 115:23–34

    Article  PubMed  Google Scholar 

  • Benelli G (2016b) Green synthesized nanoparticles in the fight against mosquito-borne diseases and cancer—a brief review. Enzym Microb Technol 95:58–68

    Article  CAS  Google Scholar 

  • Benelli G, Beier J (2017) Current vector control challenges in the fight against malaria. Acta Trop 174:91–96. https://doi.org/10.1016/j.actatropica.2017.06.028

    Article  PubMed  Google Scholar 

  • Benelli G, Duggan MF (2018) Management of arthropod vector data–Social and ecological dynamics facing the One Health perspective. Acta Trop 182:80–91, https://doi.org/10.1016/j.actatropica.2018.02.015

    Article  PubMed  Google Scholar 

  • Benelli G, Mehlhorn H (2016) Declining malaria, rising dengue and Zika virus: insights for mosquito vector control. Parasitol Res 115:1747–1754

    Article  PubMed  Google Scholar 

  • Benelli G, Romano D (2017) Mosquito vectors of Zika virus. Entomol Gen. https://doi.org/10.1127/entomologia/2017/0496

    Article  Google Scholar 

  • Benelli G, Lo Iacono A, Canale A, Mehlhorn H (2016a) Mosquito vectors and the spread of cancer: an overlooked connection? Parasitol Res 115:2131–2137

    Article  PubMed  Google Scholar 

  • Benelli G, Jeffries CL, Walker T (2016b) Biological control of mosquito vectors: past, present and future. Insects 7:52. https://doi.org/10.3390/insects7040052

    Article  PubMed Central  Google Scholar 

  • Benelli G, Pavela R, Maggi F, Petrelli R, Nicoletti M (2017a) Commentary: making green pesticides greener? The potential of plant products for nanosynthesis and pest control. J Clust Sci 28:3–10

    Article  CAS  Google Scholar 

  • Benelli G, Maggi F, Pavela R, Murugan K, Govindarajan M, Vaseeharan B et al (2017b) Mosquito control with green nanopesticides: towards the One Health approach? A review of non-target effects. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-017-9752-4

    Article  PubMed  CAS  Google Scholar 

  • Benelli G, Maggi F, Romano D, Stefanini C, Vaseeharan B, Kumar S et al (2017c) Nanoparticles as effective acaricides against ticks – a review. Ticks Tick Borne Dis. https://doi.org/10.1016/j.ttbdis.2017.08.004

    Article  PubMed  Google Scholar 

  • Bernotiene R, Palinauskas V, Iezhova T, Murauskaite D, Valkiunas G (2016) Avian haemosporidian parasites (Haemosporida): a comparative analysis of different polymerase chain reaction assays in detection of mixed infections. Exp Parasitol 163:31–37

    Article  CAS  PubMed  Google Scholar 

  • Bertolino P, Bowen DG (2015) Malaria and the liver: immunological hide-and-seek or subversion of immunity from within. Front Microbiol 18(6):41

    Google Scholar 

  • Blasco-Costa NCN (2016) Improving detection of avian malaria from host blood: a step towards a standardised protocol for diagnostics. Parasitol Res 115:3905–3911

    Article  PubMed  Google Scholar 

  • Blázquez A-B, Escribo-Romero E, Merino-Ramos T, Saiz J-C, Martin-Acerbes M (2014) Stress responses in flavivirus-infected cells: activation of unfolded protein response and autophagy. Front Microbiol 5:266

    Article  PubMed  PubMed Central  Google Scholar 

  • Boissiere A, Tchioffo M, Bacher D, Abate L, Marie Nsango SE et al (2012) Midgut microbiota of the malaria mosquito vector Anopheles gambiae and Interactions with Plasmodium falciparum infection. PLoS Pathog 8(5). https://doi.org/10.1371/journal.ppat.1002742

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bourtzis K, Lees RS, Hendrichs J, Marc JB, Vreysen MJB (2016) More than one rabbit out of the hat: radiation, transgenic and symbiont-based approaches for sustainable management of mosquito and tsetse fly populations. Acta Trop. https://doi.org/10.1016/j.actatropica.2016.01.009

    Article  PubMed  Google Scholar 

  • Bousema T, Drakely C (2011) Epidemiological and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clin Microbiol Rev 24(2):377–410

    Article  PubMed  PubMed Central  Google Scholar 

  • Bouvard V, Baan RA, Grosse Y, Lauby-Secretan B, Ghissassi FE, Benbrahim-Talias L et al (2012) Carcinogenicity of malaria and of some polyomaviruses. Lancet Oncol 13(4):339–340

    Article  PubMed  Google Scholar 

  • Bouyer J, Lefrançois T (2014) Boosting the sterile insect technique to control mosquitoes. Trends Parasitol 30:271–273

    Article  PubMed  Google Scholar 

  • Braga EM, Silveira P, Belo NO, Valkiunas G (2011) Recent advances in the study of avian malaria: an overview with an emphasis on the distribution of Plasmodium spp in Brazil. Mem Inst Oswaldo Cruz 106:S1. https://doi.org/10.1590/S0074-02762011000900002

