Abstract
Objective:
To describe the prevalence, by weeks of gestation, of post-maturity signs in newborns by ethnic origins.
Study design:
Observational cohort study (2001–2018), of all consecutive singleton births delivered at Center Hospitalier Universitaire Hospitalier Sud Reunion’s maternity (Reunion Island, French overseas department, Indian Ocean). The presence of clinical post-maturity signs was recorded by a week of gestation using Clifford’s clinical post-maturity signs in newborns (desquamation, dry skin, wrinkling fingers and cracked skin).
Results:
Of the 67,463 singleton births during the period, 58,503 newborns were from Reunion island, 5756 were of European origin (mainland France), and 4061 newborns from the archipelago of Comoros (North of Madagascar). Mean duration of gestation was 276 days in Caucasian women, 272 days in Comorian mothers and 273 days in Reunionese (p<.001). Post-maturity is defined by WHO as gestation greater than 293 days (41 weeks + 6 days). At 41 weeks (287 days) 12.1% of Caucasian babies presented post-maturity signs and 22.4% meconium-stained liquid versus respectively, 22.8 and 27.1% in Reunionese and 44 and 39.8% in Comorians (p<.001).
Conclusion:
Among African (Black) pregnancies, duration of gestation was approximately 7 days shorter than in Caucasian (White) pregnancies. In the Reunionese intermixed population and Comorians, the gestation was shorter by 3–4 days. Black newborns presented severe clinical post-maturity signs beginning around 40 weeks and 4–6 days, while it was 1 week later in white infants. Consequences of these differences, with respect to clinical outcomes, are discussed.
Keywords: Meconium staining, neonatal outcome, post-maturity, preterm births, racial disparity
Introduction
In the 1950s perinatal mortality demonstrated an enigmatic U shaped curve. Higher mortality at the lowest gestational ages and higher mortality at the highest gestational ages. At that time, post-maturity was defined as pregnancies lasting longer than 300 days or more [1]. The incidence of post-maturity was approximately 6% yet accounted for 30% of perinatal deaths. Conversely, the incidence of prematurity was approximately 9% and accounted for 36% of perinatal deaths. In addition, post-mature intrauterine fetal deaths accounted for 10% of this mortality [1,2].
Currently, the World Health Organization (WHO) defines post-term pregnancies as pregnancies that extend beyond 293 days (41 weeks and 6 days, from the first day of the last menstrual period-LMP) [3]. While approximately 10% of normal spontaneous vaginal deliveries are postdated (beyond 293 days), the clinical definition, by ethnicity, continues to be controversial. Clifford, in 1954, described the clinical post-maturity signs in newborns: dryness of the skin, desquamation, wrinkling fingers, and, at an extreme stage, also cracked skin in the folds [1]. As such, the clinical decision for induction of delivery for post-term pregnancies, by ethnicity, remains unresolved [4].
The aim of this study, spanning over 18 years, has been to record the signs of post-maturity, by gestational age and ethnicity. Since 2001, all births beyond 22-week gestation have been entered into an epidemiological perinatal database which contained information on obstetrical risk factors, description of deliveries and neonatal outcomes (see pediatric items in the Supplementary Appendix).
Materials and methods
From 1 January 2001 to 30 June 2018, the hospital records of all who women delivered at the University south Reunion Island (approximately 4300 births per year) were abstracted in standardized fashion. All data were entered into an epidemiological perinatal database that contained information on obstetrical risk factors, description of deliveries and neonatal outcomes.
As participants in the French national health care system, all pregnant women in Reunion Island have their prenatal visits, biological and ultrasound examinations, and anthropological characteristics recorded in their maternity booklet. Accessibility to maternity services is provided free of charge. Women have in average 9 prenatal visits per pregnancy and 4 ultrasonographic examinations. The population of Reunion is characterized by the multiethnic origin of inhabitants: Africa and intermixed population (65%), European (12%), Indian (20%) and Chinese (3%).
Guadeloupe (data 1993–1995) is a French overseas department in the Caribbean, where 80% of the population is from Black-African descent. Comoros is an archipelago of 4 islands (where Mayotte is also a French overseas department) in the Indian Ocean, inhabited by 95–100% Black-African population. Reunionese women comprise a melting pot of African and African intermixed populations, Dravidian Indian (South-India, Madras, and Pondicherry) and very few Chinese origin. Therefore “Reunion origin” comprises roughly African intermixed origin for approximately 75% and Dravidian Indians (South India, Tamils) for 25%.
