#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Early malaria infection, dysregulation of angiogenesis, metabolism and inflammation across pregnancy, and risk of preterm birth in Malawi: A cohort study


Autoři: Robyn E. Elphinstone aff001;  Andrea M. Weckman aff001;  Chloe R. McDonald aff001;  Vanessa Tran aff001;  Kathleen Zhong aff001;  Mwayiwawo Madanitsa aff002;  Linda Kalilani-Phiri aff002;  Carole Khairallah aff003;  Steve M. Taylor aff004;  Steven R. Meshnick aff004;  Victor Mwapasa aff002;  Feiko O. ter Kuile aff003;  Andrea L. Conroy aff006;  Kevin C. Kain aff001
Působiště autorů: Sandra Rotman Centre for Global Health, University Health Network-University of Toronto, Toronto, Ontario, Canada aff001;  College of Medicine, University of Malawi, Blantyre, Malawi aff002;  Department of Clinical Sciences, Liverpool School of Tropical Medicine, Liverpool, United Kingdom aff003;  Department of Epidemiology, Gillings School of Global Public Health, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America aff004;  Division of Infectious Diseases and Duke Global Health Institute, Duke University, Durham, North Carolina, United States of America aff005;  Department of Pediatrics, Indiana University School of Medicine, Indianapolis, United States of America aff006
Vyšlo v časopise: Early malaria infection, dysregulation of angiogenesis, metabolism and inflammation across pregnancy, and risk of preterm birth in Malawi: A cohort study. PLoS Med 16(10): e32767. doi:10.1371/journal.pmed.1002914
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pmed.1002914

Souhrn

Background

Malaria in pregnancy is associated with adverse birth outcomes. However, the underlying mechanisms remain poorly understood. Tight regulation of angiogenic, metabolic, and inflammatory pathways are essential for healthy pregnancies. We hypothesized that malaria disrupts these pathways leading to preterm birth (PTB).

Methods and findings

We conducted a secondary analysis of a randomized trial of malaria prevention in pregnancy conducted in Malawi from July 21, 2011, to March 18, 2013. We longitudinally assessed circulating mediators of angiogenic, metabolic, and inflammatory pathways during pregnancy in a cohort of HIV-negative women (n = 1,628), with a median age of 21 years [18, 25], and 562 (35%) were primigravid. Pregnancies were ultrasound dated, and samples were analyzed at 13 to 23 weeks (Visit 1), 28 to 33 weeks (Visit 2), and/or 34 to 36 weeks (Visit 3). Malaria prevalence was high; 70% (n = 1,138) had PCR-positive Plasmodium falciparum infection at least once over the course of pregnancy and/or positive placental histology. The risk of delivering preterm in the entire cohort was 20% (n = 304/1506). Women with malaria before 24 weeks gestation had a higher risk of PTB (24% versus 18%, p = 0.005; adjusted relative risk [aRR] 1.30, 95% confidence interval [CI] 1.04–1.63, p = 0.021); and those who were malaria positive only before week 24 had an even greater risk of PTB (28% versus 17%, p = 0.02; with an aRR of 1.67, 95% CI 1.20–2.30, p = 0.002). Using linear mixed-effects modeling, malaria before 24 weeks gestation was associated with altered kinetics of inflammatory (C-Reactive Protein [CRP], Chitinase 3-like protein-1 [CHI3L1], Interleukin 18 Binding Protein [IL-18BP], soluble Tumor Necrosis Factor receptor II [sTNFRII], soluble Intercellular Adhesion Molecule-1 [sICAM-1]), angiogenic (soluble Endoglin [sEng]), and metabolic mediators (Leptin, Angiopoietin-like 3 [Angptl3]) over the course of pregnancy (χ2 > 13.0, p ≤ 0.001 for each). Limitations include being underpowered to assess the impact on nonviable births, being unable to assess women who had not received any antimalarials, and, because of the exposure to antimalarials in the second trimester, there were limited numbers of malaria infections late in pregnancy.

