Malaria and Fetal Growth Alterations in the 3rd Trimester of Pregnancy: A Longitudinal Ultrasound Study

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Schmiegelow, Christentze ^a,g   Minja, Daniel ^a,b,g   Oesterholt, Mayke ^c   Pehrson, Caroline ^a,g   Suhrs, Hannah Elena ^a,g   Boström, Stéphanie ^d   Lemnge, Martha ^b   Magistrado, Pamela ^a,g   Rasch, Vibeke ^e   Nielsen, Birgitte Bruun ^f   Lusingu, John ^a,b,g   Theander, Thor G ^a,g  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (Tanzania)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d STOCKHOLM UNIVERSITY   (Sweden)

^e ODENSE UNIVERSITY HOSPITAL   (Denmark)

^f AARHUS UNIVERSITY HOSPITAL   (Denmark)

^g Mental Health Services CPH   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ADOLESCENT; ADULT; ARTICLE; BIRTH WEIGHT; CONTROLLED STUDY; FEMALE; FETUS; FETUS ECHOGRAPHY; FETUS GROWTH; FETUS WEIGHT; HUMAN; INTRAUTERINE GROWTH RETARDATION; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALARIA; MALE; NEWBORN; OBSERVATIONAL STUDY; PREGNANT WOMAN; PRENATAL EXPOSURE; PRIMIGRAVIDA; TANZANIA; THIRD TRIMESTER PREGNANCY;

ADULT; BIRTH WEIGHT; FEMALE; FETAL DEVELOPMENT; FETAL GROWTH RETARDATION; GESTATIONAL AGE; HUMANS; INFANT, NEWBORN; LONGITUDINAL STUDIES; MALARIA; PREGNANCY; PREGNANCY COMPLICATIONS, PARASITIC; PREGNANCY TRIMESTER, THIRD; TANZANIA; ULTRASONOGRAPHY, PRENATAL;

EID: 84872260236     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0053794     Document Type: Article

References (57)

