Spatiotemporal clustering of malaria in southern-central Ethiopia: A community-based cohort study
Autoři:
Tarekegn Solomon aff001; Eskindir Loha aff001; Wakgari Deressa aff004; Taye Gari aff001; Bernt Lindtjørn aff002
Působiště autorů:
School of Public Health, College of Medicine and Health Sciences, Hawassa University, Hawassa, Ethiopia
aff001; Centre for International Health, University of Bergen, Bergen, Norway
aff002; Department of Infectious Disease Epidemiology, London School of Hygiene and Tropical Medicine, London, England, United Kingdom
aff003; Department of Preventive Medicine, School of Public Health, College of Health Sciences, Addis Ababa University, Addis Ababa, Ethiopia
aff004
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0222986
Souhrn
Introduction
Understanding the spatiotemporal clustering of malaria transmission would help target interventions in settings of low malaria transmission. The aim of this study was to assess whether malaria infections were clustered in areas with long-lasting insecticidal nets (LLINs) alone, indoor residual spraying (IRS) alone, or a combination of LLINs and IRS interventions, and to determine the risk factors for the observed malaria clustering in southern-central Ethiopia.
Methods
A cohort of 34,548 individuals residing in 6,071 households was followed for 121 weeks, from October 2014 to January 2017. Both active and passive case detection mechanisms were used to identify clinical malaria episodes, and there were no geographic heterogeneity in data collection methods. Using SaTScan software v 9.4.4, a discrete Poisson model was used to identify high rates of spatial, temporal, and spatiotemporal malaria clustering. A multilevel logistic regression model was fitted to identify predictors of spatial malaria clustering.
Results
The overall incidence of malaria was 16.5 per 1,000 person-year observations. Spatial, temporal, and spatiotemporal clustering of malaria was detected in all types of malaria infection (P. falciparum, P. vivax, or mixed). Spatial clustering was identified in all study arms: for LLIN + IRS arm, a most likely cluster size of 169 cases in 305 households [relative risk (RR) = 4.54, P<0.001]; for LLIN alone arm a cluster size of 88 cases in 103 households (RR = 5.58, P<0.001); for IRS alone arm a cluster size of 58 cases in 50 households (RR = 7.15, P<0.001), and for control arm a cluster size of 147 cases in 377 households (RR = 2.78, P<0.001). Living 1 km closer to potential vector breeding sites increased the odds of being in spatial clusters by 41.32 fold (adjusted OR = 41.32, 95% CI = 3.79–138.89).
Conclusions
The risk of malaria infection varied significantly between kebeles, within kebeles, and even among households in areas targeted for different types of malaria control interventions in low malaria transmission setting. The results of this study can be used in planning and implementation of malaria control strategies at micro-geographic scale.
Trial registration
PACT R2014 11000 882128 (8 September 2014).
Klíčová slova:
Ethiopia – Lakes – Malaria – Malarial parasites – Medical risk factors – Plasmodium – Plasmodium falciparum – Plasmodium vivax
Zdroje
1. WHO. World malaria report. Geneva, Switzerland: World Health Organization, 2018.
2. Ethiopian Federal Ministry of Health. An epidemiological profile of malaria in Ethiopia. Addis Ababa, Ethiopia: Public Health Institute, Ministry of Health, 2014.
3. Taffese HS, Hemming-Schroeder E, Koepfli C, Tesfaye G, Lee M-c, Kazura J, et al. Malaria epidemiology and interventions in Ethiopia from 2001 to 2016. Infectious Diseases of Poverty. 2018; 7:103. doi: 10.1186/s40249-018-0487-3 30392470
4. Ghebreyesus TA, Haile M, Witten KH, Getachew A, Yohannes M, Lindsay SW, et al. Household risk factors for malaria among children in the Ethiopian highlands. Trans R Soc Trop Med Hyg. 2000; 94, pp.17–21. doi: 10.1016/s0035-9203(00)90424-3 10748890
5. Woyessa A, Deressa W, Ali A, Lindtjorn B. Prevalence of malaria infection in Butajira area, south-central Ethiopia. Malar J. 2012; 11:84. doi: 10.1186/1475-2875-11-84 22443307
6. Ethiopian Federal Minsitry of Health. National malaria Guidelines. Thrid edition. Addis Ababa, Ethiopia: Federal Minsitry of Health, 2012.