Conclusions

Current interventions for the prevention of malaria in pregnancy are initiated at the first antenatal visit, usually in the second trimester. In this study, we found that many women are already malaria-infected by their first visit. Malaria infection before 24 weeks gestation was associated with dysregulation of essential regulators of angiogenesis, metabolism, and inflammation and an increased risk of PTB. Preventing malaria earlier in pregnancy may reduce placental dysfunction and thereby improve birth outcomes in malaria-endemic settings.

Klíčová slova:

Histology – Inflammation – Labor and delivery – leptin – Malaria – Pregnancy – Preterm birth – placenta


Zdroje

1. World Health Organization Global Malaria Programme. World Malaria Report 2015. World Health Organization [Internet], December 2015: 1–280. https://www.who.int/malaria/publications/world-malaria-report-2015/report/en/. [cited 2018 Feb 11].

2. Rogerson SJ, Desai M, Mayor A, Sicuri E, Taylor SM, van Eijk AM. Burden, pathology, and costs of malaria in pregnancy: new developments for an old problem. The Lancet infectious diseases. 2018;18(4):e107–e18. doi: 10.1016/S1473-3099(18)30066-5 29396010.

3. De Beaudrap P, Turyakira E, Nabasumba C, Tumwebaze B, Piola P, Boum Ii Y, et al. Timing of malaria in pregnancy and impact on infant growth and morbidity: a cohort study in Uganda. Malaria journal. 2016;15:92. doi: 10.1186/s12936-016-1135-7 26879849

4. Desai M, ter Kuile FO, Nosten F, McGready R, Asamoa K, Brabin B, et al. Epidemiology and burden of malaria in pregnancy. The Lancet infectious diseases. 2007;7(2):93–104. doi: 10.1016/S1473-3099(07)70021-X 17251080.

5. Raju TNK, Pemberton VL, Saigal S, Blaisdell CJ, Moxey-Mims M, Buist S, et al. Long-Term Healthcare Outcomes of Preterm Birth: An Executive Summary of a Conference Sponsored by the National Institutes of Health. J Pediatr. 2017;181:309–18 e1. doi: 10.1016/j.jpeds.2016.10.015 27806833.

6. Marchant T, Willey B, Katz J, Clarke S, Kariuki S, ter Kuile F, et al. Neonatal mortality risk associated with preterm birth in East Africa, adjusted by weight for gestational age: individual participant level meta-analysis. PLoS Med. 2012;9(8):e1001292. doi: 10.1371/journal.pmed.1001292 22904691

7. Lee AC, Kozuki N, Cousens S, Stevens GA, Blencowe H, Silveira MF, et al. Estimates of burden and consequences of infants born small for gestational age in low and middle income countries with INTERGROWTH-21(st) standard: analysis of CHERG datasets. Bmj. 2017;358:j3677. doi: 10.1136/bmj.j3677 28819030

8. Calkins K, Devaskar SU. Fetal origins of adult disease. Current problems in pediatric and adolescent health care. 2011;41(6):158–76. doi: 10.1016/j.cppeds.2011.01.001 21684471.

9. Luu TM, Katz SL, Leeson P, Thebaud B, Nuyt AM. Preterm birth: risk factor for early-onset chronic diseases. CMAJ: Canadian Medical Association journal = journal de l’Association medicale canadienne. 2016;188(10):736–46. doi: 10.1503/cmaj.150450 26644500

10. Sullivan AD, Nyirenda T, Cullinan T, Taylor T, Harlow SD, James SA, et al. Malaria infection during pregnancy: intrauterine growth retardation and preterm delivery in Malawi. The Journal of infectious diseases. 1999;179(6):1580–3. doi: 10.1086/314752 10228088.

11. Steketee RW, Wirima JJ, Hightower AW, Slutsker L, Heymann DL, Breman JG. The effect of malaria and malaria prevention in pregnancy on offspring birthweight, prematurity, and intrauterine growth retardation in rural Malawi. The American journal of tropical medicine and hygiene. 1996;55(1 Suppl):33–41. doi: 10.4269/ajtmh.1996.55.33 8702035.