1. Shulman CE, Marshall T, Dorman EK, Bulmer JN, Cutts F, et al. (2001) Malaria in pregnancy: adverse effects on haemoglobin levels and birthweight in primigravidae and multigravidae. Trop Med Int Health 6: 770-778.
2. Ishaque S, Yakoob MY, Imdad A, Goldenberg RL, Eisele TP, et al. (2011) Effectiveness of interventions to screen and manage infections during pregnancy on reducing stillbirths: a review. BMC Public Health 11 Suppl 3: S3.
3. Sullivan AD, Nyirenda T, Cullinan T, Taylor T, Harlow SD, et al. (1999) Malaria infection during pregnancy: intrauterine growth retardation and preterm delivery in Malawi. J Infect Dis 179: 1580-1583.
4. Steketee RW, Wirima JJ, Hightower AW, Slutsker L, Heymann DL, et al. (1996) The effect of malaria and malaria prevention in pregnancy on offspring birthweight, prematurity, and intrauterine growth retardation in rural Malawi. Am J Trop Med Hyg 55: 33-41.
5. Meuris S, Piko BB, Eerens P, Vanbellinghen AM, Dramaix M, et al. (1993) Gestational malaria: assessment of its consequences on fetal growth. Am J Trop Med Hyg 48: 603-609.
6. Verhoeff FH, Brabin BJ, van BS, Chimsuku L, Kazembe P, et al. (2001) An analysis of intra-uterine growth retardation in rural Malawi. Eur J Clin Nutr 55: 682-689.
7. Huynh BT, Fievet N, Gbaguidi G, Dechavanne S, Borgella S, et al. (2011) Influence of the timing of malaria infection during pregnancy on birth weight and on maternal anemia in Benin. Am J Trop Med Hyg 85: 214-220.
8. Claris O, Beltrand J, Levy-Marchal C, (2010) Consequences of intrauterine growth and early neonatal catch-up growth. Semin Perinatol 34: 207-210.
9. Christensen DL, Kapur A, Bygbjerg IC, (2011) Physiological adaption to maternal malaria and other adverse exposure: low birth weight, functional capacity, and possible metabolic disease in adult life. Int J Gynaecol Obstet 115 Suppl 1: S16-S19.
10. Rogerson SJ, Mwapasa V, Meshnick SR, (2007) Malaria in pregnancy: linking immunity and pathogenesis to prevention. Am J Trop Med Hyg 77: 14-22.
11. Desai M, Ter Kuile FO, Nosten F, McGready R, Asamoa K, et al. (2007) Epidemiology and burden of malaria in pregnancy. Lancet Infect Dis 7: 93-104.
12. Mahajan S, Aalinkeel R, Shah P, Singh S, Gupta N, et al. (2008) Nutritional anaemia dysregulates endocrine control of fetal growth. Br J Nutr 100: 408-417.
13. Dorman EK, Shulman CE, Kingdom J, Bulmer JN, Mwendwa J, et al. (2002) Impaired uteroplacental blood flow in pregnancies complicated by falciparum malaria. Ultrasound Obstet Gynecol 19: 165-170.
14. Umbers AJ, Boeuf P, Clapham C, Stanisic DI, Baiwog F, et al. (2011) Placental malaria-associated inflammation disturbs the insulin-like growth factor axis of fetal growth regulation. J Infect Dis 203: 561-569.
15. Rogerson SJ, Pollina E, Getachew A, Tadesse E, Lema VM, et al. (2003) Placental monocyte infiltrates in response to Plasmodium falciparum malaria infection and their association with adverse pregnancy outcomes. Am J Trop Med Hyg 68: 115-119.
16. Umbers AJ, Aitken EH, Rogerson SJ (2011) Malaria in pregnancy: small babies, big problem. Trends Parasitol.
17. Muehlenbachs A, Mutabingwa TK, Edmonds S, Fried M, Duffy PE, (2006) Hypertension and maternal-fetal conflict during placental malaria. PLoS Med 3: 2124-2130.
18. Taha TT, Gray RH, Mohamedani AA, (1993) Malaria and low birth weight in central Sudan. Am J Epidemiol 138: 318-325.
19. Kalilani L, Mofolo I, Chaponda M, Rogerson SJ, Meshnick SR, (2010) The effect of timing and frequency of Plasmodium falciparum infection during pregnancy on the risk of low birth weight and maternal anemia. Trans R Soc Trop Med Hyg 104: 416-422.
20. Rogerson SJ, van den Broek NR, Chaluluka E, Qongwane C, Mhango CG, et al. (2000) Malaria and anemia in antenatal women in Blantyre, Malawi: a twelve-month survey. Am J Trop Med Hyg 62: 335-340.
21. Cottrell G, Mary JY, Barro D, Cot M, (2007) The importance of the period of malarial infection during pregnancy on birth weight in tropical Africa. Am J Trop Med Hyg 76: 849-854.
22. Valea I, Tinto H, Drabo MK, Huybregts L, Sorgho H, et al. (2012) An analysis of timing and frequency of malaria infection during pregnancy in relation to the risk of low birth weight, anaemia and perinatal mortality in Burkina Faso. Malar J 11: 71.
23. McGready R, Lee S, Wiladphaingern J, Ashley E, Rijken M et al. (2011) Adverse effects of falciparum and vivax malaria and the safety of antimalarial treatment in early pregnancy: a population-based study. Lancet Infect Dis.
24. Wilcox AJ, (2001) On the importance-and the unimportance-of birthweight. Int J Epidemiol 30: 1233-1241.
25. Mondry A, Pengbo L, Loh M, Mongelli M, (2005) Z-velocity in screening for intrauterine growth restriction. Ultrasound Obstet Gynecol 26: 634-638.
26. Chang TC, Robson SC, Spencer JA, Gallivan S, (1993) Identification of fetal growth retardation: comparison of Doppler waveform indices and serial ultrasound measurements of abdominal circumference and fetal weight. Obstet Gynecol 82: 230-236.
27. Hemachandra AH, Klebanoff MA, (2006) Use of serial ultrasound to identify periods of fetal growth restriction in relation to neonatal anthropometry. Am J Hum Biol 18: 791-797.
