Skip to main content
Top
Published in: Malaria Journal 1/2016

Open Access 01-12-2016 | Research

Spatial heterogeneity of malaria in Ghana: a cross-sectional study on the association between urbanicity and the acquisition of immunity

Authors: Clemens Frank, Ralf Krumkamp, Nimako Sarpong, Peter Sothmann, Julius N Fobil, Geoffrey Foli, Anna Jaeger, Lutz Ehlkes, Ellis Owusu-Dabo, Yaw Adu-Sarkodie, Florian Marks, Ralf R. Schumann, Jürgen May, Benno Kreuels

Published in: Malaria Journal | Issue 1/2016

Login to get access

Abstract

Background

Malaria incidence has declined considerably over the last decade. This is partly due to a scale-up of control measures but is also attributed to increasing urbanization. This study aimed to analyse the association between malaria and urbanization and the effect of urbanicity on the acquisition of semi-immunity.

Methods

In 2012, children with fever presenting to St Michael’s Hospital Pramso/Ghana were recruited. The malaria-positive-fraction (MPF) of fever cases was calculated on community-level to approximate the malaria risk. The mean age of malaria cases was calculated for each community to estimate the acquisition of semi-immunity. The level of urbanicity for the communities was calculated and associations between MPF, urbanicity and immunity were modelled using linear regression.

Results

Twenty-six villages were included into the study with a mean MPF of 35 %. A linear decrease of 5 % (95 % CI: 4–6 %) in MPF with every ten-point increase in urbanicity was identified. The mean age of malaria patients increased by 2.9 months (95 % CI: 1.0–4.8) with every ten-point increase in urbanicity.

