![[Feedback]](/icons/banner/feedbackACT.gif){kind=icon}
![[For Subscribers]](/icons/banner/subscriberACT.gif){kind=icon}
![[Archive]](/icons/banner/archiveACT.gif){kind=icon}
![[Search]](/icons/banner/searchACT.gif){kind=icon}
![[Contents]](/icons/banner/tocACT.gif){kind=icon}
|
|
|
|
|
||
,**
* Department of International Health, Center for Human Nutrition, Johns Hopkins Bloomberg School of Public Health,
Johns Hopkins Hospital and
** Department of Obstetrics and Gynecology, Johns Hopkins School of Medicine, Baltimore, MD 21205-2179
3To whom correspondence and reprint requests should be addressed. E-mail: kobrien{at}jhsph.edu.
 |
ABSTRACT |
|---|
 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
KEY WORDS: • adolescents • pregnancy • hemoglobin • preterm birth • low birth weight
Extremes of iron status during pregnancy may adversely impact birth outcomes. Relationships between anemia and adverse birth outcomes have been inconsistent: some studies have found anemia to significantly increase the risk of adverse birth outcomes (1–5), whereas others have not (6–10). At the other end of the spectrum, elevated hemoglobin concentrations during pregnancy also increase the risk of adverse birth outcomes, including preterm delivery, low birth weight (LBW), fetal death and intrauterine growth retardation (2–4,11). This U-shaped distribution, with higher risks of adverse birth outcomes at both extremes of the hemoglobin or hematocrit distribution, have been described primarily in adult populations (2,4). At this time, limited data are available on the impact of iron status on birth outcomes in pregnant adolescents.
Pregnant women are particularly vulnerable to anemia due to the increased iron demands of pregnancy. In pregnant adolescents, risk of iron deficiency is increased, because the adolescent must supply adequate iron for not only her own growth but also that needed for fetal demands and expansion of the red-cell mass. Among the low income pregnant women recruited in the U.S. Pregnancy Nutrition Surveillance System (1979–1990), the prevalence of anemia among adolescent girls who entered prenatal care during the first, second and third trimesters was 11, 16 and 37%, respectively (12). These values were higher than those found in adult women at similar stages of gestation (8.9–10, 12.7–13.5 and 30.2–32.8%, respectively) (12).
Several studies have indicated that the normal hemoglobin distribution is shifted to the left in African-Americans, and this group has on average an 8 g/L lower hemoglobin concentration in comparison with Caucasian groups (13). African-American adolescents have the highest risk of early childbearing (14) and have increased risks of anemia and adverse birth outcomes. However, few studies have described hemoglobin concentrations and birth outcomes in this vulnerable group.
The objective of this study was to characterize the prevalence of prenatal anemia and the impact of maternal factors on anemia in a cohort of pregnant African-American adolescents who had received prenatal care at an inner-city maternity clinic between 1990 and 2000. In addition, associations between maternal hemoglobin concentrations and adverse birth outcomes in this adolescent population were examined.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
A 10-y retrospective medical chart review was undertaken of a cohort of pregnant African-American adolescents (≤17 y of age) who had received prenatal care at an inner-city maternity clinic [Maternity Center East (MCE)] affiliated with Johns Hopkins Hospital. To simplify the interpretation of results, the study cohort was restricted to African-American adolescents because of reported race-ethnicity heterogeneity in hemoglobin concentrations and rates of adverse birth outcomes (13,14). This restriction did not significantly limit the study population, because the majority (>94%) of adolescents attending the MCE self-reported their racial group as African-American. Additional inclusion criteria included a singleton pregnancy and delivery at Johns Hopkins Hospital. This study was approved by the Joint Committee of Clinical Investigation at Johns Hopkins Hospital.
Study population.
In total, 1214 medical charts were reviewed. This cohort represented 96% of the entire pregnant adolescent patient population seen at MCE between 1990 and 2000. The remaining 4% of adolescents (51 medical records) were not included, because medical files were not available. Of the 1214 medical charts that were reviewed, 87 (7%) were excluded, because these adolescents were not African-American, and 7 (0.6%) were excluded because of multiple births. An additional 202 medical charts were not included in the final analysis, because birth results were not available as a result of abortion, miscarriage, transfer to another health care provider or loss to follow-up. Further comparison of the excluded cohort indicated that there were no significant differences between the 202 excluded adolescents and the 918 nonexcluded subjects with respect to the distribution of covariates such as maternal age, prepregnancy BMI, height, parity, smoking status and adequacy of prenatal care.