12. Kalilani L, Mofolo I, Chaponda M, Rogerson SJ, Meshnick SR. The effect of timing and frequency of Plasmodium falciparum infection during pregnancy on the risk of low birth weight and maternal anemia. Transactions of the Royal Society of Tropical Medicine and Hygiene. 2010;104(6):416–22. doi: 10.1016/j.trstmh.2010.01.013 20207387.

13. Moore KA, Simpson JA, Wiladphaingern J, Min AM, Pimanpanarak M, Paw MK, et al. Influence of the number and timing of malaria episodes during pregnancy on prematurity and small-for-gestational-age in an area of low transmission. BMC Med. 2017;15(1):117. doi: 10.1186/s12916-017-0877-6 28633672

14. De Beaudrap P, Turyakira E, White LJ, Nabasumba C, Tumwebaze B, Muehlenbachs A, et al. Impact of malaria during pregnancy on pregnancy outcomes in a Ugandan prospective cohort with intensive malaria screening and prompt treatment. Malaria journal. 2013;12:139. doi: 10.1186/1475-2875-12-139 23617626

15. Sharma L, Shukla G. Placental Malaria: A New Insight into the Pathophysiology. Frontiers in medicine. 2017;4:117. doi: 10.3389/fmed.2017.00117 28791290

16. Conroy AL, Silver KL, Zhong K, Rennie M, Ward P, Sarma JV, et al. Complement activation and the resulting placental vascular insufficiency drives fetal growth restriction associated with placental malaria. Cell host & microbe. 2013;13(2):215–26. doi: 10.1016/j.chom.2013.01.010 23414761.

17. Boeuf P, Aitken EH, Chandrasiri U, Chua CL, McInerney B, McQuade L, et al. Plasmodium falciparum malaria elicits inflammatory responses that dysregulate placental amino acid transport. PLoS Pathog. 2013;9(2):e1003153. doi: 10.1371/journal.ppat.1003153 23408887

18. McDonald CR, Darling AM, Conroy AL, Tran V, Cabrera A, Liles WC, et al. Inflammatory and Angiogenic Factors at Mid-Pregnancy Are Associated with Spontaneous Preterm Birth in a Cohort of Tanzanian Women. PLoS ONE. 2015;10(8):e0134619. doi: 10.1371/journal.pone.0134619 26247200

19. Darling AM, McDonald CR, Conroy AL, Hayford KT, Liles WC, Wang M, et al. Angiogenic and inflammatory biomarkers in midpregnancy and small-for-gestational-age outcomes in Tanzania. American journal of obstetrics and gynecology. 2014;211(5):509 e1–8. doi: 10.1016/j.ajog.2014.05.032 24881826

20. Silver KL, Zhong K, Leke RG, Taylor DW, Kain KC. Dysregulation of angiopoietins is associated with placental malaria and low birth weight. PLoS ONE. 2010;5(3):e9481. doi: 10.1371/journal.pone.0009481 20208992

21. Thevenon AD, Zhou JA, Megnekou R, Ako S, Leke RG, Taylor DW. Elevated levels of soluble TNF receptors 1 and 2 correlate with Plasmodium falciparum parasitemia in pregnant women: potential markers for malaria-associated inflammation. Journal of immunology. 2010;185(11):7115–22. doi: 10.4049/jimmunol.1002293 20980627

22. Conroy AL, McDonald CR, Gamble JL, Olwoch P, Natureeba P, Cohan D, et al. Altered angiogenesis as a common mechanism underlying preterm birth, small for gestational age, and stillbirth in women living with HIV. American journal of obstetrics and gynecology. 2017;217(6):684 e1–e17. doi: 10.1016/j.ajog.2017.10.003 29031892

23. Griffin JB, Lokomba V, Landis SH, Thorp JM Jr., Herring AH, Tshefu AK, et al. Plasmodium falciparum parasitaemia in the first half of pregnancy, uterine and umbilical artery blood flow, and foetal growth: a longitudinal Doppler ultrasound study. Malaria journal. 2012;11:319. doi: 10.1186/1475-2875-11-319 22963509

24. McDonald CR, Cahill LS, Gamble JL, Elphinstone R, Gazdzinski LM, Zhong KJY, et al. Malaria in pregnancy alters l-arginine bioavailability and placental vascular development. Sci Transl Med. 2018;10(431). doi: 10.1126/scitranslmed.aan6007 29514999.

