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-
1
Greenwood B, Marsh K, Snow R, 1991. Why do some African children develop severe malaria? Parasitol Today 7 :277–281.
-
2
Snow R, Marsh K, 2002. The consequences of reducing transmission of Plasmodium falciparum in Africa. Adv Parasitol 52 :235–264.
-
3
Trape JF, Rogier C, 1996. Combating malaria morbidity and mortality by reducing transmission. Parasitol Today 12 :236–240.
-
4
Snow R, Omumbo J, Lowe B, Molyneux CS, Obiero JO, Palmer A, Weber MW, Pinder M, Nahlen B, Obonyo C, Newbold C, Gupta S, Marsh K, 1997. Relation between severe malaria morbidity in children and level of Plasmodium falciparum transmission in Africa. Lancet 349 :1650–1654.
-
5
Smith T, Leuenberger R, Lengeler C, 2001. Child mortality and malaria transmission intensity in Africa. Trends Parasitol 17 :145–149.
-
6
Marsh K, Snow R, 1999. Malaria transmission and morbidity. Parassitologia 41 :241–246.
-
7
Reyburn H, Drakeley C, Carneiro I, Jones C, Cox J, Bruce J, Riley E, Greenwood B, Whitty C, 2004. The epidemiology of severe malaria due to Plasmodium falciparum at different transmission intensities in NE Tanzania. LSHTM Malaria Centre Report 2002–2003: 6–7.
-
8
Todd J, de Francisco A, O’Dempsey TJ, Greenwood BM, 1994. The limitations of verbal autopsy in a malaria-endemic region. Ann Trop Paediatr 14 :31–36.
-
9
Quigley MA, Armstrong-Schellenberg JR, Snow R, 1996. Algorithms for verbal autopsies: a validation study in Kenyan children. Bull World Health Organ 74 :147–154.
-
10
Ezzati M, Vander Hoorn S, Rodgers A, Lopez A, Mathers C, Murray C, the Comparative Risk Assessment Collaborating Group, 2003. Estimates of global and regional potential health gains from reducing multiple major risk factors. Lancet 362 :271–280.
-
11
Berkley J, Mwarumba S, Bramham K, Lowe B, Marsh K, 1999. Bacteraemia complicating severe malaria in children. Trans R Soc Trop Med Hyg 93 :283–286.
-
12
Molineaux L, 1997. Nature’s experiment: what implications for malaria prevention? Lancet 349 :1636–1637.
-
13
Snow RW, Korenromp EL, Gouws E, 2004. Pediatric mortality in Africa: Plasmodium falciparum malaria as a cause or risk? Am J Trop Med Hyg 71 :16–24.
-
14
Molineaux L, 1997. Malaria and mortality: some epidemiological considerations. Ann Trop Med Parasitol 91 :811–825.
-
15
Giglioli G, 1972. Changes in the pattern of mortality following the eradication of hyperendemic malaria from a highly susceptible community. Bull World Health Org 46 :181–202.
-
16
Molineaux L, 1985. The impact of parasitic diseases and their control, with an emphasis on malaria and Africa. Vallin J., Lopez A, eds. Health Policy, Social Policy and Mortality Prospects. Liege, Belgium: Ordina, 13–44.
-
17
Newman P, 1977. Malaria and mortality. J Am Stat Assoc 72 :257–263.
-
18
Bradley DJ, 1991. Morbidity and mortality at Pare-Taveta, Kenya and Tanzania, 1954–66: the effects of a period of malaria control. Feachem RG, Jamison DT, eds. Disease and Mortality in Sub-Saharan Africa. Washington, DC: World Bank.
-
19
Alonso PL, Lindsay SW, Armstrong-Schellenberg JR, Conteh M, Hill AG, David PH, Fegan G, de Francisco A, Hall AJ, Shenton F, 1991. The effect of insecticide-treated bed nets on mortality of Gambian children. Lancet 337 :1499–1502.
-
20
Molineaux L, Gramiccia G, 1980. The Garki Project. Geneva: World Health Organization.