7. WHO, UNICEF. Achieving the malaria MDG target: Reversing the incidence of malaria 2000–2015. Geneva, Switzerland: World Health Organization and the United Nations Children’s Fund, 2015.
8. Deribew A, Dejene T, Kebede B, Tessema GA, Melaku YA, Misganaw A, et al. Incidence, prevalence and mortality rates of malaria in Ethiopia from 1990 to 2015: analysis of the global burden of diseases 2015. Malar J. 2017; 16:271. doi: 10.1186/s12936-017-1919-4 28676108
9. WHO. World malaria report. Geneva, Switzerland: World Health Organization, 2017.
10. Carter R, Mendis KN, Roberts D. Spatial targeting of interventions against malaria. Bull World Health Organ. 2000; 78, pp.1401–1411. 11196487
11. Bousema T, Griffin JT, Sauerwein RW, Smith DL, Churcher TS, Takken W, et al. Hitting hotspots: spatial targeting of malaria for control and elimination. PLoS Med. 2012; 9:e1001165. doi: 10.1371/journal.pmed.1001165 22303287
12. Ostfeld RS, Glass GE, Keesing F. Spatial epidemiology: an emerging (or re-emerging) discipline. Trends Ecol Evol. 2005; 20, pp.328–336. doi: 10.1016/j.tree.2005.03.009 16701389
13. 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; 201:1764–1774. doi: 10.1086/652456 20415536
14. Woolhouse ME, Dye C, Etard JF, Smith T, Charlwood JD, Garnett GP, et al. Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proc Natl Acad Sci U S A. 1997; 94, pp.338–342. doi: 10.1073/pnas.94.1.338 8990210
15. Kitron U. Landscape ecology and epidemiology of vector-borne diseases: tools for spatial analysis. J Med Entomol. 1998; 35, pp.435–445. doi: 10.1093/jmedent/35.4.435 9701925
16. Yeshiwondim AK, Gopal S, Hailemariam AT, Dengela DO, Patel HP. Spatial analysis of malaria incidence at the village level in areas with unstable transmission in Ethiopia. Int J Health Geogr. 2009; 8:5. doi: 10.1186/1476-072X-8-5 19171051
17. Ribeiro JM, Seulu F, Abose T, Kidane G, Teklehaimanot A. Temporal and spatial distribution of anopheline mosquitos in an Ethiopian village: implications for malaria control strategies. Bull World Health Organ. 1996; 74, pp.299–305. 8789928
18. Drakeley C, Schellenberg D, Kihonda J, Sousa CA, Arez AP, Lopes D, et al. An estimation of the entomological inoculation rate for Ifakara: a semi-urban area in a region of intense malaria transmission in Tanzania. Trop Med Int Health. 2003; 8, pp.767–774. doi: 10.1046/j.1365-3156.2003.01100.x 12950662
19. Loha E, Lunde TM, Lindtjorn B. Effect of bednets and indoor residual spraying on spatio-temporal clustering of malaria in a village in south Ethiopia: a longitudinal study. PLoS One 2012; 7:e47354. doi: 10.1371/journal.pone.0047354 23077598
20. Gaudart J, Poudiougou B, Dicko A, Ranque S, Toure O, Sagara I, et al. Space-time clustering of childhood malaria at the household level. a dynamic cohort in a Mali village. BMC Public Health. 2006; 6:286. doi: 10.1186/1471-2458-6-286 17118176
21. Siraj AS, Santos-Vega M, Bouma MJ, Yadeta D, Ruiz Carrascal D, Pascual M. Altitudinal changes in malaria incidence in highlands of Ethiopia and Colombia. Science. 2014; 343, pp.1154–1158. doi: 10.1126/science.1244325 24604201
22. Real LA, Biek R. Spatial dynamics and genetics of infectious diseases on heterogeneous landscapes. J R Soc Interface. 2007; 4, pp.935–948. doi: 10.1098/rsif.2007.1041 17490941
23. Kibret S, Wilson GG, Tekie H, Petros B. Increased malaria transmission around irrigation schemes in Ethiopia and the potential of canal water management for malaria vector control. Malaria J. 2014; 13:360.
