|
 
 |
| ORIGINAL ARTICLE |
|
| Year : 2015 | Volume
: 17
| Issue : 2 | Page : 91-96 |
|
Prevalence of malaria parasitaemia among residents proximal to environmental waste dumpsites in Gwagwalada metropolis, Abuja, Nigeria
Idris Abdullahi Nasir1, Maryam Aliyu Muhammad2, Anthony Uchenna Emeribe3, Adamu Babayo4, Muhammad Sagir Shehu4
1 Department of Medical Microbiology and Parasitology, University of Abuja Teaching Hospital, Abuja, Nigeria
2 Department of Medical Microbiology, Ahmadu Bello University Teaching Hospital, Shika, Zaria, Kaduna State, Nigeria
3 Department of Medical Laboratory Services, University of Abuja Teaching Hospital, Abuja, Nigeria
4 Department of Medical Laboratory Science, College of Medical Sciences, University of Maiduguri, Borno State, Nigeria
| Date of Web Publication | 5-Aug-2015 |
Correspondence Address:
Idris Abdullahi Nasir
Department of Medical Microbiology and Parasitology, University of Abuja Teaching Hospital, PMB 228, Gwagwalada, Abuja
Nigeria
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/2276-7096.161511
Background: Malaria is a widely explored public health topic which has been documented to constitute more burden among communities residing in proximity to environmental waste dumpsites and poor drainage systems.
Objective: This present study sets to examine and compare whether there are more cases of malaria parasitemia burden among people residing proximal and those not proximal to dump sites at Gwagwalada metropolis.
Materials and Methods: This was a cross-sectional comparative survey which involved 100 blood samples collected from 25 households proximal to environmental waste dumpsites (test subjects) and another 100 from 25 households that are not proximal to dumpsites (control subjects) in Gwagwalada metropolis of Federal Capital Territory Abuja. These samples were analyzed using standard malaria microscopy.
Results: Prevalence of malaria parasitemia was 82.0% among test subjects and 26.0% among control subjects. The highest malaria density recorded was >10,000 parasites/μL in 34 test subjects whereas none was observed from control subjects. Malaria parasitemia among test subjects was common among children (1-10 years) and least among 41-50 years. There was statistical relationship between malaria parasitemia among residents proximal to environmental waste dumpsites, more so with their age distribution (P < 0.05) but not with sex distribution (P > 0.05).
Conclusion: The findings of this study are a clear demonstration that accumulation of waste dumpsites in proximity to residential areas constitutes a pathway to malaria burden, consequently dumpsites should be properly located and managed to minimize their effects on the environment and health of man. Keywords: Environmental dumpsites, Gwagwalada, public health, Malaria parasitaemia
How to cite this article:
Nasir IA, Muhammad MA, Emeribe AU, Babayo A, Shehu MS. Prevalence of malaria parasitaemia among residents proximal to environmental waste dumpsites in Gwagwalada metropolis, Abuja, Nigeria. J Med Trop 2015;17:91-6 |
How to cite this URL:
Nasir IA, Muhammad MA, Emeribe AU, Babayo A, Shehu MS. Prevalence of malaria parasitaemia among residents proximal to environmental waste dumpsites in Gwagwalada metropolis, Abuja, Nigeria. J Med Trop [serial online] 2015 [cited 2022 May 17];17:91-6. Available from: https://www.jmedtropics.org/text.asp?2015/17/2/91/161511 |
| Introduction | |  |
Solid waste and drainage systems remained an intractable environmental sanitation problem in Nigeria. [1] This problem has manifested in the form of piles of indiscriminately disposed heaps of uncovered waste and illegal dumpsites along major roads and at street corners in cities and urban areas. This problem is compounded by the rapid urbanization and population growth which has led to the generation of enormous quantities of solid waste which are often discarded by open dumping. [1] These waste dumps may contain a mixture of general waste and toxic, infectious or radioactive wastes and are susceptible to burning and exposure to scavengers. There are a number of major risks and impacts of the dump sites in the environment which include breeding sites for arthropods causing infections and diseases. [2]
Malaria is transmitted by the bite of female mosquitoes of the genus Anopheles. The transmission cycle is only between man and mosquitoes. [3] Man acts as the intermediate host or reservoir and the mosquitoes as the vector. Protozoan parasites of the genus Plasmodium have to undergo complex development and multiplication processes both in man and mosquito before they can be further transmitted. Only the female mosquitoes are of importance for transmission, as they need a blood meal for oviposition. [4]