Discussion

The results confirm an association between an increase in urbanicity and declining malaria risk and demonstrate that the acquisition of semi-immunity is heterogeneous on a micro-epidemiological scale and is associated with urbanicity.
Appendix
Available only for authorised users
Literature
1.
go back to reference Gething PW, Patil AP, Smith DL, Guerra CA, Elyazar IRF, Johnston GL, et al. A new world malaria map: Plasmodium falciparum endemicity in 2010. Malar J. 2011;10:378.PubMedCentralCrossRefPubMed Gething PW, Patil AP, Smith DL, Guerra CA, Elyazar IRF, Johnston GL, et al. A new world malaria map: Plasmodium falciparum endemicity in 2010. Malar J. 2011;10:378.PubMedCentralCrossRefPubMed
2.
go back to reference WHO. World Malaria Report 2013. Geneva: World Health Organization; 2013. WHO. World Malaria Report 2013. Geneva: World Health Organization; 2013.
4.
go back to reference WHO. World Health Statistics 2012. Geneva: World Health Organization; 2012. WHO. World Health Statistics 2012. Geneva: World Health Organization; 2012.
5.
go back to reference Tatem AJ, Guerra CA, Kabaria CW, Noor AM, Hay SI. Human population, urban settlement patterns and their impact on Plasmodium falciparum malaria endemicity. Malar J. 2008;7:218.PubMedCentralCrossRefPubMed Tatem AJ, Guerra CA, Kabaria CW, Noor AM, Hay SI. Human population, urban settlement patterns and their impact on Plasmodium falciparum malaria endemicity. Malar J. 2008;7:218.PubMedCentralCrossRefPubMed
6.
go back to reference UN. World urbanization prospects—the 2011 Revision. New York: 2011. UN. World urbanization prospects—the 2011 Revision. New York: 2011.
7.
8.
go back to reference Trape J-F, Zoulani A. Malaria and urbanization in central Africa: the example of Brazzaville Part III: relationships between urbanization and the intensity of malaria transmission. Trans R Soc Trop Med Hyg. 1987;81:19–25.CrossRefPubMed Trape J-F, Zoulani A. Malaria and urbanization in central Africa: the example of Brazzaville Part III: relationships between urbanization and the intensity of malaria transmission. Trans R Soc Trop Med Hyg. 1987;81:19–25.CrossRefPubMed
9.
10.
go back to reference Kreuels B, Kobbe R, Adjei S, Kreuzberg C, Von Reden C, Bater K, et al. Spatial variation of malaria incidence in young children from a geographically homogeneous area with high endemicity. J Infect Dis. 2008;197:85–93.CrossRefPubMed Kreuels B, Kobbe R, Adjei S, Kreuzberg C, Von Reden C, Bater K, et al. Spatial variation of malaria incidence in young children from a geographically homogeneous area with high endemicity. J Infect Dis. 2008;197:85–93.CrossRefPubMed
11.
go back to reference Bousema T, Drakeley C, Gesase S, Hashim R, Magesa S, Mosha F, et al. Identification of hot spots of malaria transmission for targeted malaria control. J Infect Dis. 2010;201:1764–74.CrossRefPubMed Bousema T, Drakeley C, Gesase S, Hashim R, Magesa S, Mosha F, et al. Identification of hot spots of malaria transmission for targeted malaria control. J Infect Dis. 2010;201:1764–74.CrossRefPubMed
12.
go back to reference Reyburn H, Mbatia R, Drakeley C, Bruce J, Carneiro I, Olomi R, et al. Association of transmission intensity and age with clinical manifestations and case fatality of severe Plasmodium falciparum malaria. JAMA. 2005;293:1461–70.CrossRefPubMed Reyburn H, Mbatia R, Drakeley C, Bruce J, Carneiro I, Olomi R, et al. Association of transmission intensity and age with clinical manifestations and case fatality of severe Plasmodium falciparum malaria. JAMA. 2005;293:1461–70.CrossRefPubMed
13.
go back to reference Greenwood B. The microepidemiology of malaria and its importance to malaria control. Trans R Soc Trop Med Hyg. 1989;83:25–9.CrossRefPubMed Greenwood B. The microepidemiology of malaria and its importance to malaria control. Trans R Soc Trop Med Hyg. 1989;83:25–9.CrossRefPubMed
14.
go back to reference Snow RW, Omumbo JA, Lowe B, Molyneux CS, Obiero JO, Palmer A, et al. Relation between severe malaria morbidity in children and level of Plasmodium falciparum transmission in Africa. Lancet. 1997;349:1650–4.CrossRefPubMed Snow RW, Omumbo JA, Lowe B, Molyneux CS, Obiero JO, Palmer A, et al. Relation between severe malaria morbidity in children and level of Plasmodium falciparum transmission in Africa. Lancet. 1997;349:1650–4.CrossRefPubMed