-
21
Williams TN, Mwangi TW, Wambua S, Alexander N, Kortok M, Snow RW, Marsh K, 2005. Sickle cell trait and the risk of Plasmodium falciparum malaria and other childhood diseases. J Infect Dis 192 :178–186.
-
22
Smith T, Killeen G, Maire N, Ross A, Molineaux L, Tediosi F, Hutton G, Utzinger J, Dietz K, Tanner M, 2006. Mathematical modeling of the impact of malaria vaccines on the clinical epidemiology and natural history of Plasmodium falciparum malaria: overview. Am J Trop Med Hyg 75 (Suppl 2):1–10.
-
23
Smith T, Ross A, Maire N, Rogier C, Trape JF, Molineaux L, 2006. An epidemiologic model of the incidence of acute illness in Plasmodium falciparum malaria. Am J Trop Med Hyg 75 (Suppl 2):56–62.
-
24
Ross A, Smith T, 2006. The effect of malaria transmission intensity on neonatal mortality in endemic areas. Am J Trop Med Hyg 75 (Suppl 2):74–81.
-
25
Maire N, Smith T, Ross A, Owusu-Agyei S, Dietz K, Molineaux L, 2006. A model for natural immunity to asexual blood stages of Plasmodium falciparum in endemic areas. Am J Trop Med Hyg 75 (Suppl 2):19–31.
-
26
Kirkpatrick S, Gelatt CD Jr, Vecchi MP, 1983. Optimization by simulated annealing. Science 220 :671–680.
-
27
Press WH, Flannery BP, Teukolsky SA, Vetterling WT, 1988. Numerical recipes in C: The art of scientific computing. Cambridge, United Kingdom: Cambridge University Press.
-
28
Korenromp EL, Williams BG, Gouws E, Dye C, Snow R, 2003. Measurement of trends in childhood malaria mortality in Africa: an assessment of progress toward targets based on verbal autopsy. Lancet Infect Dis 3 :349–358.
-
29
Snow R, Craig M, Newton C, Steketee RW, 2003. The Public Health Burden of Plasmodium falciparum Malaria in Africa: Deriving the Numbers. Bethesda, MD: Fogarty International Center, National Institutes of Health.
-
30
INDEPTH Network, 2002. Population, Health and Survival at INDEPTH Sites. Ottawa, Ontario, Canada: International Development Research Centre.
-
31
Dietz K, Raddatz G, Molineaux L, 2006. A mathematical model of the first wave of Plasmodium falciparum asexual parasitemia in non-immune and vaccinated individuals. Am J Trop Med Hyg 75 (Suppl 2):46–55.
-
32
Snow R, Bastos de Azevedo I, Lowe B, Kabiru EW, Nevill C, Mwankusye S, Kassiga G, Marsh K, Teuscher T, 1994. Severe childhood malaria in two areas of markedly different falciparum transmission in East Africa. Acta Trop 57 :289–300.
-
33
Macintosh CL, Beeson JG, Marsh K, 2004. Clinical features and pathogenesis of severe malaria. Trends Parasitol 20 :597–603.
-
34
Reyburn H, Mbatia R, Drakeley C, Carneiro I, Mwakasungula E, Mwerinde O, Saganda K, Shao J, Kitua A, Olomi R, Greenwood BM, Whitty CJ, 2004. Overdiagnosis of malaria in patients with severe febrile illness in Tanzania: a prospective study. BMJ 329 :1212.
-
35
Makani J, Matuja W, Liyombo E, Snow R, Marsh K, Warrell DA, 2003. Admission diagnosis of cerebral malaria in adults in an endemic area of Tanzania: implications and clinical description. QJM 96 :355–362.
-
36
Binka F, Hodgson A, Adjuik M, Smith T, 2002. Mortality in a seven-and-a-half-year follow-up of a trial of insecticide-treated mosquito nets in Ghana. Trans R Soc Trop Med Hyg 96 :597–599.
-
37
Brown V, Abdir IM, Rossi M, Barboza P, Paugam A, 1998. Epidemic of malaria in north-eastern Kenya. Lancet 352 :1356–1357.