25. Silver KL, Conroy AL, Leke RG, Leke RJ, Gwanmesia P, Molyneux ME, et al. Circulating soluble endoglin levels in pregnant women in Cameroon and Malawi—associations with placental malaria and fetal growth restriction. PLoS ONE. 2011;6(9):e24985. doi: 10.1371/journal.pone.0024985 21966395

26. Madanitsa M, Kalilani L, Mwapasa V, van Eijk AM, Khairallah C, Ali D, et al. Scheduled Intermittent Screening with Rapid Diagnostic Tests and Treatment with Dihydroartemisinin-Piperaquine versus Intermittent Preventive Therapy with Sulfadoxine-Pyrimethamine for Malaria in Pregnancy in Malawi: An Open-Label Randomized Controlled Trial. PLoS Med. 2016;13(9):e1002124. doi: 10.1371/journal.pmed.1002124 27622558

27. Wylie BJ, Kalilani-Phiri L, Madanitsa M, Membe G, Nyirenda O, Mawindo P, et al. Gestational age assessment in malaria pregnancy cohorts: a prospective ultrasound demonstration project in Malawi. Malaria journal. 2013;12:183. doi: 10.1186/1475-2875-12-183 23734718

28. Conroy AL, Phiri H, Hawkes M, Glover S, Mallewa M, Seydel KB, et al. Endothelium-based biomarkers are associated with cerebral malaria in Malawian children: a retrospective case-control study. PLoS ONE. 2010;5(12):e15291. doi: 10.1371/journal.pone.0015291 21209923

29. International Fetal and Newborn Growth Consortium for the 21st Century. International Standards for Size at Birth (v1.0.5934.26288): University of Oxford; 2017. http://intergrowth21.ndog.ox.ac.uk. [cited 2016 Aug 15].

30. Romero R, Chaiworapongsa T, Erez O, Tarca AL, Gervasi MT, Kusanovic JP, et al. An imbalance between angiogenic and anti-angiogenic factors precedes fetal death in a subset of patients: results of a longitudinal study. The journal of maternal-fetal & neonatal medicine: the official journal of the European Association of Perinatal Medicine, the Federation of Asia and Oceania Perinatal Societies, the International Society of Perinatal Obstet. 2010;23(12):1384–99. doi: 10.3109/14767051003681121 20459337

31. Bates D. Fitting linear mixed-effects models using lme4. J Stat Software. 2015;67:1–48.

32. R: A language and environment for statistical computing. R Foundation for Statistical Computing; Vienna, Austria. Version 3.5.1 [software]. 2018 July 02. http://www.R-project.org/.[cited 2019 Jun 4].

33. Harrell Jr. FE. rms: Regression Modeling Strategies. R Package Version 5.1–3.1 [software]. 2019 Apr 22. https://CRAN.R-project.org/package=rms. [cited 2019 Jun 4]

34. Harrell Jr. FE. Regression Modeling Strategies [Internet]. Vanderbilt University Department of Biostatistics: BIOS330; c1995-2019. http://hbiostat.org/doc/rms.pdf. [cited 2019 Jun 4]

35. March of Dimes, PMNCH, Save the Children, WHO. Born Too Soon: The Global Action Report on Preterm Birth. Eds CP Howson, MV Kinney, JE Lawn. World Health Organization [internet]. Geneva, 2012: p. 1–126. https://www.who.int/pmnch/media/news/2012/preterm_birth_report/en/index1.html. [cited 2018 Jan 15].

