Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-27T21:37:24.518Z Has data issue: false hasContentIssue false

Re-assessing the relationship between sporozoite dose and incubation period in Plasmodium vivax malaria: a systematic re-analysis

Published online by Cambridge University Press:  13 February 2014

ANDREW A. LOVER*
Affiliation:
Infectious Diseases Programme, Saw Swee Hock School of Public Health, National University of Singapore, MD3, 16 Medical Drive, Singapore 117597, Singapore
RICHARD J. COKER
Affiliation:
Infectious Diseases Programme, Saw Swee Hock School of Public Health, National University of Singapore, MD3, 16 Medical Drive, Singapore 117597, Singapore The Communicable Diseases Policy Research Group, Faculty of Public Health, London School of Hygiene and Tropical Medicine, Mahidol University, 9th Floor, Satharanasukwisit Building, 420/1 Rajvithi Road, Bangkok 10400, Thailand
*
* Corresponding author. Infectious Diseases Programme, Saw Swee Hock School of Public Health, National University of Singapore, MD3, 16 Medical Drive, Singapore 117597, Singapore. E-mail: Andrew.A.Lover@gmail.com or ephaal@nus.edu.sg

Summary

Infections with the malaria parasite Plasmodium vivax are noteworthy for potentially very long incubation periods (6–9 months), which present a major barrier to disease elimination. Increased sporozoite challenge has been reported to be associated with both shorter incubation and pre-patent periods in a range of human challenge studies. However, this evidence base has scant empirical foundation, as these historical analyses were limited by available analytic methods, and provides no quantitative estimates of effect size. Following a comprehensive literature search, we re-analysed all identified studies using survival and/or logistic models plus contingency tables. We have found very weak evidence for dose-dependence at entomologically plausible inocula levels. These results strongly suggest that sporozoite dosage is not an important driver of long-latency. Evidence presented suggests that parasite strain and vector species have quantitatively greater impacts, and the potential existence of a dose threshold for human dose-response to sporozoites. Greater consideration of the complex interplay between these aspects of vectors and parasites are important for human challenge experiments, vaccine trials, and epidemiology towards global malaria elimination.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Animut, A., Balkew, M., Gebre-Michael, T. and Lindtjørn, B. (2013). Blood meal sources and entomological inoculation rates of anophelines along a highland altitudinal transect in south-central Ethiopia. Malaria Journal 12, 76. doi: 10.1186/1475-2875-12-76.CrossRefGoogle ScholarPubMed
Boyd, M. F. (1940). The influence of sporozoite dosage in vivax malaria. American Journal of Tropical Medicine and Hygiene s1–20, 279286.CrossRefGoogle Scholar
Brasil, P., de, P., Costa, A., Pedro, R. S., da, S., Bressan, C., da Silva, S., Tauil, P. L. and Daniel-Ribeiro, C. T. (2011). Unexpectedly long incubation period of Plasmodium vivax malaria, in the absence of chemoprophylaxis, in patients diagnosed outside the transmission area in Brazil. Malaria Journal 10, 122. doi: 10.1186/1475-2875-10-122.CrossRefGoogle ScholarPubMed
Coatney, G. R., Cooper, W. C., Ruhe, D. S., Young, M. D. and Burgess, R. W. (1950 a). Studies in human malaria XVIII. The life pattern of sporozoite-induced St. Elizabeth strain vivax malaria. American Journal of Hygiene 51, 200215.Google Scholar