16.
go back to reference Ghana Statistical Service. GSS Population & Housing Census. 2010. Ghana Statistical Service. GSS Population & Housing Census. 2010.
17.
go back to reference DeVellis RF. Scale development: theory and aplications. 2nd ed. vol 26. Thousand Oaks: Sage Publications Inc.; 2003. DeVellis RF. Scale development: theory and aplications. 2nd ed. vol 26. Thousand Oaks: Sage Publications Inc.; 2003.
18.
go back to reference Netemeyer RG, Bearden WO, Sharma S. Scaling procedures—issues and applications. Tousand Oaks: Sage Publications Inc; 2003. Netemeyer RG, Bearden WO, Sharma S. Scaling procedures—issues and applications. Tousand Oaks: Sage Publications Inc; 2003.
19.
go back to reference Van Eijk AM, Hill J, Larsen DA, Webster J, Steketee RW, Eisele TP, et al. Coverage of intermittent preventive treatment and insecticide-treated nets for the control of malaria during pregnancy in sub-Saharan Africa: a synthesis and meta-analysis of national survey data, 2009-11. Lancet Infect Dis. 2013;13:1029–42.CrossRefPubMed Van Eijk AM, Hill J, Larsen DA, Webster J, Steketee RW, Eisele TP, et al. Coverage of intermittent preventive treatment and insecticide-treated nets for the control of malaria during pregnancy in sub-Saharan Africa: a synthesis and meta-analysis of national survey data, 2009-11. Lancet Infect Dis. 2013;13:1029–42.CrossRefPubMed
20.
go back to reference Wang S-J, Lengeler C, Smith TA, Vounatsou P, Diadie DA, Pritroipa X, et al. Rapid urban malaria appraisal (RUMA) I: epidemiology of urban malaria in Ouagadougou. Malar J. 2005;4:43.PubMedCentralCrossRefPubMed Wang S-J, Lengeler C, Smith TA, Vounatsou P, Diadie DA, Pritroipa X, et al. Rapid urban malaria appraisal (RUMA) I: epidemiology of urban malaria in Ouagadougou. Malar J. 2005;4:43.PubMedCentralCrossRefPubMed
21.
go back to reference Robert V, Macintyre K, Keating J, Trape J-F, Duchemin J-B, Warren M, et al. Malaria transmission in urban sub-Saharan Africa. Am J Trop Med Hyg. 2003;68:169–76.PubMed Robert V, Macintyre K, Keating J, Trape J-F, Duchemin J-B, Warren M, et al. Malaria transmission in urban sub-Saharan Africa. Am J Trop Med Hyg. 2003;68:169–76.PubMed
22.
go back to reference Dahly DL, Adair LS. Quantifying the urban environment: a scale measure of urbanicity outperforms the urban-rural dichotomy. Soc Sci Med. 2007;64:1407–19.PubMedCentralCrossRefPubMed Dahly DL, Adair LS. Quantifying the urban environment: a scale measure of urbanicity outperforms the urban-rural dichotomy. Soc Sci Med. 2007;64:1407–19.PubMedCentralCrossRefPubMed
23.
go back to reference Jones-Smith JC, Popkin BM. Understanding community context and adult health changes in China: development of an urbanicity scale. Soc Sci Med. 2010;71:1436–46.PubMedCentralCrossRefPubMed Jones-Smith JC, Popkin BM. Understanding community context and adult health changes in China: development of an urbanicity scale. Soc Sci Med. 2010;71:1436–46.PubMedCentralCrossRefPubMed
24.
go back to reference Novak NL, Allender S, Scarborough P, West D. The development and validation of an urbanicity scale in a multi-country study. BMC Public Health. 2012;12:530.PubMedCentralCrossRefPubMed Novak NL, Allender S, Scarborough P, West D. The development and validation of an urbanicity scale in a multi-country study. BMC Public Health. 2012;12:530.PubMedCentralCrossRefPubMed
25.
go back to reference Trape J-F, Zoulani A. Malaria and urbanization in central Africa: the example of Brazzaville. Part II: results of entomological surveys and epidemiological analysis. Trans R Soc Trop Med Hyg. 1987;81:10–8.CrossRefPubMed Trape J-F, Zoulani A. Malaria and urbanization in central Africa: the example of Brazzaville. Part II: results of entomological surveys and epidemiological analysis. Trans R Soc Trop Med Hyg. 1987;81:10–8.CrossRefPubMed
26.
