Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-26T21:50:54.315Z Has data issue: false hasContentIssue false
  • English
  • Français

Evaluation of the standard membrane feeding assay (SMFA) for the determination of malaria transmission-reducing activity using empirical data

Published online by Cambridge University Press:  13 December 2004

M. VAN DER KOLK ,
S. J. DE VLAS ,
A. SAUL ,
M. VAN DE VEGTE-BOLMER ,
W. M. ELING  and
W. SAUERWEIN
M. VAN DER KOLK
Affiliation:
UMC Nijmegen, Medical Microbiology, PB 9101, 6500 HB Nijmegen, The Netherlands Institut de Recherche pour le Développement, rue La Fayette 75480 Paris cedex 10, Paris, France Organisation de Coordination pour la lutte contre les Endémies en Afrique Centrale (OCEAC), Laboratoire de Recherche sur le Paludisme, BP 288, Yaoundé, Cameroun
S. J. DE VLAS
Affiliation:
Erasmus MC University Medical Center Rotterdam, Department of Public Health, PB 1738, 3000 DR Rotterdam, The Netherlands
A. SAUL
Affiliation:
Malaria Vaccine Development Unit, NIAID/LPD, NIH, Rockville, MD, USA
M. VAN DE VEGTE-BOLMER
Affiliation:
UMC Nijmegen, Medical Microbiology, PB 9101, 6500 HB Nijmegen, The Netherlands
W. M. ELING
Affiliation:
UMC Nijmegen, Medical Microbiology, PB 9101, 6500 HB Nijmegen, The Netherlands
W. SAUERWEIN
Affiliation:
UMC Nijmegen, Medical Microbiology, PB 9101, 6500 HB Nijmegen, The Netherlands
Get access Rights & Permissions [Opens in a new window]

Abstract

Host responses to the transmittable stages of the malaria parasite may reduce transmission effectively. Transmission-reducing activity (TRA) of human serum can be determined as a percentage, using the Standard Membrane Feeding Assay (SMFA). This laboratory assay was evaluated using the results of 121 experiments with malaria-endemic sera among which many repeated measurements were obtained. The assay consists of the feeding of Anopheles stephensi mosquitoes with cultured Plasmodium falciparum gametocytes, mixed with human red blood cells, and control and experimental sera. The TRA of individual sera was determined by the comparison of oocyst densities between these sera. Bootstrap data on oocyst densities in individual mosquitoes in control feeds were used to construct confidence limits for TRA percentages of serum feeds. Low (<20%) and high TRA (>90%) values for individual sera were usually reproduced in a second experiment, whereas this was more difficult for values between 20% and 90%. The observed variability of TRA values is explained in part by the variability in oocyst density per mosquito. Oocyst densities in control feeds varied more between experiments than within experiments and showed a slight decline over the 3 years of experiments. Reproducibility of TRA of field sera was low (20%) between experiments, but much higher (61%) within experiments. A minimum of 35 oocysts per mosquito in control feeds gave optimal reproducibility (44%) between experiments. We recommend that (1) sera are compared within an experiment, or (2) assays are only analysed where controls have at least 35 oocysts per mosquito. The SMFA is under the recommended conditions appropriate for the study of factors that may influence TRA, e.g. transmission blocking vaccines.

Keywords

malariatransmission-blocking activitymembrane feedingPlasmodium falciparumAnopheles stephensitransmission-blocking vaccine
Type
Research Article
Information
Parasitology , Volume 130 , Issue 1 , January 2005 , pp. 13 - 22
Copyright
© 2004 Cambridge University Press