Malaria covers not only all developing countries, but is present on almost the entire land surface between the latitudes 40°N and 60°S. However, the distribution is not uniform and depends mainly on climate, altitude, population density, and the specific environmental requirements of the mosquitos' species. Highly endemic areas are Sub-Saharan Africa, Central America and the northern part of South America, the Indian subcontinent and Southeast Asia. [4]
In the last two decades, a growing number of malaria cases have been observed. [4] This cannot only be explained by the increasing population, to a large extent, this is also due to the increasing numbers of environmental activities such as irrigation, waste dump sites and drainage schemes or hydro-electric dams. With the introduction of new open water surfaces in the form of canals, ponds and artificial lakes, new mosquito breeding sites have been created. [5]
However, the persistence of the disease is also due to the absence of effective long-lasting vaccines, and the growing resistance of malaria pathogens and mosquitoes to treatment and insecticides, respectively. [3],[5] Furthermore, malaria transmission is not only related to illegal waste dumpsites. Deforestation, mining, road construction and all the negative consequences of rapid, and uncontrolled urbanization are also contributing to the creation of mosquito breeding sites. In this context, urban waste dump sites play two key roles. On the one hand, it is an essential and effective tool for reducing and eliminating mosquito breeding sites by advocating against rampant dumpsites and by eliminating unnecessary scattered and numerous dump sites, these can represent potential breeding sites for various mosquito species if they are permanently flooded and heaped by household disposals. [5]
Solid waste disposal sites are found on the outskirts of the urban areas, turning into the sources of contamination due to the incubation and proliferation of flies, mosquitoes, and rodents; that in turn transmits malaria, cholera, dengue, onchocerciasis and some filariasis that affect population's health. The said situation produces gastrointestinal, dermatological, respiratory, genetic, and several other kinds of infectious diseases such as malaria. Consequently, dumping sites and poor drainages have a very high economic and social cost in the public health services and have not yet been completely estimated by governments, industries, and families. [6]
Apart from proximity to solid waste, other determinants of high susceptibility to malaria include quality of housing, household income, use of anti-mosquitoes measures (e.g., long lasting insecticide treated nets), access to treatment, and rural travel. [7]
Gwagwalada is one of the fast-growing and influential towns in Federal Capital Territory (FCT) of Nigeria. Over the years, the town is threatened by environmental waste dump sites and pollution making the inhabitant vulnerable to health hazards with malaria infections. The situation is likely to be exacerbated by poor economic situation of the inhabitant, poor planning system, high standard of living caused by proximity of the town to the FCT and being the University town of the FCT. Due to poor adherence to proper environmental waste disposal and its health implications on the inhabitants of the town, this study was instigated.
The inappropriate environmental waste disposal and drainage system in Gwagwalada area council has led to the presence of stagnant water bodies which serve as breeding sites for this mosquito vectors and indeed are the agent of malaria transmission.
The increase in numbers of these solid waste dump sites might increase the risk of mosquitos' activities (e.g., laying/hatching so many eggs and night bites); hence making close-by residents much vulnerable to malaria parasitemia. [7]
An estimated 200 million persons in Sub-Sahara Africa live currently in urban centers in malaria endemic areas [7] and 24-103 million clinical attacks occur annually in those areas. [8] In addition, Nigeria has highest malaria prevalence, with about 97% of its estimated 150 million population at risk and about 100 million cases and 300,000 deaths annually. [4],[8] Malaria is endemic in Nigeria as high-intensity transmission occurs all year round, with rates of transmission higher in the wet season than in the dry season, and with more victims in the northern than in the southern part.