In this study population hemoglobin status was typically evaluated twice during pregnancy, once at entry into prenatal care and again at 
28 wk of gestation. Hemoglobin and hematocrit determinations were made in the core laboratory at Johns Hopkins Hospital. In some cases, only one hemoglobin and hematocrit measure was available during pregnancy, primarily due to either late entry into prenatal care or early delivery. For the sake of data analysis, data were grouped according to the trimester at which the hemoglobin information was collected (Fig. 1).
|
Data management.
Data on variables of interest were collected from medical records and from computerized archives. Data were collected in a standardized manner using a statistical software package (Statview, version 5.01; SAS Institute, Cary, NC). The following information was extracted from the medical charts: age at entry into prenatal care, last menstrual period (LMP), self-reported prepregnancy weight, height, prepregnancy BMI (kg/m2), maternal education, insurance status, parity, number of prenatal visits, self-reported history of cigarette use, hemoglobin concentration and hematocrit (both measured directly), occurrence of pre-eclampsia, week of gestation at delivery and infant birth weight.
Anemia classification.
Anemia was defined using the CDC criteria for anemia during pregnancy. With these criteria the hemoglobin cutoff used to define anemia during the first and third trimesters was 110 g/L and during the second trimester was 105 g/L. The corresponding cutoff for hematocrit was 0.33 during the first and third trimesters, and 0.32 during the second trimester (15). Hemoglobin concentrations were adjusted for smoking status using the criteria developed by the CDC (15).
Other measurements.
The gestational age of the fetus was estimated using both the mother’s LMP and the best obstetric estimate as determined from a physical examination and sonogram. The gestational age of the fetus was determined using the LMP if there was a <10-d difference between the LMP and the best obstetric estimate. If these two measures differed by >10 d, the earliest ultrasound measure of gestational age was used as the gestational age. Low birth weight was defined as a birth weight of <2500 g, and preterm delivery was defined as <37 completed weeks of gestation. Preterm births that were related to spontaneous onset of preterm labor or premature rupture of the fetal membranes were further classified as spontaneous preterm birth. Preterm births that did not meet the above criteria were classified as induced preterm birth. Pre-eclampsia was defined as high blood pressure (>140/90 mm Hg), abnormally high urinary protein (2+ or higher by standard turbidimetric methods) and symptoms of edema during pregnancy.
Prepregnancy BMI was calculated using measured height and self-reported prepregnancy weight. Women were classified into three categories of BMI using the Institute of Medicine guidelines: underweight, <19.8 kg/m2; normal weight, 19.8–26.0 kg/m2; overweight, 26.1–29 kg/m2; and very overweight, >29.0 kg/m2 (16). In our study, data from overweight and very overweight women were combined.
Quality of prenatal care was assessed using Kotelchuck’s adequacy of prenatal use index (17). This index evaluates the adequacy of prenatal care according to the timing of enrollment into prenatal care, the number of prenatal visits and the gestational age at delivery. Four levels of prenatal care quality were defined: inadequate, intermediate, adequate and adequate plus. In our study we defined the latter two groups as adequate.
Screening for sexually transmitted diseases (STD), including chlamydia and gonorrhea, were routinely performed by cervical culture at entry into prenatal care and again during the third trimester. Patients were classified as negative if all tests were negative during pregnancy. Classification as positive indicated that the patient had a positive test for chlamydia, gonorrhea or both at any point during pregnancy.
Statistical analyses.
