Skip to main content
Top
Published in: Malaria Journal 1/2007

Open Access 01-12-2007 | Research

Standardizing estimates of the Plasmodium falciparum parasite rate

Authors: David L Smith, Carlos A Guerra, Robert W Snow, Simon I Hay

Published in: Malaria Journal | Issue 1/2007

Login to get access

Abstract

Background

The Plasmodium falciparum parasite rate (PfPR) is a commonly reported index of malaria transmission intensity. PfPR rises after birth to a plateau before declining in older children and adults. Studies of populations with different age ranges generally report average PfPR, so age is an important source of heterogeneity in reported PfPR data. This confounds simple comparisons of PfPR surveys conducted at different times or places.

Methods

Several algorithms for standardizing PfPR were developed using 21 studies that stratify in detail PfPR by age. An additional 121 studies were found that recorded PfPR from the same population over at least two different age ranges; these paired estimates were used to evaluate these algorithms. The best algorithm was judged to be the one that described most of the variance when converting the PfPR pairs from one age-range to another.

Results

The analysis suggests that the relationship between PfPR and age is predictable across the observed range of malaria endemicity. PfPR reaches a peak after about two years and remains fairly constant in older children until age ten before declining throughout adolescence and adulthood. The PfPR pairs were poorly correlated; using one to predict the other would explain only 5% of the total variance. By contrast, the PfPR predicted by the best algorithm explained 72% of the variance.