A number of studies have investigated the incidence of malaria all over the world. [9],[10],[11],[12] It is estimated that the annual death resulting from this disease is between 1.1 and 2.7 million people out of which over 1 million are children under the age of five in the Sub-Sahara Africa. [13] Much attention was focused on pregnant women and children due to their high vulnerability and exposure to conditions that malaria can cause. There is limited evidence from the results of all these studies to suggest that the breeding and multiplication of mosquitoes on solid waste dumps can lead to increase in the incidence of malaria. [14]
The World Health Organization (WHO) recommends a parasite-based diagnosis of malaria infection. [14] Microscopic examination using Giemsa-stained blood slides for detection of malaria parasites remains, in spite of the availability of the other various methods, the reference standard and it is routinely relied upon as a primary endpoint measurement for patient care, epidemiological studies, operational research, intervention studies, as well as clinical trials. [15] It is the only method that is widely and practically available for quantifying malaria parasite density by comparing the ratio of counted parasites within a given number of microscopic fields, against either counted white blood cells (WBCs) or counted red blood cells (RBCs) within those same fields, and then multiplying that ratio by either the measured or estimated/assumed density of the patient's actual WBCs or RBCs. [15]
This present study examined and compared whether there are more cases of malaria parasitemia burden among people residing proximal to waste dump sites compared to those residing far away or not proximal to dump sites at Gwagwalada metropolis. The outcome of this study might therefore justify the need to encourage periodic surveillance of mosquito activities and their effects on health in the community.
| Materials and Methods | | |
Study Area
This study concentrates on Gwagwalada town of the FCT of Nigeria. The town is about 45 km away from the FCT. It is one of the six area council headquarters of the FCT. The town lies in the downstream of River Usuma and is located between latitude 8°55' and 9°00'N and longitudinal 7°00' and 7°05'E. [16]
The centrality of this town in relation to other area councils' headquarters makes it influential and important in various socio-economic activities. Climate of this town is not farfetched from that of the tropics having several climatic elements in common; most especially the wet and dry season, characteristic. The temperature of the area ranges from 30°C to 37°C yearly, with the highest temperature experienced in the month of March and with mean total rainfall of approximately 1650 mm/annum. About 60% of this rain falls between the months of July to September. The area council is an industrial zone of FCT that stands out as the second most cosmopolitan city of the FCT, after the capital city with 10 political ward and consist of over 26 Federal agencies which includes Sharia court of Appeal, University of Abuja Teaching hospital etc., These have brought about the inflow of people into the council. [16]
Gwagwalada Area Council had an estimated population of over 600,000 people. This comprises original settlers (indigenes) and immigrant population of other Nigerians and foreigners. Gwagwalada town records over 300 households. [16]
Sample Collection
Venous blood samples were collected from four residents from 50 houses residing close to environmental dump sites in Gwagwalada area council, FCT Abuja. The samples were then transported to parasitology unit of medical laboratory department at the university of Abuja teaching hospital for microscopy of stained slides for malaria parasite. A total of 200 blood samples were collected from these residents within the period of May 2013 to August 2013.
Sample Size
The sample size was determined using Hassan, 2012 [17] prevalence rate. This was calculated using Naing's statistical expression. Thus, n = 349. However, due to noncompliance of some residents, we were able to recruit 200 subjects that consented to take part in the study.
Residents Selection Process
The study considered one important measure of exposure to malaria infection, the distance between residences from environmental waste dumpsite. Thus, in the study area, two residential areas were carefully delineated. The first area designated has households located within the range of distance between 100 and 500 m from waste dump sites. While 100 of our subjects reside in this area, the remaining 100 control subjects reside in the second area which was also in the same town but beyond 500 m from waste dump sites, this was considered essentially hygienic zone.
Sample Collection and Storage
Two milliliter of peripheral blood was collected from the residents by vein puncture from any of the cephalic, medial, or basilic veins with a sterile syringe and barrel into a new ethylene diamine tetra acetic acid (EDTA) anticoagulant container. The blood samples were then transported to the laboratory. Upon reaching the laboratory, Thick and thin blood films were made with each of the samples on a clean grease-free slide using the appropriate laboratory number given to each and every individual. The smeared slides were allowed to air dry whilst arranged on slide holders.
Malaria Parasite Microscopy
Procedure
Staining blood smears
One set of smears was stained and the duplicate unstained. The latter will prove useful if a problem occurs during the staining process. Giemsa-staining procedure was used for detect and quantify malaria parasites on thick films.
Staining procedure
To ensure that proper staining results be achieved, a positive smear (malaria) was included with each new batch of working Giemsa-stain. Blood specimens were collected in an EDTA bottle, which has enough parasites so that at least one can be found in every two to three fields. Thick blood smears were stained using 1 in 10 dilution of the Giemsa-stain for 10 min.
Estimation of parasite density
Parasite densities were recorded as a ratio of parasites to WBCs in thick films. Plasmodium parasites were counted against 200 WBC on the thick film. Five hundred WBCs were counted where <9 parasites were counted after counting against 200 WBC.
