Malaria and irrigated crops, Accra, Ghana.We investigated the prevalence of malaria and associated risk factors in children living in urban Ghana. Malaria prevalence was associated with low hemoglobin hemoglobin (hē`məglō'bĭn), respiratory protein found in the red blood cells (erythrocytes) of all vertebrates and some invertebrates. concentration, low socioeconomic status socioeconomic status, n the position of an individual on a socio-economic scale that measures such factors as education, income, type of occupation, place of residence, and in some populations, ethnicity and religion. , and higher age. Our findings indicate that African urban poor are seriously affected by malaria and irrigated agriculture may increase this risk. ********* Malaria is predominantly a rural disease in Africa. Previous studies have shown that Anopheles Anopheles: see mosquito. mosquito breeding decreases with increasing proximity to the center of urban areas (1,2). Although the complex factors that contribute to malaria risk are not fully understood (2), availability of vector breeding sites is clearly essential. Urban agriculture, promoted as a means of increasing food security, improving nutrition, and alleviating poverty (3), can, especially when irrigated, create breeding habitats that could increase malaria transmission in cities. This potential risk was indicated by other authors (3-6), but only a limited number of studies have attempted to quantify the impact of urban agriculture on malaria transmission (4,7,8), and virtually all used only entomologic en·to·mol·o·gy n. The scientific study of insects. en  to·mo·log parameters (e.g., the entomologic inoculation inoculation, in medicine, introduction of a preparation into the tissues or fluids of the body for the purpose of preventing or curing certain diseases. The preparation is usually a weakened culture of the agent causing the disease, as in vaccination against rate, an estimate of the number of infected bites received per person
per unit of time) in their analyses. Such measures are only proxies of
actual malaria risk, and no studies have assessed the malaria parasite
prevalence, a direct indicator of the impact of malaria, in communities
with and without urban agriculture. By 2025, an estimated 700 million
people will live in urban communities in Africa, which is approximately
double the current urban population (9). With such rapid expansion,
identification of the risk factors for urban malaria requires urgent
attention (10).The Study From October 2002 to January 2003, we investigated malaria parasite prevalence in central Accra, Ghana, in communities bordering irrigated urban agriculture areas and in control communities (defined as sites located >l km from an urban agricultural area, based on the likely appetitive flight distance of female mosquitoes) (11) (Figure 1). Communities around the main agricultural sites in Accra were selected and based on them representative control communities in terms of socioeconomic status, housing and crowding were selected. Different types of urban agriculture exist: basic backyard farming in or around the house, cultivation of stable crops such as maize maize: see corn. on (temporary) fallow land fallow land, cropland that is not seeded for a season; it may or may not be plowed. The land may be cultivated or chemically treated for control of weeds and other pests or may be left unaltered. , and cultivation of ornamental plants, mostly along roadsides. An important part of agriculture in the city is commercial cultivation of vegetables, such as lettuce, onion, and cabbage (Figure 2). These crops are irrigated from wells or streams with watering cans, and crops are sometimes cultivated on raised beds with water-filled furrows. Irrigated farming has the greatest potential to create additional breeding sites, and irrigated, open-spaced vegetable farming has been linked to higher anopheline anopheline pertaining to the anopheles genus of mosquitoes. densities in Kumasi, Ghana (4). The study focused on this type of urban agriculture, which refers to irrigated, open-spaced, commercial vegetable production. In the selected communities, we conducted a cross-sectional house-to-house survey to assess malaria parasitemia parasitemia /par·a·si·te·mia/ (par?ah-si-te´me-ah) the presence of parasites, especially malarial forms, in the blood. par·a·si·te·mi·a n. The presence of parasites in the blood. and hemoglobin (Hb) concentration in children 6 to 60 months of age. A team consisting of technicians and trained enumerators went house to house to collect data. Houses were selected arbitrarily and queried regarding the presence of children <5 years of age. For each community, the whole area was covered to account for spatial heterogeneity Environments with a wide variety of habitats such as different topographies, soil types and climates are able to accommodate a greater amount of species. Spatial heterogeneity . If most compounds or houses had children <5 years of age, houses were omitted to obtain the target sample size of 150 children from the community. Informed consent was obtained from each child's caregiver. Thick and thin blood films were collected and read according to according to prep. 1. As stated or indicated by; on the authority of: according to historians. 2. In keeping with: according to instructions. 