https://orcid.org/0000-0002-7711-8133
Figures
Abstract
Objective
The study evaluated the socio-demographic characteristics, obstetric variables and foeto-maternal complications associated with low birth weight (LBW) in order to provide better treatment and management options.
Methods
The prospective study conducted from February, 2019 to June, 2020 recruited 312 primigravid pregnant women who reported for antenatal care in three tertiary referral hospitals in northern Ghana. Their socio-demographic, obstetric and adverse foeto-maternal outcome information were obtained with a well-structured questionnaire according to the World Health Organisation (WHO) guidelines. Participants’ blood samples were collected for haematological tests. Odds ratio [OR, 95% confidence interval (CI)] for the association between socio-demographic, obstetric characteristics, foeto-maternal complications and haematological tests in relation to LBW were assessed using logistic regression model.
Results
This study reported a LBW prevalence of 13.5%. Increasing maternal systolic blood pressure (SBP) and diastolic blood pressure (DBP) at 1st visit, before and after delivery significantly increased the odds of LBW. Preterm delivery (PTD<37 weeks) (COR = 9.92, 95% CI (4.87–2020), p<0.001), preeclampsia (PE) (COR = 5.94, 95% CI (2.96–11.94), p<0.001), blood transfusion (COR = 14.11, 95% CI (2.50–79.65), p = 0.003), caesarian delivery (COR = 3.86, 95% CI (1.96–7.58), p<0.001) and male sex neonates (COR = 2.25, 95%CI (1.14–4.47), P = 0.020) presented with increased odds of LBW. Increasing gestational age at delivery presented with 28% reduced odds of LBW (COR = 0.72, 95% CI (1.12–4.40), P = 0.023). Upon controlling for potential confounders in multivariate logistic regression, only gestational age at delivery (AOR = 0.67, 95% CI (0.47–0.96), P = 0.030) remained significantly associated with reduced odds of LBW.
Conclusion
This study found that high blood pressure at 1st visit, before and after delivery results in increased chances of delivering a baby with LBW. Furthermore, PTD<37 weeks, having PE in current pregnancy, and male sex potentiate the risk of LBW. On the other hand, increasing gestational age reduces the risk of LBW. Thus, we recommend that midwives should intensify education to pregnant women on the benefits of regular ANC visits to aid in the early detection of adverse foeto-maternal complications. We also recommend proper clinical management of pregnancies associated with an elevated blood pressure at registration. Also, maternal intrapartum blood pressure measurement could be used to predict LBW in low resourced settings.
Citation: Ahenkorah B, Sakyi SA, Helegbe G, Owiredu E-W, Fondjo LA, Ofosu W, et al. (2022) Foeto-maternal complications associated with low birth weight: A prospective multicenter study in northern Ghana. PLoS ONE 17(4): e0266796. https://doi.org/10.1371/journal.pone.0266796
Editor: Hüsniye Dinç Kaya, Istanbul Universitesi-Cerrahpasa, TURKEY
Received: November 17, 2020; Accepted: March 11, 2022; Published: April 8, 2022
Copyright: © 2022 Ahenkorah et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: Data is available at: (https://doi.org/10.6084/m9.figshare.14854449).
Funding: The author(s) received no specific funding for this work.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Low birth weight (LBW) is defined by the World Health Organization (WHO) as weight at birth less than 2500 g (5.5 lb). LBW is a significant public health problem globally and it is associated with a range of short and long-term consequences. Overall, it is estimated that 15% to 20% of all births worldwide are LBW, representing more than 20 million births per year [1]. LBW is a complex foetal complication which occurs as a result of preterm delivery (PTD<37 weeks), microsomia at term and the overlap between these two complications [2].
In sub-Saharan Africa, risk factors such as high risk pregnancies, younger and advanced maternal age, anaemia during pregnancy as well as hypertensive disorders of pregnancy including gestational hypertension, preeclampsia (PE), eclampsia and poor nutritional status of mother are widely reported to be associated with LBW [3, 4]. Progress made in reducing neonatal mortality has been slower in sub-Saharan Africa compared to any other regions in the world [5].