    Article  Google Scholar 

  • Brooker S, Akhwale W, Pullan R, Estambale B, Clarke SE, Snow RW et al (2007) Epidemiology of Plasmodium-Helminth Co-infection in Africa: populations at risk, potential impact on Anemia and prospects for combining control. Am J Trop Med Hyg 77(S6):88–98

    Article  CAS  PubMed  Google Scholar 

  • Buckley A, Dawson A, Moss SR, Hinsley SA, Bellamy PE, Gould EA (2003) Serological evidence of West Nile virus, Usutu virus and Sindbis virus infection of birds in the UK. J Gen Virol 84:2807–2817

    Article  CAS  PubMed  Google Scholar 

  • Cancer Research UK (2017) https://www.cancerresearchuk.org/about-cancer/prostate-cancer/treatment/hormone-therapy/about-hormone-therapy

  • Chandel K, Mendki MI, Parikh RY, Kulkarni G, Tikar SN, Sukumaran D et al (2013) Midgut microbial community of Culex quinquefasciatus mosquito populations from India. PLoS One 8(11):e80453

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chang TT, Chang TY, Chen CC, Young KC, Roan JN, Lee YC et al (2001) Existence of Hepatitis C virus in Culex quinquefasciatus after ingestion of infected blood: experimental approach to evaluating transmission by mosquitoes. J Clin Microbiol 39:3353–3355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chavshin AR, Oshaghi MA, Vatandoost H, Pourmand MR, Raeisi A, Enayati AA et al (2012) Identification of bacterial microflora in the midgut of the larvae and adult of wild caught Anopheles stephensi: a step toward finding suitable paratransgenesis candidates. Acta Trop 121:129–134

    Article  PubMed  Google Scholar 

  • Chene A (2009) Impact of malaria on B-cell homeostasis and Epstein-Barr virus re-activation. Endemic Burkitt’s lymphoma pathogenesis. Publications from Karolinska Institute, Solna

    Google Scholar 

  • Cicin-Sain L, Brien JD, Uhrlaub JL, Drabig A, Marandu TF, Nikolich-Zugich J (2012) Cytomegaloma virus infection impairs immune responses and accentuates T-cell pool changes observed in mice with aging. PLoS Pathog. https://doi.org/10.1371/journalppat.1002849

  • Ciliao HL, Camargo-Godoy RB, Barcelos GRM, Zanuto A, Delfino VDA, Colus LM (2016) Long-term genotoxic effects of immunosuppressive drugs on lymphocytes of kidney transplant recipients. Mutat Res Genet Toxicol Environ Mutagen 806:47–52

    Article  CAS  Google Scholar 

  • Coffey LL, Page BL, Greninger AL, Herring BL, Russell RC, Doggett SL et al (2014) Enhanced arbovirus surveillance with deep sequencing. Identification of novel rhabdoviruses and bunyaviruses in Austrian mosquitoes. Virology 448:146–158

    Article  CAS  PubMed  Google Scholar 

  • Colpitts TM, Conway MJ, Montgomery RR, Fikrig E (2012) West Nile virus: biology, transmission, and human infection. Clin Microbiol Rev 25:635–648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conway MJ, Watson AM, Colpitts TM, Dragovic SM, Zhiyong L, Wang P et al (2014) Mosquito Saliva Serine protease enhances dissemination of Dengue virus into the mammalian host. J Virol 88:164–175

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Corradin G, Levitskaya J (2014) Priming of CD8(+) T-cell responses to liver stage malaria parasite antigens. Front Immunol 5:527

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cox FEG (2010) History of the discovery of the malaria parasites and their vectors. Parasit Vectors 3:5. https://doi.org/10.1186/1756-3305-3-5

    Article  PubMed  PubMed Central  Google Scholar 

  • Cox-Singh J, Davis TM, Lee KS, Shamsui SS, Matusop A, Ratnam S et al (2008) Plasmodium knowlesi malaria in humans is widely distributed and potentially life threatening. Clin Infect Dis 46(2):165–171

    Article  CAS  PubMed  Google Scholar 

  • Crans WJ (2004) A classification system for mosquito life-cycles: life cycle types for mosquitoes of the Northeastern United States. J Vector Ecol 29(1):1–10

    PubMed  Google Scholar 

  • Dalianis T, Hirsch HH (2013) Human polyomaviruses in disease and cancer. Virology 437(2):63–72

    Article  CAS  PubMed  Google Scholar 

  • Damian RT (1997) Parasite immune evasion and exploitation: reflections and projections. Parasitology 115:S169–S175

    Article  PubMed  Google Scholar 

  • Spielman A, D’Antonio M (2001) Mosquito: the story of man’s deadliest foe. Hyperion, New York ISBN:0-7868-8667-6

    Google Scholar 

  • Davison KL, Crowcroft NS, Ramsay ME, Brown DWG, Andrews NJ (2013) Viral encephalitis in England 1989-1999; What did we miss? Emerg Infect Dis 9:234–240