Conclusion

The PfPR in older children is useful for standardization because it has good biological, epidemiological and statistical properties. It is also historically consistent with the classical categories of hypoendemic, mesoendemic and hyperendemic malaria. This algorithm provides a reliable method for standardizing PfPR for the purposes of comparing studies and mapping malaria endemicity. The scripts for doing so are freely available to all.
Appendix
Available only for authorised users
Literature
1.
go back to reference Smith DL, McKenzie FE, Snow RW, Hay SI: Revisiting the basic reproductive number for malaria and its implications for malaria control. PLoS Biol. 2007, 5: e42-PubMedCentralCrossRefPubMed Smith DL, McKenzie FE, Snow RW, Hay SI: Revisiting the basic reproductive number for malaria and its implications for malaria control. PLoS Biol. 2007, 5: e42-PubMedCentralCrossRefPubMed
2.
go back to reference Snow RW, Marsh K: The consequences of reducing transmission of Plasmodium falciparum in Africa. Adv Parasitol. 2002, 52: 235-264.CrossRefPubMed Snow RW, Marsh K: The consequences of reducing transmission of Plasmodium falciparum in Africa. Adv Parasitol. 2002, 52: 235-264.CrossRefPubMed
3.
go back to reference Dietz K: Mathematical models for transmission and control of malaria. Malaria, Principles and Practice of Malariology. Edited by: Wernsdorfer WH, McGregor I. 1988, Edinburgh: Churchill Livingstone, 1091-1133. Dietz K: Mathematical models for transmission and control of malaria. Malaria, Principles and Practice of Malariology. Edited by: Wernsdorfer WH, McGregor I. 1988, Edinburgh: Churchill Livingstone, 1091-1133.
4.
go back to reference Smith DL, Dushoff J, Snow RW, Hay SI: The entomological inoculation rate and Plasmodium falciparum infection in African children. Nature. 2005, 438: 492-495.PubMedCentralCrossRefPubMed Smith DL, Dushoff J, Snow RW, Hay SI: The entomological inoculation rate and Plasmodium falciparum infection in African children. Nature. 2005, 438: 492-495.PubMedCentralCrossRefPubMed
5.
go back to reference Gupta S, Snow RW, Donnelly C, Newbold C: Acquired immunity and postnatal clinical protection in childhood cerebral malaria. Proc R Soc Lond Ser B-Biol Sci. 1999, 266: 33-38.CrossRef Gupta S, Snow RW, Donnelly C, Newbold C: Acquired immunity and postnatal clinical protection in childhood cerebral malaria. Proc R Soc Lond Ser B-Biol Sci. 1999, 266: 33-38.CrossRef
6.
go back to reference Gupta S, Snow RW, Donnelly CA, Marsh K, Newbold C: Immunity to non-cerebral severe malaria is acquired after one or two infections. Nat Med. 1999, 5: 340-343.CrossRefPubMed Gupta S, Snow RW, Donnelly CA, Marsh K, Newbold C: Immunity to non-cerebral severe malaria is acquired after one or two infections. Nat Med. 1999, 5: 340-343.CrossRefPubMed
7.
go back to reference Baird JK, Jones TR, Danudirgo EW, Annis BA, Bangs MJ, Basri H, Purnomo , Masbar S: Age-dependent acquired protection against Plasmodium falciparum in people having two years exposure to hyperendemic malaria. The American Journal of Tropical Medicine and Hygiene. 1991, 45: 65-76.PubMed Baird JK, Jones TR, Danudirgo EW, Annis BA, Bangs MJ, Basri H, Purnomo , Masbar S: Age-dependent acquired protection against Plasmodium falciparum in people having two years exposure to hyperendemic malaria. The American Journal of Tropical Medicine and Hygiene. 1991, 45: 65-76.PubMed
8.
go back to reference Baird JK, Purnomo , Basri H, Bangs MJ, Andersen EM, Jones TR, Masbar S, Harjosuwarno S, Subianto B, Arbani PR: Age-specific prevalence of Plasmodium falciparum among six populations with limited histories of exposure to endemic malaria. The American Journal of Tropical Medicine and Hygiene. 1993, 49: 707-719.PubMed Baird JK, Purnomo , Basri H, Bangs MJ, Andersen EM, Jones TR, Masbar S, Harjosuwarno S, Subianto B, Arbani PR: Age-specific prevalence of Plasmodium falciparum among six populations with limited histories of exposure to endemic malaria. The American Journal of Tropical Medicine and Hygiene. 1993, 49: 707-719.PubMed
9.