In 2013, 16.5% of the 11,647 neonates born in the major tertiary referral hospital in Ghana (Korle-Bu Teaching Hospital) had LBW [6]. In 2016, the prevalence of LBW neonates in Ghana was 9.69% [7]. Since then, Ghana has not recorded any significant reduction in LBW [8]. Additionally, about 46% of all LBW babies in Ghana die in the first 28 days of life [9].
Several studies evaluating factors associated with LBW have been conducted in some African countries [10–15]. However, there is paucity of current data in Ghana, particularly in the northern areas of the country where adequate health care is wanting. It is against this background that we prospectively studied the factors associated with LBW in northern Ghana. Findings from the study will provide data which will facilitate the development of policies regarding maternal and foetal health.
Methods
Study area
The study was conducted in three major referral (tertiary) hospitals in northern Ghana. The hospitals were the Tamale Teaching Hospital (TTH) in Tamale (Northern Region), the Bolgatanga Regional Hospital (RHB) in Bolgatanga (Upper East Region) and the Bawku Presbyterian Hospital (BPH) in Bawku (Upper East Region). Table 1 shows the antenatal and delivery information for the three study sites for the year 2019.
Study design and population
The study was a prospective multicenter study conducted following the STROBE checklist [16] from February, 2019 to June, 2020. The participants were primigravid pregnant women aged between 15–43 years who reported for antenatal care at the three selected hospitals. The expected sample size was based on the estimated prevalence of LBW (9.69%) [7]. Based on the formula: n = z2pq/d2; where n = minimum sample size, z = confidence limit at 95% = 1.96, p = prevalence of LBW = 0.0969, q = complimentary probability = 1-p, d = precision = 0.05, the minimum sample size required for the study was 134 participants. In this study, 312 pregnant women were recruited. The women included did not have deliveries with birth defect, gestational diabetes, still births, had singleton gestations and did not have a history of LBW (Fig 1).
Obstetric characteristics and perinatal outcomes
The obstetric characteristics evaluated were maternal age, gestational age at delivery and parity. Delivery characteristics such as mode of delivery, maternal blood pressure at booking, before delivery and after delivery were recorded. Adverse maternal outcomes were blood transfusion, labour induction, sickle cell disease (SCD) crisis, preterm delivery (PTD) <37 weeks, PE and eclampsia. Perinatal outcome indicators associated with LBW were sex of new born, birth weight and intrauterine growth retardation (IUGR) (Fig 1).
Blood pressure measurement
Using a mercury sphygmomanometer and a stethoscope, trained personnel measured the blood pressure of participants. Measurements were taken from the left upper arm after the subjects had been sitting for over 5 minutes. Two readings were documented at 15 minutes interval and the average was considered the participant’s blood pressure.
Anthropometric characteristics
Adhering to WHO standard procedure, a hospital grade electronic weighing scale (China) of capacity 150kg weight and 70~190cm height was used to measure body weight and height respectively, as previously described [17]. Body mass index (BMI) was calculated by dividing weight (kg) by height squared (m2).
Haematological tests
Haematological tests were performed by drawing 5ml of blood from veins located within the antecubital fossa. Assays conducted include ABO/Rh blood grouping, sickling test, haemoglobin electrophoresis, haemoglobin concentration at 1st visit and glucose-6-phosphate dehydrogenase (G6PD) quantitative test. ABO and Rh blood grouping was conducted by utilizing commercially prepared monoclonal anti-A, anti-B, and anti-D antisera (Agappe Diagnostics Ltd., India) according to Cheesbrough protocol [18]. Haemoglobin levels were determined using the Sysmex KX-21 N Automated Hematology Analyzer (Sysmex Corporation Kobe, Japan). Haemoglobin variants determined were AA, AS, SS & SC genotypes. This was done at an alkaline pH of 8.5 (Beijing Liuyi Instrument Factory, China).
G6PD status was determined quantitatively (RANDOX, UK). Study participants were classified as: G6PD Normal if G6PD activity was ≥ 4000 mU/gHb (≥4.00 U/gHb), G6PD Partial Defect if G6PD activity was 1000 to 3999 mU/gHb (1.00–3.99 U/gHb) and G6PD full defect if G6PD activity was <1000 mU/gHb (<1.00 U/gHb) [19].