    Article  Google Scholar 

  • Degos F, Perez P, Roche B, Mahmoodi A, Asselineau J, Voitot H et al (2010) Diagnostic accuracy of FibroScan and comparison to liver fibrosis biomarkers in chronic viral hepatitis: a multicenter prospective study (the FIBROSTIC study). J Hepatol 53:1013–1021

    Article  PubMed  Google Scholar 

  • Depinay N, Hacini F, Beghdadi W, Peronet R, Metheri S (2006) Mast cell dependent down-regulation of antigen specific immune responses by mosquito bites. J Immunol 176:4141–4146

    Article  CAS  PubMed  Google Scholar 

  • Dodd RY (2010) Emerging pathogens in transfusion medicine. Clin Lab Med 30:499–509

    Article  PubMed  PubMed Central  Google Scholar 

  • Efferth T, Romero MR, Wolf DG, Stamminger T, Marin JJG, Marschall M (2008) The anteviral activities of artemisin and artesunate. Clin Infect Dis 47(6):804–811

    Article  CAS  PubMed  Google Scholar 

  • Fang J (2010) Ecology: a world without mosquitoes. Nature 466:432–434

    Article  CAS  PubMed  Google Scholar 

  • Feltcamp MCW, Kazem S, Meijden els van der Lauber C, Garbalenya AE (2013) From Stockholm to Malawi: recent developments in studying human polyomaviruses. J Gen Virol 94:482–496

    Article  CAS  Google Scholar 

  • Ferguson HM, Dornhaus A, Beeche Borgemeister C, Gottlieb M, Mulla MS et al (2010) Ecology: a pre-requisite for malaria elimination and eradication. PLoS Med. https://doi.org/10.1371/journal.pmed.1000303

    Article  PubMed  PubMed Central  Google Scholar 

  • Fernandez-Grandon GM, Gezan SA, Armour JAL, Pickett JA, Logan JG (2015) Heritability of attractiveness to mosquitoes. PLoS One 10(4):e0122716

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Figueirido JC, Richter J, Borja N, Balaca A, Costa S, Belo S, Gracio MA (2015) Prostate adenocarcinoma associated with prostatic infection due to Schistosoma haematobium. Case report and systemic review. Parasitol Res 114(2):351–358

    Article  Google Scholar 

  • Finlay BB, McFadden G (2006) Anti-immunology: evasion of the host immune system by bacterial and viral pathogens. Cell 124:767–782

    Article  CAS  PubMed  Google Scholar 

  • Fouche A, Crewe RM, Windsor IM, Abdool Karim SS (1990) Persistence of Hepatitis B antigen in Culex quinquefasciatus. J Med Entomol 27:697–700

    Article  CAS  PubMed  Google Scholar 

  • Gokhale NS, Vazquez C, Horner SM (2014) Hepatitis C virus: strategies to evade antiviral responses. Future Virol 9(12):1061–1075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Granerod J, Ambrose HE, Davies NWS, Clewley JP, Walsh AL, Morgan D et al (2010) Causes of encephalitis and differences in their clinical presentations in England: a multicentre, population-based prospective study. Lancet 10:835–844

    Article  Google Scholar 

  • Gupta VP, Perez-Perez GI, Dorsey G, Rosenthal PJ, Blaser MJ (2012) The seroprevalence of Helicobacter pylori and its relationship to malaria in Ugandan children. Trans R Soc Trop Med Hyg 106(1):35–42

    Article  PubMed  Google Scholar 

  • Hancock BW (1985) Immunosuppression in cancer. In: Hancock BW (ed) Immunological aspects of cancer, vol 21. Springer, Berlin. https://doi.org/10.1007/978-1-4613-2557-4

    Chapter  Google Scholar 

  • Hellgren O (2015) Allelic variation at innate immune genes (avian β-defensins) within a natural population of great tits. J Avian Biol 46:113–119

    Article  Google Scholar 

  • Hellgren O, Perez-Tris J, Bensch S (2009) A jack -of-all-trades and still a master of some: prevalence and host range in avian malaria and related blood parasites. Ecology 90:2840–2849

    Article  PubMed  Google Scholar 

  • Hellgren O, Atkinson CT, Bensch S, Albayrak T, Dimitrov D, Ewen JG et al (2015) Global phylogeography of the avian malaria pathogen Plasmodium relictum based on MSP1 allelic diversity. Ecography (8, 8):842

    Google Scholar 

  • Higashimoto Y, Ohta A, Nishiyama Y, Ihira M, Sugata K, Asano Y et al (2012) Development of a human herpesvirus 6 species specific immunoblotting assay. J Clin Microbiol 50:1245–1251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hooper SJ, Crean SJ, Lewis MAO, Spratt DA, Wade WG, Wilson MJ (2006) Viable bacteria present within oral squamous cell carcinoma tissue. J Clin Microbiol 44:1719–1725

    Article  PubMed  PubMed Central  Google Scholar 

  • Hou J, Wang D, Zhang R, Wang H (2008) Experimental therapy of hepatoma with artemisinin and its derivatives in vitro and in vivo activity, chemosensitization, and mechanisms of action. Clin Cancer Res 14:5519