Coatney, G. R., Cooper, W. C. and Young, M. D. (1950 b). Studies in human malaria XXX. A summary of 204 sporozoite-induced infections with the Chesson strain of Plasmodium vivax . Journal of the National Malaria Society 9, 381396.Google ScholarPubMed
Collins, W. E. (2002). Nonhuman primate models: II. Infection of Saimiri and Aotus monkeys with Plasmodium vivax . In Malaria Methods and Protocols (ed. Doolan, D. L.), pp. 8592. Humana Press, Totowa, NJ, USA.CrossRefGoogle Scholar
Collins, W. E., Skinner, J. C., Pappaioanou, M., Broderson, J. R., Filipski, V. K., McClure, H. M., Strobert, E., Sutton, B. B., Stanfill, P. S. and Huong, A. Y. (1988). Sporozoite-induced infections of the Salvador I strain of Plasmodium vivax in Saimiri sciureus boliviensis monkeys. Journal of Parasitology 74, 582585.CrossRefGoogle Scholar
Collins, W. E., Morris, C. L., Richardson, B. B., Sullivan, J. S. and Galland, G. G. (1994). Further studies on the sporozoite transmission of the Salvador I strain of Plasmodium vivax . Journal of Parasitology 80, 512517.CrossRefGoogle Scholar
Collins, W. E., Sullivan, J. A. S., Morris, C. L., Galland, G. G. and Richardson, B. B. (1996). Observations on the biological nature of Plasmodium vivax sporozoites. Journal of Parasitology 82, 216219.CrossRefGoogle ScholarPubMed
Frischknecht, F., Baldacci, P., Martin, B., Zimmer, C., Thiberge, S., Olivo-Marin, J.-C., Shorte, S. L. and Ménard, R. (2004). Imaging movement of malaria parasites during transmission by Anopheles mosquitoes. Cellular Microbiology 6, 687694. doi: 10.1111/j.1462-5822.2004.00395.x.CrossRefGoogle ScholarPubMed
Galinski, M. R. and Barnwell, J. W. (2008). Plasmodium vivax: who cares? Malaria Journal 7 (Suppl. 1), S9. doi: 10.1186/1475-2875-7-S1-S9.CrossRefGoogle ScholarPubMed
Gething, P. W., Elyazar, I. R. F., Moyes, C. L., Smith, D. L., Battle, K. E., Guerra, C. A., Patil, A. P., Tatem, A. J., Howes, R. E., Myers, M. F., George, D. B., Horby, P., Wertheim, H. F. L., Price, R. N., Mueller, I., Baird, J. K. and Hay, S. I. (2012). A long neglected world malaria map: Plasmodium vivax endemicity in 2010. PLoS Neglected Tropical Diseases 6, e1814. doi: 10.1371/journal.pntd.0001814.CrossRefGoogle ScholarPubMed
Glynn, J. R. (1994). Infecting dose and severity of malaria: a literature review of induced malaria. Journal of Tropical Medicine and Hygiene 97, 300316.Google ScholarPubMed
Guilbride, D. L., Guilbride, P. D. L. and Gawlinski, P. (2012). Malaria's deadly secret: a skin stage. Trends in Parasitology 28, 142150. doi: 10.1016/j.pt.2012.01.002.CrossRefGoogle ScholarPubMed
Herrera, S., Fernandez, O., Manzano, M. R., Murrain, B., Vergara, J., Blanco, P., Palacios, R., Velez, J. D., Epstein, J. E., Chen-Mok, M., Reed, Z. H. and Arevalo-Herrera, M. (2009). Successful sporozoite challenge model in human volunteers with Plasmodium vivax strain derived from human donors. American Journal of Tropical Medicine and Hygiene 81, 740746. doi: 10.4269/ajtmh.2009.09-0194.Google Scholar
Herrera, S., Solarte, Y., Jordan-Villegas, A., Echavarria, J. F., Rocha, L., Palacios, R., Ramirez, O., Velez, J. D., Epstein, J. E., Richie, T. L. and Arevalo-Herrera, M. (2011). Consistent safety and infectivity in sporozoite challenge model of Plasmodium vivax in malaria-naive human volunteers. American Journal of Tropical Medicine and Hygiene 84, 411. doi: 10.4269/ajtmh.2011.09-0498.CrossRefGoogle ScholarPubMed
Hosmer, D. W., Hosmer, T., Le Cessie, S. and Lemeshow, S. (1997). A comparison of goodness-of-fit tests for the logistic regression model. Statistics in Medicine 16, 965980.Google Scholar
James, S. P. (1931). Some general results of a study of induced malaria in England. Transactions of the Royal Society of Tropical Medicine and Hygiene 24, 477525.CrossRefGoogle Scholar