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

AKIM, N. I., URASSA, H., DRAKELEY, C. J., SAUERWEIN, R. W. & KITUA, A. Y. ( 2002). Immunity to the sexual stages of Plasmodium falciparum in mothers, neonates and infants subject to intense and perennial malarial transmission. Annals of Tropical Medicine and Parasitology 96, 735–737.CrossRefGoogle Scholar
BILLINGSLEY, P. F., MEDLEY, G. F., CHARLWOOD, D. & SINDEN, R. E. ( 1994). Relationship between prevalence and intensity of Plasmodium falciparum infection in natural populations of Anopheles mosquitoes. American Journal of Tropical Medicine and Hygiene 51, 260–270.CrossRefGoogle Scholar
BONNET, S., GOUAGNA, C., SAFEUKUI, I., MEUNIER, J. Y. & BOUDIN, C. ( 2000). Comparison of artificial membrane feeding with direct skin feeding to estimate infectiousness of Plasmodium falciparum gametocyte carriers to mosquitoes. Transactions of the Royal Society of Tropical Medicine and Hygiene 94, 103–106.CrossRefGoogle Scholar
BOUDIN, C., LYANNAZ, J., BOSSENO, M. F., CARNEVALE, P. & AMBROISE-THOMAS, P. ( 1991). Epidemiology of Plasmodium falciparum in a rice field and a savanna area in Burkina Faso: seasonal fluctuations of gametocytaemia and malarial infectivity. Annals of Tropical Medicine and Parasitology 85, 377–385.CrossRefGoogle Scholar
GITHEKO, A. K., BRANDLING-BENNETT, A. D., BEIER, M., ATIELI, F., OWAGA, M. & COLLINS, F. H. ( 1992). The reservoir of Plasmodium falciparum malaria in a holoendemic area of western Kenya. Transactions of the Royal Society of Tropical Medicine and Hygiene 86, 355–358.CrossRefGoogle Scholar
GRAVES, P. M., BURKOT, T. R., CARTER, R., CATTANI, J. A., LAGOG, M., PARKER, J., BRABIN, B. J., GIBSON, F. D., BRADLEY, D. J. & ALPERS, M. P. ( 1988). Measurement of malarial infectivity of human populations to mosquitoes in the Madang area, Papua New Guinea. Parasitology 96, 251–263.CrossRefGoogle Scholar
ICHIMORI, K., CURTIS, C. F. & TARGETT, G. A. ( 1990). The effects of chloroquine on the infectivity of chloroquine-sensitive and -resistant populations of Plasmodium yoelii nigeriensis to mosquitoes. Parasitology 100, 377–381.CrossRefGoogle Scholar
MEDLEY, G. F., SINDEN, R. E., FLECK, S., BILLINGSLEY, P. F., TIRAWANCHAI, N. & RODRIGUEZ, M. H. ( 1993). Heterogeneity in patterns of malarial oocyst infections in the mosquito vector. Parasitology 106, 441–449.CrossRefGoogle Scholar
LENSEN, A., VAN DRUTEN, J., BOLMER, M., VAN GEMERT, G., ELING, W. & SAUERWEIN, R. ( 1996). Measurement by membrane feeding of reduction in Plasmodium falciparum transmission induced by endemic sera. Transactions of the Royal Society of Tropical Medicine and Hygiene 90, 20–22.CrossRefGoogle Scholar
LENSEN, A. H., BOLMER-VAN DE VEGTE, M., VAN GEMERT, G. J., ELING, W. M. & SAUERWEIN, R. W. ( 1997). Leukocytes in a Plasmodium falciparum-infected blood meal reduce transmission of malaria to Anopheles mosquitoes. Infection and Immunity 65, 3834–3837.Google Scholar
LENSEN, A., MULDER, L., TCHUINKAM, T., WILLEMSEN, L., ELING, W. & SAUERWEIN, R. ( 1998). Mechanisms that reduce transmission of Plasmodium falciparum malaria in semiimmune and nonimmune persons. Journal of Infectious Diseases 177, 1358–1363.CrossRefGoogle Scholar
LENSEN, A., BRIL, A., VAN DE VEGTE, M., VAN GEMERT, G. J., ELING, W. & SAUERWEIN, R. ( 1999). Plasmodium falciparum: infectivity of cultured, synchronized gametocytes to mosquitoes. Experimental Parasitology 91, 101–103.CrossRefGoogle Scholar
MUIRHEAD-THOMSON, R. C. ( 1954). Factors determining the true reservoir of infection for Plasmodium falciparum and Wucheria bancrofti in a West-African village. Transactions of the Royal Society of Tropical Medicine and Hygiene 48, 208–225.CrossRefGoogle Scholar
MULDER, B., LENSEN, T., TCHUINKAM, T., ROEFFEN, W., VERHAVE, J. P., BOUDIN, C. & SAUERWEIN, R. ( 1999). Plasmodium falciparum: membrane feeding assays and competition ELISAs for the measurement of transmission reduction in sera from Cameroon. Experimental Parasitology 92, 81–86.CrossRefGoogle Scholar