36. Erdman LK, Petes C, Lu Z, Dhabangi A, Musoke C, Cserti-Gazdewich CM, et al. Chitinase 3-like 1 is induced by Plasmodium falciparum malaria and predicts outcome of cerebral malaria and severe malarial anaemia in a case-control study of African children. Malaria journal. 2014;13:279. doi: 10.1186/1475-2875-13-279 25047113

37. Conroy AL, Hawkes MT, Elphinstone R, Opoka RO, Namasopo S, Miller C, et al. Chitinase-3-like 1 is a biomarker of acute kidney injury and mortality in paediatric severe malaria. Malaria journal. 2018;17(1):82. doi: 10.1186/s12936-018-2225-5 29448936

38. Adukpo S, Kusi KA, Ofori MF, Tetteh JK, Amoako-Sakyi D, Goka BQ, et al. High plasma levels of soluble intercellular adhesion molecule (ICAM)-1 are associated with cerebral malaria. PLoS ONE. 2013;8(12):e84181. doi: 10.1371/journal.pone.0084181 24386348

39. Cserti-Gazdewich CM, Dzik WH, Erdman L, Ssewanyana I, Dhabangi A, Musoke C, et al. Combined measurement of soluble and cellular ICAM-1 among children with Plasmodium falciparum malaria in Uganda. Malaria journal. 2010;9:233. doi: 10.1186/1475-2875-9-233 20712868

40. Jakobsen PH, Morris-Jones S, Ronn A, Hviid L, Theander TG, Elhassan IM, et al. Increased plasma concentrations of sICAM-1, sVCAM-1 and sELAM-1 in patients with Plasmodium falciparum or P. vivax malaria and association with disease severity. Immunology. 1994;83(4):665–9. 7533138

41. Nagamine Y, Hayano M, Kashiwamura S, Okamura H, Nakanishi K, Krudsod S, et al. Involvement of interleukin-18 in severe Plasmodium falciparum malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene. 2003;97(2):236–41. doi: 10.1016/s0035-9203(03)90130-1 14584384.

42. Unger HW, Hansa AP, Buffet C, Hasang W, Teo A, Randall L, et al. Sulphadoxine-pyrimethamine plus azithromycin may improve birth outcomes through impacts on inflammation and placental angiogenesis independent of malarial infection. Scientific reports. 2019;9(1):2260. doi: 10.1038/s41598-019-38821-2 30783215

43. Ruizendaal E, Schallig H, Bradley J, Traore-Coulibaly M, Lompo P, d’Alessandro U, et al. Interleukin-10 and soluble tumor necrosis factor receptor II are potential biomarkers of Plasmodium falciparum infections in pregnant women: a case-control study from Nanoro, Burkina Faso. Biomarker research. 2017;5:34. doi: 10.1186/s40364-017-0114-7 29255607

44. Kabyemela ER, Muehlenbachs A, Fried M, Kurtis JD, Mutabingwa TK, Duffy PE. Maternal peripheral blood level of IL-10 as a marker for inflammatory placental malaria. Malaria journal. 2008;7:26. doi: 10.1186/1475-2875-7-26 18230163

45. Mockenhaupt FP, Rong B, Gunther M, Beck S, Till H, Kohne E, et al. Anaemia in pregnant Ghanaian women: importance of malaria, iron deficiency, and haemoglobinopathies. Transactions of the Royal Society of Tropical Medicine and Hygiene. 2000;94(5):477–83. doi: 10.1016/s0035-9203(00)90057-9 11132370.

46. Mockenhaupt FP, Rong B, Till H, Eggelte TA, Beck S, Gyasi-Sarpong C, et al. Submicroscopic Plasmodium falciparum infections in pregnancy in Ghana. Tropical medicine & international health: TM & IH. 2000;5(3):167–73. 10747278.

47. Saad AA, Mohamed OE, Ali AA, Bashir AM, Ali NI, Elbashir MI, et al. Acute-phase proteins in pregnant Sudanese women with severe Plasmodium falciparum malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene. 2012;106(9):570–2. doi: 10.1016/j.trstmh.2012.06.004 22818740.

48. Borzychowski AM, Sargent IL, Redman CW. Inflammation and pre-eclampsia. Seminars in fetal & neonatal medicine. 2006;11(5):309–16. doi: 10.1016/j.siny.2006.04.001 16828580.