3. standard World Health Organization protocols. Hb levels were assessed by using a blood hemoglobin photometer Photometer An instrument used for making measurements of light, or electromagnetic radiation, in the visible range. In general, photometers may be divided into two classifications: laboratory photometers, which are usually fixed in position and yield results (HemoCue, Angelhohn, Sweden). Children with parasitemias or Hb levels <8.0 g/dL were provided free treatment at a local clinic. The epidemiologic data were related to proximity to sites of urban agriculture, socioeconomic status based on household assets following a World Bank template (12), and possible confounding confounding when the effects of two, or more, processes on results cannot be separated, the results are said to be confounded, a cause of bias in disease studies. confounding factor factors obtained by questionnaire from the child's caregiver. The location of each house, study site boundaries, land marks, and urban agricultural areas were mapped by using a hand-held global positioning system Global Positioning System: see navigation satellite. Global Positioning System (GPS) Precise satellite-based navigation and location system originally developed for U.S. military use. . For each household in the urban agricultural communities, the shortest distance to the nearest agricultural site was calculated by using Arcinfo (ESRI (Environmental Systems Research Institute, Inc., Redlands, CA, www.esri.com) The world's leading developer of geographic information systems (GIS) software, including programs that plot ZIP codes and addresses, demographic information and detailed, color-coded data. , Redlands, CA, USA). Ethical approval was granted by the Liverpool School of Tropical Medicine The Liverpool School of Tropical Medicine (LSTM), England, was founded on 12 November 1898, by a donation from Sir Alfred Lewis Jones, a Liverpool Shipowner. The donation of £350 created the first school of its kind. and the University of Ghana The University of Ghana is the oldest and largest of the five Ghanaian public universities. It was founded in 1948[1] as the University College of the Gold Coast, and was originally an affiliate college of the University of London[2] , Legon. A total of 1,757 children from 938 households in 12 different communities were enrolled in the study. Table 1 shows the baseline characteristics of the children with Plasmodium-positive and -negative slides, and Table 2 shows the characteristics for the urban agricultural and control communities. Of 261 infections detected, 258 were P. falciparum, 2 were P. malariae, and 1 was a mixed infection with P. Jalciparum and P. malariae. The average Hb level was 10.82 g/dL (SD 1.47), and 78 (4.5%) of 1,738 children had moderate-to-severe anemia (Hb <8.0 g/dL). Overall malaria parasite prevalence was 14.9% (261/1,757, range 6%-22%) and was higher in communities around urban agricultural sites than in control communities (16.5% and 11.4%, respectively, odds ratio [OR] 1.53, 95% confidence interval confidence interval, n a statistical device used to determine the range within which an acceptable datum would fall. Confidence intervals are usually expressed in percentages, typically 95% or 99%. [CI] 1.10-2.14, p = 0.008). In a univariate analysis (Pearson chi square chi square (kī), n a nonparametric statistic used with discrete data in the form of frequency count (nominal data) or percentages or proportions that can be reduced to frequencies. for binominal Bi`nom´i`nal a. 1. Of or pertaining to two names; binomial. Adj. 1. binominal - having or characterized by two names, especially those of genus and species in taxonomies; "binomial nomenclature of bacteria" variables and t test for continuous variables), Hb concentration (negative association, p<0.001); moderate-to-severe anemia (OR 3.49, 95% CI 1.98-6.11, p<0.001); having netting in front of windows, doors, or both (OR 0.65, 95% CI 0.46-0.92, p = 0.012); socioeconomic status (negative association, p<0.001); and age (positive association peaking at [approximately equal to] 3 years of age, p = 0.002) showed significant associations with presence of malaria parasites. Reported bed net use by a household was 33% (range 6%-53% in different communities) but was not significantly associated with presence of malaria parasites in the blood. A generalized linear mixed model (GLMM GLMM General Linear Mixed Model GLMM Great Lakes Maritime Museum (Sebewaing, Michigan) ) approach, using an SAS (1) (SAS Institute Inc., Cary, NC, www.sas.com) A software company that specializes in data warehousing and decision support software based on the SAS System. Founded in 1976, SAS is one of the world's largest privately held software companies. See SAS System. macro (Glimmix 800, SAS Inc., Cary, NC, USA) that allowed a logistic link function, was used to investigate the association between putative predictor variables and malaria parasite prevalence. Covariates with p<0.1 in the univariate analysis were entered in the multivariate model. Household was nested within community, and both variables were treated as random effects Random effects can refer to:
adj. That can be presumed or taken for granted; reasonable as a supposition: presumable causes of the disaster. because presence of nets was associated with a higher socioeconomic status (p<0.001). In urban agricultural communities, GLMM analysis with parasitemia as the outcome was conducted with age group, distance to an urban agricultural site, socioeconomic status, and house effects. The Hb level was omitted because it was likely to be the result of malaria infection and its inclusion could obscure the effect of distance. Two of the districts, Mle (p = 0.021) and Kbu (p = 0.014), showed decreases in prevalence with distance from an urban agricultural site; the odds of infection were reduced [approximately equal to] 50% every 100 m from the site. However, these results need to be interpreted with caution because it is difficult to detect a putative decrease in prevalence with distance against the noise introduced by small, unidentified, often transitory TRANSITORY. That which lasts but a short time, as transitory facts that which may be laid in different places, as a transitory action. , breeding sites. Their presence may explain why 2 sites, Rom (p = 0.043) and Dzor (p = 0.039), showed a significant increase in prevalence with distance, while 2 others, Air and Koto koto (kō`tō), a Japanese string instrument related in structure to the zither. It consists of an elongated rectangular wooden body, strung lengthwise with 7 to 13 silk strings. , showed a significant effect when distance in 100-m intervals was cross-tabulated with prevalence (p<0.001, Fisher exact test). Since unidentified breeding sites may also introduce unknown data structuring that cannot be incorporated into a GLMM, the probabilities obtained may be lower than are appropriate. Conclusions The parasitemia levels obtained in this study are worrisome because high-density urban African populations are not often considered particularly vulnerable to malaria infection. In other West African West Africa A region of western Africa between the Sahara Desert and the Gulf of Guinea. It was largely controlled by colonial powers until the 20th century. West African adj. & n. urban areas, malaria prevalence rates from 2% to 16% have been reported with large variation between communities (5,13). Recently, several authors focused attention on urban malaria (2,12) and stressed the need to investigate risk factors for urban malaria. In our study, the parasitemic children were more likely to be anemic anemic pertaining to anemia. , have a lower socioeconomic status, and live in a community close to areas of urban agriculture. Since recent travel to a rural area did not affect outcome, local malaria transmission is indicated. Our entomologic studies in these study areas (unpub. data) have found Anopheles gambiae Anopheles gambiae, refers to a complex of morphologically indistinguishable mosquitoes in the genus Anopheles, which contains the most important vectors of malaria in Sub-Saharan Africa [1], and the most efficient malaria vectors in the world. S form breeding in irrigation irrigation, in agriculture, artificial watering of the land. Although used chiefly in regions with annual rainfall of less than 20 in. (51 cm), it is also used in wetter areas to grow certain crops, e.g., rice. water at urban agricultural sites and resting at higher densities in houses in urban agricultural communities. These findings are based on a point prevalence In epidemiology, point prevalence is a measure of the proportion of people in a population who have a disease or condition at a particular time, such as a particular date. It is like a snap shot of the disease in time. survey in the dry season. Although we continue to obtain data during the wet season, analysis of data indicates that the urban poor in Africa may be at higher risk for malaria than expected and that malaria can no longer be regarded only as a rural phenomenon. This finding is of great concern because in Africa the current urban population growth rate of 3.5% is >3 times the rural population growth rate, and by 2015 a total of 25 countries in sub-Saharan Africa will have urban populations larger than the rural populations (9). Although levels of transmission in urban areas may be lower than in contiguous rural areas, high population densities and possible lower immunity (6) may result in more disease impact in urban settings. Furthermore, although not the sole cause, irrigated urban agriculture may further increase the risk for malaria by providing suitable breeding sites. Further research on the interaction between type of urban agriculture and vector biology is needed because most African cities irrigate ir·ri·gate v. To wash out a cavity or wound with a fluid. agricultural areas with water from polluted pol·lute tr.v. pol·lut·ed, pol·lut·ing, pol·lutes 1. To make unfit for or harmful to living things, especially by the addition of waste matter. See Synonyms at contaminate. 2. sources that is generally not favored by malaria vectors, although several studies have reported anophelines breeding in heavily contaminated contaminated, v 1. made radioactive by the addition of small quantities of radioactive material. 2. made contaminated by adding infective or radiographic materials. 3. an infective surface or object. water (14,15). The advantages of urban agriculture for alleviating poverty are numerous, but care must be taken that unregulated growth does not compromise its success. Integration of the activities of municipal authorities, agriculturalists, health professionals, and communities is essential to reduce the existing impact of malaria and to prevent future increases.