    Article  CAS  PubMed  Google Scholar 

  • Huang S, Li JY, Wu J, Meng L, Shou CC (2001) Mycoplasma infections and different human carcinomas. World J Gastroenterol 7(2):266–269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huff CG (1951) Observations on the pre-erythrocytic stages of Plasmodium relictum, Plasmodium cathermerium, and Plasmodium gallinaceum in various birds. J Infect Dis 88:17–26

    Article  CAS  PubMed  Google Scholar 

  • Hughes T, Irwin P, Hofmeister E, Paskewitz SM (2010) Occurrence of Avian Plasmodium and West Nile virus in Culex species in Wisconsin. J Am Mosq Control Assoc 26(1):24–31

    Article  CAS  PubMed  Google Scholar 

  • Hutchings SJ, Rushton L (2012) Occupational cancer in Britain. Br J Cancer 107:S92–S103. https://doi.org/10.1038/hjc.2012.123

    Article  PubMed  PubMed Central  Google Scholar 

  • IARC Monograph 100B (2012) Biological agents. Lyon, France

    Google Scholar 

  • Inci A, Yildirim A, Njabo KY, Duzlu O, Biskin Z, Ciloglu A (2012) Detection and molecular characterization of avian Plasmodium from mosquitoes in central Turkey. Vet Parasitol 188(1–2):179–184

    Article  CAS  PubMed  Google Scholar 

  • James EA, Gates TJ, LaFond RE, Yamamoto S, Ni C, Mai D et al (2016) Neuroinvasive West Nile infection elicits elevated and atypically polarized T-cell responses that promote a pathogenic outcome. PLoS Pathog. https://doi.org/10.1371/journal.ppat.1005375

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Janeway CA Jr, Travers P, Walport M et al (2001) Pathogens have evolved various means of evading or subverting normal host defences. Immunobiology: the immune system in health and disease, 5th edn. Garland Science, New York

    Google Scholar 

  • Johansson O (2009) Disturbance of the immune system by electromagnetic fields – a potentially underlying cause for cellular damage and tissue repair reduction which could lead to disease and impairment. Pathophysiology 16:157–177

    Article  PubMed  Google Scholar 

  • Johansson O, Ward M (2016) The human immune system’s response to carcinogenic and other infectious agents transmitted by mosquito vectors. Parasitol Res. https://doi.org/10.1007/s00436-016-5272-2

    Article  PubMed  Google Scholar 

  • Jones EK, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL (2008) Global trends in emerging infectious diseases. Nature 451:990–993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kato Y, Flodstrom S, Wamgard L (1998) Initiation and promotion of altered hepatic foci in female rats and inhibition of cell-cell communication by the imidazole fungicide prochloraz. Chemosphere 37(3):393–403

    Article  CAS  PubMed  Google Scholar 

  • Khazare K, Blatner NR, Khan MW, Gounari F, Gounaris E, Dennis K et al (2011) The significant role of mast cells in Cancer. Cancer Metastasis Rev 30:45–60

    Article  CAS  Google Scholar 

  • Krief S, Escalente AA, Pacheco MA, Mugisha L, Andre C, Halbwax M (2010) On the diversity of Malaria Parasites in African Apes and the origin of Plasmodium falciparum from Bonobos. PLoS Pathog. https://doi.org/10.1371/journal.ppat.1000765

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lai HC, Singh NP, Sasaki T (2012) Development of Artemisinin compounds for Cancer treatment. Investig New Drugs 31:230–246

    Article  CAS  Google Scholar 

  • Lauron EJ, Loiseau C, Bowie RCK, Spicer GS, Smith TB, Melo M et al (2014) Coevolutionary patterns and diversification of avian malaria parasites in African sunbirds (Family Nectariniidae). Parasitology 142:635–647

    Article  PubMed  Google Scholar 

  • Lednicky JA, Butel JS (1999) Polyomaviruses and human tumours: a brief review of current concepts and interpretations. Front Biosci 4:153–164

    Google Scholar 

  • Li Y, Shan F, Wu J-M, Wu GS, Ding J, Xiao D et al (2001) Novel anti-tumor artemisin derivatives targeting GI phase of the Cell Cycle. Bioorg Med Chem Lett 11:5–8

    Article  PubMed  Google Scholar 

  • Li LM, Hu ZB, Zhou ZX, Liu FY, Zhang JF, Shen HB (2010) Serum microRNA profiles serve as novel biomarkers for HBV infection and diagnosis of HBV-positive hepatocarcinoma. Cancer Res 70(23). https://doi.org/10.1158/0008-5472.CAN-10-1001

    Article  CAS  PubMed  Google Scholar 

  • Lindh JM, Terenius O, Faye I (2005) 16S rRNA gene-based identification of midgut bacteria from field caught Anopheles gambiae Sensu Lato and A. funestus mosquitoes reveals new species related to known insect symbionts. Appl Environ Microbiol 71:7217–7223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin RJ, Liao CL, Lin YL (2004) Replication-incompetent virions of Japanese encephalitis virus trigger neuronal cell death by oxidative stress in a culture system. J Gen Virol 85(2):521–533