The French Constitution forbids ethnicity, religion or political opinions of the citizens on viral records. Therefore, the geographical origin of the mother is used as a proxy for ethnicity.
This study was derived from de-identified records as was exempt from approval of institutional review board (Comité de Protection des Personnes Sud-Ouest et Outre Mer III). In addition, following French guidelines, written consent was not needed for this study.
Epidemiological data were recorded and analyzed using software EPI-INFO 7.1.5 (2008, CDC, Atlanta, OMS) software, EpiData 3.0 and EpiData Analysis V2.2.2.183 (Denmark).
Results
There were 72,393 deliveries after 21-week gestation at the south Reunion maternity service during the period and 73,848, that comprised live-born singleton and multiple newborns. After exclusion of multiple births (N = 1455 pregnancies and 2942 infants), in utero singleton fetal deaths (N = 957), women from Madagascar (N = 1089), from Mauritius (N = 543), from “other places” (N = 677), and unknown origin (N = 37), the study population consisted of 67,463 singleton live-born newborns. During the period, there were 58,503 singletons whose mothers’ were from Reunion (all ethnic groups), 5756 from European origin (mainland France), and 4061 from the island of Mayotte or the other islands of the Comoro archipelago. It is of note that European mothers are permanent residents of the island, and therefore, live equivalently in the tropical surroundings like all others in this study.
Table 1 represents the mean gestation length by different maternal origins: European babies, and thus, their gestational duration, have been used as the reference based on the WHO definition. There was a shorter mean term of 4–8 days for Comorian and Guadeloupean (African descent) babies as compared to Europeans (p < .0001). Reunionese babies, as an intermixed African population have a shorter duration of gestation of 3 days (p < .0001). At week 41 (287 days), 14% European had not yet delivered versus approximately 8% of the others.
Table 1.
Mean gestation length (weeks and days) by different ethnicities, singleton pregnancies.
| Europeans Réunion N = 5756 | Réunion (all ethnic groups) N = 58,503 | Mayotte & Comores N = 4061 | Guadeloupeans 1993–1995 N = 5558 | |
|---|---|---|---|---|
| Mean terma (weeks gest.) | 38.87 ± 2.3 | 38.38 ± 2.1 # | 38.35 ± 2.2 # | 38.0 ± 2.6 # |
| Mean term by LMP (weeks)b | 39.48 ± 1.7 N = 2390 | 39.02 ± 2.1 N = 23916 # | 38.88 ± 2.0 N = 1468 # | 38.2 ± 2.7 N = 3673 # |
| Mean duration of gestation in daysb | 276 ± 12.2 N = 2466 | 273 ± 13.8 N = 23,485 # | 272 ± 14.1 N = 1468 # | 268 ± 18.9 N = 3673 # |
| Reference | –3 days | –4 days | –8 days | |
| Clinical signs of postmaturity newborns (%) | 6.6% | 9.2% OR 1.4 [1.3–1.6]# | 19.6% OR 3.5 [3.1–4.0]# | 30.6% # |
| Mean birthweight (g) | 3173 ± 560 Reference | 3073 ± 566 100 g# | 3084 ± 570 87g# | 3029 ± 634 125g# |
| Prematurity < 37SA (%) | 7.1% | 10.3% OR 1.5 [1.35–1.67]# | 9.8% OR 1.42 [1.23–1.64]# | 14.7% # |
| % of women having not yet delivered at 41 weeks + 0 | 14.0% Reference | 7.7% # | 7.6% # | 8.9% # |
Data from Réunion 2001–2018 (Indian Ocean) and Guadeloupe 1995–1997 (French-West-Indies), 2 French Overseas departments.
Completed weeks gestation.
Women knowing their LMP date, confirmed by ultrasonography.
p < .0001 as compared with Europeans.
Table 2 and Figure 1 shows the evolution of the 4 different post maturity signs (dry skin, desquamation, wrinkling fingers, cracked skin) per week of gestation and maternal origins. The last line of Table 2 ad Figure 2 shows the incidence of meconium staining at birth by different populations. All these results show a gradually growing incidence of post maturity signs per week of gestation, but they differ by maternal origins.