Table 1. Summary of variables measured for children with and
without malaria parasites, with results of univariate
(Pearson chi-square or t) tests *
Plasmodium-positive
Variables blood slide (n = 261)
Mean Hb, g/dL (SD) 10.17 (1.62)
Hb <8 g/dL, % 11.3 (29/257)
Mean age, months (SD) 36.44 (16.03)
Mean socioeconomic score ([dagger]) (SD) 1.42 (0.99)
Male (%) 123 (47.1)
Travel to village ([double dagger]) (%) 17 (6.5)
Taken malaria medication in
last 2 wk ([section]) (%) 63 (24.1)
History of fever ([section]) (%) 64 (24.5)
HH with reporting bed net use (%) 89 (34.1)
HH who spray weekly ([paragraph]) (%) 71 (27.2)
HH with netting at windows/doors (%) 208 (79.7)
HH without ceiling (%) 77 (29.8)
Plasmodium-
negative blood
Variables slide (n = 1,496) p value
Mean Hb, g/dL (SD) 10.94 (1.42) <0.001
Hb <8 g/dL, % 3.3 (49/1,481) <0.001
Mean age, months (SD) 32.92 (17.19) <0.001
Mean socioeconomic score ([dagger]) (SD) 1.74 (0.98) <0.001
Male (%) 739 (49.4) 0.498
Travel to village ([double dagger]) (%) 93 (6.2) 0.855
Taken malaria medication in
last 2 wk ([section]) (%) 344 (23.0) 0.686
History of fever ([section]) (%) 293 (19.6) 0.067
HH with reporting bed net use (%) 499 (33.4) 0.814
HH who spray weekly ([paragraph]) (%) 435 (29.1) 0.537
HH with netting at windows/doors (%) 1282 (85.8) 0.012
HH without ceiling (%) 382 (25.6) 0.147
* Hb, hemoglobin; HH, household.
([dagger]) Composite measure of socioeconomic status used was the asset
factor score of the World Bank for Ghana (www.worldbank.com/hnp).
([double dagger]) Persons who had traveled to a rural (potentially
malarious) area in the previous 3 weeks.
([section]) In the last 48 hours, as reported by the caregiver.
([paragraph]) Proprietary brands of insecticide aerosols.