28. de Jong CL, Francis A, van Geijn HP, Gardosi J, (1999) Fetal growth rate and adverse perinatal events. Ultrasound Obstet Gynecol 13: 86-89.
29. Mmbando BP, Vestergaard LS, Kitua AY, Lemnge MM, Theander TG, et al. (2010) A progressive declining in the burden of malaria in north-eastern Tanzania. Malar J 9: 216-224.
30. Schmiegelow C, Minja D, Oesterholt M, Pehrson C, Suhrs HE, et al. (2012) Factors associated with and causes of perinatal mortality in northeastern Tanzania. Acta Obstet Gynecol Scand 91: 1061-1068.
31. Schmiegelow C, Scheike T, Oesterholt M, Minja D, Pehrson C et al. (2012) Development of a Fetal Weight Chart Using Serial Trans-Abdominal Ultrasound in an East African Population: A Longitudinal Observational Study. PLoS ONE 7: doi:10.1371/journal.pone.0044773.
32. Hendrix N, Berghella V, (2008) Non-placental causes of intrauterine growth restriction. Semin Perinatol 32: 161-165.
33. Kramer MS, (2003) The epidemiology of adverse pregnancy outcomes: an overview. J Nutr 133: 1592S-1596S.
34. Kyabayinze DJ, Tibenderana JK, Nassali M, Tumwine LK, Riches C, et al. (2011) Placental Plasmodium falciparum malaria infection: operational accuracy of HRP2 rapid diagnostic tests in a malaria endemic setting. Malar J 10: 306.
35. Minja DT, Schmiegelow C, Oesterholt M, Magistrado PA, Bostrom S, et al. (2012) Reliability of rapid diagnostic tests in diagnosing pregnancy-associated malaria in north-eastern Tanzania. Malar J 11: 211.
36. World Health Organisation (2010) World Malaria Report.
37. Hadlock FP, Shah YP, Kanon DJ, Lindsey JV, (1992) Fetal crown-rump length: reevaluation of relation to menstrual age (5-18 weeks) with high-resolution real-time US. Radiology 182: 501-505.
38. Chitty LS, Altman DG, Henderson A, Campbell S, (1994) Charts of fetal size: 2. Head measurements. Br J Obstet Gynaecol 101: 35-43.
39. Hadlock FP, Harrist RB, Sharman RS, Deter RL, Park SK, (1985) Estimation of fetal weight with the use of head, body, and femur measurements-a prospective study. Am J Obstet Gynecol 151: 333-337.
40. Owen P, Donnet ML, Ogston SA, Christie AD, Howie PW, et al. (1996) Standards for ultrasound fetal growth velocity. Br J Obstet Gynaecol 103: 60-69.
41. Ott WJ, (2002) Diagnosis of intrauterine growth restriction: comparison of ultrasound parameters. Am J Perinatol 19: 133-137.
42. Lampl M, Jeanty P, (2003) Timing is everything: a reconsideration of fetal growth velocity patterns identifies the importance of individual and sex differences. Am J Hum Biol 15: 667-680.
43. de Jong CL, Gardosi J, Baldwin C, Francis A, Dekker GA, et al. (1998) Fetal weight gain in a serially scanned high-risk population. Ultrasound Obstet Gynecol 11: 39-43.
44. Figueras F, Gardosi J, (2011) Intrauterine growth restriction: new concepts in antenatal surveillance, diagnosis, and management. Am J Obstet Gynecol 204: 288-300.
45. Shulman CE, Graham WJ, Jilo H, Lowe BS, New L, et al. (1996) Malaria is an important cause of anaemia in primigravidae: evidence from a district hospital in coastal Kenya. Trans R Soc Trop Med Hyg 90: 535-539.
46. Rijken MJ, Papageorghiou AT, Thiptharakun S, Kiricharoen S, Dwell SL, et al. (2012) Ultrasound evidence of early fetal growth restriction after maternal malaria infection. PLoS ONE 7: e31411.
47. Scifres CM, Nelson DM, (2009) Intrauterine growth restriction, human placental development and trophoblast cell death. J Physiol 587: 3453-3458.
48. Rijken MJ, Moroski WE, Kiricharoen S, Karunkonkowit N, Stevenson G, et al. (2012) Effect of malaria on placental volume measured using three-dimensional ultrasound: a pilot study. Malar J 11: 5.
49. Griffin JB, Lokomba V, Landis SH, Thorp JM Jr, Herring AH, et al. (2012) Plasmodium falciparum parasitaemia in the first half of pregnancy, uterine and umbilical artery blood flow, and foetal growth: a longitudinal Doppler ultrasound study. Malar J 11: 319.
50. Huynh BT, Fievet N, Briand V, Borgella S, Massougbodji A, et al. (2012) Consequences of gestational malaria on birth weight: finding the best timeframe for intermittent preventive treatment administration. PLoS ONE 7: e35342.
51. Kalanda BF, van BS, Verhoeff FH, Brabin BJ, (2005) Anthropometry of fetal growth in rural Malawi in relation to maternal malaria and HIV status. Arch Dis Child Fetal Neonatal Ed 90: F161-F165.
52. Kalanda BF, Verhoeff FH, Chimsuku L, Harper G, Brabin BJ, (2006) Adverse birth outcomes in a malarious area. Epidemiol Infect 134: 659-666.
53. Landis SH, Lokomba V, Ananth CV, Atibu J, Ryder RW et al. (2008) Impact of maternal malaria and under-nutrition on intrauterine growth restriction: a prospective ultrasound study in Democratic Republic of Congo. Epidemiol Infect 1-11.
54. Ott WJ, (2006) Sonographic diagnosis of fetal growth restriction. Clin Obstet Gynecol 49: 295-307.
55. Nahum GG, Stanislaw H, (2003) Ultrasonographic prediction of term birth weight: how accurate is it? Am J Obstet Gynecol 188: 566-574.
56. Scioscia M, Vimercati A, Ceci O, Vicino M, Selvaggi LE, (2008) Estimation of birth weight by two-dimensional ultrasonography: a critical appraisal of its accuracy. Obstet Gynecol 111: 57-65.
57. Mirghani HM, Weerasinghe S, Ezimokhai M, Smith JR, (2005) Ultrasonic estimation of fetal weight at term: an evaluation of eight formulae. J Obstet Gynaecol Res 31: 409-413.