Log in

Can we be sure that the human Plasmodium exoerythrocytic developmental stages occur exclusively in the liver?

  • Protozoology - Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

The development cycle of the malaria parasite, Plasmodium sp., in humans takes place after an infected female Anopheles mosquito injects motile infective forms called sporozoites into the bloodstream. Sporozoites migrate via blood vessels to the liver. This pre-erythrocytic tissue stage is widely accepted to occur in humans exclusively in the liver, contrary to avian malaria where this may occur also in other parenchymatous organs. This concept is based on research conducted by English researchers Henry Shortt and P.C.C. Garnham in the late 1940s. Although Italian researchers as, e.g., Giulio Raffaele, additionally claimed the presence of the parasites in the bone marrow, this is not well acknowledged. So, the question remains whether there exists also a tissue life cycle stage in humans.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Canada)

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bray RS (1957) Studies on the exo-erythrocytic cycle in the genus Plasmodium. London, Lewis. London School of Hygiene and Tropical Medicine, Memoir No. 12

  • Bray RS (1959) Pre-erythrocytic stages of human malaria parasites: Plasmodium malariae. BMJ 2(5153):679–680

    CAS  PubMed  Google Scholar 

  • Bruce-Chwatt LJ (1981) P. C. C. Garnham, Master, Mentor, Friend: The Published Works of P. C. C. Garnham, F. R. S., from 1922–1981. In: Canning EU (ed) Parasitological topics: a presentation volume to P. C. C. Garnham (F.R.S.) on the occasion of his 80th birthday. Allen Press, Kansas, pp 1–18

  • Bruce-Chwatt L, de Zulueta J (1980) The rise and fall of malaria in Europe. Oxford University Press, Oxford

    Google Scholar 

  • Casini G (1939) La fase apigmentata di evoluzione dei plasmodidi nella malaria cronica. Riv Malariol 18:73

    Google Scholar 

  • Catell JM, Catell J (1933) American men of science : a biographical directory, 5th ed. Science Press, New York

    Google Scholar 

  • Crawford DG (1930) Rolle of the Indian medical services 1615–1930. Thacker, London

    Google Scholar 

  • Dünschede H-B (1971) Tropenmedizinische Forschung bei Bayer. Düsseldorfer Arbeiten zur Geschichte der Medizin, Vol 11. Düsseldorf, Michael Triltsch Verlag Düsseldorf

    Google Scholar 

  • Fischer I (1962) Biographisches Lexikon der hervorragenden Ärzte der letzten fünfzig Jahre. Urban & Schwarzenberg, München-Berlin

    Google Scholar 

  • Franken G (2016) Gibt es malaria-Rückfälle durch das Plasmmodium ovale?: Eine kritische Literaturanalyse, Düsseldorf

  • Franken G, Bruijns-Pötschke M, Richter J, Mehlhorn H, Labisch A (2017) Malaria relapses were already known before 1900-a discussion. Parasitol Res 116(1):185–189

    PubMed  Google Scholar 

  • Garnham PCC (1947) Exoerthrocytic schizogony in Plasmodium kochi Laveran: a preliminary note. Trans R Soc Trop Med Hyg 40(5):719–722

    CAS  PubMed  Google Scholar 

  • Garnham PCC (1948a) Exo-erythrocytic schizogony in malaria. Trop Dis Bull 45(10):831–844

    CAS  PubMed  Google Scholar 

  • Garnham PCC (1948b) The developmental cycle of Hepatocystis (Plasmodium) kochi in the monkey host. Trans R Soc Trop Med Hyg 41(5):601–616

    CAS  PubMed  Google Scholar 

  • Garnham PCC (1988) Henry Edward Shortt: 15 April 1887–9 November 1987. Biogr Mem Fellows R Soc 34:713–751

    CAS  PubMed  Google Scholar 

  • Garnham PCC, Bray RS, Cooper WC, Lainson R, Awad FI, Williamson J (1954) Pre-erythrocytic stages of human malaria: Plasmodium Ovale: a preliminary note. BMJ:257

  • Hegner R, Wolfson F (1938) Toxoplasma-like parasites in canaries infected with Plasmodium. Am J Hyg 27:212–230

    Google Scholar 

  • Hegner R, Wolfson F (1939) Tissue-culture studies of parasites in reticulo-endothelial cells in birds infected with Plasmodium. Am J Hyg 29(sect. C):83–87