-
38
Ceita JGV, Buck AA, 1986. Malaria in São Tomé and Principe. Washington, DC: American Institute of Biological Sciences.
-
39
Smith T, Genton B, Betuela I, Rare L, Alpers MP, 2002. Mosquito nets for the elderly? Trans R Soc Trop Med Hyg 96 :37–38.
-
40
de Savigny D, Mayombana C, Mwageni E, Masanja H, Minhaj A, Mkilindi Y, Mbuya C, Kasale H, Reid G, 2004. Care-seeking patterns for fatal malaria in Tanzania. Malar J 3 :27.
-
41
Tediosi F, Maire N, Smith T, Hutton G, Utzinger J, Ross A, Tanner M, 2006. An approach to model the costs and effects of case management of Plasmodium falciparum malaria in sub-Saharan Africa. Am J Trop Med Hyg 75 (Suppl 2):90–103.
-
42
Lengeler C, Cattani J, de Savigny D, 1996. Net Gain, a new method for preventing malaria deaths. Geneva: International Development Research Centre/World Health Organization.
-
43
Schellenberg D, Menendez C, Kahigwa E, Aponte J, Vidal J, Tanner M, Mshinda H, Alonso PL, 2001. Intermittent treatment for malaria and anaemia control at time of routine vaccinations in Tanzanian infants: a randomised, placebo-controlled trial. Lancet 357 :1471–1477.
-
44
Graves P, Gelband H, 2003. Vaccines for preventing malaria. Cochrane Database Syst Rev: CD000129
-
45
Goodman CA, Coleman PG, Mills A, 2000. Economic analysis of malaria control in sub-Saharan Africa. Geneva: Global Forum for Health Research.
-
46
Snow RW, Mung’ala VO, Foster D, Marsh K, 1994. The role of the district hospital in child survival at the Kenyan Coast. Afr J Health Sci 1 :71–75.
-
47
Smith T, Charlwood JD, Kihonda J, Mwankusye S, Billingsley P, Meuwissen J, Lyimo E, Takken W, Teuscher T, Tanner M, 1993. Absence of seasonal variation in malaria parasitaemia in an area of intense seasonal transmission. Acta Trop 54 :55–72.
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Cuzin-Ouattara N, van den Broek AH, Habluetzel A, Diabate A, Sanogo-Ilboudo E, Diallo DA, Cousens SN, Esposito F, 1999. Wide-scale installation of insecticide-treated curtains confers high levels of protection against malaria transmission in a hyperendemic area of Burkina Faso. Trans R Soc Trop Med Hyg 93 :473–479.
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Ilboudo-Sanogo E, Cuzin-Ouattara N, Diallo DA, Cousens SN, Esposito F, Habluetzel A, Sanon S, Ouedraogo AP, 2001. Insecticide-treated materials, mosquito adaptation and mass effect: entomological observations after five years of vector control in Burkina Faso. Trans R Soc Trop Med Hyg 95 :353–360.
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Robert V, Gazin P, Boudin C, Molez JF, Ouedraogo V, Carnevale P, 1985. The transmission of malaria in a wooded savannah area and a rice-growing area around Bobo Dioulasso (Burkina Faso). Ann Soc Belg Med Trop 65 (Suppl 2):201–214.
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Modiano D, Petrarca V, Sirima BS, Nebie I, Diallo D, Esposito F, Coluzzi M, 1996. Different response to Plasmodium falciparum malaria in west African sympatric ethnic groups: possible implications for control strategies. Proc Natl Acad Sci USA 93 :13206–13211.
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Mbogo CN, Snow R, Kabiru EW, Ouma J, Githure JI, Marsh K, Beier JC, 1993. Low-level Plasmodium falciparum transmission and the incidence of severe malaria infections on the Kenyan coast. Am J Trop Med Hyg 49 :245–253.
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Beier JC, Oster CN, Onyango FK, Bales JD, Sherwood JA, Perkins PV, Chumo DK, Koech DV, Whitmire RE, Roberts CR, 1994. Plasmodium falciparum incidence relative to entomologic inoculation rates at a site proposed for testing malaria vaccines in western Kenya. Am J Trop Med Hyg 50 :529–536.