49. Cotechini T, Graham CH. Aberrant maternal inflammation as a cause of pregnancy complications: A potential therapeutic target? Placenta. 2015;36(8):960–6. doi: 10.1016/j.placenta.2015.05.016 26094029.

50. Challis JR, Lockwood CJ, Myatt L, Norman JE, Strauss JF 3rd, Petraglia F. Inflammation and pregnancy. Reproductive sciences. 2009;16(2):206–15. doi: 10.1177/1933719108329095 19208789.

51. Chen DB, Zheng J. Regulation of placental angiogenesis. Microcirculation. 2014;21(1):15–25. doi: 10.1111/micc.12093 23981199

52. Huppertz B, Peeters LL. Vascular biology in implantation and placentation. Angiogenesis. 2005;8(2):157–67. doi: 10.1007/s10456-005-9007-8 16211358.

53. Yinon Y, Nevo O, Xu J, Many A, Rolfo A, Todros T, et al. Severe intrauterine growth restriction pregnancies have increased placental endoglin levels: hypoxic regulation via transforming growth factor-beta 3. The American journal of pathology. 2008;172(1):77–85. doi: 10.2353/ajpath.2008.070640 18156205

54. Romero R, Nien JK, Espinoza J, Todem D, Fu W, Chung H, et al. A longitudinal study of angiogenic (placental growth factor) and anti-angiogenic (soluble endoglin and soluble vascular endothelial growth factor receptor-1) factors in normal pregnancy and patients destined to develop preeclampsia and deliver a small for gestational age neonate. The journal of maternal-fetal & neonatal medicine: the official journal of the European Association of Perinatal Medicine, the Federation of Asia and Oceania Perinatal Societies, the International Society of Perinatal Obstet. 2008;21(1):9–23. doi: 10.1080/14767050701830480 18175241

55. Bostrom S, Ibitokou S, Oesterholt M, Schmiegelow C, Persson JO, Minja D, et al. Biomarkers of Plasmodium falciparum infection during pregnancy in women living in northeastern Tanzania. PLoS ONE. 2012;7(11):e48763. doi: 10.1371/journal.pone.0048763 23155405

56. Muehlenbachs A, Mutabingwa TK, Edmonds S, Fried M, Duffy PE. Hypertension and maternal-fetal conflict during placental malaria. PLoS Med. 2006;3(11):e446. doi: 10.1371/journal.pmed.0030446 17105340

57. Carbone C, Piro G, Merz V, Simionato F, Santoro R, Zecchetto C, et al. Angiopoietin-Like Proteins in Angiogenesis, Inflammation and Cancer. International journal of molecular sciences. 2018;19(2). doi: 10.3390/ijms19020431 29389861.

58. Henson MC, Castracane VD. Leptin in pregnancy: an update. Biology of reproduction. 2006;74(2):218–29. doi: 10.1095/biolreprod.105.045120 16267210.

59. Henson MC, Castracane VD. Leptin in pregnancy. Biology of reproduction. 2000;63(5):1219–28. doi: 10.1095/biolreprod63.5.1219 11058523.

60. Perez-Perez A, Vilarino-Garcia T, Fernandez-Riejos P, Martin-Gonzalez J, Segura-Egea JJ, Sanchez-Margalet V. Role of leptin as a link between metabolism and the immune system. Cytokine & growth factor reviews. 2017;35:71–84. doi: 10.1016/j.cytogfr.2017.03.001 28285098.

61. Conroy AL, Liles WC, Molyneux ME, Rogerson SJ, Kain KC. Performance characteristics of combinations of host biomarkers to identify women with occult placental malaria: a case-control study from Malawi. PLoS ONE. 2011;6(12):e28540. doi: 10.1371/journal.pone.0028540 22174834

62. Kabyemela ER, Fried M, Kurtis JD, Mutabingwa TK, Duffy PE. Fetal responses during placental malaria modify the risk of low birth weight. Infection and immunity. 2008;76(4):1527–34. doi: 10.1128/IAI.00964-07 18212078