Statistical analyses were performed using the Stata software package (Stata 7.0; Stata, College Station, TX). One-way ANOVA and Student’s t test were used to test for potential differences in risk characteristics associated with hemoglobin concentrations during the combined first and second trimester and during the third trimester. Log-linear regression analysis (unadjusted and adjusted) was used to examine associations between maternal hemoglobin concentrations and adverse pregnancy outcomes. To eliminate potential confounding effects, data were controlled for maternal age, parity, prepregnancy BMI, history of maternal use of cigarettes, pre-eclampsia and gestational age at hemoglobin concentration measurement. Confounding variables were identified as those that were associated with both the main covariate (hemoglobin) and other outcome variables. Confounders that were related to both outcome variables included the following: parity, prepregnancy BMI, smoking history, pre-eclampsia and adequacy of prenatal care. We also adjusted for the timing of the hemoglobin assessment (week of gestation) to account for differences in the timing of this measure. Continuous covariates such as age and prepregnancy BMI were treated as continuous confounding variables in the models. We further examined whether any of these confounding factors acted as effect modifiers on the relationships observed between hemoglobin concentrations and birth outcomes. None were found to act as effect modifiers. The generalized estimating equation method was used when patients contributed more than one pregnancy over the 10-y study interval (10 patients in the second trimester and 48 patients in the third trimester) (18,19). Unadjusted and adjusted risk ratio (RR) and their 95% CI were derived from the log-linear regression coefficients. In all statistical analyses, an alpha level of 0.05 was applied to decrease the possibility of type I errors. Differences were considered significant if P < 0.05.
|
RESULTS |
|---|
|
TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
49% of adolescents entered prenatal care during the first trimester, 37% entered during the second trimester and 14% entered during the third trimester.
|
|
|
|
|
In our third-trimester cohort a U-shaped distribution existed when we adjusted the reference hemoglobin grouping downward to 96–105 g/L. Using this more conservative cutoff, substantially higher rates of LBW were observed at both the lower (≤95 g/L; RR = 1.91; P = 0.127) and higher (>105 g/L; RR = 1.97; P = 0.023) hemoglobin concentrations. Moreover, higher risks of preterm delivery were evident at both the lower (RR = 2.06; P = 0.047) and higher (RR = 1.85; P = 0.025) hemoglobin concentrations (Tables 4, and 5). We were unable to examine the impact of a downward-adjusted reference category of hemoglobin concentrations during the second trimester due to insufficient statistical power.
Possible relationships between hemoglobin concentrations and births that were small for gestational age (SGA) were also examined, where SGA was defined as a birth weight of less than the 10th percentile for a given gestational age (20). Using either 96–105 or 106–120 g/L as the reference group, no significant associations were evident between maternal hemoglobin concentration and SGA during the second or third trimester. Removing induced preterm birth from our regression model did not affect the strength of the associations during the second or third trimester. We therefore presented these results without adjusting for the type of preterm birth.
|
DISCUSSION |
|---|
|
TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
The etiology of the anemia observed in this group is multifactorial and may be influenced by the increased iron demands of this age group, noncompliance with prenatal iron supplementation, poor dietary quality and other nonnutritional factors. Because many studies have indicated that >80% of anemia during pregnancy is explained by iron deficiency (23,24), it is likely that iron deficiency was prevalent in this group of adolescents. Studies in adult women have estimated that between 3 and 8 mg/d absorbed iron is needed to meet the iron demands of pregnancy (25). Adolescents are estimated to require an additional 0.33 mg/d absorbed iron to meet the iron demands of growth (26). In this clinic population all adolescents were prescribed daily prenatal supplements containing 90 mg of elemental iron and additional iron up to 120 mg Fe/d was prescribed if they were classified as anemic on the basis of their hemoglobin concentration and hematocrit. This dosage of iron is high, and unpleasant side effects of iron supplementation, such as nausea, vomiting and constipation, may have adversely affected compliance (27). Unfortunately no data on compliance with these recommendations were available in the medical charts. Previous studies, however, have found pregnant adolescents to be relatively noncompliant with respect to prenatal supplementation (26,28), and based on the degree of anemia observed, it is unlikely that this group was compliant with respect to prenatal supplement intakes.
Characterization of anemia during pregnancy must take into account the alterations that occur in red-cell mass and expansion of plasma volume during pregnancy. These normal physiological processes cause an expected fall in hemoglobin concentrations, and this expected decrease influences the criteria used to define anemia during pregnancy (29,30). Elevated hemoglobin concentrations during the second and third trimesters may be due to high iron status or may occur if maternal blood volume expansion is not sufficient (29). Previous data have reported that inadequate plasma volume expansion during pregnancy is associated with poor reproductive outcomes (29,31).