24. Degefa T, Zeynudin A, Godesso A, Michael YH, Eba K, Zemene E, et al. Malaria incidence and assessment of entomological indices among resettled communities in Ethiopia: a longitudinal study. Malar J. 2015; 14:24. doi: 10.1186/s12936-014-0532-z 25626598
25. Seyoum D, Yewhalaw D, Duchateau L, Brandt P, Rosas-Aguirre A, Speybroeck N. Household level spatio-temporal analysis of Plasmodium falciparum and Plasmodium vivax malaria in Ethiopia. Parasit Vectors. 2017; 10:196. doi: 10.1186/s13071-017-2124-6 28427451
26. Alemu K, Worku A, Berhane Y. Malaria infection has spatial, temporal, and spatiotemporal heterogeneity in unstable malaria transmission areas in northwest Ethiopia. PLoS One. 2013; 8:e79966. doi: 10.1371/journal.pone.0079966 24223209
27. Loha E, Deressa W, Gari T, Balkew M, Kenea O, Solomon T, et al. Long-lasting insecticidal nets and indoor residual spraying may not be sufficient to eliminate malaria in a low malaria incidence area: results from a cluster randomized controlled trial in Ethiopia. Malar J. 2019; 18:141. doi: 10.1186/s12936-019-2775-1 30999957
28. Deressa W, Loha E, Balkew M, Hailu A, Gari T, Kenea O, et al. Combining long-lasting insecticidal nets and indoor residual spraying for malaria prevention in Ethiopia: study protocol for a cluster randomized controlled trial. Trials. 2016; 17:20. doi: 10.1186/s13063-016-1154-2 26758744
29. Ethiopian National Meteorology Agency. Adami Tullu and Zeway Town annual meteorology data. Ethiopia Meteorology Agency, Hawassa Branch, 2016 (Unpublished).
30. Federal Democratic Republic of Ethiopia. Summary and statistical report of the 2007 population and housing census. In: Population Census Commission, Editor. Addis Ababa: UNFPA, 2008.
31. Mengesha T, Nigatu W, Ghiorgis W, Eshete H, Balcha F, Ishii A, et al. The 1991 malaria epidemic in Ethiopia, with reference to the outbreak in central Ethiopia. Ethiop J Health Dev 1998, 12, pp.111–114.
32. Kibret S, Alemu Y, Boelee E, Tekie H, Alemu D, Petros B. The impact of a small-scale irrigation scheme on malaria transmission in Ziway area, Central Ethiopia. Tropical Medicine and International Health. 2010; 15, pp.41–50. doi: 10.1111/j.1365-3156.2009.02423.x 19917039
33. Bekele D, Belyhun Y, Petros B, Deressa W. Assessment of the effect of insecticide-treated nets and indoor residual spraying for malaria control in three rural kebeles of Adami Tulu District, South Central Ethiopia. Malar J. 2012; 11:127. doi: 10.1186/1475-2875-11-127 22533789
34. Gari T, Kenea O, Loha E, Deressa W, Hailu A, Balkew M, et al. Malaria incidence and entomological findings in an area targeted for a cluster-randomized controlled trial to prevent malaria in Ethiopia: results from a pilot study. Malar J. 2016; 15:145. doi: 10.1186/s12936-016-1199-4 26957044
35. International Federation of Red Cross Ethiopia. Drought-Emergency plan of action operations update number 3 (MDRET0016). International Federation of Red Cross and Red Crescent Societies, 2015. Available: http://reliefweb.int/report/ethiopia/mdret0016. Accessed 28 Jan 2016.