Jin, Y., Kebaier, C. and Vanderberg, J. (2007). Direct microscopic quantification of dynamics of Plasmodium berghei sporozoite transmission from mosquitoes to mice. Infection and Immunity 75, 55325539. doi: 10.1128/IAI.00600-07.Google Scholar
Kim, S.-J., Kim, S.-H., Jo, S.-N., Gwack, J., Youn, S.-K. and Jang, J.-Y. (2013). The long and short incubation periods of Plasmodium vivax malaria in Korea: the characteristics and relating factors. Infection and Chemotherapy 45, 184193. doi: 10.3947/ic.2013.45.2.184.CrossRefGoogle Scholar
Krotoski, W. A., Garnham, P. C. C., Cogswell, F. B., Collins, W. E., Bray, R. S., Gwadz, R. W., Killick-Kendrick, R., Wolf, R. H., Sinden, R. and Hollingdale, M. (1986). Observations on early and late post-sporozoite tissue stages in primate malaria. IV. Pre-erythrocytic schizonts and/or hypnozoites of Chesson and North Korean strains of Plasmodium vivax in the chimpanzee. American Journal of Tropical Medicine and Hygiene 35, 263274.Google Scholar
Li, J., Collins, W. E., Wirtz, R. A., Rathore, D., Lal, A. and McCutchan, T. F. (2001). Geographic subdivision of the range of the malaria parasite Plasmodium vivax . Emerging Infectious Diseases 7, 3542.CrossRefGoogle ScholarPubMed
Lover, A. A. and Coker, R. J. (2013). Quantifying effect of geographic location on epidemiology of Plasmodium vivax malaria. Emerging Infectious Diseases 19, 10581065. doi: 10.3201/eid1907.121674.Google Scholar
Markus, M. B. (2012). Dormancy in mammalian malaria. Trends in Parasitology 28, 3945. doi: 10.1016/j.pt.2011.10.005.CrossRefGoogle ScholarPubMed
Mayne, B. (1933). The injection of mosquito sporozoites in malaria therapy. Public Health Reports 48, 909916. doi: 10.2307/4580870.CrossRefGoogle Scholar
Medica, D. L. and Sinnis, P. (2005). Quantitative dynamics of Plasmodium yoelii sporozoite transmission by infected anopheline mosquitoes. Infection and Immunity 73, 43634369. doi: 10.1128/IAI.73.7.4363-4369.2005.Google Scholar
Ménard, R., Tavares, J., Cockburn, I., Markus, M., Zavala, F. and Amino, R. (2013). Looking under the skin: the first steps in malarial infection and immunity. Nature Reviews Microbiology 11, 701712. doi: 10.1038/nrmicro3111.Google Scholar
Mueller, I., Galinski, M. R., Baird, J. K., Carlton, J. M., Kochar, D. K., Alonso, P. L. and del Portillo, H. A. (2009). Key gaps in the knowledge of Plasmodium vivax, a neglected human malaria parasite. Lancet Infectious Diseases 9, 555566. doi: 10.1016/S1473-3099(09)70177-X.CrossRefGoogle ScholarPubMed
Pampana, E. (1969). A Textbook of Malaria Eradication. Oxford University Press, London, UK.Google Scholar
Paul, R. E., Diallo, M. and Brey, P. T. (2004). Mosquitoes and transmission of malaria parasites – not just vectors. Malaria Journal 3, 39. doi: 10.1186/1475-2875-3-39.CrossRefGoogle Scholar
Price, R. N., Tjitra, E., Guerra, C. A., Yeung, S., White, N. J. and Anstey, N. M. (2007). Vivax malaria: neglected and not benign. American Journal of Tropical Medicine and Hygiene 77, 7987.CrossRefGoogle Scholar
Ramasamy, R., Ramasamy, M. S., Wijesundera, D. A., Wijesundera, A. P., Dewit, I., Ranasinghe, C., Srikrishnaraj, K. A. and Wickremaratne, C. (1992). High seasonal malaria transmission rates in the intermediate rainfall zone of Sri Lanka. Annals of Tropical Medicine and Parasitology 86, 591600.Google Scholar
Rattanarithikul, R., Konishi, E. and Linthicum, K. J. (1996). Detection of Plasmodium vivax and Plasmodium falciparum circumsporozoite antigen in anopheline mosquitoes collected in southern Thailand. American Journal of Tropical Medicine and Hygiene 54, 114121.Google Scholar