Table 2.
Incidence of postmaturity signs in different population from 37 to 42 weeks gestation (singletons).
| 37 weeks | 38 weeks | 39 weeks | 40 weeks | 41 weeks | 42 weeks | |||
|---|---|---|---|---|---|---|---|---|
| 1) | At least one | European N = 5367 (%) | 6/443 (1.5) | 30/1021 (3.0) | 82/1627 (5.1) | 154/1461 (10.6) | 94/784 (12.0) | 5/31 (16.1) |
| clinical postmaturity | Réunion N = 51,719 (%) | 184/5844 (3.1) | 732/13177 (5.6) | 1577/16767 (9.4) | 1718/11428 (15.0) | 1023/4402 (23.3) | 26/101 (25.7) | |
| signs in newborns | Comores N = 3692 (%) | 42/421 (10.0) | 127/1016 (12.6) | 248/1185 (21.0) | 228/753 (30.3) | 136/299 (45.6) | 13/18 (72) | |
| 2) | Dry skin (dehydration) | European (%) | 6 (1.4) | 28 (2.7) | 70 (4.3) | 133 (9.1) | 83 (10.6) | 5 (16.1) |
| in newborns | Réunion (%) | 158 (2.7) | 648 (4.9) | 1412 (8.4) | 1571 (13.7) | 933 (21.2) | 23 (22.8) | |
| Comoros (%) | 42 (10.0) | 117 (11.5) | 232 (19.6) | 215 (28.6) | 131 (43.8) | 11 (61) | ||
| 3) | Desquamation | European (%) | 4 (0.9) | 16 (1.6) | 53 (3.3) | 103 (7.0) | 71 (9.4) | 4 (12.9) |
| in newborns | Réunion (%) | 116 (2.2) | 527 (4.0) | 1143 (6.8) | 1287 (11.3) | 817 (18.6) | 22 (21.8) | |
| Comoros (%) | 35 (8.3) | 96 (9.4) | 183 (15.4) | 188 (25.0) | 120 (40.1) | 12 (66.7) | ||
| 4) | Wrinkling fingers | European (%) | 2 (0.5) | 21 (2.1) | 56 (3.4) | 109 (7.5) | 65 (8.3) | 2 (6.5) |
| in newborns | Réunion (%) | 129 (2.2) | 527 (4.0) | 1109 (6.6) | 1187 (10.4) | 796 (18.1) | 21 (20.8) | |
| Comoros (%) | 32 (7.6) | 78 (7.7) | 173 (14.6) | 176 (23.4) | 109 (36.5) | 11 (61.1) | ||
| 5) | Cracked skin | European (%) | 1 (0.2) | 4 (0.4) | 19 (1.2) | 44 (3.0) | 28 (3.6) | 0 (0) |
| (dehydration++) | Réunion (%) | 59 (1.0) | 199 (1.5) | 473 (2.8) | 527 (4.6) | 366 (8.3) | 9 (8.9) | |
| Comoros (%) | 18 (4.3) | 55 (5.4) | 97 (8.2) | 101 (13.4) | 67 (22.4) | 10 (55.6) | ||
| 6) | Meconium staining | European (%) | 20 (4.5) | 77 (7.5) | 222 (13.6) | 309 (21.1) | 176 (22.4) | 8 (25.8) |
| At delivery | Réunion (%) | 373 (6.4) | 1358 (10.3) | 2839 (16.9) | 2752 (24.1) | 1198 (27.2) | 23 (22.8) | |
| Comoros (%) | 44 (10.5) | 193 (19.0) | 310 (26.2) | 259 (34.4) | 119 (39.8) | 13 (72.2) |
Figure 1.
Clinical postmaturity signs by different populations.
Figure 2.
Incidence of meconium staining at birth by week gestation and ethnicity (35 weeks onward).
Table 3: Using week 41 as a reference (i.e. 287–293 days, which is below the WHO definition of post-maturity: 294 days and plus), Reunionese babies had twice and Black-Comorians almost 4 times more post-maturity signs than Europeans. Further, Reunionese babies had a 25% and Black-Comorians 77% increase in meconium staining at birth.
Table 3.