36. Kulldorff M. SaTScan User Guide for version 9.4; 2015. Available: http://www.satscan.org/.
37. Tobler W. A computer movie simulating urban growth in the Detroit region. Econ Geogr.1970; 46, pp.234–240.
38. Loha E, Lindtjorn B. Predictors of Plasmodium falciparum Malaria Incidence in Chano Mille, South Ethiopia: A Longitudinal Study. Am J Trop Med Hyg. 2012; 87(3), pp. 450–459. doi: 10.4269/ajtmh.2012.12-0155 22826493
39. Roberts D, Matthews G. Risk factors of malaria in children under the age of five years old in Uganda. Malar J. 2016; 15:246. doi: 10.1186/s12936-016-1290-x 27121122
40. Coleman M, Coleman M, Mabaso MLH, Mabuza AM, Kok G, Coetzee M, et al. Household and microeconomic factors associated with malaria in Mpumalanga, South Africa. Trans R Soc Trop Med Hyg. 2010;104, pp.143–147. doi: 10.1016/j.trstmh.2009.07.010 19732924
41. Vyas S, Kumaranayake L. Constructing socio-economic status indices: how to use principal components analysis. Health Policy Plan 2006, 21, pp.459–468. doi: 10.1093/heapol/czl029 17030551
42. Howe LD, Hargreaves JR, Huttly SR. Issues in the construction of wealth indices for the measurement of socio-economic position in low-income countries. Emerg Themes Epidemiol. 2008; 5:3. doi: 10.1186/1742-7622-5-3 18234082
43. Alemu K, Worku A, Berhane Y, Kumie A. Spatiotemporal clusters of malaria cases at village level, northwest Ethiopia. Malar J. 2014; 13:223. doi: 10.1186/1475-2875-13-223 24903061
44. Kenea O, Balkew M, Tekie H, Gebre-Michael T, Deressa W, Loha E, et al. Human-biting activities of Anopheles species in south-central Ethiopia. Parasit Vectors. 2016; 9:527. doi: 10.1186/s13071-016-1813-x 27716416
45. Sherrard-Smith E, Skarp JE, Beale AD, Fornadel C, Norris LC, Moore SJ, et al. Mosquito feeding behavior and how it influences residual malaria transmission across Africa. PNAS. 2019; 116, pp.15086–15095. doi: 10.1073/pnas.1820646116 31285346
46. Noden BH, Kent MD, Beier JC. The impact of variations in temperature on early Plasmodium falciparum development in Anopheles stephensi. Parasitology. 1995; 111, pp.539–545. doi: 10.1017/s0031182000077003 8559585
47. Ifatimehin OO, Falola OO, Odogbo EV. An analysis of the spatial distribution of Plasmodium sporozoites and effects of climatic correlates on malaria infection in Anyigba town, Nigeria. Glob J Health Sci. 2013; 6, pp.115–126. doi: 10.5539/gjhs.v6n1p115 24373271
48. Peterson I, Borrell LN, El-Sadr W, Teklehaimanot A. A temporal-spatial analysis of malaria transmission in Adama, Ethiopia. Am J Trop Med Hyg. 2009; 81, pp.944–949. doi: 10.4269/ajtmh.2009.08-0662 19996421
49. Teklehaimanot HD, Lipsitch M, Teklehaimanot A, Schwartz J. Weather-based prediction of Plasmodium falciparum malaria in epidemic-prone regions of Ethiopia I. Patterns of lagged weather effects reflect biological mechanisms. Malar J. 2004; 3:41. doi: 10.1186/1475-2875-3-41 15541174
50. Kenea O, Balkew M, Gebre-Michael T. Environmental factors associated with larval habitats of anopheline mosquitoes (Diptera: Culicidae) in irrigation and major drainage areas in the middle course of the Rift Valley, central Ethiopia. J Vector Borne Dis. 2011; 48, pp.85–92. 21715730
51. Staedke SG, Nottingham EW, Cox J, Kamya MR, Rosenthal PJ, Dorsey G. Short report: proximity to mosquito breeding sites as a risk factor for clinical malaria episodes in an urban cohort of Ugandan children. Am J Trop Med Hyg. 2003; 69, pp.244–246. 14628938
52. Alemu A, Tsegaye W, Golassa L, Abebe G. Urban malaria and associated risk factors in Jimma town, south-west Ethiopia. Malar J. 2011; 10:173. doi: 10.1186/1475-2875-10-173 21699741
53. Nissen A, Cook J, Loha E, Lindtjorn B. Proximity to vector breeding site and risk of Plasmodium vivax infection: a prospective cohort study in rural Ethiopia. Malar J. 2017; 16:380. doi: 10.1186/s12936-017-2031-5 28927422
54. Clark TD, Greenhouse B, Njama-Meya D, Nzarubara B, Maiteki-Sebuguzi C, Staedke SG, et al. Factors determining the heterogeneity of malaria incidence in children in Kampala, Uganda. J Infect Dis 2008; 198, pp.393–400. doi: 10.1086/589778 18522503
55. Ethiopian Federal Ministry of Health. National Strategic Plan for Malaria Prevention, Control and Elimination in Ethiopia: 2014–2020. Addis Ababa, Ethiopia: Federal Ministry of Health, 2014.