    Google Scholar 

  • Huff CG (1947) Life cycle of malarial parasites. Annu Rev Microbiol 1:43–60

    Google Scholar 

  • Huff CG (1949) Life cycles of malaria parasites with special reference to the newer knowledge of pre-erythrocytic stages. In: Boyd MF (ed) Malariology: A Comprehensive survey of all aspects of this group of diseases from a global standpoint, vol 1, London, pp 54–64

  • Huff CG, Bloom W (1935) A malaria parasite infecting all blood and all blood forming cells of birds. J Infect Dis 57:315–336

    Google Scholar 

  • James SP (1931) The use of plasmoquine in the prevention of malarial infections. Proc Section of Sciences 34:1424–1425

    Google Scholar 

  • James SP (1939) The incidence of exo-erythrocytic schizogony in Plasmodium gallinaceum in relation to the mode of infection. Trans R Soc Trop Med Hyg 32:763–769

    Google Scholar 

  • James SP, Tate P (1937) Preparations illustrating the recently discovered cycle of avian malaria parasites in reticulo-endothelial cells. Trans R Soc Trop Med Hyg 31:4–5

    Google Scholar 

  • James SP, Tate P (1938) Exo-erythrocytic schizogony in Plasmodium gallinaceum Brumpt. Parasitol 30:128–139

    Google Scholar 

  • Kikuth W (1937) Endotheliale Schizogonie bei Hühnermalaria (Pl. gallinaceum, E. Brumpt 1935). Centralb Bakteriol, Parasitenkd, Infektionskrankh 140:227–230

    Google Scholar 

  • Kikuth W, Mudrow L (1937) Über pigmentlose Schizogonieformen bei der Vogelmalaria. Klin Wochenschr 48:1690–1691

    Google Scholar 

  • Kikuth W, Mudrow L (1938a) Die endothelialen Stadien der Malariaparasiten in experiment und Theorie. Centralb Bakteriol, Parasitenkd, Infektionskrankh, Abt Originale 142(3/4):113–132

    Google Scholar 

  • Kikuth W, Mudrow L (1938b) Malariaübertragungsversuche mit Blut und Organen sporozoeninfizierter Kanarienvögel. Riv Malariol Sez. I(1):1–14

  • Kikuth W, Mudrow L (1940a) Die Entwicklung der Sporozoiten von P. cathemerium im Kanarienvogel. Centralb Bakteriol, Parasitenkd, Infektionskrankh. Abt Originale 145:81–88

    Google Scholar 

  • Kikuth W, Mudrow L (1940b) Die Umwandlung der Sporozoiten in die endotheliale Phase der Malariaparasiten. Riv Malariol 19:1–15

    Google Scholar 

  • Kikuth W, Mudrow L (1941a) Die endotheliale Phase der Malariaparasiten und ihre theoretische und praktische Bedeutung. Ergebnisse der Hygiene, Bakteriologie, Immunitätsforschung und experimentellen Therapie 24:1–86

    Google Scholar 

  • Kikuth W, Mudrow L (1941b) Ueber die Entwicklung der Sporozoiten der Malariaparasiten. Centralb Bakteriol, Parasitenkd, Infektionskrankh, Abt Originale 147:284–288

    Google Scholar 

  • Kikuth W, Mudrow L (1943) Noch einmal: Ueber die Entwicklung der Sporozoiten der Malariaparasiten. Centralb Bakteriol, Parasitenkd, Infektionskrankh, Abt Originale 149:98–101

    Google Scholar 

  • Levaditi C, Schoen R (1932) Sur un parasite sporulé du Singe. Comptes Rendus Hebdom Sèances et Mém Soc Biologie et Filiales 1:343–346

    Google Scholar 

  • Mannweiler E (1998) Geschichte des Instituts für Schiffs- und Tropenkrankheiten in Hamburg 1900–1945. Hamburg, Goecke & Evers

    Google Scholar 

  • Manwell RD (1939) Toxoplasma or exo-erythrocytic schizogony in malaria? Riv Malariol 18:76–88

    Google Scholar 

  • Markus MB (2011) Origin of recurrent Plasmodium vivax malaria: a new theory. S Afr Med J 101(10):682

    PubMed  Google Scholar 

  • Markus MB (2012) Source of homologous parasites in recurrent Plasmodium vivax malaria. J Infect Dis 206(4):622–623

