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ORIGINAL RESEARCH |
From the Department of Neonatology, Lis Maternity Hospital, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel; and Magella Medical Associates, P.A., Dallas, Texas.
Address reprint requests to: Francis B. Mimouni, MD, Department of Neonatology, Lis Maternity Hospital, Tel Aviv-Sourasky Medical Center, 6 Weizman Street, Tel Aviv 64239, Israel, E-mail: mimouni{at}tasmc.health.gov.il
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Abstract |
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Methods: We compared absolute nucleated RBC counts taken during the first 12 hours of life in two groups of term, vaginally delivered, AGA infants, one group born to mothers who smoked during pregnancy (n = 30) and the other born to mothers who did not smoke (n = 30). We excluded infants of women with diabetes, hypertension, or alcohol or drug abuse, and infants with heart rate abnormalities, hemolysis, blood loss, or chromosomal anomalies.
Results: There were no differences between the groups in birth weight, gestational age, maternal age, gravidity, parity, maternal analgesia during labor, 1- and 5-minute Apgar scores, corrected white blood cell counts, lymphocyte counts, or hematocrits. The median absolute nucleated RBC count in infants of smoking mothers was 0.5 x 109/L (range 0 to 5.0) versus 0.0005 x 109/L (range 0 to 0.6) in nonsmoking controls (P < .002). Regression analysis that included Apgar scores, gestational age, and number of cigarettes smoked per day showed a significant correlation of absolute nucleated RBC count only with the number of cigarettes smoked per day (P < .001).
Conclusion: At birth, term AGA infants born to smoking mothers have increased circulating absolute nucleated RBC counts compared with controls. The absolute nucleated RBC count in newborns correlates with the number of cigarettes smoked during pregnancy.
Cigarette smoking during pregnancy is a major risk factor for the fetus and infant. Maternal smoking significantly increases the risks of spontaneous abortion and preterm or low birth weight delivery.1 Smoking appears to restrict growth in the third trimester2 and to increase infant mortality rates, and it is associated with increased neonatal morbidity such as neonatal asphyxia, intraventricular hemorrhage,3 reduced lung function, and sudden infant death syndrome.4 Maternal cigarette smoking during pregnancy also increases the risk of neurodevelopmental impairment during later childhood.5 Although the mechanism of fetal injury appears to have many factors, it is likely that chronic fetal hypoxia affects the process. We hypothesized that a marker of fetal hypoxia, the absolute number of circulating nucleated red blood cells (RBCs) measured at birth, would be increased in infants of smoking mothers.
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Materials and Methods |
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Venous blood samples for complete blood cell counts were collected from each infant within 12 hours of birth and were analyzed according to laboratory routine using an STK-S counter (Coulter Corporation, Hialeah, FL). Differential cell counts were done manually, and absolute nucleated RBC counts were expressed per 100 white blood cells (WBCs). We recorded nucleated RBCs as an absolute number rather than per 100 leukocytes, and we expressed the WBC count as corrected for the presence of nucleated RBCs. We showed previously that leukocyte counts and absolute nucleated RBC numbers are not independent.7 Thus, the traditional expression of nucleated RBCs as the number per 100 WBCs might introduce a substantial bias.7
Data are reported as mean ± standard deviation (SD) or median (range). Statistical analysis included Kruskal-Wallis test, because of the non-normal distribution of absolute nucleated RBCs, and backward stepwise regression analysis. P < .05 was considered significant.
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). The mean number of cigarettes smoked per day was 9.2 ± 4.6 (range 2–20). The absolute nucleated RBC count was significantly higher in infants of smoking mothers than in controls. We found no significant differences in WBC counts, platelet counts, RBC counts, hematocrit levels, or lymphocyte counts. In the smoking group, we conducted a backward stepwise regression analysis using gestational age, Apgar scores, and cigarettes smoked as independent variables, and the absolute nucleated RBC count as the dependent variable. One patient, with an extremely high absolute nucleated RBC count of 5 x 109/L and ten cigarettes smoked per day, was considered an outlier and was excluded from analysis. The only variable that remained significantly correlated with the absolute nucleated RBC count was cigarettes smoked per day (R2 = 0.394, P < .001). The regression is plotted in Figure 1. Inclusion of the outlier made R2 = 0.279, P < .001.
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Discussion |
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The data provide evidence that absence of growth restriction should not be interpreted as evidence of normal fetal oxygenation. Similarly, Varvarigou et al14 found increased cord blood erythropoietin concentrations in AGA infants born to smoking mothers. Although increased erythropoietin was not seen in all infants born to smoking mothers, the authors concluded that "one of five fetuses who are exposed to tobacco smoke are in a state of chronic hypoxia."14
We defined the normal absolute nucleated RBC count in term, AGA newborns as less than 1.0 x 109/L (90th percentile).7 The control group in the present study had a median absolute nucleated RBC count of 0.0005 (range 0–0.6) x 109/L, with a 90th percentile of 0.4 x 109/L. Each of these groups of newborns had similar study criteria despite different sites and laboratory analyses, so the difference between the normal absolute nucleated RBC counts might result from technical or population differences. In the present study, the group born to smoking mothers had a median absolute nucleated RBC count of 0.5 (range 0–5.0) x 109/L, many times higher than that in controls. Although both study groups had mean absolute nucleated RBC counts lower than the published norm, the increased value in the smoking group is consistent with at least a relative increase in erythropoiesis.