Table 2. Summary statistics for variables measured in children in
communities near urban agricultural sites and control communities,
with results of univariate (Pearson chi-square or t) tests *
Children in urban
agricultural
communities
(n = 1,223)
Variables ([dagger])
Children with Plasmodium-positive
slide, % 16.4 (200/1,223)
Mean Hb, g/dL (SD) 10.93 (1.46)
Hb <8 g/dL, % 3.4 (41/1,215)
Mean age, months (SD) 33.3 (17.1)
Mean socioeconomic score
([double dagger]) (SD) 1.78 (0.96)
Travel to village ([section]), (%) 7.9
Taken malaria medication in
last 2 wk ([paragraph]) (%) 23.5
History of fever ([paragraph])(#), (%) 21.2
HH reporting bed net use, (%) 37.7
Children
in control
communities
Variables (n = 534) p value
Children with Plasmodium-positive
slide, % 11.4 (61/534) 0.008
Mean Hb, g/dL (SD) 10.59 (1.46) <0.001
Hb <8 g/dL, % 5.5 (29/529) 0.039
Mean age, months (SD) 33.8 (17.0) 0.601
Mean socioeconomic score
([double dagger]) (SD) 1.49 (l.02) <0.001
Travel to village ([section]), (%) 2.4 <0.001
Taken malaria medication in
last 2 wk ([paragraph]) (%) 22.3 0.600
History of fever ([paragraph])(#), (%) 18.2 0.155
HH reporting bed net use, (%) 24.2 <0.001
* Hb, hemoglobin; HH, household. Control communities were those >1 km
from an urban agricultural area.
([dagger]) Number of children in the urban agricultural community
group is higher because small plots of agriculture were discovered
in 2 communities originally designated control sites. If these 2
communities were omitted from the analysis, similar results
were obtained and significance remained the same except
for children with moderate-to-severe anemia, which was no
longer significant (p = 0.065) (data not shown).
([double dagger]) Composite measure of socioeconomic status
used was the asset factor score of the World Bank for Ghana
(www.worldbank.com/hnp).
([section]) Persons who had traveled to a rural (potentially
malarious) area in the previous 3 weeks.
([paragraph) As reported by the caregiver.
(#) In the last 48 h.
Acknowledgments We thank Guy Barnish and Imelda Bates Bates , Katherine Lee 1859-1929. American educator and writer best known for her poem "America the Beautiful," written in 1893 and revised in 1904 and 1911. for advice, facilitation Facilitation The process of providing a market for a security. Normally, this refers to bids and offers made for large blocks of securities, such as those traded by institutions. , and technical assistance; the field teams who assisted with data collection; and the assembly men and people in the study communities for their cooperation. The views in this paper are the opinions of the authors and do not reflect the policy of the Department for International Development. This is a project of the Consultative Group on International Agricultural Research The Consultative Group on International Agricultural Research (CGIAR) was originally created at the initiative of the Rockefeller Foundation, which had sponsored international meetings of agronomists at its Bellagio Conference Center in Lake Como, Italy, from 1968 onwards. system-wide Initiative on Malaria and Agriculture. This study was partially supported by the Department of International Development-funded Malaria Knowledge Programme of the Liverpool School of Tropical Medicine. References (1.) Warren M, Billig P, Bendahmane DB, Wijeyaratne P. Malaria in urban and peri-urban areas in sub-Sahara Africa. August 1999 EHP EHP abbr. 1. effective horsepower 2. electric horsepower activity report 71. [cited 20 May 2005]. Available from www.ehpproject.org (2.) Robert V, Macintyre K, Keating J, Trape JF, Duchemin JB, Warren M et al. Malaria transmission in urban sub-Saharan Africa. Am J Trop Med Hyg. 2003;68:169-76. (3.) Smit J, Ratta A, Nasr J, Urban agriculture, food, jobs and sustainable cities. New York New York, state, United States New York, Middle Atlantic state of the United States. It is bordered by Vermont, Massachusetts, Connecticut, and the Atlantic Ocean (E), New Jersey and Pennsylvania (S), Lakes Erie and Ontario and the Canadian province of : United Nations Development Program; 1996. (4.) Afrane YA, Klinkenberg E, Drechsel P, Owusu-Daaku K, Ganns R. Kruppa T. Does irrigated urban agriculture influence the transmission of malaria in the city of Kumasi, Ghana? Acta Trop. 2004;89:125-34. (5.) Vercruysse J, Jancloes M, van de Velden L. Epidemiology of seasonal falciparum malaria fal·cip·a·rum malaria n. Malaria caused by Plasmodium falciparum and characterized by severe malarial paroxysms that recur about every 48 hours and often by acute cerebral, renal, or gastrointestinal manifestations. in an urban area of Senegal. Bull World Health Organ. 