Sources of data
Participant antenatal and delivery information outlining socio-demographic, obstetric characteristics and perinatal outcomes were obtained by trained interviewers (midwives) through structured questionnaires at time of study inclusion, at delivery and 48 hours postpartum.
Outcome
Birth weight in grams (g) was measured within 24 hours after birth and LBW was diagnosed if a neonate weighed less than 2500g [20].
Statistical analysis
Categorical variables were presented as frequencies and percentages. Continuous data were presented as mean ± SD. Logistic regression analysis was used to evaluate the risk factors associated with LBW. To determine potential factors associated with birth weight, we first performed univariate logistic regression analysis. This was followed by multivariate logistic regression analysis using the enter method for variables with p-values <0.05 after univariate analysis to identify independent risk factors. Statistical analysis was performed using Stata version 14.2, GraphPad Prism 8 and MedCalc statistical software version 19.8. The receiver operating characteristics (ROC) curve was computed at an estimated prevalence of LBW, 9.69% and confidence interval (CI) of 95%. All tests were two-sided and p-value < 0.05 was considered statistically significant.
Ethics approval and consent to participate
Ethical approval for this study was obtained from the institutional review board of the Navrongo Health Research Centre of the Ghana Health Service with approval number NHRCIRB326. Written informed consent was obtained from all participants who opted to participate after the aims and objectives of the study had been explained to them. Consent for minors were obtained from the parents/guardians. Participation was voluntary, and respondents were assured that the information obtained was strictly for research and academic purposes only and were guaranteed the liberty to opt out from the study at their own convenience.
Results
Antenatal and delivery information for the three sites for the year 2019 is represented in Table 1.
General characteristics of participants
A total of 312 pregnant women with average age and BMI of 27.22 ± 6.08 years old and 25.44 ± 6.79 kg/m2 respectively, were enrolled in the study. A higher proportion of the women enrolled in the study were of Northern ethnicity (278/312 vs. 34/312), were married (91.67%) and nulliparous (38.46%), had O positive blood group (33.94%), were of haemoglobin genotype AA (82.69%) and anaemic defined by haemoglobin level <11 g/dl at 1st ANC visit (53.85%). Majority of the participants did not deliver prematurely (96.15%), did not have PE (92.31%) and eclampsia (96.89%) in the current pregnancy. Majority of neonates had an appearance, grimace, activity and respiration (APGAR) score >7 at 1 minute (87.82%) and 5 minutes (94.23%), respectively (Table 2).
Among the 312 participants, the prevalence of Normal birth weight (NBW) and Low birth weight (LBW) were 86.5% (270/312) and 13.5% (42/312), respectively (Fig 2).
Crude (COR) and adjusted odds ratio (AOR) for factors potentially associated with LBW
Pregnant women with PTD <37 weeks (COR = 9.92, 95% CI (4.87–20.20), p<0.001), PE in current pregnancy (COR = 5.94, 95% CI (2.96–11.94), p<0.001), participants who had blood transfusion (COR = 14.11, 95% CI (2.5–79.65), p = 0.003), male sex neonates (COR = 2.25, 95% CI (1.14–4.47), p = 0.020) and caesarian section (COR = 3.86, 95% CI (1.96–7.58), p<0.001) presented with significantly higher odds of LBW. Increasing gestational age at delivery presented with 28% reduced odds of LBW (COR = 0.72, 95% CI (0.64–0.80), p<0.001). Additionally, a unit increase in systolic blood pressure (SBP) and diastolic blood pressure (DBP) at 1st visit, before delivery and post-delivery presented with significantly higher odds of LBW. Upon controlling for potential confounders in multivariate logistic regression, only gestational age at delivery (AOR = 0.67, 95% CI (0.47–0.96), p = 0.030) remained significantly associated with reduced odds of LBW (Table 3).
Diagnostic performance of systolic and diastolic blood pressure measurements at study inclusion, at delivery and 48 hours post-delivery in predicting LBW
DBP at 1st ANC visit, and at delivery and SBP at 48 hours post-delivery presented with excellent sensitivities (88.90%, 88.24% and 80.00%, respectively) and a good to moderate Area under the curve (AUC) (0.715(0.660–0.765), 0.767(0.709–0.817) and 0.671 (0.604–0.734), respectively), in predicting LBW. SBP at 1st visit had the lowest sensitivity (33.33%) but the highest specificity (90.91%) followed by SBP at delivery (78.38%). DBP at 1st visit was the least specific (45.00%) in predicting LBW (Fig 3 and Table 4).