Our finding of no significant associations between low hemoglobin concentrations (≤105 g/L) and adverse birth outcomes may be due in part to the fact that most of our population had mild-to-moderate, but not severe, anemia. Previous studies have found that severe anemia (hemoglobin < 80.0 g/L) is associated with adverse birth outcomes (32). In our study population few patients (<0.5% during the third trimester) had hemoglobin concentrations of <80.0 g/L, which may have made comparisons at the low extreme of the hemoglobin distribution difficult. The impact of mild-to-moderate anemia during early pregnancy on subsequent adverse birth outcomes has provided conflicting results (24,32). This may be further confounded by the lack of differentiating mild-to-moderate anemia caused by normal physiologic expansion of plasmavolume from iron-deficiency (33). A study conducted in pregnant adolescents and adults from Camden, New Jersey, indicated that iron-deficiency anemia, but not anemia due to other causes, is associated with an increased risk of LBW and preterm delivery (23). Despite our inability to distinguish the cause of anemia, the relationship between low hemoglobin concentration and adverse birth outcomes observed in our population during the second trimester was consistent with that of other studies (6–10). A recent meta-analysis addressing the relationship between maternal anemia and birth outcomes indicated that maternal anemia during early pregnancy is not associated with LBW and fetal growth restriction. However, a slightly increased risk of preterm birth was found in anemic mothers (34).
Several studies have found an increased incidence of LBW and preterm birth in association with either a high maternal hemoglobin concentration (2–4,6,7,35) or high hematocrit (2,36). In our population, women with high hemoglobin concentrations (>120 g/L) during the second trimester had 3.1-fold and 2.3-fold higher risks of having a LBW infant and preterm birth, respectively. The significance of this finding persisted into third trimester for LBW infant but not for preterm birth after adjusting for potential confounders. The mechanisms by which this effect was mediated are not known. Clinical and epidemiological evidence has revealed that high hemoglobin concentrations may be due to maternal complications such as pregnancy-induced hypertension or pre-eclampsia, which are causally associated with perinatal morbidity and mortality (37–39) or due to cigarette smoking during pregnancy (24). In our study, significantly higher hemoglobin concentrations were also observed in women with pre-eclampsia throughout pregnancy. However, the association between high hemoglobin concentrations and poor birth outcomes remained significant even when controlled for pre-eclampsia and a history of cigarette use. This indicates that factors other than these two potential confounding factors accounted for this observed relationship. Another possible mediator for this relationship is high blood viscosity (32). High hemoglobin concentrations, due to inadequate plasma volume expansion, may increase blood viscosity, which leads to poor placental blood flow and compromised nutrient delivery to the fetus, thus limiting fetal growth (40).
Our data also indicated that low hemoglobin concentrations (≤105 g/L) during the third trimester played a marginally protective role on the risk of having both a LBW infant and preterm birth, although this finding was not significant. This result is supported by two previous studies (11,41). Steer and colleagues (11,32) studied a large population of 153,602 pregnancies and reported that the lowest hemoglobin concentrations during pregnancy (85–105 g/L) is associated with maximum mean birth weight and the lowest incidences of LBW and preterm delivery. Another study on racial differences in hematocrit levels and its impact on birth outcomes in a population of 17,149 low-income, iron- and folate-supplemented pregnant women found that hematocrit levels <32% at 31–34 wk are nonsignificantly associated with a lower incidence of preterm birth and intrauterine growth retardation in black but not white women (41).
An additional variable to consider when characterizing hemoglobin concentrations is racial group. Several studies have found that hemoglobin concentrations are 8–10 g/L lower in African-American women compared with those in white women (13). This shift in the hemoglobin curve doesnot appear to be explained by iron status or other demographic factors (42). Potential racial differences may shift the data in African-American populations and make comparisons to Caucasian cohorts more difficult to interpret. Using a more conservative reference hemoglobin range of 96–105 g/L, a U-shaped relationship was evident for the third-trimester cohort between hemoglobin concentrations and both LBW and preterm delivery.