go back to reference Trape JF, Rogier C, Konate L, Diagne N, Bouganali H, Canque B, Legros F, Badji A, Ndiaye G, Ndiaye P: The Dielmo project: a longitudinal study of natural malaria infection and the mechanisms of protective immunity in a community living in a holoendemic area of Senegal. The American Journal of Tropical Medicine and Hygiene. 1994, 51: 123-137.PubMed Trape JF, Rogier C, Konate L, Diagne N, Bouganali H, Canque B, Legros F, Badji A, Ndiaye G, Ndiaye P: The Dielmo project: a longitudinal study of natural malaria infection and the mechanisms of protective immunity in a community living in a holoendemic area of Senegal. The American Journal of Tropical Medicine and Hygiene. 1994, 51: 123-137.PubMed
10.
go back to reference Baird JK: Host age as a determinant of naturally acquired-immunity to Plasmodium falciparum. Parasitol Today. 1995, 11: 105-111.CrossRefPubMed Baird JK: Host age as a determinant of naturally acquired-immunity to Plasmodium falciparum. Parasitol Today. 1995, 11: 105-111.CrossRefPubMed
11.
go back to reference Bagster-Wilson D: Malaria incidence in central and south Africa. Malariology A comprehensive survey of all aspects of this group of diseases from a global standpoint. Edited by: Boyd MF. 1949, Philadelphia and London: W. B. Saunders Company, II: 800-809. Bagster-Wilson D: Malaria incidence in central and south Africa. Malariology A comprehensive survey of all aspects of this group of diseases from a global standpoint. Edited by: Boyd MF. 1949, Philadelphia and London: W. B. Saunders Company, II: 800-809.
12.
go back to reference Garnham PCC: Malaria immunity in Africans: effects in infancy and early childhood. Ann Trop Med Parasitol. 1949, 43: 47-61.PubMed Garnham PCC: Malaria immunity in Africans: effects in infancy and early childhood. Ann Trop Med Parasitol. 1949, 43: 47-61.PubMed
13.
go back to reference Guerra CA, Hay SI, Lucioparedes LS, Gikandi P, Tatem AJ, Noor AM, Snow RW: Assembling a global database of malaria parasite prevalence for the Malaria Atlas Project. Malar J. 2007, 6: 17-PubMedCentralCrossRefPubMed Guerra CA, Hay SI, Lucioparedes LS, Gikandi P, Tatem AJ, Noor AM, Snow RW: Assembling a global database of malaria parasite prevalence for the Malaria Atlas Project. Malar J. 2007, 6: 17-PubMedCentralCrossRefPubMed
14.
go back to reference Dietz K, Molineaux L, Thomas A: A malaria model tested in the African savannah. Bull World Health Organ. 1974, 50: 347-357.PubMedCentralPubMed Dietz K, Molineaux L, Thomas A: A malaria model tested in the African savannah. Bull World Health Organ. 1974, 50: 347-357.PubMedCentralPubMed
15.
go back to reference Aron JL, May RM: The population dynamics of malaria. Population dynamics and infectious disease. Edited by: Anderson RM. 1982, London: Chapman and Hall, 139-179.CrossRef Aron JL, May RM: The population dynamics of malaria. Population dynamics and infectious disease. Edited by: Anderson RM. 1982, London: Chapman and Hall, 139-179.CrossRef
16.
go back to reference Aron JL: Mathematical modeling of immunity to malaria. Mathematical Biosciences. 1988, 90: 385-396.CrossRef Aron JL: Mathematical modeling of immunity to malaria. Mathematical Biosciences. 1988, 90: 385-396.CrossRef
17.
go back to reference Smith T, Hii JL, Genton B, Muller I, Booth M, Gibson N, Narara A, Alpers MP: Associations of peak shifts in age-prevalence for human malarias with bednet coverage. Trans R Soc Trop Med Hyg. 2001, 95: 1-6.CrossRefPubMed Smith T, Hii JL, Genton B, Muller I, Booth M, Gibson N, Narara A, Alpers MP: Associations of peak shifts in age-prevalence for human malarias with bednet coverage. Trans R Soc Trop Med Hyg. 2001, 95: 1-6.CrossRefPubMed
18.
go back to reference Metselaar D, van Thiel PH: Classification of malaria. Trop Geog Med. 1959, 11: 157-161. Metselaar D, van Thiel PH: Classification of malaria. Trop Geog Med. 1959, 11: 157-161.
19.
go back to reference Gemperli A, Sogoba N, Fondjo E, Mabaso M, Bagayoko M, Briet OJ, Anderegg D, Liebe J, Smith T, Vounatsou P: Mapping malaria transmission in West and Central Africa. Trop Med Int Health. 2006, 11: 1032-1046.CrossRefPubMed Gemperli A, Sogoba N, Fondjo E, Mabaso M, Bagayoko M, Briet OJ, Anderegg D, Liebe J, Smith T, Vounatsou P: Mapping malaria transmission in West and Central Africa. Trop Med Int Health. 2006, 11: 1032-1046.CrossRefPubMed
20.
go back to reference Gemperli A, Vounatsou P, Sogoba N, Smith T: Malaria mapping using transmission models: application to survey data from Mali. Am J Epidemiol. 2006, 163: 289-297.CrossRefPubMed Gemperli A, Vounatsou P, Sogoba N, Smith T: Malaria mapping using transmission models: application to survey data from Mali. Am J Epidemiol. 2006, 163: 289-297.CrossRefPubMed