63. Fakor F, Sharami SH, Milani F, Mirblouk F, Kazemi S, Pourmarzi D, et al. The association between level of maternal serum leptin in the third trimester and the occurrence of moderate preterm labor. Journal of the Turkish German Gynecological Association. 2016;17(4):182–5. doi: 10.5152/jtgga.2016.16121 27990085

64. Nejabati HR, Latifi Z, Ghasemnejad T, Fattahi A, Nouri M. Placental growth factor (PlGF) as an angiogenic/inflammatory switcher: lesson from early pregnancy losses. Gynecological endocrinology: the official journal of the International Society of Gynecological Endocrinology. 2017;33(9):668–74. doi: 10.1080/09513590.2017.1318375 28447504.

65. Mallat Z, Silvestre JS, Le Ricousse-Roussanne S, Lecomte-Raclet L, Corbaz A, Clergue M, et al. Interleukin-18/interleukin-18 binding protein signaling modulates ischemia-induced neovascularization in mice hindlimb. Circ Res. 2002;91(5):441–8. doi: 10.1161/01.res.0000033592.11674.d8 12215494.

66. Shao R. YKL-40 acts as an angiogenic factor to promote tumor angiogenesis. Front Physiol. 2013;4:122. doi: 10.3389/fphys.2013.00122 23755018

67. Deng C, Zhang D, Shan S, Wu J, Yang H, Yu Y. Angiogenic effect of intercellular adhesion molecule-1. Journal of Huazhong University of Science and Technology Medical sciences = Hua zhong ke ji da xue xue bao Yi xue Ying De wen ban = Huazhong keji daxue xuebao Yixue Yingdewen ban. 2007;27(1):9–12. doi: 10.1007/s11596-007-0103-4 17393097.

68. Turu MM, Slevin M, Matou S, West D, Rodriguez C, Luque A, et al. C-reactive protein exerts angiogenic effects on vascular endothelial cells and modulates associated signalling pathways and gene expression. BMC cell biology. 2008;9:47. doi: 10.1186/1471-2121-9-47 18764931

69. Luo D, Luo Y, He Y, Zhang H, Zhang R, Li X, et al. Differential functions of tumor necrosis factor receptor 1 and 2 signaling in ischemia-mediated arteriogenesis and angiogenesis. The American journal of pathology. 2006;169(5):1886–98. doi: 10.2353/ajpath.2006.060603 17071609

70. Varejckova M, Gallardo-Vara E, Vicen M, Vitverova B, Fikrova P, Dolezelova E, et al. Soluble endoglin modulates the pro-inflammatory mediators NF-kappaB and IL-6 in cultured human endothelial cells. Life sciences. 2017;175:52–60. doi: 10.1016/j.lfs.2017.03.014 28336397.

71. Costa C, Incio J, Soares R. Angiogenesis and chronic inflammation: cause or consequence? Angiogenesis. 2007;10(3):149–66. doi: 10.1007/s10456-007-9074-0 17457680.

72. Blencowe H, Cousens S, Oestergaard MZ, Chou D, Moller AB, Narwal R, et al. National, regional, and worldwide estimates of preterm birth rates in the year 2010 with time trends since 1990 for selected countries: a systematic analysis and implications. Lancet. 2012;379(9832):2162–72. doi: 10.1016/S0140-6736(12)60820-4 22682464.

73. van den Broek NR, White SA, Goodall M, Ntonya C, Kayira E, Kafulafula G, et al. The APPLe study: a randomized, community-based, placebo-controlled trial of azithromycin for the prevention of preterm birth, with meta-analysis. PLoS Med. 2009;6(12):e1000191. doi: 10.1371/journal.pmed.1000191 19956761

74. Valea I, Tinto H, Drabo MK, Huybregts L, Sorgho H, Ouedraogo JB, et al. 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. Malaria journal. 2012;11:71. doi: 10.1186/1475-2875-11-71 22433778

75. Taha Tel T, Gray RH, Mohamedani AA. Malaria and low birth weight in central Sudan. American journal of epidemiology. 1993;138(5):318–25. doi: 10.1093/oxfordjournals.aje.a116861 8356970.