    Article  CAS  PubMed  Google Scholar 

  • Lupi E, Hatz C, Schlagenhauf P (2013) The efficacy of repellents against Aedes, Anopheles, Culex and Ixodes spp. - a literature review. Travel Med Infect Dis 11:374–411

    Article  PubMed  Google Scholar 

  • Machicado C, Marcos LA (2016) Carcinogenesis associated with parasites other than Schistosoma, Opisthorchis and Clonorchis: a systemic review. Int J Cancer 138(12):2915–2921

    Article  CAS  PubMed  Google Scholar 

  • Magar DL (2006) Bacteria and cancer: cause, coincidence or cure? A review. J Transl Med 4:14

    Article  CAS  Google Scholar 

  • Malcolm CA (2009) Public Health Issues posed by mosquitoes. An independent report for the Chartered Institute of Environmental Health, London

    Google Scholar 

  • Marci R, Gentili V, Bortolotti D, Lo Monte G, Caselli E, Bolzani S et al (2016) Presence of HHV-6A in endometrial epithelial cells from women with primary unexplained infertility. PLoS One 11(7):e0158304. https://doi.org/10.1371/journal.pone.0158304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McAloose D, Newton AL (2009) Wildlife cancer: a conservation perspective. Nat Rev Cancer 9(7):517–526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Medeiros MC, Ricklefs RE, Brawn JD, Ruiz MO, Goldberg TL, Hamer GL (2016) Overlap in the seasonal infection patterns of avian malaria parasites and West Nile virus in vectors and hosts. Am J Trop Med Hyg 95(5):1121–1129

    Article  PubMed  PubMed Central  Google Scholar 

  • Mehlhorn H (2012) Arthropods as vectors of emerging diseases, Parasitology research monographs, vol 3. Springer, Heidelberg

    Google Scholar 

  • Melaun C, Zotzmann S, Santaella VG, Werblow A, Zumkowski-Xylander H, Kraiczy P et al (2016) Occurrence of Borrelia burgdorferi s.l. in different genera of mosquitoes Culicidae in Central Europe. Ticks Tick Borne Dis 7(2):256–263

    Article  PubMed  Google Scholar 

  • Mercer AE, Copple IM, Maggs JL, O'Neill PM, Park BK (2011) The role of heme and the mitochondrion in the chemical and molecular mechanisms of mammalian cell death induced by the artemesinin antimalarials. J Biol Chem 286:987–996

    Article  CAS  PubMed  Google Scholar 

  • Miller EC (1978) Some current perspectives on chemical carcinogen in humans and experimental animals: presidential address. Cancer Res 38:1479–1496

    CAS  PubMed  Google Scholar 

  • Minard G, Mavingui P, Moro CV (2013) Diversity and function of bacterial microbiota in the mosquito holobiont. Parasit Vectors 6:146

    Article  PubMed  PubMed Central  Google Scholar 

  • Molina-Cruz A, Zilversmit MM, Neafsey DE, Harti DL, Barillas-Mury C (2016) Mosquito vectors and the globalization of Plasmodium falciparum malaria. Annu Rev Genet 50:447–465

    Article  CAS  PubMed  Google Scholar 

  • Montagna GN, Beigier-Bompadre M, Becker M, Kroczek RA, Kaufmann SH, Matuschewski K (2014) Antigen export during liver infection of the malaria parasite augments protective immunity. MBio 29(4):5

    Google Scholar 

  • Moore PS, Chang Y (2010) Why do viruses cause cancer? Highlights of the first century of human tumour virology. Nat Rev Cancer 10:878–889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morgentaler A (2006) Testosterone and prostate cancer. an historical perspective on a modern myth. Eur Urol 50:935–939

    Article  CAS  PubMed  Google Scholar 

  • Munoz-Jordan JL, Fredericksen BL (2010) How flaviviruses activate and suppress the interferon response. Viruses 2(2):676–691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Munson L, Moresco A (2007) Comparative pathology of mammary gland cancers in domestic and wild animals. Breast Dis 28:7–21

    Article  CAS  PubMed  Google Scholar 

  • Murugan K, Vadivalagan C, Karthika P, Panneerselvam C, Paulpandi M, Subramaniam J et al (2016) DNA barcoding and molecular evolution of mosquito vectors of medical and veterinary importance. Parasitol Res 115:107–121

    Article  PubMed  Google Scholar 

  • Navratil V, de Chassey B, Meyniel L, Pradezynski F, Andre P, Rabourdin-Combe C et al (2010) System-level comparison of protein-protein interactions between viruses and the human type 1 interferon system network. J Proteome Res 9:3527–3536

    Article  CAS  PubMed  Google Scholar 

  • Neimark H, Hoff B, Ganter M (2004) Mycoplasma ovis comb nov (formerly Eperythrozoon avis) an epierythrocytic agent of haemolytic anaemia in sheep and goats. Int J Syst Evol Microbiol 54(2):365–371