Our study design was observational and involved a retrospective medical chart review resulting in several limitations with these data. Exclusion of subjects due to missing data may introduce selection bias if the distribution of specific covariates or outcome variables differs between the excluded and nonexcluded subjects. In our study, we excluded all subjects that had at least one missing value for any of the covariates or outcome measures in our regression analyses. Because we were not able to identify any significant differences between the excluded and nonexcluded subjects with respect to the distribution of covariates and outcome variables in all of our regression models, we assumed that selection bias should be minimal. In addition, several of our variables—such as prepregnancy weight, smoking status, and drug abuse—were self-reported and may introduce information bias, leading to misclassification of these exposures. We assumed that the information bias in our study was minimal due to the experience of the nurse/midwife, registered dietician and social worker in communicating with these pregnant African-American adolescents. Finally, due to the observational nature of the study, these study findings do not indicate a causal relationship between high hemoglobin concentration and adverse birth outcomes. However, given the consistency of the results among different studies and populations, the demonstrated association between high hemoglobin concentrations and adverse birth outcomes is well substantiated and warrants additional research.
In conclusion, this group of urban African-American adolescents was at a high risk of anemia during late pregnancy. Although many of our findings parallel those reported for pregnant adult women, this group of urban, minority adolescents had an even higher incidence of anemia compared with that of many other populations. At the other extreme, high hemoglobin concentrations that were not explained by cigarette use or pre-eclampsia were associated with 2.0- to 3.1-fold and 1.9- to 2.3-fold increased risk of low infant birth weight and preterm birth, respectively. Adolescents should be monitored for abnormally high hemoglobin concentrations during pregnancy to minimize the risk of adverse birth outcomes. Future studies should focus on the biological mechanisms responsible for the relationship between high hemoglobin concentrations and adverse birth outcomes, and more work is needed to optimize iron status in pregnant African-American adolescents.
|
FOOTNOTES |
|---|
2 Supported by the National Institute of Child Health and Development (HD035191).
4 Abbreviations used: LBW, low birth weight; LMP, last menstrual period; MCE, Maternity Center East; RR, risk ratio; SGA, small for gestational age; STD, sexually transmitted disease.
Manuscript received 27 December 2002. Initial review completed 28 January 2003. Revision accepted 9 April 2003.
|
LITERATURE CITED |
|---|
|
TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
1. Scholl, T. O., Hediger, M. L., Fisher, R. L. & Shearer, J. W. (1994) Anemia vs iron deficiency: increased risk of preterm delivery in a prospective study. Am. J. Clin. Nutr. 55:985-988.
2. Garn, S. M., Ridella, S. A., Petzold, A. S. & Falkner, F. (1981) Maternal hematologic levels and pregnancy outcomes. Semin. Perinatol. 5:155-162.[Medline]
3. Zhou, L. M., Yang, W. W., Hua, J. Z., Deng, C. Q., Tao, X. & Stoltzfus, R. J. (1998) Relation of hemoglobin measured at different times in pregnancy to preterm birth and low birth weight in Shanghai, China. Am. J. Epidemiol. 148:998-1006.
4. Murphy, J. F., O’Riordan, J., Newcombe, R. G., Coles, E. C. & Pearson, J. F. (1986) Relation of haemoglobin levels in first and second trimesters to outcome of pregnancy. Lancet :992-995.
5. Klebanoff, M. A., Shiono, P. H., Selby, J. V., Trachtenberg, A. I. & Graubard, B. I. (1991) Anemia and spontaneous preterm birth. Am. J. Obstet. Gynecol. 164:59-63.[Medline]
6. Knottnerus, J. A., Delgado, L., Knipschild, P. G., Essed, G. G. & Smits, F. (1986) Maternal haemoglobin and pregnancy outcome. Lancet 2:282.
7. Knottnerus, J. A., Delgado, L. R., Knipschild, P. G., Essed, G.G.M. & Smits, F. (1990) Haematologic parameter and pregnancy outcome: a prospective cohort study in the third trimester. J. Clin. Epidemiol. 5:461-466.