NAOTUNNE, T. S., KARUNAWEERA, N. D., DEL GIUDICE, G., KULARATNE, M. U., GRAU, G. E., CARTER, R. & MENDIS, K. N. ( 1991). Cytokines kill malaria parasites during infection crisis: extracellular complementary factors are essential. Journal of Experimental Medicine 173, 523–529.CrossRefGoogle Scholar
PEIRIS, J. S., PREMAWANSA, S., RANAWAKA, M. B., UDAGAMA, P. V., MUNASINGHE, Y. D., NANAYAKKARA, M. V., GAMAGE, C. P., CARTER, R., DAVID, P. H. & MENDIS, K. N. ( 1988). Monoclonal and polyclonal antibodies both block and enhance transmission of human Plasmodium vivax malaria. American Journal of Tropical Medicine and Hygiene 39, 26–32.CrossRefGoogle Scholar
PONNUDURAI, T., LENSEN, A. H., LEEUWENBERG, A. D. & MEUWISSEN, J. H. ( 1982). Cultivation of fertile Plasmodium falciparum gametocytes in semi-automated systems. 1. Static cultures. Transactions of the Royal Society of Tropical Medicine and Hygiene 76, 812–818.CrossRefGoogle Scholar
PONNUDURAI, T., LENSEN, A. H., VAN GEMERT, G. J., BENSINK, M. P., BOLMER, M. & MEUWISSEN, J. H. ( 1989). Infectivity of cultured Plasmodium falciparum gametocytes to mosquitoes. Parasitology 98, 165–173.CrossRefGoogle Scholar
PONNUDURAI, T., VAN GEMERT, G. J., BENSINK, T., LENSEN, A. H. & MEUWISSEN, J. H. ( 1987). Transmission blockade of Plasmodium falciparum: its variability with gametocyte numbers and concentration of antibody. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 491–493.CrossRefGoogle Scholar
RAMSEY, J. M., SALINAS, E. & RODRIGUEZ, M. H. ( 1996). Acquired transmission-blocking immunity to Plasmodium vivax in a population of southern coastal Mexico. American Journal of Tropical Medicine and Hygiene 54, 458–463.CrossRefGoogle Scholar
RILEY, E. M., WILLIAMSON, K. C., GREENWOOD, B. M. & KASLOW, D. C. ( 1995). Human immune recognition of recombinant proteins representing discrete domains of the Plasmodium falciparum gamete surface protein, Pfs230. Parasite Immunology 17, 11–19.CrossRefGoogle Scholar
ROEFFEN, W., LENSEN, T., MULDER, B., TEELEN, K., SAUERWEIN, R., VAN DRUTEN, J., ELING, W., MEUWISSEN, J. H. & BECKERS, P. J. ( 1995 a). A comparison of transmission-blocking activity with reactivity in a Plasmodium falciparum 48/45-kD molecule-specific competition enzyme-linked immunosorbent assay. American Journal of Tropical Medicine and Hygiene 52, 60–65.Google Scholar
ROEFFEN, W., BECKERS, P. J., TEELEN, K., LENSEN, T., SAUERWEIN, R. W., MEUWISSEN, J. H. & ELING, W. ( 1995 b). Plasmodium falciparum: a comparison of the activity of Pfs230-specific antibodies in an assay of transmission-blocking immunity and specific competition ELISAs. Experimental Parasitology 80, 15–26.Google Scholar
ROEFFEN, W., MULDER, B., TEELEN, K., BOLMER, M., ELING, W., TARGETT, G. A., BECKERS, P. J. & SAUERWEIN, R. ( 1996). Association between anti-Pfs48/45 reactivity and P. falciparum transmission-blocking activity in sera from Cameroon. Parasite Immunology 18, 103–109.Google Scholar
STOWERS, A. W., KEISTER, D. B., MURATOVA, O. & KASLOW, D. C. ( 2000). A region of Plasmodium falciparum antigen Pfs25 that is the target of highly potent transmission-blocking antibodies. Infection and Immunity 68, 5530–5538.CrossRefGoogle Scholar
STOWERS, A. & CARTER, R. ( 2001). Current developments in malaria transmission-blocking vaccines. Expert Opinion on Biology Therapy 1, 619–628.Google Scholar
TOURE, Y. T., DOUMBO, O., TOURE, A., BAGAYOKO, M., DIALLO, M., DOLO, A., VERNICK, K. D., KEISTER, D. B., MURATOVA, O. & KASLOW, D. C. ( 1998). Gametocyte infectivity by direct mosquito feeds in an area of seasonal malaria transmission: implications for Bancoumana, Mali as a transmission-blocking vaccine site. American Journal of Tropical Medicine and Hygiene 59, 481–486.CrossRefGoogle Scholar
TSUBOI, T., TACHIBANA, M., KANEKO, O. & TORII, M. ( 2003). Transmission-blocking vaccine of vivax malaria. Parasitology International 52, 1–11.CrossRefGoogle Scholar
VERMEULEN, A. N., VAN DEURSEN, J., BRAKENHOFF, R. H., LENSEN, T. H., PONNUDURAI, T. & MEUWISSEN, J. H. ( 1986). Characterization of Plasmodium falciparum sexual stage antigens and their biosynthesis in synchronised gametocyte cultures. Molecular and Biochemical Parasitology 20, 155–163.CrossRefGoogle Scholar