Rosenberg, R. (2008). Malaria: some considerations regarding parasite productivity. Trends in Parasitology 24, 487491. doi: 10.1016/j.pt.2008.07.009.CrossRefGoogle ScholarPubMed
Schwartz, E., Parise, M., Kozarsky, P. and Cetron, M. (2003). Delayed onset of malaria – implications for chemoprophylaxis in travelers. New England Journal of Medicine 349, 15101516.CrossRefGoogle ScholarPubMed
Shanks, D. G. (2012). Control and elimination of Plasmodium vivax . In Advances in Parasitology, Vol. 80 (ed. Hay, S. I., Price, R. N. and Baird, J. K.), pp. 301341. Academic Press, London, UK.Google Scholar
Sheehy, S. H., Spencer, A. J., Douglas, A. D., Sim, B. K. L., Longley, R. J., Edwards, N. J., Poulton, I. D., Kimani, D., Williams, A. R., Anagnostou, N. A., Roberts, R., Kerridge, S., Voysey, M., James, E. R., Billingsley, P. F., Gunasekera, A., Lawrie, A. M., Hoffman, S. L. and Hill, A. V. S. (2013). Optimising controlled human malaria infection studies using cryopreserved P. falciparum parasites administered by needle and syringe. PLoS ONE 8, e65960. doi: 10.1371/journal.pone.0065960.CrossRefGoogle ScholarPubMed
Shute, P. G., Lupascu, G. H., Branzei, P., Maryon, M., Constantinescu, P., Bruce-Chwatt, L. J., Draper, C. C., Killick-Kendrick, R. and Garnham, P. C. C. (1976). A strain of Plasmodium vivax characterized by prolonged incubation: the effect of numbers of sporozoites on the length of the prepatent period. Transactions of the Royal Society of Tropical Medicine and Hygiene 70, 474481.Google Scholar
Swellengrebel, N. H. and de Buck, A. (1938). Malaria in the Netherlands. Scheliema & Holkema Ltd, Amsterdam, the Netherlands.Google Scholar
Targett, G. A. T., Moorthy, V. S. and Brown, G. V. (2013). Malaria vaccine research and development: the role of the WHO MALVAC committee. Malaria Journal 12, 362. doi: 10.1186/1475-2875-12-362.CrossRefGoogle ScholarPubMed
Tiburskaja, N. A. and Vrublevskaja, O. S. (1977). The Course of Infection Caused by the North Korean Strain of Plasmodium vivax . WHO/MAL/77.985. World Health Organization, Geneva, Switzerland.Google Scholar
Ungureanu, E., Killick-Kendrick, R., Garnham, P. C. C., Branzei, P., Romanescu, C. and Shute, P. G. (1976). Prepatent periods of a tropical strain of Plasmodium vivax after inoculations of tenfold dilutions of sporozoites. Transactions of the Royal Society of Tropical Medicine and Hygiene 70, 482483.CrossRefGoogle ScholarPubMed
Vanderberg, J. P. (2014). Imaging mosquito transmission of Plasmodium sporozoites into the mammalian host: immunological implications. Parasitology International. in press. doi: 10.1016/j.parint.2013.09.010.Google Scholar
Verhave, J. P. (2013). Experimental, therapeutic and natural transmission of Plasmodium vivax tertian malaria: scientific and anecdotal data on the history of Dutch malaria studies. Parasites and Vectors 6, 19. doi: 10.1186/1756-3305-6-19.CrossRefGoogle ScholarPubMed
Warrell, D. A. and Gilles, H. M. (eds.) (2002). Essential Malariology, 4th Edn. Hodder Arnold Publishers, London, UK.Google Scholar
White, N. J. (2011). Determinants of relapse periodicity in Plasmodium vivax malaria. Malaria Journal 10, 297.CrossRefGoogle ScholarPubMed
Whorton, C. M., Kirschbaum, W., Pullman, T. N., Jones, R., Craige, B. and Alving, A. S. (1947). The Chesson strain of Plasmodium vivax malaria I. Factors influencing the incubation period. Journal of Infectious Diseases 80, 223227.CrossRefGoogle ScholarPubMed
Yang, B. (1996). Experimental and field studies on some biological characteristics of Plasmodium vivax isolated from tropical and temperate zones of China. Chinese Medical Journal 109, 266271.Google Scholar