Parasite densities (parasite/μL of whole blood) were then calculated as follows:
- Number of parasites counted/WBC counted × WBC count μL of participant.
- Furthermore, parasite densities for all participants were calculated using assumed WBC counts of 8.0 × 10 9 /L of blood; all set by WHO (as mentioned above) to be used conveniently in facilities which lack the tools to determine patients' absolute full blood count value. [18]
- The number of parasites seen per field are counted and the density scored as 1000 parasites/μL, 10,000 parasites/μL and 100,000 parasites/μL of whole blood.
Statistical Analysis
Data were analyzed using Statistical Package for Social Science (SPSS Chicago, IL, USA). version 18.0 window based program. Discrete variables were expressed as percentages and proportions were compared using the Chi-square test. Statistical significant difference was considered at value of P < 0.05.
Informed Consent
The purpose of this work was explained to the clients before they voluntarily consented to participate in the research. For the children subjects recruited, their respective parents or guardians consented on their behalf. The consent forms were appropriated filled by the investigators after which each client signed their corresponding forms.
Ethical Approval
Ethical approval for this study was obtained from the ethical and human research committee of the University of Abuja Teaching Hospital before embarking on the research.
| Results | | |
This was a cross-sectional comparative survey which involved 200 blood samples collected from 50 household residents of Gwagwalada metropolis. Hundred from 25 household reside proximal to environmental waste dump sites and serve as the test subjects while another 100 of the subjects from 25 households are those that do not reside proximal to these dump sites and serve as control subjects. 82 (82.0%) of those proximal to dumpsites were positive to the malaria parasite comprising of 60 (80.0%) males and 22 (88.0%l) females. only 26 (26.0%) of those not proximal to dumpsites were malaria parasite positive; this comprises 17 (21.3%) males and 9 females (45.0%). The highest malaria parasite semi-quantitative density recorded from those proximal to dumpsites was >10,000 parasites/μL in 34 individuals whereas the lowest density gotten was ≤1000 parasites/μL in 22 individuals. Malaria parasitemia among those proximal to dumpsites was common among age group of 1-10 years (children) and least among 41-50 years [Table 1], [Table 2] and [Table 3]. | Table 1: Sex distribution of subjects and their corresponding malaria positivity
Click here to view |
 | Table 3: Malaria parasite density distribution across test and control subjects
Click here to view |
Test subjects = those residing proximal to environmental waste dump sites.
Control subjects = those residing in absence or far from environmental waste dump sites.
From the [Table 2], the highest malaria parasite density count recorded was >10,000 parasites/μL (in 34 individuals). This value was recorded among the test subjects and none from the control subjects, P < 0.05. There is statistical relationship between the prevalence of malaria among residents close to environmental waste dump sites when compared with those that don't.
[Table 4] shows the age distribution with respect to the number of subjects positive to malaria parasites. From the table, individuals (children) in the age group 1-10 had the highest incidence of infection, 50 (25.0%). While only 6 (3.00%) individuals in the age range 41-50 had malaria parasite. There was a statistical relationship between the age distribution and malaria infection in this study (P < 0.05). More so, there was a statistical relationship between malaria parasitemia and age groups of the two subjects (P < 0.05). | Table 4: Age distribution of malaria density count across test and control subjects
Click here to view |
| Discussion | | |
Malaria is widely distributed in tropical and subtropical countries and is transmitted by night-biting female mosquitoes of the genus Anopheles. It has been shown that malaria transmission and expansion is encouraged mainly by indiscriminate environmental solid dump sites. [19]