(A) SBP at 1st visit, (B) DBP at 1st visit, (C) SBP before delivery, (D) DBP before delivery, (E) SBP after delivery, (F) DBP after delivery.
Discussion
The prevalence of LBW in this study was 13.5%. This prevalence is not very different from previously reported prevalence from similar studies conducted in southern part of Ghana by the United Nations Children’s Fund (UNICEF) and in northern Ghana by Agoringya et al. who correspondingly reported 13.0% and 13.8% prevalence, respectively [6, 21]. Contrarily, in the Brong Ahafo region, another region in the south of Ghana, Zackariah et al. reported a LBW prevalence of 11% which is lower than the prevalence reported in our study [8]. Furthermore, varying prevalence rates have been reported in other African countries. In Zimbabwe, Feresu et al. found a LBW prevalence of 16.7% [3]. Mengesha et al. reported a prevalence of 10.5% in Ethiopia [13]. In Northern Ethiopia, Gebregzabiherher et al. found a LBW prevalence of 10% [22]. Oladeinde et al. in Nigeria found a LBW prevalence of 6.3% [23]. Whereas, the prevalence of LBW in Togo in 2015 was 16.1% [24]. In 2018, a study by Zhifei et al. found LBW prevalence of 10.2% in Ghana and prevalence of 13.4%, 12.1%, 15.7% and 10% in Burkina Faso, Malawi, Senegal and Uganda, respectively [24].
In Ghana and sub-Saharan Africa, there is paucity of data on the association between birth weight and maternal blood pressure. The blood pressure measurements presented with a good predictive power for LBW. Our finding suggests that in low resourced settings, elevation in maternal blood pressure measurements at 1st visit and delivery could serve as an inexpensive predictor of LBW. In contrast, Hovi et al. in Finland and Taylor et al. in Great Britain found no significant association between maternal high blood pressure and LBW [25, 26]. These findings show that additional studies on the potential association between LBW and maternal blood pressure is required.
In this study, PE was associated with increased odds of LBW. This finding could be due to the mechanistic relationship PE has with birth weight. An abnormally implanted placenta which predisposes a woman to PE is also implicated in hypo-perfusion culminating in hypoxia which restricts fetal growth leading to low birth weight [27, 28]. The findings concurs with the findings of Bonsaffoh et al. in Ghana who showed a strong association between PE and adverse perinatal outcomes such as LBW, respiratory distress, intensive care unit admission and intrauterine growth restriction [29]. In Tanzania, Mitao and colleagues also reported a relationship between LBW and several risk factors such as PE, eclampsia, chronic hypertension, caesarian section and low maternal BMI [14].
First trimester haemoglobin concentration of pregnant women who delivered LBW babies were not significantly different from those who delivered NBW babies in this study. This is because the anaemic condition at this stage of pregnancy is often resolved with the administration of haematinics or by dietary modifications. This finding is in variance with the findings of Vanek and his colleagues in Israel who outlined an association between hypertensive disorders of pregnancy and several risk factors such as blood transfusions, labour induction, hydramnios and gestational diabetes resulting in low birth weight [30].
We also found caesarian delivery and PTD<37 as risk factors for LBW. Our study agrees with Chen et al., who found LBW to be associated with maternal and fetal complications necessitating caesarian delivery in avoidance of intrauterine foetal demise, still birth and neonatal death at term [31]. Chronic intrauterine hypoxia and growth restriction characterizes LBW as a result of an impaired oxygen and nutrient transfer from maternal compartment to foetus. Furthermore, increasing gestational age at delivery (in weeks) consistently reduced the odds of LBW even after multivariate adjustment. The mechanism underlying the birth of premature neonates still needs further scientific investigations. We hypothesise that preterm infants are mostly underweight since they do not have adequate time for optimum intrauterine fetal growth. As a result, term delivery results in normal birth weight. Consistent with our study findings is a WHO multi-country survey on maternal and new born health by Ota et al, who related preterm deliveries (early deliveries) to gestational hypertensions, PE and eclampsia [32]. This is because complications associated with hypertensive disorders of pregnancies resolve only after delivery of the placenta hence caesarean delivery before term is the best option resulting in neonates with LBW. Furthermore, similar studies have related preterm delivery to LBW due to subclinical infections culminating in membrane rupture, to micronutrient deficiencies and placental abnormalities as a result of increased serum alpha-fetoprotein levels [33–35].