Week 41 (day 287–day 293) only. Clinical post maturity signs in newborns (OR calculated with European newborns as reference).
| Europeans (reference) N = 784 | Réunion N = 4402 | Odds ratios [CI] | p Value | Comoros N = 299 | Odds ratios [CI] | p Value | |
|---|---|---|---|---|---|---|---|
| Presenting at least one postmaturity sign (%) | 94 (12.2) | 1023 (23.3) | 2.22 [1.8–2.8] | 0.0001 | 136 (45.6) | 6.14 [4.5–8.4] | .0001 |
| Desquamation (%) | 74 (9.4) | 817 (18.6) | 2.19 [1.7–2.8] | 0.0001 | 120 (40.3) | 6.47 [4.6–9.0] | .0001 |
| Dry skin (%) | 83 (10.6) | 933 (21.2) | 2.27 [1.8–2.9] | 0.0001 | 131 (44.0) | 6.63 [4.8–9.2] | .0001 |
| Wrinkling fingers (%) | 65 (8.3) | 796 (18.1) | 2.44 [1.9–3.2] | 0.0001 | 109 (36.6) | 6.38 [4.5–9.0] | .0001 |
| Cracked skin (%) | 28 (3.6) | 366 (8.3) | 2.45 [1.7–3.6] | 0.0001 | 67 (22.5) | 7.83 [4.9–12.5] | .0001 |
| Meconium staining (%) | 176 (22.4) | 1198 (27.2) | 1.29 [1.1–1.6] | 0.0001 | 118 (39.6) | 2.26 [1.7–3.0] | .0001 |
| Presence at birth pediatrician (%) | 148 (19.4) | 1079 (25.9) | 1.45 [1.2–7.8] | 0.0001 | 67 (23.8) | 1.30 [0.9–1.8] | .11 |
| Abnormal fetal # Monitoring (%) | 135/778 (17.4) | 1046/4329 (24.2) | 1.52 [1.2–1.9] | 0.0001 | 60/286 (21.0) | 1.26 [0.9–1.8] | .17 |
Abnormal fetal cardiac monitoring during delivery: Dip2, bradycardia (10 mn), micro-oscillating fetal heart rate.
Figure 3. With respect to birth weight, all babies had the same growth regardless of the origin of the mother. The global 100 g mean difference between non-Europeans and European babies could be due to the “week or half-week missing” in the different durations of gestation.
Figure 3.
Fetal growth (singletons live-birth) by week of gestation (mean birthweight) and by origin: Réunion, Guadeloupe, Comores, Europe, University’s maternity South-Reunion 2001–2018, Guadeloupe 1993–1995.
Figure 4 is a photograph of two babies presenting all post-maturity signs (including the last step cracked skin). A Black baby (Comoros archipelago) has all these signs at 40 weeks + 6 days, while the European baby (mainland France) at 41 weeks + 4 days (with confirmed LMP dates for these two mothers and confirmed by ultrasonographies at 10–12-week gestation).
Figure 4.
Two newborns with all signs of postmaturity (and cracked skin). European 41 weeks + 4 days, Comorian 40 weeks + 6.
Discussion
This study demonstrates that post maturity signs in nonwhite newborns were shifted on the left by approximately one week as compared with Europeans. In Table 1, the data show that at 41 weeks 14% of European mothers had not delivered as compared to 8% for the other populations (p < .001).
In a population-based study on 475,000 births in Sweden, Oberg et al. reported that at 41 weeks 21% of Swedish women had not yet delivered, and 5.5% at 42 weeks [5]. That Indian-ocean-origin women in Reunion deliver 3–4 days before their European counterparts (Table 1) and many of these newborns were labeled as “unrecognized post-term” (Omigbodun & Adewuyi [6]).
Table 1 and Figure 1 suggest that at 41 weeks, 3.6% of European babies present the most severe signs of post-maturity (cracked skin, last stage of severe dehydration), as compared to 8.3% in Reunionese (intermixed population) and 22% among Black-Comorian babies.
Meconium staining has been considered an additional clinical marker of fetal maturity [7,8].
The authors of this manuscript reported two decades ago that Black-African descent was an independent risk factor for meconium staining at birth (adjusted OR 1.5, p < .001) [7]. Moreover, this paper described an identical pattern of meconium staining from 37 weeks to 42 as seen in Figure 2 in the present study.
This current manuscript is the first to report, at this scale, longitudinal clinical observation of post-maturity signs in newborns.