1983;61:821-31. (6.) Trape JF, 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(Suppl 2):19-25. (7.) Robert V, Awono-Ambene HE Thionlouse J. Ecology of larval larval 1. pertaining to larvae. 2. larvate. larval migrans see cutaneous and visceral larva migrans. mosquitoes, with special reference to Anopheles arabiensis (Diptera: Culcidae) in marker-garden wells in urban Dakar, Senegal. J Med Entomol. 1998;35:948-55. (8.) Dossou-Yovo J, Doannio JMC JMC Joint Military Commission JMC Jefferson Medical College JMC Jax Money Crew (computer gaming) JMC Joint Munitions Command (US Army; Rock Island Arsenal, Rock Island IL) JMC James Madison College , Diarrassouba S, Chauvancy G. The impact of rice fields on the transmission of malaria in Bouake, Cote d'lvoire. Bull Soc Pathol Exot. 1998;91:327-33. (9.) United Nations Population Division of the Department of Economic and Social Affairs of the United Nations Secretariat United Nations Secretariat Administrative body that coordinates United Nations activities. Its staff, recruited on the basis of merit, is composed of several thousand permanent professional experts from member states, including translators, clerks, technicians, . World population prospects: The 2002 revision and world urbanization prospects: the 2001 revision.[cited 20 May 2005]. Available from http://esa.un.org/unpp (10.) Keiser J, Utzinger J, Caldas de Castro M, Smith TA, Tanner M, Singer BH. Urbanization in sub-Saharan Africa and implication for malaria control. Am J Trop Med Hyg. 2004;71(Suppl 2):118-27. (11.) Service MW. Mosquito (Diptera: Culicidae) dispersal: the long and short of it. J Med Entomol. 1997:34:579-88. (12.) Gwatkin DR, Rustein S, Johnson K, Pande RP, Wagstaff A. Socioeconomic differences in health, nutrition and population in Ghana. HNP/Poverty Thematic Group Of The World Bank May 2000. [cited 20 May 2005]. Available from http://poverty.worldbank.org/library/ subtopic/4346/ (13.) Sabatinelli G, Bosman A, Lamizana L, Rossi P. Prevalence of malaria in Ouagadougou and the surrounding rural environment during the period of maximal transmission. Parassitologia. 1986:28:17-31. (14.) Chinery WA. Effects of ecological changes on the malaria vectors Anophles funestus and the Anopheles gambiae complex of mosquitoes in Accra, Ghana. J Trop Med Hyg. 1984;87:75-81. (15.) Keating J, Macintyre K, Mbogo CM. Githure JI, Beier JC. Characterization of potential larval habitats for Anopheles mosquitoes in relation to urban land-use in Malindi, Kenya. Int J Health Geogr. 2004:3:9. Eveline Klinkenberg, * ([dagger]) P.J. McCall, * Ian M. Hastings, * Michael D. Wilson, ([double dagger double dagger n. A reference mark (  ) used in printing and writing. Also called diesis.Noun 1. ]) Felix P. Amerasinghe, ([section]) and Martin J. Donnelly * * Liverpool School of Tropical Medicine, Liverpool, United Kingdom; ([double dagger]) International Water Management Institute (West Africa West Africa A region of western Africa between the Sahara Desert and the Gulf of Guinea. It was largely controlled by colonial powers until the 20th century. West African adj. & n. ), Accra, Ghana; ([double dagger]) Noguchi Memorial Institute for Medical Research, Legon, Ghana; and ([section]) International Water Management Institute Headquarters, Colombo, Sri Lanka Sri Lanka (srē läng`kə) [Sinhalese,=resplendent land], formerly Ceylon, ancient Taprobane, officially Democratic Socialist Republic of Sri Lanka, island republic (2005 est. pop. Ms. Klinkenberg is an associate expert in water and health at the International Water Management institute and a doctoral student at the Liverpool School of Tropical Medicine. Her main interest is the interaction between irrigated agriculture and health. Address for correspondence: Martin J. Donnelly, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, United Kingdom; fax: 44-151-705-3369; email: m.j.donnelly@liv.ac.nk |
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