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AN EPIDEMIOLOGIC MODEL OF SEVERE MORBIDITY AND MORTALITY CAUSED BY PLASMODIUM FALCIPARUM
AMANDA ROSS
AMANDA ROSS
Swiss Tropical Institute, Basel, Switzerland; World Health Organization, Geneva, Switzerland
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NICOLAS MAIRE
NICOLAS MAIRE
Swiss Tropical Institute, Basel, Switzerland; World Health Organization, Geneva, Switzerland
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LOUIS MOLINEAUX
LOUIS MOLINEAUX
Swiss Tropical Institute, Basel, Switzerland; World Health Organization, Geneva, Switzerland
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THOMAS SMITH
THOMAS SMITH
Swiss Tropical Institute, Basel, Switzerland; World Health Organization, Geneva, Switzerland
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The intensity of Plasmodium falciparum transmission has multifarious and sometimes counter-intuitive effects on age-specific rates of severe morbidity and mortality in endemic areas. This has led to conflicting speculations about the likely impact of malaria control interventions. We propose a quantitative framework to reconcile the various apparently contradictory observations relating morbidity and mortality rates to malaria transmission. Our model considers two sub-categories of severe malaria episodes. These comprise episodes with extremely high parasite densities in hosts with little previous exposure, and acute malaria episodes accompanied by co-morbidity or other risk factors enhancing susceptibility. In addition to direct malaria mortality from severe malaria episodes, the model also considers the enhanced risk of indirect mortality following acute episodes accompanied by co-morbidity after the parasites have been cleared. We fit this model to summaries of field data from endemic areas of Africa, and show that it can account for the observed age- and exposure-specific patterns of pediatric severe malaria and malaria-associated mortality in children. This model will allow us to make predictions of the long-term impact of potential malaria interventions. Predictions for children will be more reliable than those for older people because there is a paucity of epidemiologic studies of adults and adolescents.
Author Notes
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1
Greenwood B, Marsh K, Snow R, 1991. Why do some African children develop severe malaria? Parasitol Today 7 :277–281.
-
2
Snow R, Marsh K, 2002. The consequences of reducing transmission of Plasmodium falciparum in Africa. Adv Parasitol 52 :235–264.
-
3
Trape JF, Rogier C, 1996. Combating malaria morbidity and mortality by reducing transmission. Parasitol Today 12 :236–240.
-
4
Snow R, Omumbo J, Lowe B, Molyneux CS, Obiero JO, Palmer A, Weber MW, Pinder M, Nahlen B, Obonyo C, Newbold C, Gupta S, Marsh K, 1997. Relation between severe malaria morbidity in children and level of Plasmodium falciparum transmission in Africa. Lancet 349 :1650–1654.
-
5
Smith T, Leuenberger R, Lengeler C, 2001. Child mortality and malaria transmission intensity in Africa. Trends Parasitol 17 :145–149.
-
6
Marsh K, Snow R, 1999. Malaria transmission and morbidity. Parassitologia 41 :241–246.
-
7
Reyburn H, Drakeley C, Carneiro I, Jones C, Cox J, Bruce J, Riley E, Greenwood B, Whitty C, 2004. The epidemiology of severe malaria due to Plasmodium falciparum at different transmission intensities in NE Tanzania. LSHTM Malaria Centre Report 2002–2003: 6–7.
-
8
Todd J, de Francisco A, O’Dempsey TJ, Greenwood BM, 1994. The limitations of verbal autopsy in a malaria-endemic region. Ann Trop Paediatr 14 :31–36.
-
9
Quigley MA, Armstrong-Schellenberg JR, Snow R, 1996. Algorithms for verbal autopsies: a validation study in Kenyan children. Bull World Health Organ 74 :147–154.
-
10
Ezzati M, Vander Hoorn S, Rodgers A, Lopez A, Mathers C, Murray C, the Comparative Risk Assessment Collaborating Group, 2003. Estimates of global and regional potential health gains from reducing multiple major risk factors. Lancet 362 :271–280.