Every household produces a certain amount of waste or refuses daily. If these refuses are thrown outside the house, they encourage the breeding of diseases' vectors like houseflies, mosquitoes, cockroaches, and rats. [19] These vectors spread many infections, thereby affecting the health well-being of the community. This is thus expected as many indiscriminate refuse disposals at varying decomposing stages were observed within Gwawgalada metropolis. Findings from this study showed that 82 (82.0%) of test subject were positive to the malaria parasite and only 26 (26.0%) of the control subjects were malaria parasite positive. This invariably affirms that poor environmental sanitary conditions could be a major risk factor for a high prevalence of mosquito bite and malaria in a community. [20] This is also in agreement with a study done at South Western Nigeria, which shows that incessant dumping of refuse by Ijebu-Ode citizens in different parts of the town is highly unpleasant as this has been a major factor in the prevalence of malaria in Ijebu-Ode as reported by Fasunwon et al. [21]
The findings of the present study support the argument that the relative significance of mosquitoes breeding in the water holding containers found in refuse dump sites is indicative that malaria and other water-borne disease will be prevalent in the area. [22]
The high burden of malaria especially among the most vulnerable groups such as children, and other likely diseases arising from poor management of municipal solid waste should make this sector an obvious priority for the metropolis. [23] This will help to reduce the number of mosquito breeding habitats and increase the time required for vectors to locate oviposition sites. [24] The prevalence and density proportionally decreased with age, this could be attributed to the fact that individuals of these ages have developed immunity against Plasmodium parasite. [25] The low densities of parasitaemia seen in these individuals could be attributed to immunity derived from persistent attacks due to malaria. [25]
Infection prevalence among the males and females showed that out of 75 male residents proximal to waste dumpsites examined, 60 (80.0%) of males were positive for malaria; while out of 25 female residents proximal to waste dump sites examined, 22 (88.0%) were positive for malaria. It appeared that malaria is more prevalent among female residents, but at 5% level of significance, the difference was not statistically significant. This also agrees with the finding of Mbanugo and Ejim, [26] who reported that sex did not affect the prevalence among individuals.
Our results constitute an eloquent testimony that children living in low income and poor neighborhoods are often at greater risk of exposure to environment-based hazards than other age groups. In highly endemic areas, younger children have highest rates of infection, so this could contribute to the observed differences. [27],[28],[29]
These indiscriminate and uncontrolled solid wastes disposal may result in health and other welfare loss. The sanitary state of an area is largely influenced by proper handling of solid waste practices of the residents and the measures in place for safe waste evacuation and disposal. This study is a clear demonstration that accumulation of solid waste in proximity to residential areas constitutes a pathway of many chronic diseases including malaria.
Dump sites should be properly located and managed to minimize its effects on the environment. The government and municipality should revise laws regarding the locations of dump sites. These laws should include properly managed sites, which are well fenced in and away from human settlements. The government should annex laws which see to it that dump sites are located properly and if it is not then action should be taken according to the law.
There is a great need to explore the wastes-malaria paradigm based on recommended safe distances from dump sites or high-risk locations in environmental health studies with the view to developing new strategies for intervention and prevention of this disease.
| Acknowledgments | | |
We will like to acknowledge Dr. Yunusa Thairu and Mr. Bala Samari of Medical Laboratory Department, University of Abuja Teaching Hospital for their technical guide and assistance respectively.
| References | | |
| 1. | Uwakwe V. Solid Waste Management: A Case Study of Eneka, Port Harcourt, Rivers State. Vol. 5. WordPress; 2012. p. 19. Available from: www.wordpress.com. [Last accessed on 2014 Sep 15].  |
| 2. | Rushbrook P. Guidance on Minimum Approaches for Improvements to Existing Municipal Waste Dumpsites. Copenhagen, Denmark: WHO Regional Office; 2001. |
| 3. | Center for Disease Control and Prevention (CDC). Frequently Asked Questions on Malaria; 2013. Available from: http://www.cdc.gov/about/faqs.htm. [Last accessed on 2014 Oct 14]. |