8. Rasmussen, S. & Qian, P. (1993) First- and second-trimester hemoglobin levels: relation to birth weight and gestational age. Acta Obstet. Gynecol. Scand. 72:246-251.[Medline]
9. Meis, P. J., Michielutte, R., Peters, T. J., Wells, H. B., Sands, R. E., Coles, E. C. & Johns, K. A. (1995) Factors associated with preterm birth in Cardiff, Wales. II. Indicated and spontaneous preterm birth. Am. J. Obstet. Gynecol. 173:597-602.[Medline]
10. Siega-Riz, A. M., Adair, L. S. & Hobel, C. J. (1998) Maternal hematologic changes during pregnancy and effect of iron status on preterm delivery in a west Los Angles population. Am. J. Perinatol. 15:515-522.[Medline]
11. Steer, P., Alam, M. A., Wadsworth, J. & Welch, A. (1995) Relation between maternal haemoglobin concentration and birth weight in different ethnic groups. BMJ 310:489-491.
12. Kim, I., Hungerford, D. W., Yip, R., Kuester, S. A., Zyrkowski, C. & Trowbridge, F. A. (1992) Pregnancy nutrition surveillance system-United States, 1979–1990. MMWR CDC Surveill. Summ. 41:25-41.
13. Johnson-Spear, M. A. & Yip, R. (1994) Hemoglobin difference between black and white women with comparable status: justification for race-specific anemia criteria. Am. J. Clin. Nutr. 60:117-121.
14. Martin, J. A., Hamilton, B. E., Ventura, S. J., Menacker, F. & Park, M. M. (2002) Birth: final data for 2000: CDC national vital statistics reports. Natl. Vital Stat. Rep. 50:1-101.[Medline]
15. Centers for Disease Control (1989) CDC criteria for anemia in children and childbearing age women. MMWR Morb. Mortal. Wkly. Rep. 38:400-404.[Medline]
16. Institute of Medicine (1990) Effect of gestational weight gain on outcome in singleton pregnancies. Nutrition during Pregnancy: Weight Gain, Nutrient Supplements 1990:176-211 National Academy Press Washington, DC.
17. Kotelchuck, M. (1994) An evaluation of the Kessner adequacy of prenatal care index and a proposed adequacy of prenatal care utilization index. Am. J. Public Health 84:1414-1420.
18. Liang, K. Y. & Zeger, S. L. (1986) Longitudinal data analysis using generalized linear models. Biometrika 73:13-22.
19. Zeger, S. L., Liang, K. Y. & Albert, P. S. (1988) Models for longitudinal data: a generalized estimating equation approach. Biometrics 44:1049-1060.[Medline]
20. Alexander, G. R., Himes, J. H., Kaufman, R., Mor, J. & Kogan, M. (1996) A United States national reference for fetal growth. Obstet. Gynecol. 87:163-168.[Medline]
21. Kilbride, J., Baker, T. G., Parapia, L. A., Khoury, S. A., Shuqaidef, S. W. & Jerwood, D. (1999) Anemia during pregnancy as a risk factor for iron-deficiency anemia in infancy: a case-control study in Jordon. Int. J. Epidemiol. 28:461-468.
22. Grantham-McGregor, S. & Ani, C. (2001) A review of studies on the effect of iron deficiency on cognitive development in children. J. Nutr. 131:649S-668S.
23. Scholl, T. O., Hediger, M. L., Huang, J., Johnson, F. E., Smith, W. & Ances, I. G. (1992) Young maternal age and parity influences on pregnancy outcome. Ann. Epidemiol. 2:565-575.[Medline]
24. Yip, R. (2000) Significance of an abnormally low or high hemoglobin concentration during pregnancy: special consideration of iron nutrition. Am. J. Clin. Nutr. 72(suppl.):272S-279S.
25. Viteri, F. E. (1994) The consequences of iron deficiency and anemia in pregnancy. Allen, L. H. King, J. Lonnerdal, B. eds. Nutrient Regulation during Pregnancy, Lactation, and Infant Growth 1994:128 Plenum New York. .