Our study found the male sex to be associated with higher odds of LBW. On the contrary, Tshotetsi et al., in South Africa and Ayuurebobi et al., in Ghana could not find an association between male sex and LBW [36, 37]. Similar studies found the male sex to be associated with higher risk for LBW [38, 39]. Roy et al. in India found the male sex to be disadvantaged due to its poor perinatal outcomes and higher risk of LBW leading to septicaemia and neonatal demise [38]. Stevenson et al., in the United States also found a higher mortality and postnatal complications in very LBW males than in females [39]. Higher proportions of these male neonates in their cohort had lower Apgar scores, respiratory distress syndrome or lung related injuries and disabilities, and were generally less stable than female neonates.
Strength and limitation of the study
The study included several risk factors for LBW; socio-demographic, obstetric characteristics, haematological tests and foeto-maternal complications of pregnancy in one study. Additionally, the relationship between foeto-maternal complications of pregnancies such as PE, PTD<37 weeks, blood transfusion, caesarian deliveries and LBW were evaluated. Our study is limited due to the small sample size. Additionally, a substantial number of pregnant women who deliver in the 3 tertiary hospitals used for the study typically register for antenatal care elsewhere and are referred to tertiary hospitals to deliver when there is any suspicion of possible complications. Hence, care should be taken when interpreting the data since the results may not be generalizable to the entire population
Conclusion
This study found that high blood pressure at 1st visit, before and after delivery results in increased chances of delivering a baby with LBW. Furthermore, PTD<37 weeks, having PE in current pregnancy, male sex and blood transfusion potentiate the risk of LBW. On the other hand, increasing gestational age reduces the risk of LBW. Thus, we recommend that midwives should intensify education to pregnant women on the benefits of regular ANC visits to aid in the early detection of adverse foeto-maternal complications. We further recommend proper clinical management of pregnancies associated with an elevated blood pressure at registration. Also, maternal intrapartum blood pressure measurement could be used to predict LBW in low resourced settings.
Acknowledgments
The authors express their gratitude to all staff and patients of the Tamale Teaching Hospital, Bolgatanga Regional Hospital and the Bawku Presbyterian Hospital who actively participated in the study.
References
- 1.
WORLD HEALTH ORGANIZATION. What’s at stake Low Birth Weight Policy Brief. Who. 2014; 1–7.
- 2. Risnes KR, Vatten LJ, Baker JL, Jameson K, Sovio U, Kajantie E, et al. Birthweight and mortality in adulthood: a systematic review and meta-analysis. Int J Epidemiol. 2011;40: 647–661. pmid:21324938
- 3. Feresu SA, Harlow SD, Woelk GB. Risk factors for low birthweight in Zimbabwean women: A secondary data analysis. PLoS One. 2015;10. pmid:26114867
- 4. Chaman R, Amiri M, Khosravi A, Raei M, Ajami M-E, Sadeghian A. Bajo peso al nacer y sus factores de riesgo en el noreste de Irán. Iran J Pediatr. 2013;23: 701–4. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4025130&tool=pmcentrez&rendertype=abstract pmid:24910751
- 5. Abubakari A, Kynast-Wolf G, Jahn A. Prevalence of abnormal birth weight and related factors in Northern region, Ghana. BMC Pregnancy Childbirth. 2015;15: 335. pmid:26670886
- 6.