56. Doda Z, Solomon T, Loha E, Gari T, Lindtjørn B. A qualitative study of use of long-lasting insecticidal nets (LLINs) for intended and unintended purposes in Adami Tullu, East Shewa Zone, Ethiopia. Malaria J. 2018; 17:69.
57. Solomon T, Loha E, Deressa W, Balkew M, Gari T, Overgaard HJ, et al. Bed nets used to protect against malaria do not last long in a semi-arid area of Ethiopia: a cohort study. Malar J. 2018; 17:239. doi: 10.1186/s12936-018-2391-5 29925371
58. Solomon T, Loha E, Deressa W, Gari T, Overgaard HJ, Lindtjorn B. Low use of long-lasting insecticidal nets for malaria prevention in south-central Ethiopia: A community-based cohort study. PLoS One. 2019; 14:e0210578. doi: 10.1371/journal.pone.0210578 30629675
59. Ranadive N, Kunene S, Darteh S, Ntshalintshali N, Nhlabathi N, Dlamini N, et al: Limitations of Rapid Diagnostic Testing in Patients with Suspected Malaria: A Diagnostic Accuracy Evaluation from Swaziland, a Low-Endemicity Country Aiming for Malaria Elimination. Clinical Infectious Diseases. 2017; 64, pp.1221–1227. doi: 10.1093/cid/cix131 28369268
60. Mahende C, Ngasala B, Lusingu J, Yong T-S, Lushino P, Lemnge M, et al.Performance of rapid diagnostic test, blood-film microscopy and PCR for the diagnosis of malaria infection among febrile children from Korogwe District, Tanzania. Malar J. 2016; 15:391. doi: 10.1186/s12936-016-1450-z 27459856
61. Okell LC, Ghani AC, Lyons E, Drakeley CJ. Submicroscopic infection in Plasmodium falciparum-endemic populations: a systematic review and meta-analysis. J Infect Dis. 2009; 200, pp.1509–1517. doi: 10.1086/644781 19848588
62. Okell LC, Bousema T, Griffin JT, Ouedraogo AL, Ghani AC, Drakeley CJ. Factors determining the occurrence of submicroscopic malaria infections and their relevance for control. Nat Commun. 2012; 3:1237. doi: 10.1038/ncomms2241 23212366
63. Mogeni P, Williams TN, Omedo I, Kimani D, Ngoi JM, Mwacharo J, et al. Detecting Malaria Hotspots: A Comparison of Rapid Diagnostic Test, Microscopy, and Polymerase Chain Reaction. J Infect Dis. 2017; 216, pp.1091–1098. doi: 10.1093/infdis/jix321 28973672
64. Diaz PB, Lozano PM, Rincon JM, Garcia L, Reyes F, Llanes AB. Quality of malaria diagnosis and molecular confirmation of Plasmodium ovale curtisi in a rural area of the southeastern region of Ethiopia. Malar J. 2015; 14:357. doi: 10.1186/s12936-015-0893-y 26383920
Článek vyšel v časopise
PLOS One
2019 Číslo 9
- Tisícileté topoly, mokří psi, stárnoucí kočky a ospalé octomilky – „jednohubky“ z výzkumu 2024/41
- Jaké jsou aktuální trendy v léčbě karcinomu slinivky?
- Menstruační krev má značný diagnostický potenciál, mimo jiné u diabetu
- Proč jsou nemocnice nepřítelem spánku? A jak to změnit?
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?