21.
go back to reference Omumbo JA, Hay SI, Snow RW, Tatem AJ, Rogers DJ: Modelling malaria risk in East Africa at high-spatial resolution. Trop Med Int Health. 2005, 10: 557-566.PubMedCentralCrossRefPubMed Omumbo JA, Hay SI, Snow RW, Tatem AJ, Rogers DJ: Modelling malaria risk in East Africa at high-spatial resolution. Trop Med Int Health. 2005, 10: 557-566.PubMedCentralCrossRefPubMed
23.
go back to reference Kleinschmidt I, Bagayoko M, Clarke GPY, Craig M, Le Sueur D: A spatial statistical approach to malaria mapping. Int J Epidemiol. 2000, 29: 355-361.CrossRefPubMed Kleinschmidt I, Bagayoko M, Clarke GPY, Craig M, Le Sueur D: A spatial statistical approach to malaria mapping. Int J Epidemiol. 2000, 29: 355-361.CrossRefPubMed
24.
go back to reference Kleinschmidt I, Omumbo J, Briet O, van de Giesen N, Sogoba N, Mensah NK, Windmeijer P, Moussa M, Teuscher T: An empirical malaria distribution map for West Africa. Trop Med Int Health. 2001, 6: 779-786.CrossRefPubMed Kleinschmidt I, Omumbo J, Briet O, van de Giesen N, Sogoba N, Mensah NK, Windmeijer P, Moussa M, Teuscher T: An empirical malaria distribution map for West Africa. Trop Med Int Health. 2001, 6: 779-786.CrossRefPubMed
25.
go back to reference Kazembe LN, Kleinschmidt I, Holtz TH, Sharp BL: Spatial analysis and mapping of malaria risk in Malawi using point-referenced prevalence of infection data. Int J Health Geogr. 2006, 5: 41-PubMedCentralCrossRefPubMed Kazembe LN, Kleinschmidt I, Holtz TH, Sharp BL: Spatial analysis and mapping of malaria risk in Malawi using point-referenced prevalence of infection data. Int J Health Geogr. 2006, 5: 41-PubMedCentralCrossRefPubMed
26.
go back to reference Mayor A, Aponte JJ, Fogg C, Saute F, Greenwood B, Dgedge M, Menendez C, Alonso PL: The epidemiology of malaria in adults in a rural area of southern Mozambique. Malar J. 2007, 6: 3-PubMedCentralCrossRefPubMed Mayor A, Aponte JJ, Fogg C, Saute F, Greenwood B, Dgedge M, Menendez C, Alonso PL: The epidemiology of malaria in adults in a rural area of southern Mozambique. Malar J. 2007, 6: 3-PubMedCentralCrossRefPubMed
27.
go back to reference McKenzie FE, Sirichaisinthop J, Miller RS, Gasser RA, Wongsrichanalai C: Dependence of malaria detection and species diagnosis by microscopy on parasite density. The American Journal of Tropical Medicine and Hygiene. 2003, 69: 372-376.PubMedCentralPubMed McKenzie FE, Sirichaisinthop J, Miller RS, Gasser RA, Wongsrichanalai C: Dependence of malaria detection and species diagnosis by microscopy on parasite density. The American Journal of Tropical Medicine and Hygiene. 2003, 69: 372-376.PubMedCentralPubMed
28.
go back to reference Pull JH, Grab B: A simple epidemiological model for evaluating the malaria inoculation rate and the risk of infection in infants. Bull World Health Organ. 1974, 51: 507-516.PubMedCentralPubMed Pull JH, Grab B: A simple epidemiological model for evaluating the malaria inoculation rate and the risk of infection in infants. Bull World Health Organ. 1974, 51: 507-516.PubMedCentralPubMed
29.
go back to reference Ross R: The prevention of malaria. 1910, London: John Murray Ross R: The prevention of malaria. 1910, London: John Murray
30.
go back to reference Muench H: Catalytic models in epidemiology. 1959, Cambridge: Harvard University PressCrossRef Muench H: Catalytic models in epidemiology. 1959, Cambridge: Harvard University PressCrossRef
31.
go back to reference Molineaux L, Storey J, Cohen JE, Thomas A: A longitudinal study of human malaria in the West African Savanna in the absence of control measures: relationships between different Plasmodium species, in particular P. falciparum and P. malariae. The American Journal of Tropical Medicine and Hygiene. 1980, 29: 725-737.PubMed Molineaux L, Storey J, Cohen JE, Thomas A: A longitudinal study of human malaria in the West African Savanna in the absence of control measures: relationships between different Plasmodium species, in particular P. falciparum and P. malariae. The American Journal of Tropical Medicine and Hygiene. 1980, 29: 725-737.PubMed
32.
go back to reference R Development Core Team: R: a language and environment for statistical computing. Book R: a language and environment for statistical computing. 2006, City: R Foundation for Statistical Computing R Development Core Team: R: a language and environment for statistical computing. Book R: a language and environment for statistical computing. 2006, City: R Foundation for Statistical Computing