The State of the World’s Children 2013: Children with Disabilities | UNICEF Publications | UNICEF. [cited 9 Apr 2020]. Available: https://www.unicef.org/publications/index_69379.html
- 7. Agbozo F, Abubakari A, Der J, Jahn A. Prevalence of low birth weight, macrosomia and stillbirth and their relationship to associated maternal risk factors in Hohoe Municipality, Ghana. Midwifery. 2016;40: 200–206. pmid:27474932
- 8. Adam Z, Ameme DK, Nortey P, Afari EA, Kenu E. Determinants of low birth weight in neonates born in three hospitals in Brong Ahafo region, Ghana, 2016- an unmatched case-control study. BMC Pregnancy Childbirth. 2019;19. pmid:31096938
- 9.
Ghana Statistical Service. Ghana Multiple Indicator Cluster Survey 2011 [FR262]—FR262.pdf. 2012 [cited 9 Apr 2020]. Available: https://microdata.worldbank.org/index.php/catalog/2046
- 10. OM Muchemi EEAM. Factors associated with low birth weight among neonates born at Olkalou District hospital, Central region. Kenya Pan African Med J. 2015;20: 108–114.
- 11. BM Zeleke MZNM. Incidence and correlates of low birth weight at a referral hospital in northwest. Ethiop Pan African Med J. 2012;12: 4.
- 12. He Z, Bishwajit G, Yaya S, Cheng Z, Zou D, Zhou Y. Prevalence of low birth weight and its association with maternal body weight status in selected countries in Africa: a cross-sectional study. BMJ Open. 2018;8: 20410. pmid:30158218
- 13. Mengesha HG, Wuneh AD, Weldearegawi B, Selvakumar DL. Low birth weight and macrosomia in Tigray, Northern Ethiopia: Who are the mothers at risk? BMC Pediatr. 2017;17. pmid:28606178
- 14. Mitao M, Philemon R, Obure J, Mmbaga BT, Msuya S, Mahande MJ. Risk factors and adverse perinatal outcome associated with low birth weight in Northern Tanzania: A registry-based retrospective cohort study. Asian Pacific J Reprod. 2016;5: 75–79.
- 15. Demelash H, Motbainor A, Nigatu D, Gashaw K, Melese A. Risk factors for low birth weight in Bale zone hospitals, South-East Ethiopia: A case-control study. BMC Pregnancy Childbirth. 2015;15: 264. pmid:26463177
- 16. Epidemiologico C del conocimiento. STROBE Statement—Checklist of items that should be included in reports of. Univ los Andes. 2020; 1–2. Available: http://files.figshare.com/422353/Checklist_S1.doc
- 17. Lee J-W, Lim N-K, Baek T-H, Park S-H, Park H-Y. Anthropometric indices as predictors of hypertension among men and women aged 40–69 years in the Korean population: the Korean Genome and Epidemiology Study. BMC Public Health. 2015;15: 140. pmid:25886025
- 18.
England MC-PI, 2000 U. Parasitological tests. District laboratory practices in tropical countries.
- 19. Owusu R, Asante KP, Mahama E, Awini E, Anyorigiya T, Dosoo D, et al. Glucose-6-phosphate dehydrogenase deficiency and haemoglobin drop after sulphadoxine-pyrimethamine use for intermittent preventive treatment of malaria during pregnancy in Ghana—A cohort study. PLoS One. 2015;10. pmid:26327623
- 20.
Organization WH. Guidelines on optimal feeding of low birth-weight infants in low-and middle-income countries. World Health Organization; 2011.
- 21. Agorinya IA, Kanmiki EW, Nonterah EA, Tediosi F, Akazili J, Welaga P, et al. Socio-demographic determinants of low birth weight: Evidence from the Kassena-Nankana districts of the Upper East Region of Ghana. PLoS One. 2018;13. pmid:30427882
- 22. Gebregzabiherher Y, Haftu A, Weldemariam S, Gebrehiwet H. The Prevalence and Risk Factors for Low Birth Weight among Term Newborns in Adwa General Hospital, Northern Ethiopia. Obstet Gynecol Int. 2017;2017. pmid:28744313
- 23. Oladeinde HB, Oladeinde OB, Omoregie R, Onifade AA. Prevalence and determinants of low birth weight: The situation in a traditional birth home in Benin city, Nigeria. Afr Health Sci. 2015;15: 1123–1129. pmid:26958012
- 24.