-
11
Berkley J, Mwarumba S, Bramham K, Lowe B, Marsh K, 1999. Bacteraemia complicating severe malaria in children. Trans R Soc Trop Med Hyg 93 :283–286.
-
12
Molineaux L, 1997. Nature’s experiment: what implications for malaria prevention? Lancet 349 :1636–1637.
-
13
Snow RW, Korenromp EL, Gouws E, 2004. Pediatric mortality in Africa: Plasmodium falciparum malaria as a cause or risk? Am J Trop Med Hyg 71 :16–24.
-
14
Molineaux L, 1997. Malaria and mortality: some epidemiological considerations. Ann Trop Med Parasitol 91 :811–825.
-
15
Giglioli G, 1972. Changes in the pattern of mortality following the eradication of hyperendemic malaria from a highly susceptible community. Bull World Health Org 46 :181–202.
-
16
Molineaux L, 1985. The impact of parasitic diseases and their control, with an emphasis on malaria and Africa. Vallin J., Lopez A, eds. Health Policy, Social Policy and Mortality Prospects. Liege, Belgium: Ordina, 13–44.
-
17
Newman P, 1977. Malaria and mortality. J Am Stat Assoc 72 :257–263.
-
18
Bradley DJ, 1991. Morbidity and mortality at Pare-Taveta, Kenya and Tanzania, 1954–66: the effects of a period of malaria control. Feachem RG, Jamison DT, eds. Disease and Mortality in Sub-Saharan Africa. Washington, DC: World Bank.
-
19
Alonso PL, Lindsay SW, Armstrong-Schellenberg JR, Conteh M, Hill AG, David PH, Fegan G, de Francisco A, Hall AJ, Shenton F, 1991. The effect of insecticide-treated bed nets on mortality of Gambian children. Lancet 337 :1499–1502.
-
20
Molineaux L, Gramiccia G, 1980. The Garki Project. Geneva: World Health Organization.
-
21
Williams TN, Mwangi TW, Wambua S, Alexander N, Kortok M, Snow RW, Marsh K, 2005. Sickle cell trait and the risk of Plasmodium falciparum malaria and other childhood diseases. J Infect Dis 192 :178–186.
-
22
Smith T, Killeen G, Maire N, Ross A, Molineaux L, Tediosi F, Hutton G, Utzinger J, Dietz K, Tanner M, 2006. Mathematical modeling of the impact of malaria vaccines on the clinical epidemiology and natural history of Plasmodium falciparum malaria: overview. Am J Trop Med Hyg 75 (Suppl 2):1–10.
-
23
Smith T, Ross A, Maire N, Rogier C, Trape JF, Molineaux L, 2006. An epidemiologic model of the incidence of acute illness in Plasmodium falciparum malaria. Am J Trop Med Hyg 75 (Suppl 2):56–62.
-
24
Ross A, Smith T, 2006. The effect of malaria transmission intensity on neonatal mortality in endemic areas. Am J Trop Med Hyg 75 (Suppl 2):74–81.
-
25
Maire N, Smith T, Ross A, Owusu-Agyei S, Dietz K, Molineaux L, 2006. A model for natural immunity to asexual blood stages of Plasmodium falciparum in endemic areas. Am J Trop Med Hyg 75 (Suppl 2):19–31.
-
26
Kirkpatrick S, Gelatt CD Jr, Vecchi MP, 1983. Optimization by simulated annealing. Science 220 :671–680.
-
27
Press WH, Flannery BP, Teukolsky SA, Vetterling WT, 1988. Numerical recipes in C: The art of scientific computing. Cambridge, United Kingdom: Cambridge University Press.
-
28
Korenromp EL, Williams BG, Gouws E, Dye C, Snow R, 2003. Measurement of trends in childhood malaria mortality in Africa: an assessment of progress toward targets based on verbal autopsy. Lancet Infect Dis 3 :349–358.
-
29
Snow R, Craig M, Newton C, Steketee RW, 2003. The Public Health Burden of Plasmodium falciparum Malaria in Africa: Deriving the Numbers. Bethesda, MD: Fogarty International Center, National Institutes of Health.