The mechanism by which maternal smoking increases circulating neonatal absolute nucleated RBC counts is unknown. A likely explanation is relative fetal hypoxia. Nicotine can cause a transient constriction in placental blood vessels and might cause transient fetal hypoxia.15 Other mechanisms also might be involved, such as decreased blood flow to the placenta,15 production of fetal carboxyhemoglobin with decreased fetal tissue oxygenation, and placental vascular disease,16 all of which might contribute to sustained fetal hypoxia. Other indicators of fetal hypoxia include FGR,2 increased risk of spontaneous abortion,1 and neurodevelopmental anomalies,1 which occur more frequently among infants of smoking mothers.
In this study, the mean hematocrit did not differ significantly between infants of smoking mothers and those of nonsmokers. This might be due to our exclusion of infants who might have experienced the most severe hypoxia (ie, SGA, abnormal electronic intrapartum monitoring, and low Apgar scores). In those cases, prolonged or pronounced hypoxia might sufficiently stimulate the bone marrow to cause a rise in hematocrit. In our study patients, hypoxia might not have been sufficient to cause a major erythropoietic response and elevated hematocrits. Our study was not intended to compare hematocrits and did not control for factors that significantly affect postnatal hematocrits, such as the time of sampling (blood in our study was collected within 12 hours, but not at a specific time after birth) or the time of cord clamping (which was at the discretion of the attending obstetrician).17
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Footnotes |
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Received June 17, 1998. Received in revised form September 4, 1998. Accepted September 24, 1998.
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2. Lieberman E, Gremy I, Lang JM, Cohen AP. Low birth weight at term and the timing of fetal exposure to maternal smoking. Am J Public Health 1994;84:1127–31.
3. Spinillo A, Ometto A, Stronati M, Piazzi G, Iasci A, Rondini G. Epidemiologic association between maternal smoking during pregnancy and intracranial hemorrhage in preterm infants. J Pediatr 1995;127:472–8.[Medline]
4. Hoffman HJ, Damus K, Hillman L, Krongrad E. Risk factor for SIDS: Results of the National Institute of Child Health and Human Development Cooperative Epidemiological Study. Ann N Y Acad Sci 1988;533:13–30.[Medline]
5. Olds DL, Henderson CR, Tatelbaum R. Intellectual impairment in children of women who smoke cigarettes during pregnancy. Pediatrics 1994;93:221–7.
6. Lubchenco LO, Hansman C, Dressler M, Boyd E. Intrauterine growth as estimated from live-born birth weight data at 24 to 42 weeks gestation. Pediatrics 1963;32:793–9.
7. Green DW, Mimouni F. Nucleated erythrocytes in healthy infants and in infants of diabetic mothers. J Pediatr 1990;116:129–31.[Medline]
8. Meberg A, Halvorsen S, Orstavik I. Transient thrombocytopenia in small-for-date infants possibly related to maternal smoking. Lancet 1977;ii:303–4.
9. Bernstein PS, Minior VK, Divon MY. Neonatal nucleated red blood cell counts in small-for-gestational-age fetuses with abnormal umbilical artery Doppler studies. Am J Obstet Gynecol 1997;177: 1079–84.[Medline]
10. Leikin E, Garry D, Visintainer P, Verma U, Tejani N. Correlation of neonatal nucleated red blood cell counts in preterm infants with histologic chorioamnionitis. Am J Obstet Gynecol 1997;177:27–30.[Medline]
11. Mimouni F, Miodovnik M, Siddiqi TA, Butler JB, Holroyde J, Tsang RC. Neonatal polycythemia in infants of insulin-dependent diabetic mothers. Obstet Gynecol 1986;68:370–2.[Medline]
12. Green DW, Hendon B, Mimouni F. Nucleated erythrocytes and intraventricular hemorrhage in preterm neonates. Pediatrics 1995; 96:475–8.
13. Naeye RL, Localio R. Determining the time before birth when ischemia and hypoxemia initiated cerebral palsy. Obstet Gynecol 1995;86:713–9.[Abstract]
14. Varvarigou A, Beratis NG, Makri M, Vagenakis AG. Increased levels and positive correlation between erythropoietin and hemoglobin concentrations in newborn children of mothers who are smokers. J Pediatr 1994;124:480–2.[Medline]
15. Morrow RJ, Ritchie JW, Bull SB. Maternal cigarette smoking: The effects on umbilical and uterine blood flow velocity. Am J Obstet Gynecol 1988;159:1069–71.[Medline]
16. Gupta I, Hillier VF, Edwards JM. Multiple vascular profiles in the umbilical cord; an indication of maternal smoking habits and intrauterine distress. Placenta 1993;14:117–23.[Medline]
17. Shohat M, Reisner SH, Mimouni F, Merlob P. Neonatal polycythemia: II. Definition related to time of sampling. Pediatrics 1984;73: 11–3.
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