Botswana Nutrition Profile—Global Nutrition Report. [cited 22 Jul 2020]. Available: https://globalnutritionreport.org/resources/nutrition-profiles/africa/western-africa/togo/
- 25. Taylor SJC, Hird K, Whincup P, Cook D. Relation between birth weight and blood pressure is independent of maternal blood pressure [5]. British Medical Journal. 1998. p. 680. pmid:9728009
- 26. Hovi P, Vohr B, Ment LR, Doyle LW, McGarvey L, Morrison KM, et al. Blood Pressure in Young Adults Born at Very Low Birth Weight: Adults Born Preterm International Collaboration. Hypertension. 2016;68: 880–887. pmid:27572149
- 27. Kintiraki E, Papakatsika S, Kotronis G, Goulis DG, Kotsis V. Pregnancy-Induced hypertension. Hormones. Hellenic Endocrine Society; 2015. pp. 211–223. pmid:26158653
- 28. Jammeh A, Sundby J, Vangen S. Maternal and obstetric risk factors for low birth weight and preterm birth in rural Gambia: a hospital-based study of 1579 deliveries. Open J Obstet Gynecol. 2011;01: 94–103.
- 29. Adu-bonsaffoh K, Ntumy MY, Obed SA, Seffah JD. Perinatal outcomes of hypertensive disorders in pregnancy at a tertiary hospital in Ghana. 2017; 1–7. pmid:29157196
- 30. Vanek M, Sheiner E, Levy A, Mazor M. Chronic hypertension and the risk for adverse pregnancy outcome after superimposed pre-eclampsia. Int J Gynecol Obstet. 2004;86: 7–11. pmid:15207662
- 31. Chen Y, Wu L, Zhang W, Zou L, Li G, Fan L. Delivery modes and pregnancy outcomes of low birth weight infants in China. J Perinatol. 2016;36: 41–46. pmid:26540243
- 32. Ota E, Ganchimeg T, Morisaki N, Vogel JP, Pileggi C, Ortiz-Panozo E, et al. Risk Factors and Adverse Perinatal Outcomes among Term and Preterm Infants Born Small-for-Gestational-Age: Secondary Analyses of the WHO Multi-Country Survey on Maternal and Newborn Health. Lambalk CB, editor. PLoS One. 2014;9: e105155. pmid:25119107
- 33.
Scholl T, Hediger M, … RF-TA journal, 1992 undefined. Anemia vs iron deficiency: increased risk of preterm delivery in a prospective study. academic.oup.com. [cited 29 May 2021]. Available: https://academic.oup.com/ajcn/article-abstract/55/5/985/4715164
- 34.
Gibbs R, Romero R, Hillier S, … DE-A journal of, 1992 undefined. A review of premature birth and subclinical infection. Elsevier. [cited 29 May 2021]. Available: https://www.sciencedirect.com/science/article/pii/000293789291628N
- 35. Weiner CP, Grant SS, Williamson RA. Relationship Between Second Trimester Maternal Serum Alpha-Fetoprotein and Umbilical Artery Doppler Velocimetry and Their Association with Preterm Delivery. Am J Perinatol. 1991;8: 263–268. pmid:1720619
- 36. Tshotetsi L, Dzikiti L, Hajison P, Feresu S. Maternal factors contributing to low birth weight deliveries in Tshwane District, South Africa. PLoS One. 2019;14. pmid:30822317
- 37. Ayuurebobi Ae-Ngibise K, Wylie BJ, Boamah-Kaali E, Jack DW, Oppong FB, Chillrud SN, et al. Prenatal maternal stress and birth outcomes in rural Ghana: sex-specific associations. [cited 17 Oct 2020]. pmid:31664941
- 38. Roy P, Kumar A, Kaur IR, Faridi MMA. Gender differences in outcomes of low birth weight and preterm neonates: The male disadvantage. Journal of Tropical Pediatrics. Oxford University Press; 2014. pp. 480–481. pmid:25096219
- 39. Stevenson DK, Tyson JE, Korones SB, Bauer CR, Stoll BJ, Papile LA, et al. Sex differences in outcomes of very low birthweight infants: The newborn male disadvantage. Arch Dis Child Fetal Neonatal Ed. 2000;83: F182. pmid:11040165