go back to reference Trape J-F. Malaria and urbanization in central Africa the example of Brazzaville Part IV: parasitological and serological surveys in urban and surrounding areas. Trans R Soc Trop Med Hyg. 1987;81:26–33.CrossRefPubMed Trape J-F. Malaria and urbanization in central Africa the example of Brazzaville Part IV: parasitological and serological surveys in urban and surrounding areas. Trans R Soc Trop Med Hyg. 1987;81:26–33.CrossRefPubMed
27.
go back to reference Machault V, Vignolles C, Pagès F, Gadiaga L, Gaye A, Sokhna C, et al. Spatial heterogeneity and temporal evolution of malaria transmission risk in Dakar, Senegal, according to remotely sensed environmental data. Malar J. 2010;9:252.PubMedCentralCrossRefPubMed Machault V, Vignolles C, Pagès F, Gadiaga L, Gaye A, Sokhna C, et al. Spatial heterogeneity and temporal evolution of malaria transmission risk in Dakar, Senegal, according to remotely sensed environmental data. Malar J. 2010;9:252.PubMedCentralCrossRefPubMed
28.
go back to reference Machault V, Vignolles C, Pagès F, Gadiaga L, Tourre YM, Gaye A, et al. Risk mapping of Anopheles gambiae s.l. densities using remotely-sensed environmental and meteorological data in an urban area: Dakar, Senegal. PLoS One. 2012;7:e50674.PubMedCentralCrossRefPubMed Machault V, Vignolles C, Pagès F, Gadiaga L, Tourre YM, Gaye A, et al. Risk mapping of Anopheles gambiae s.l. densities using remotely-sensed environmental and meteorological data in an urban area: Dakar, Senegal. PLoS One. 2012;7:e50674.PubMedCentralCrossRefPubMed
29.
30.
go back to reference Fobil JN, Kraemer A, Meyer CG, May J. Neighborhood urban environmental quality conditions are likely to drive malaria and diarrhea mortality in Accra, Ghana. J Environ Public Health. 2011;2011:484010.PubMedCentralCrossRefPubMed Fobil JN, Kraemer A, Meyer CG, May J. Neighborhood urban environmental quality conditions are likely to drive malaria and diarrhea mortality in Accra, Ghana. J Environ Public Health. 2011;2011:484010.PubMedCentralCrossRefPubMed
31.
32.
go back to reference Ghana Health Service. Expanded programme on immunization report. 2008. Ghana Health Service. Expanded programme on immunization report. 2008.
33.
go back to reference Ghani AC, Sutherland CJ, Riley EM, Drakeley CJ, Griffin JT, Roly D, et al. Loss of population levels of immunity to malaria as a result of exposure-reducing interventions: consequences for interpretation of disease trends. PLoS One. 2009;4:e4383.PubMedCentralCrossRefPubMed Ghani AC, Sutherland CJ, Riley EM, Drakeley CJ, Griffin JT, Roly D, et al. Loss of population levels of immunity to malaria as a result of exposure-reducing interventions: consequences for interpretation of disease trends. PLoS One. 2009;4:e4383.PubMedCentralCrossRefPubMed
34.
go back to reference Bandeiras C, Trovoada MJ, Gonçalves LA, Marinho CR, Turner L, Hviid L, et al. Modeling malaria infection and immunity against variant surface antigens in Príncipe Island, West Africa. PLoS One. 2014;9:e88110.PubMedCentralCrossRefPubMed Bandeiras C, Trovoada MJ, Gonçalves LA, Marinho CR, Turner L, Hviid L, et al. Modeling malaria infection and immunity against variant surface antigens in Príncipe Island, West Africa. PLoS One. 2014;9:e88110.PubMedCentralCrossRefPubMed
35.
go back to reference Carneiro I, Roca-Feltrer A, Griffin JT, Smith L, Tanner M, Schellenberg A, et al. Age-patterns of malaria vary with severity, transmission intensity and seasonality in sub-Saharan Africa: a systematic review and pooled analysis. PLoS One. 2010;5:e8988.PubMedCentralCrossRefPubMed Carneiro I, Roca-Feltrer A, Griffin JT, Smith L, Tanner M, Schellenberg A, et al. Age-patterns of malaria vary with severity, transmission intensity and seasonality in sub-Saharan Africa: a systematic review and pooled analysis. PLoS One. 2010;5:e8988.PubMedCentralCrossRefPubMed
36.
go back to reference Gardiner C, Biggar RJ, Collins WE, Nkrumah FK. Malaria in urban and rural areas of southern Ghana: a survey of parasitaemia, antibodies, and antimalarial practices. Bull World Health Organ. 1984;62:607–13.PubMedCentralPubMed Gardiner C, Biggar RJ, Collins WE, Nkrumah FK. Malaria in urban and rural areas of southern Ghana: a survey of parasitaemia, antibodies, and antimalarial practices. Bull World Health Organ. 1984;62:607–13.PubMedCentralPubMed