    Article  CAS  PubMed  Google Scholar 

  • Ng TFF, Willner DL, Lim YW, Schmieder R, Chau B, Nilsson C et al (2011) Broad surveys of DNA viral diversity obtained through viral metagenomics of mosquitoes. PLoS One 6(6):e20579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Njabo KY, Cornel A, Sehgal RNM, Loiseau C, Buermann W, Harrigan R et al (2009) Coquillettidia (Culicidae, Diptera) mosquitoes are natural vectors of avian malaria in Africa. Malar J 8:193

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Outlaw DC, Harvey JA, Nagle MS, Drovetski SV, Voelker G (2016) Diversity and distribution of avian haemosporidians in sub-Saharan Africa: an inter-regional biographic overview. Parasitology 8:1–9

    Google Scholar 

  • Parkin J, Cohen B (2001) An overview of the immune system. Lancet 357(9270):1777–1789

    Article  CAS  PubMed  Google Scholar 

  • Perez-Tris J, Bensch S (2005) Diagnosing genetically diverse avian malarial infections using mixed-sequence analysis and TA-cloning. Parasitology 131(1):15–23

    Article  CAS  PubMed  Google Scholar 

  • Perkins SL (2014) Malaria’s many mates: past, present, and future of the systematics of the order Haemosporida. J Parisitol 100(1):11–25

    Article  Google Scholar 

  • Perz JF, Armstrong GL, Farrington LA, Hutin YJF, Bell BP (2006) The contributions of hepatitis B virus and hepatitis C virus infections to cirrhosis and primary liver cancer worldwide. J Hepatol 45:529–538

    Article  PubMed  Google Scholar 

  • Peterson LR, Brault AC, Nasci RS (2013) West Nile virus: review of the literature. JAMA 310:3

    Google Scholar 

  • Pick C, Ebersberger I, Spielmann T, Bruchhaus I, Burmaster T (2011) Phylogenomic analyses of malaria parasites and evolution of their exported proteins. BMC Evol Biol 11:167. https://doi.org/10.1186/1471-2148-11-167

    Article  PubMed  PubMed Central  Google Scholar 

  • Prugnolle F, Durand P, Ollamo B, Duval L, Ariey F, et al (2011) A fresh look at the origin of Plasmodium falciparum, the most malignant malaria agent. PLoS Pathog 7(2):e1001283. https://doi.org/10.1371/journal.ppat.1001283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramiro RS, Khan SM, Franke-Fayard B, Janse CJ, Obbard DJ, Reece SE (2015) Hybridization and pre-zygotic reproductive barriers in Plasmodium. Proc Biol Sci 282(1806):20143027

    Article  PubMed  PubMed Central  Google Scholar 

  • Richard FA, Sehgal RNM, Jones HI, Smith TB (2002) A comparative analysis of PCR- based detection methods for avian malaria. J Parasitol 88:819–822

    Article  CAS  PubMed  Google Scholar 

  • Rivera Z, Stranese O, Bertino P, Yang H, Pass H, Carbone M (2008) The relationship between Simian virus 40 and mesothelioma. Curr Opin Pulm Med 14(4):316–321

    Article  PubMed  Google Scholar 

  • Ronco G, Dillner J, Elfstrom KM, Tunesi S, Snijders PJF, Arbyn M (2013) Efficacy of HPV-based screening for prevention of invasive cervical cancer: follow-up of four European randomised controlled trials. Lancet. https://doi.org/10.1016/s0140-6736(13)62218-7

    Article  Google Scholar 

  • Rothschild BM, Tanke DH, Helbling M, Martin LD (2003) Epidemiological study of tumors in dinosaurs. Naturwissenshaften 90:495–500

    Article  CAS  Google Scholar 

  • Salmanizadeh S, Bouzari M, Talebi A (2011) Detection of torque teno midi virus/small anellovirus (TTMDV/SAV) in chronic cervicitis and cervical tumors in Isfahan, Iran. Arch Virol 157:291–295

    Article  PubMed  CAS  Google Scholar 

  • Samaras V, Rafailidis PI, Mourtzoukou EG, Peppes G, Falagas ME (2010) Chronic bacterial and parasitical infections and cancer: a review. J Infect Dev Ctries 4(5):267–281.2

    PubMed  Google Scholar 

  • Sapi E, Balasubramanian K, Poruri A, Maghsoudlou JS, Socarras KM, Timmarajou AV (2016) Evidence of in vivo existence of Borrelia biofilm in borrelial lymphocytomas. Eur J Microbiol Immunol. https://doi.org/10.1556/1886.2015.00049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sasaki H, Igaki H, Ishizuka T, Kogoma Y, Sugimura T, Terada M (1995) Presence of Streptococcus DNA sequence in surgical specimens of gastric cancer. Jpn J Cancer Res 86:791–794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Savastano DM, Gorbach AM, Eden HS, Brady SM, Reynolds JC, Yanovski JA (2009) Adiposity and human regional body temperature. Am J Clin Nutr 90:1124–1131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmid-Hempel P (2009) Immune defence, parasite evasion strategies and their relevance for macroscopic phenomena’ such as virulence. Philos Trans R Soc Lond Ser B Biol Sci 364(1513):85–98