-
30
INDEPTH Network, 2002. Population, Health and Survival at INDEPTH Sites. Ottawa, Ontario, Canada: International Development Research Centre.
-
31
Dietz K, Raddatz G, Molineaux L, 2006. A mathematical model of the first wave of Plasmodium falciparum asexual parasitemia in non-immune and vaccinated individuals. Am J Trop Med Hyg 75 (Suppl 2):46–55.
-
32
Snow R, Bastos de Azevedo I, Lowe B, Kabiru EW, Nevill C, Mwankusye S, Kassiga G, Marsh K, Teuscher T, 1994. Severe childhood malaria in two areas of markedly different falciparum transmission in East Africa. Acta Trop 57 :289–300.
-
33
Macintosh CL, Beeson JG, Marsh K, 2004. Clinical features and pathogenesis of severe malaria. Trends Parasitol 20 :597–603.
-
34
Reyburn H, Mbatia R, Drakeley C, Carneiro I, Mwakasungula E, Mwerinde O, Saganda K, Shao J, Kitua A, Olomi R, Greenwood BM, Whitty CJ, 2004. Overdiagnosis of malaria in patients with severe febrile illness in Tanzania: a prospective study. BMJ 329 :1212.
-
35
Makani J, Matuja W, Liyombo E, Snow R, Marsh K, Warrell DA, 2003. Admission diagnosis of cerebral malaria in adults in an endemic area of Tanzania: implications and clinical description. QJM 96 :355–362.
-
36
Binka F, Hodgson A, Adjuik M, Smith T, 2002. Mortality in a seven-and-a-half-year follow-up of a trial of insecticide-treated mosquito nets in Ghana. Trans R Soc Trop Med Hyg 96 :597–599.
-
37
Brown V, Abdir IM, Rossi M, Barboza P, Paugam A, 1998. Epidemic of malaria in north-eastern Kenya. Lancet 352 :1356–1357.
-
38
Ceita JGV, Buck AA, 1986. Malaria in São Tomé and Principe. Washington, DC: American Institute of Biological Sciences.
-
39
Smith T, Genton B, Betuela I, Rare L, Alpers MP, 2002. Mosquito nets for the elderly? Trans R Soc Trop Med Hyg 96 :37–38.
-
40
de Savigny D, Mayombana C, Mwageni E, Masanja H, Minhaj A, Mkilindi Y, Mbuya C, Kasale H, Reid G, 2004. Care-seeking patterns for fatal malaria in Tanzania. Malar J 3 :27.
-
41
Tediosi F, Maire N, Smith T, Hutton G, Utzinger J, Ross A, Tanner M, 2006. An approach to model the costs and effects of case management of Plasmodium falciparum malaria in sub-Saharan Africa. Am J Trop Med Hyg 75 (Suppl 2):90–103.
-
42
Lengeler C, Cattani J, de Savigny D, 1996. Net Gain, a new method for preventing malaria deaths. Geneva: International Development Research Centre/World Health Organization.
-
43
Schellenberg D, Menendez C, Kahigwa E, Aponte J, Vidal J, Tanner M, Mshinda H, Alonso PL, 2001. Intermittent treatment for malaria and anaemia control at time of routine vaccinations in Tanzanian infants: a randomised, placebo-controlled trial. Lancet 357 :1471–1477.
-
44
Graves P, Gelband H, 2003. Vaccines for preventing malaria. Cochrane Database Syst Rev: CD000129
-
45
Goodman CA, Coleman PG, Mills A, 2000. Economic analysis of malaria control in sub-Saharan Africa. Geneva: Global Forum for Health Research.
-
46
Snow RW, Mung’ala VO, Foster D, Marsh K, 1994. The role of the district hospital in child survival at the Kenyan Coast. Afr J Health Sci 1 :71–75.
-
47
Smith T, Charlwood JD, Kihonda J, Mwankusye S, Billingsley P, Meuwissen J, Lyimo E, Takken W, Teuscher T, Tanner M, 1993. Absence of seasonal variation in malaria parasitaemia in an area of intense seasonal transmission. Acta Trop 54 :55–72.
-
48
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