The debate on the differential duration of gestation between ethnicities has been raised by Henderson and Kay some five decades ago [9] and revisited in the 1990s [6,10,11]. Studies from the 1980–1990s have reported the same conundrum: prematurity rates were far higher in black pregnancies than whites, but, specific-morbidity for each week of gestation below 34 weeks was better in black newborns than in whites [12–15]. Studies made in the 1990s are fundamental and irreplaceable as they cannot absolutely be reproduced. Data from this epoch reported results at an earlier time where (1) surfactant therapy did not exist, and therefore babies presenting hyaline membrane diseases were very sick (an average of 1 week of intubated ventilation with oxygen therapy) and (2) maternal corticoid therapy for fetal lung maturation did not exist.
This may be the explanation of the findings of a recent paper where the authors could not find a survival advantage among Black preterm neonates “as described in cohorts from previous decades” (their data being from 2002 to 2008 in 12 different states in the USA [16]). Coming back to the 1990s studies, reports in the USA and the Caribbean showed that fetal maturation (when maternal corticosteroid therapy did not exist) occurred much earlier in Black newborns with respect to the fundamental viability-marker which is the lung fetal maturation [17,18]. Hyaline membrane disease almost vanished after 32 weeks in black newborns, and not after the 34th week in white newborns [17].
The higher rate of prematurity in black women has been extensively reported in the literature, especially by US scholars. Suggestions for this disparity range from environmental and genetic [19,20], socioeconomical [21] or stressful life factors [22–24]. Goldenberg et al. in 1996 stated that medical, psychosocial, and behavioral risk factors could not explain the increased risk for low birth weight among black women [25]. Recently, Loftin et al., with data from 294,000 births in Ohio, asserted that clinical markers clearly supported the notion that “evidence for different gestational lengths” between whites and blacks [26]. They argued that black and white neonates have similar frequency distribution of neonatal morbidity in all the spectrum of gestation weeks, but the curve for black births was systematically shifted to the left by 1 week.
They also reported that neonatal morbidity was lower in black newborns before 37 weeks, but became higher after 37 weeks. This rise in risk has also been described by Mohamed [27] finding that male sex and black race were associated with an increased prevalence of term birth asphyxia.
Loftin et al. stated also that the lowest morbidity for black neonates was when the birth occurred at 38 weeks, while it is at 39 weeks in white newborns [26]. This persistent 1-week shift to the left in black newborns was viewed and an indication for a shorter gestational length. They then also concluded that post-term risk of adverse outcome occurs at an earlier gestational age in black than in white mothers. Data shown in this study are in line with this view.
Reflecting on the whole spectrum of gestation duration, if post-maturity syndrome in blacks occurs at 41 weeks (287 days), then we may extend the concept that prematurity should be defined at 36 weeks in black pregnancies and not at 37 weeks. In Réunion Island, the prematurity rate is also higher (11.4%) than among European women living on the territory (8%). If a prematurity threshold is defined at the 36th week, this Reunionese rate becomes similar (7.3%). This may be also in line with a recent WHO study arguing that definition of low-birthweight should be different (<2200 g in Africa, <2100 g in Asia, <2200 g in Latin America) between different populations, and no longer defined as the universal threshold below 2500 g [28]. Finally, it is of note that in this 18-year survey, European mothers were permanent residents of the island and exposed to the exact same climate than other populations [29].
Conclusion
In Black African pregnancies duration of gestation being approximately 7 days shorter than in white pregnancies, over going 41-week gestation (287 days) is deleterious. The universal WHO definition of post-maturity seems inadequate for these populations. In their recent study, Keulen et al. [4] report that “around 85% of participating women were of white ethnicity”. In our experience of Reunionese intermixed population (European and African), the frame is intermediary: shorter duration of gestation of 3–5 days, but, practically the threshold of the 41st week (287 days) to induce deliveries to avoid the post-maturity problem seems valid. Meanwhile, this study demonstrates that black newborns present severe clinical post-maturity signs for 40 weeks and 4–6 days, while it is 1 week later in white infants.
Supplementary Material
Acknowledgements
No special funding besides the normal existence of the perinatal database.
Footnotes
Disclosure statement
No potential conflict of interest was reported by the authors.
Data availability
Accessible under request.
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