    Article  Google Scholar 

  • Schneider BS, Higgs S (2008) The enhancement of arbovirus transmission and disease by mosquito saliva is associated with modulation of the host immune response. Trans R Soc Trop Med Hyg 102(5):600–608

    Article  Google Scholar 

  • Schneider BS, Soong L, ZeiderNS HS (2004) Aedes aegypti salivary gland extracts modulate anti-viral and TH1/TH2 cytokine responses to Sindbis virus infection. Viral Immunol 17(4):565–573

    Article  CAS  PubMed  Google Scholar 

  • Schuster FL, Ramirez-Avila L (2008) Current world status of Balantidium coli. Clin Microbiol Rev 21(4):626–638

    Article  PubMed  PubMed Central  Google Scholar 

  • Scuda N, Hoffman J, Cavignac-Spencer S, Ruprecht K, Liman P, Kuhn J et al (2011) A novel human polyomavirus closely related to the African Green Monkey-derived lymphotropic polyomavirus. J Virol 85(9):4586–4590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Secord AL, Patnode KA, Carter C, Redman E, Gefell DJ, Major AR et al (2015) Contaminants of emerging concern in bats from the Northeastern United States. Arch Environ Contam Toxicol 69:411–421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sen GC (2001) Viruses and interferons. Annu Rev Microbiol 55:255–281

    Article  CAS  PubMed  Google Scholar 

  • Sevik M (2012) Oncogenic viruses and mechanisms of oncogenesis. Turk J Vet Anim Sci 36(4):323–329

    CAS  Google Scholar 

  • Shen Y, Zhu H, Shenk T (1997) Human cytomegalomavirus IE1 and IE2 proteins are mutagenic and mediate “hit-and-run” oncogenic transformation in cooperation with the adenovirus E1A proteins. Proc Natl Acad Sci U S A 94(7):3341–3345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh NP, Lai HC (2004) Artemisinin induces apoptosis in human cancer cells. Anticancer Res 4:2277–2280

    Google Scholar 

  • Sternberg ED, Ng’habi KR, Lyimo IN, Kessy ST, Farenhorst M, Thomas MB et al (2016) Eave tubes for malaria control in Africa: initial development and semi- field evaluations in Tanzania. Malar J 15:447

    Article  PubMed  PubMed Central  Google Scholar 

  • Styer LM, Lim P-Y, Louie KL, Albright RG, Kramer LD, Bernard KA (2011) Mosquito saliva causes enhancement of West Nile virus infection in mice. J Virol 85:1517–1527

    Article  CAS  PubMed  Google Scholar 

  • Sutherland CJ, Tanomsing N, Nolder D, Oguike M, Jennison C, Pukrittayakamee S et al (2010) Two nonrecombining sympatric forms of the human malaria parasite Plasmodium ovale occur globally. J Infect Dis 201(10):1544–1550

    Article  CAS  PubMed  Google Scholar 

  • Ta TH, Hisam S, Lanza M, Jiram AI, Ismail N, Rubio JM (2014) First case of a naturally acquired human infection with Plasmodium cynomolgi. Malar J 413:68

    Article  Google Scholar 

  • Tai AK, Luka J, Ablashi D, Huber BT (2009) HHV-6A infection induces expression of HERV-K18-encoded superantigen. J Clin Virol 46:47–48

    Article  CAS  PubMed  Google Scholar 

  • Tan LV, Ha DQ, Hien VM, van der Hoek L, de Jong MD (2008) Me Tre virus: a Semliki Forest virus strain from Vietnam? J Gen Virol 89:2132–2135

    Article  PubMed  CAS  Google Scholar 

  • Thangamani S, Higgs S, Zieglers S, Vanlandingham D, Tesh R, Wikel S (2010) Host immune response to mosquito-transmitted Chikungunya virus differs from that elicited by needle inoculated virus. PLoS One 5(8):e12137

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tsochatzis EA, Gurusamy KS, Ntaoula S, Cholongitas E, Davidson BR, Burroughs AK (2011) Elastography for the diagnosis of severity of fibrosis in chronic liver disease: a meta-analysis of diagnostic accuracy. J Hepatol 54(4):650–659

    Article  CAS  PubMed  Google Scholar 

  • Vasilakopoulou A, Dinasongona K, Samakarli A, Papadimitris K, Avlami A (2003) Balantidium coli pneumonia in an immunocompromised patient. Scand J Infect Dis 35(2):144–146

    Article  PubMed  Google Scholar 

  • Vythilingam I, Noorazian YM, Huat TC, Jiram AI, Yusri YM, Azahari AH (2008) Plasmodium knowlesi in humans, macaques and mosquitoes in peninsular Malaysia. Parasit Vectors 1:26

    Article  PubMed  PubMed Central  Google Scholar 

  • Waite JL, Lynch PA, Thomas MB (2016) Eave tubes for malaria control in Africa: a modelling assessment of potential impact on transmission. Malar J 15:449