| 4. | |
| 5. | Madramootoo CA, Johnson WR, Willardson LS. Management of Agricultural Drainage Water quality, Rome, Italy: Food and Agriculture Organization of the United Nations; 1997. p. 64-7. |
| 6. | Abul S. Environmental and health impact of solid waste disposal at Mangwaneni dumpsite in Manzini: Swaziland. J Sustain Dev Afr 2010;12:64-78. |
| 7. | Wang SS. Changing Malaria Epidemiology in Four Urban Settings in Sub-Saharan Africa. Phd Thesis, Department of Public Health, University of Basel, Switzerland; 2005. p. 235. |
| 8. | 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;71:118-27. |
| 9. | Gerritsen AA, Kruger P, van der Loeff MF, Grobusch MP. Malaria incidence in Limpopo Province, South Africa, 1998-2007. Malar J 2008;7:162. |
| 10. | Ceesay SJ, Casals-Pascual C, Erskine J, Anya SE, Duah NO, Fulford AJ, et al. Changes in malaria indices between 1999 and 2007 in The Gambia: A retrospective analysis. Lancet 2008;372:1545-54. |
| 11. | Tiono AB, Kaboré Y, Traoré A, Convelbo N, Pagnoni F, Sirima SB. Implementation of Home based management of malaria in children reduces the work load for peripheral health facilities in a rural district of Burkina Faso. Malar J 2008;7:201. |
| 12. | Killeen GF, Smith TA, Ferguson HM, Mshinda H, Abdulla S, Lengeler C, et al. Preventing childhood malaria in Africa by protecting adults from mosquitoes with insecticide-treated nets. PLoS Med 2007;4:e229. |
| 13. | Ikhisemoge T. Health Encyclopedia: Diseases and Conditions; A Seminar on New Trends of Malaria Management in Nigeria, Pharmanews; October, 2006. |
| 14. | World Health Organization. Guidelines for the Treatment of Malaria. Geneva, Switzerland: World Health Organization; 2010. |
| 15. | O′Meara WP, Barcus M, Wongsrichanalai C, Muth S, Maguire JD, Jordan RG, et al. Reader technique as a source of variability in determining malaria parasite density by microscopy. Malar J 2006;5:118. |
| 16. | Balogun O. The Federal Capital Territory of Nigeria: A Geography of Its Development. Ibadan: University of Ibadan Press Limited; 2001. |
| 17. | Hassan AA. Changes of malaria control in peri-urban communities of high endemicity. Resh J Environ Earth Sci 2012;4:844-9. |
| 18. | McKenzie FE, Prudhomme WA, Magill AJ, Forney JR, Permpanich B, Lucas C, et al. White blood cell counts and malaria. J Infect Dis 2005;192:323-30. |
| 19. | Sarojini TR. Refuse Disposal. 3 rd ed. Owerri, Nigeria: AFP Africana First Publishers Ltd.; 2005. p. 1-528. |
| 20. | Okwa OO, Rasheed A, Adeyemi A, Omoyeni M, Oni I. Anopheles species abundances and vectoral competence in six areas of Lagos, Nigeria. J Cell Anim Biol 2007;2:19-23. |
| 21. | Fasunwon BT, Adewoga TO, Adelana OP. Comparative prevalence level of malaria patients reporting to Hospital in Ijebu District of Ogun State. Bull Sci Assoc Niger 2006;27:23-31. |
| 22. | Onyido AE, Ezike VI, Nwankwo EA. Water-borne disease vectors of public health importance: Mosquitoes of Onu-Anyim Agbaja-Izzi in Abakaliki LGA of Ebonyi state Southeastern Nigeria. Proceedings of the 3 rd Society for Occupational Safety and Environmental Health (Soseh). Annual National Conference; 2006. p. 144-7. |
| 23. | Nkwocha EE, Egejuru RO, Pat-Mbano EC, Njoku-Tony RF. Proximity of municipal waste dumpsites to residential neighbourhoods and rate of hospitalization for malaria. Int J Adv Biotechnol Res 2011;2:159-67. |
| 24. | Oguoma VM, Nwaorgu OC, Mbanefo EC, Ikeze OO, Umeh JM. Species composition of Anopheles mosquito in three villages of Uratta Owerri North Local Government Area of Imo State of Nigeria. RIF 2010;1:192-6. |
| 25. | Strüchler D. How much malaria is there worldwide? Parasitol Today 1989;5:39-40. |
| 26. | Mbanugo JI, Ejim DO. Plasmodium Infections in Children Aged 0-5 Years in Awka Metropolis, Anambra State, Nigeria. Niger J Parasitol 2000;21:55-9. |
| 27. | Olayemi IK. Influence of land-use on the fitness of Anopheles gambiae, the principal vector of malaria in Nigeria. Online J Health Allied Sci 2008;7:3-8. |
| 28. | Mabunda S, Aponte JJ, Tiago A, Alonso P. A country-wide malaria survey in Mozambique. II. Malaria attributable proportion of fever and establishment of malaria case definition in children across different epidemiological settings. Malar J 2009;8:74. |
| 29. | De Silva PM, Marshall JM. Factors contributing to urban malaria transmission in sub-saharan Africa: A systematic review. J Trop Med 2012;2012:819563. |
[Table 1], [Table 2], [Table 3], [Table 4]
|
Search Pubmed for