37.
go back to reference Okiro EA, Al-Taiar A, Reyburn H, Idro R, Berkley JA, Snow RW. Age patterns of severe paediatric malaria and their relationship to Plasmodium falciparum transmission intensity. Malar J. 2009;8:4.PubMedCentralCrossRefPubMed Okiro EA, Al-Taiar A, Reyburn H, Idro R, Berkley JA, Snow RW. Age patterns of severe paediatric malaria and their relationship to Plasmodium falciparum transmission intensity. Malar J. 2009;8:4.PubMedCentralCrossRefPubMed
38.
go back to reference Roca-Feltrer A, Carneiro I, Smith L, Schellenberg JRA, Greenwood B, Schellenberg D. The age patterns of severe malaria syndromes in sub-Saharan Africa across a range of transmission intensities and seasonality settings. Malar J. 2010;9:282.PubMedCentralCrossRefPubMed Roca-Feltrer A, Carneiro I, Smith L, Schellenberg JRA, Greenwood B, Schellenberg D. The age patterns of severe malaria syndromes in sub-Saharan Africa across a range of transmission intensities and seasonality settings. Malar J. 2010;9:282.PubMedCentralCrossRefPubMed
39.
go back to reference Meara WPO, Mwangi TW, Williams TN, Mckenzie FE, Robert W, Marsh K. Relationship between exposure, clinical malaria, and age in an area of changing transmission intensity. Am J Trop Med Hyg. 2008;79:185–91. Meara WPO, Mwangi TW, Williams TN, Mckenzie FE, Robert W, Marsh K. Relationship between exposure, clinical malaria, and age in an area of changing transmission intensity. Am J Trop Med Hyg. 2008;79:185–91.
40.
go back to reference Bejon P, Williams TN, Nyundo C, Hay SI, Benz D, Gething PW, et al. A micro-epidemiological analysis of febrile malaria in Coastal Kenya showing hotspots within hotspots. Elife. 2014;3:e02130.PubMedCentralCrossRefPubMed Bejon P, Williams TN, Nyundo C, Hay SI, Benz D, Gething PW, et al. A micro-epidemiological analysis of febrile malaria in Coastal Kenya showing hotspots within hotspots. Elife. 2014;3:e02130.PubMedCentralCrossRefPubMed
41.
go back to reference Snow RW, Marsh K. The consequences of reducing transmission of Plasmodium falciparum in Africa. Adv Parasitol. 2002;52:235–64.CrossRefPubMed Snow RW, Marsh K. The consequences of reducing transmission of Plasmodium falciparum in Africa. Adv Parasitol. 2002;52:235–64.CrossRefPubMed
42.
go back to reference Jensen TP, Bukirwa H, Njama-Meya D, Francis D, Kamya MR, Rosenthal PJ, et al. Use of the slide positivity rate to estimate changes in malaria incidence in a cohort of Ugandan children. Malar J. 2009;8:213.PubMedCentralCrossRefPubMed Jensen TP, Bukirwa H, Njama-Meya D, Francis D, Kamya MR, Rosenthal PJ, et al. Use of the slide positivity rate to estimate changes in malaria incidence in a cohort of Ugandan children. Malar J. 2009;8:213.PubMedCentralCrossRefPubMed
43.
go back to reference Seyoum A, Sikaala C, Bayoh N, Huho B, Brie O, Killeen G. Consistently high estimates for the proportion of human exposure to malaria vector populations occurring indoors in rural Africa. Int J Epidemiol. 2013;42:235–47.PubMedCentralCrossRefPubMed Seyoum A, Sikaala C, Bayoh N, Huho B, Brie O, Killeen G. Consistently high estimates for the proportion of human exposure to malaria vector populations occurring indoors in rural Africa. Int J Epidemiol. 2013;42:235–47.PubMedCentralCrossRefPubMed
Metadata
Title
Spatial heterogeneity of malaria in Ghana: a cross-sectional study on the association between urbanicity and the acquisition of immunity
Authors
Clemens Frank
Ralf Krumkamp
Nimako Sarpong
Peter Sothmann
Julius N Fobil
Geoffrey Foli
Anna Jaeger
Lutz Ehlkes
Ellis Owusu-Dabo
Yaw Adu-Sarkodie
Florian Marks
Ralf R. Schumann
Jürgen May
Benno Kreuels
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2016
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-016-1138-4

Other articles of this Issue 1/2016

Malaria Journal 1/2016 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
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 discusses last year's major advances in heart failure and cardiomyopathies.