    Article  PubMed  PubMed Central  Google Scholar 

  • Ward M, Benelli G (2017a) Avian and simian malaria: do they have a cancer connection? Parasitol Res 116:839–845

    Article  PubMed  Google Scholar 

  • Ward M, Benelli G (2017b) Culiseta annulata - just a biting nuisance or a deadly foe? Pathog Glob Health. https://doi.org/10.1080/20477724.2017.1397876

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ward M, Ward A, Johansson O (2016) Does the mosquito have more of a role in certain cancers than is currently appreciated? - the mosquito cocktail hypothesis. Med Hypotheses 86:85–91

    Article  CAS  PubMed  Google Scholar 

  • Waters AP, Higgins DG, McCutchan TF (1991) Plasmodium falciparum appears to have arisen as a result of lateral transfer between avian and human hosts. Proc Natl Acad Sci U S A 88:3140–3144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Webster JP, Gower CM, Knowles SCL, Molyneux DH, Fenton A (2016) One health-an ecological and evolutionary framework for tackling Neglected Zoonotic Diseases. Evol Appl 9(2):313–333. https://doi.org/10.1111/eva.12341

    Article  PubMed  PubMed Central  Google Scholar 

  • West SA (2002) Cooperation, virulence and siderophore production in bacterial parasites. Proc R Soc B 270:37–44

    Article  Google Scholar 

  • Whitaker NJ, Glenn WK, Sahrudin A, Orde MM, Delprado W, Lawson JS (2012) Human papilloma virus and Epstein Barr virus in prostate cancer: Koilocytes indicate potential oncogenic influences of human papillomavirus in prostate cancer. Prostate. https://doi.org/10.1002/pros.22562

    Article  PubMed  CAS  Google Scholar 

  • White MK, Gordon J, Reiss K, Del Valle L, Croul S, Giordao A et al (2005) Human polyomaviruses and brain tumours. Brain Res Rev 50(1):69–85

    Article  CAS  PubMed  Google Scholar 

  • WHO (2016) Vector-borne diseases. Mediacentre factsheet

    Google Scholar 

  • Worasith C, Kamamia C, Yakovleva A, Duenngai K, Wangboon C, Sithithaworn J et al (2015) Advances in the diagnosis of human opisthorchiasis: development of Opisthorchis viverrini antigen detection in urine. PLoS Negl Trop Dis 9(10):e0004157

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang N, Tan S, Ng S, Shi Y, Zhou J, Tan KSW et al (2014) Artesunate induces cell death in human cancer cells via enhancing lysosomal function and lysosomal degradation of ferritin. J Biol Chem 289:33425–33441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yazar S, Altuntas F, Sahin I, Atambay M (2004) Dysentery caused by Balantidium coli in a patient with non-Hodgkins lymphoma from Turkey. World J Gastroenterol 10:458–459

    Article  PubMed  PubMed Central  Google Scholar 

  • Yeda R, Ingasia LA, Cheruiyot AC, Okudo C, Chebon LJ, Cheruiyot J (2016) The genotypic and phenotypic stability of Plasmodium falciparum field isolates in continuous in vitro culture. PLoS One 11(1):e0143565. https://doi.org/10.1371/journal.pone.0143565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zákovská A, Nejedia P, Holiková A, Dendis M (2002) Positive findings of Borrelia burgdorferi in Culex (Culex) pipiens pipiens larvae in the surroundings of Brno city determined by the PCR method. Ann Agric Environ Med 9(2):257–259

    PubMed  Google Scholar 

  • Zehtindjiev P, Krizanauskiene A, Bensch S, Palinauskas V, Asghar M, Dimitrov D (2012) A new morphologically distinct malaria parasite that fails detection by established polymerase chain reaction-based protocols for amplification of the cytochrome B gene. J Parasitol 98:657–665

    Article  PubMed  Google Scholar 

  • Zhang Z, Shi Q, An X (2009) NK/T-cell lymphoma in a child with hypersensitivity to mosquito bites. J Pediatr Hematol Oncol 31:855–857

    Article  PubMed  Google Scholar 

  • Zhang X, Sheng J, Plevka P, Kuhn RJ, Diamond MS, Rossman MG (2013) Dengue structure differs at the temperatures of its human and mosquito hosts. Proc Natl Acad Sci U S A 110:6795–6799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zur Hausen H (1996) Papillomavirus infections – a major cause of human cancers. Biochim Biophys Acta Rev Cancer 1288:55–78

    Article  Google Scholar 

Download references

Conflict of Interest

The authors declare no competing interests.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Martin Ward or Giovanni Benelli .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Ward, M., Benelli, G. (2018). Mosquitoes, Plasmodium Parasites, and Cancer: Where from, Where to?. In: Benelli, G., Mehlhorn, H. (eds) Mosquito-borne Diseases. Parasitology Research Monographs, vol 10. Springer, Cham. https://doi.org/10.1007/978-3-319-94075-5_14

Download citation

Publish with us

Policies and ethics