33.
go back to reference Snow RW, Omumbo JA, Lowe B, Molyneux CS, Obiero JO, Palmer A, Weber MW, Pinder M, Nahlen B, Obonyo C: Relation between severe malaria morbidity in children and level of Plasmodium falciparum transmission in Africa. Lancet. 1997, 349: 1650-1654.CrossRefPubMed Snow RW, Omumbo JA, Lowe B, Molyneux CS, Obiero JO, Palmer A, Weber MW, Pinder M, Nahlen B, Obonyo C: Relation between severe malaria morbidity in children and level of Plasmodium falciparum transmission in Africa. Lancet. 1997, 349: 1650-1654.CrossRefPubMed
34.
go back to reference Port GR, Boreham PFL, Bryan JH: The relationship of host size to feeding by mosquitoes of the Anopheles gambiae Giles complex (Diptera: Culicidae). Bulletin of Entomological Research. 1980, 70: 133-144.CrossRef Port GR, Boreham PFL, Bryan JH: The relationship of host size to feeding by mosquitoes of the Anopheles gambiae Giles complex (Diptera: Culicidae). Bulletin of Entomological Research. 1980, 70: 133-144.CrossRef
35.
go back to reference Smith T, Beck HP, Kitua A, Mwankusye S, Felger I, Fraser-Hurt N, Irion A, Alonso P, Teuscher T, Tanner M: Age dependence of the multiplicity of Plasmodium falciparum infections and of other malariological indices in an area of high endemicity. Trans R Soc Trop Med Hyg. 1999, 93: 15-20.CrossRefPubMed Smith T, Beck HP, Kitua A, Mwankusye S, Felger I, Fraser-Hurt N, Irion A, Alonso P, Teuscher T, Tanner M: Age dependence of the multiplicity of Plasmodium falciparum infections and of other malariological indices in an area of high endemicity. Trans R Soc Trop Med Hyg. 1999, 93: 15-20.CrossRefPubMed
36.
go back to reference al-Yaman F, Genton B, Reeder JC, Anders RF, Smith T, Alpers MP: Reduced risk of clinical malaria in children infected with multiple clones of Plasmodium falciparum in a highly endemic area: a prospective community study. Trans R Soc Trop Med Hyg. 1997, 91: 602-605.CrossRefPubMed al-Yaman F, Genton B, Reeder JC, Anders RF, Smith T, Alpers MP: Reduced risk of clinical malaria in children infected with multiple clones of Plasmodium falciparum in a highly endemic area: a prospective community study. Trans R Soc Trop Med Hyg. 1997, 91: 602-605.CrossRefPubMed
37.
go back to reference Snow RW, Molyneux CS, Warn PA, Omumbo J, Nevill CG, Gupta S, Marsh K: Infant parasite rates and immunoglobulin M seroprevalence as a measure of exposure to Plasmodium falciparum during a randomized controlled trial of insecticide-treated bed nets on the Kenyan coast. The American Journal of Tropical Medicine and Hygiene. 1996, 55: 144-149.PubMed Snow RW, Molyneux CS, Warn PA, Omumbo J, Nevill CG, Gupta S, Marsh K: Infant parasite rates and immunoglobulin M seroprevalence as a measure of exposure to Plasmodium falciparum during a randomized controlled trial of insecticide-treated bed nets on the Kenyan coast. The American Journal of Tropical Medicine and Hygiene. 1996, 55: 144-149.PubMed
38.
go back to reference Snow RW, Shenton FC, Lindsay SW, Greenwood BM, Bennett S, Wheeler J, Delgiudice G, Verdini AS, Pessi A: Sporozoite antibodies and malaria in children in a rural area of The Gambia. Ann Trop Med Parasitol. 1989, 83: 559-568.PubMed Snow RW, Shenton FC, Lindsay SW, Greenwood BM, Bennett S, Wheeler J, Delgiudice G, Verdini AS, Pessi A: Sporozoite antibodies and malaria in children in a rural area of The Gambia. Ann Trop Med Parasitol. 1989, 83: 559-568.PubMed
39.
go back to reference Drakeley C, Sutherland C, Bouserna JT, Sauerwein RW, Targett GAT: The epidemiology of Plasmodium falciparum gametocytes: weapons of mass dispersion. Trends Parasitol. 2006, 22: 424-430.CrossRefPubMed Drakeley C, Sutherland C, Bouserna JT, Sauerwein RW, Targett GAT: The epidemiology of Plasmodium falciparum gametocytes: weapons of mass dispersion. Trends Parasitol. 2006, 22: 424-430.CrossRefPubMed
Metadata
Title
Standardizing estimates of the Plasmodium falciparum parasite rate
Authors
David L Smith
Carlos A Guerra
Robert W Snow
Simon I Hay
Publication date
01-12-2007
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2007
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-6-131

Other articles of this Issue 1/2007

Malaria Journal 1/2007 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.