    PubMed  Google Scholar 

  • Markus MB (2015) Do hypnozoites cause relapse in malaria? Trends Parasitol 31(6):239–245

    PubMed  Google Scholar 

  • Mudrow L (1942) Über die Entwicklung der Sporozoiten bei verschiedenen Vogelmalariaarten. Riv Malariol 21:29–46

    Google Scholar 

  • Raffaele G (1934) Un ceppo italiano di Plasmodium elongatum. Riv Malariol 13:332–336

    Google Scholar 

  • Raffaele G (1936a) Il doppio ciclo schizogonico di Plasmodium elongatum. Riv Malariol 15:309–317

    Google Scholar 

  • Raffaele G (1936b) Presumibili forme iniziali di evoluzione di Plasmodium relictum. Riv Malariol 15:318–324

    Google Scholar 

  • Raffaele G (1937) Ricerche sul ciclo di evoluzione iniziale dei parassiti malarici umami. Riv Malariol 16:413–418

    Google Scholar 

  • Raffaele G (1940) Ulteriori ricerche sulla fas monogonica primaria dei plasmodidi nell'uomo i negli uccelli. Riv Malariol 19(4):195–225

    Google Scholar 

  • Schaudinn F (1903) Studien über krankheitserregende Protozoen. II. Plasmodium vivax (Grassi et Feletti) der Erreger des Tertianfiebers beim Menschen. Arbeiten des Kaiserlichen Gesundheitsamtes 19:169–250

    Google Scholar 

  • Shortt HE (1948) The pre-erythrocytic cycle of P. cynomolgi. Proceedings of the 4th international congresses on trop Medi and malaria 4:607–617

  • Shortt HE, Garnham PCC (1948a) Pre-erythrocytic stage in mammalian malaria parasites. Nature 161:126

    CAS  PubMed  Google Scholar 

  • Shortt HE, Garnham PCC (1948b) The exoerythrocytic parasites of Plasmodium cynomolgi: demonstration. Trans R Soc Trop Med Hyg 41(5):705–716

    CAS  PubMed  Google Scholar 

  • Shortt HE, Garnham PCC (1948c) The pre-erythrocytic development of Plasmodium cynomolgi and Plasmodium vivax. Trans R Soc Trop Med Hyg 41(6):785–795

    CAS  PubMed  Google Scholar 

  • Shortt HE, Garnham PCC, Malamos B (1948) The pre-erythrocytic stage of mammalian malaria. BMJ 1:192–194

    CAS  PubMed  Google Scholar 

  • Shortt HE, Fairley NH, Covell G, Shute PG, Garnham PCC (1949) The pre-erythrocytic stage of Plasmodium falciparum: a preliminary note. BMJ 2(4635):1006–1008

    CAS  PubMed  Google Scholar 

  • Shute PG, Lupascu G, Branzei P, Maryon M, Constantinescu P, Bruce-Chwatt LJ, Draper CC, Killick-Kendrick R, Garnham PCC (1976) A strain of Plasmodium vivax characterized by prolonged incubation: the effect of numbers of sporozoites on the length of the prepatent period. Trans R Soc Trop Med Hyg 70(5/6):474–481

    CAS  PubMed  Google Scholar 

  • Tarsitano A, Lucrezi G (1939) Reperti di forme apigmentate del parassita malarico. Arch ital Scienze Med Trop Parassitol 20:65

    Google Scholar 

  • Vaccaro G (1956) Panorama biografico degli italiani d’oggi, Vol. 2. Roma, Curcio

    Google Scholar 

  • Westphal A (1962) Zur Problematik der Blutinfektion mit Plasmodien und Methodik des mikroscopischen Pigmentnachweises. Z Tropenmed Parasitol 13:460–471

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work is part of a medical thesis by Gabriele Franken (Franken 2016). The text was translated from German by Sandra Tillmann, International Science Editing, Shannon, Ireland. Medical English was revised by Hannah Raval and Dr. Gabriela Equihua-Martinez.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gabriele Franken.

Additional information

Section Editor: Tobili Sam-Yellowe

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Franken, G., Richter, J. & Labisch, A. Can we be sure that the human Plasmodium exoerythrocytic developmental stages occur exclusively in the liver?. Parasitol Res 119, 667–673 (2020). https://doi.org/10.1007/s00436-019-06564-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-019-06564-8

Keywords

Navigation