26. Beard, J. L. (2000) Iron requirements in adolescent females. J. Nutr. 130:440S-442S.
27. Hyder, S. M., Persson, L. A., Chowdhury, A. M. & Ekstrom, E. C. (2002) Do side-effects reduce compliance to iron supplementation? A study of daily- and weekly-dose regimens in pregnancy. J. Health Popul. Nutr. 20:175-179.[Medline]
28. Stang, J., Story, M., Harnack, L. & Neumark-Sztainer, D. (2000) Relationships between vitamin and mineral supplement use, dietary intake, and dietary adequacy among adolescents. J. Am. Diet. Assoc. 100:905-910.[Medline]
29. Goodlin, R. C., Dorby, C. A., Anderson, J. C., Woods, R. E. & Quaife, M. (1983) Clinical signs of normal volume expansion during pregnancy. Am. J. Obstet. Gynecol. 145:1001-1009.[Medline]
30. Lund, C. J. & Donovan, J. C. (1967) Blood volume during pregnancy: significance of plasma and red cell volumes. Am. J. Obstet. Gynecol. 98:394-403.[Medline]
31. Koller, O., Sagen, N., Ulstein, M. & Vaula, D. (1979) Fetal growth retardation associated with inadequate hemodilution in otherwise uncomplicated pregnancy. Acta Obstet. Gynecol. Scand. 58:9-13.[Medline]
32. Steer, P. J. (2000) Maternal hemoglobin concentration and birth weight. Am. J. Clin. Nutr. 71(suppl.):1285S-1287S.
33. Klebanoff, M. A., Shiono, P. H., Berendes, H. W. & Rhoads, G. G. (1989) Facts and artifacts about anemia and preterm delivery. JAMA 262:511-515.
34. Xiong, X., Buekens, P., Alexander, S., Demianczuk, N. & Wollast, E. (2000) Anemia during pregnancy and birth outcome: a meta-analysis. Am. J. Perinatol. 17:137-146.[Medline]
35. Scanlon, K. S., Yip, R., Schieve, L. A. & Cogswell, M. E. (2000) High and low hemoglobin levels during pregnancy: differential risks for preterm birth and small for gestational age. Obstet. Gynecol. 96:741-748.[Medline]
36. Lu, Z. M., Goldenberg, R. L., Cliver, S. P., Cutter, G. & Blankson, M. L. (1991) The relationship between maternal hematocrit and pregnancy outcome. Obstet. Gynecol. 77:190-194.[Medline]
37. Heilman, L., Siekmann, U., Schmid-Schonbein, H. & Ludwig, H. (1981) Hemoconcentration and pre-eclampsia. Arch. Gynecol. 231:7-21.[Medline]
38. Huisman, A. & Aranoudse, J. G. (1986) Increased 2nd trimester hemoglobin concentration in pregnancies later complicated by hypertension and growth retardation: early evidence of reduced plasma volume. Acta Obstet. Gynecol. Scand. 65:605-608.[Medline]
39. Sagen, N., Koller, O. & Haram, K. (1982) Haemoconcentration in severe pre-eclampsia. Br. J. Obstet. Gynaecol. 89:802-805.[Medline]
40. Zondervan, H. A., Voorhorst, F. J., Robertson, E. A., Kurver, P. H. & Massen, C. (1985) Is maternal whole blood viscosity a factor in fetal growth?. Eur. J. Obstet. Gynecol. Reprod. Biol. 20:145-151.[Medline]
41. Blankson, M. L., Goldenberg, R. L., Cutter, G. & Cliver, S. P. (1993) The relationship between maternal hematocrit and pregnancy outcome: black-white difference. J. Natl. Med. Assoc. 85:130-134.[Medline]
42. Perry, G. S., Byers, T., Yip, R. & Margen, S. (1992) Iron nutrition does not account for the hemoglobin differences between blacks and whites. J. Nutr. 122:1417-1424.
This article has been cited by other articles:
|
|
 |
|
  J. N. Nielsen, K. O O'Brien, F. R Witter, S.-C. Chang, J. Mancini, M. S. Nathanson, and L. E Caulfield High gestational weight gain does not improve birth weight in a cohort of African American adolescents Am. J. Clinical Nutrition, July 1, 2006; 84(1): 183 - 189. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. L. Iannotti, K. O. O'Brien, S.-C. Chang, J. Mancini, M. Schulman-Nathanson, S. Liu, Z. L. Harris, and F. R. Witter Iron Deficiency Anemia and Depleted Body Iron Reserves Are Prevalent among Pregnant African-American Adolescents J. Nutr., November 1, 2005; 135(11): 2572 - 2577. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