76. Hadlock FP, Harrist RB, Martinez-Poyer J. How accurate is second trimester fetal dating? Journal of ultrasound in medicine: official journal of the American Institute of Ultrasound in Medicine. 1991;10(10):557–61. doi: 10.7863/jum.1991.10.10.557 1942221.

77. Mkandawire P. Gestational Age at First Antenatal Care Visit in Malawi. Maternal and child health journal. 2015;19(11):2366–74. doi: 10.1007/s10995-015-1754-6 26152889.

78. Papageorghiou AT, Kemp B, Stones W, Ohuma EO, Kennedy SH, Purwar M, et al. Ultrasound-based gestational-age estimation in late pregnancy. Ultrasound in obstetrics & gynecology: the official journal of the International Society of Ultrasound in Obstetrics and Gynecology. 2016;48(6):719–26. doi: 10.1002/uog.15894 26924421.

79. World Health Organization Global Malaria Programme. WHO policy brief for the implementation of intermittent preventive treatment of malaria in pregnancy using sulfadoxine-pyrimethamine (IPTp-SP). World Health Organization [internet] 2014: p. 1–13. https://www.who.int/malaria/publications/atoz/policy_brief_iptp_sp_policy_recommendation/en/. [cited 2019 Jan 15].

80. Kakuru A, Jagannathan P, Muhindo MK, Natureeba P, Awori P, Nakalembe M, et al. Dihydroartemisinin-Piperaquine for the Prevention of Malaria in Pregnancy. The New England journal of medicine. 2016;374(10):928–39. doi: 10.1056/NEJMoa1509150 26962728

81. Kayentao K, Garner P, van Eijk AM, Naidoo I, Roper C, Mulokozi A, et al. Intermittent preventive therapy for malaria during pregnancy using 2 vs 3 or more doses of sulfadoxine-pyrimethamine and risk of low birth weight in Africa: systematic review and meta-analysis. JAMA: the journal of the American Medical Association. 2013;309(6):594–604. doi: 10.1001/jama.2012.216231 23403684

82. Desai M, Gutman J, L’Lanziva A, Otieno K, Juma E, Kariuki S, et al. Intermittent screening and treatment or intermittent preventive treatment with dihydroartemisinin-piperaquine versus intermittent preventive treatment with sulfadoxine-pyrimethamine for the control of malaria during pregnancy in western Kenya: an open-label, three-group, randomised controlled superiority trial. Lancet. 2015;386(10012):2507–19. doi: 10.1016/S0140-6736(15)00310-4 26429700

83. Radeva-Petrova D, Kayentao K, ter Kuile FO, Sinclair D, Garner P. Drugs for preventing malaria in pregnant women in endemic areas: any drug regimen versus placebo or no treatment. Cochrane Database Syst Rev. 2014;(10): doi: 10.1002/14651858.CD000169.pub3 25300703

84. Peters PJ, Thigpen MC, Parise ME, Newman RD. Safety and toxicity of sulfadoxine/pyrimethamine: implications for malaria prevention in pregnancy using intermittent preventive treatment. Drug safety: an international journal of medical toxicology and drug experience. 2007;30(6):481–501. doi: 10.2165/00002018-200730060-00003 17536875

Štítky
Interní lékařství

Článek vyšel v časopise

PLOS Medicine


2019 Číslo 10
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Hypertenze a hypercholesterolémie – synergický efekt léčby
nový kurz
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Multidisciplinární zkušenosti u pacientů s diabetem
Autoři: Prof. MUDr. Martin Haluzík, DrSc., prof. MUDr. Vojtěch Melenovský, CSc., prof. MUDr. Vladimír Tesař, DrSc.

Úloha kombinovaných preparátů v léčbě arteriální hypertenze
Autoři: prof. MUDr. Martin Haluzík, DrSc.

Halitóza
Autoři: MUDr. Ladislav Korábek, CSc., MBA

Terapie roztroušené sklerózy v kostce
Autoři: MUDr. Dominika Šťastná, Ph.D.

Všechny kurzy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#