American Journal of Hematology 82:611–614 (2007)
Hematologic Reference Values for African American Children and Adolescents Edwin B. Robins* and Steve Blum Department of Pediatrics, Bronx Lebanon Hospital Center, Department of Pediatrics, Bronx, New York
Anemia is prevalent among African American children. When evaluating pediatric patients for anemia, clinicians refer to the normative hematological reference values in reference textbooks. These reference values are used in spite of evidence that healthy African American people of all ages have average hemoglobin concentrations from 0.5 to 0.73 g/dl below those of Whites. In an earlier study, using samples from 2,161 healthy African American children from 2 to 18 years old, we found a statistically significant difference (P < 0.0001) in the mean hemoglobin value for each age group as compared to reference normative mean hemoglobin values. Here we present the results of a comparative analysis of the data set from our previous study and the data set from the National Health and Nutrition Examination Surveys III (NHANES III) 1988–1994. We found no statistically significant difference between these data sets with respect to the hemoglobin values for any age or sex group, confirming that African American children and adolescents have lower mean hemoglobin values than do Whites. Use of the reference hemoglobin values presented here will help prevent the misdiagnosis of anemia in African American children and thereby minimize unnecessary hematological workups and treatment. C 2006 Wiley-Liss, Inc. Am. J. Hematol. 82:611–614, 2007. V Key words: anemia; hemoglobin; children; African American
INTRODUCTION
Anemia is one of the most common abnormalities encountered by general pediatricians. The causes of anemia during childhood and adolescence are well known. In 1979, Dallman and Siimes [1] established percentile curves for hemoglobin and mean corpuscular volume for children between 5 and 16 years of age based on a large sample of white children of nonindigent parents. By design, these authors gathered information from 9,946 \White children," only making reference to the fact that the hemoglobin concentrations would have been lower if \Blacks" had been included in the survey. When evaluating pediatric patients for anemia, clinicians usually check their suspicion of this disorder by referring to the normative hematological reference values for children and adolescents in reference textbooks, such as that by Nathan and Oski [2]. These standard reference values are uniformly used for all racial and ethnic groups. They are used in spite of evidence in the medical literature, originating as far back as 1930, that healthy people of all ages who are of African extraction have average hemoglobin concentrations ranging from 0.5 to 0.73 g/dl below those of Whites, independent of statistiC 2006 Wiley-Liss, Inc. V
cal matching, and controlled for selected variables, including iron deficiency, age, sex, hemoglobinopathies, and socioeconomic factors [3,4]. A review of the medical literature over the past few decades suggests that African Americans have lower baseline hemoglobin concentrations than do Whites. Differences in socioeconomic status or iron deficiency and other causes of anemia do not account for this difference [5–7]. Anemia remains common among African American children, having been identified as one of the five most prevalent conditions in this population [8]. According to the Pediatric Nutrition Surveillance 2002 report [9], 19.3% of black children were diagnosed with anemia between 1993 and 2002. The same report stated that while anemia has continued to decline since the *Correspondence to: Edwin B. Robins, Department of Pediatrics, Bronx Lebanon Hospital Center, 1650 Selwyn Ave, Bronx, NY 10457. E-mail:
[email protected] Received for publication 19 June 2006; Revised 27 September 2006; Accepted 16 October 2006 Published online 18 December 2006 in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/ajh.20848
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1980’s, it has declined least among African American and Asian or Pacific Islander children. Studies done in the 1960’s attributed lower hematological values in African Americans to diet and nutritional status but this has since been disproved [10]. Nduka et al. [11] compared hematologic indices of 512 Africans and 196 Caucasians residing in the same Nigerian town and found marked differences between the two groups, with Caucasians having higher hemoglobin levels. The hemoglobin values for African women, in particular, were much lower than those previously reported, but the authors made no mention of diet, living conditions, or hygiene as possible causes of this difference. The National Health and Nutrition Examination Survey II (NHANES II), 1976– 1980 [12], not only confirmed racial differences in mean hemoglobin and hematocrit levels, with African Americans having consistently lower mean values than those of Whites, but also found that those differences were independent of gender, age, poverty status, or nutrition, although there was some variation with age. This survey provided clinicians and researchers with suggested reference ranges for specific population subgroups. In a previous study [13], we obtained samples from 3,000 healthy African American children, 2–18 years old. These children were from three independent pediatric practices in Manhattan, a borough of New York City. These practices have a service area spanning Central and East Harlem, Morningside Heights, Washington Heights, and the Upper West Side, areas having high populations of African Americans. In its methodology, this study addressed some of the limitations of earlier studies. The methodology included a complete dietary history and excluded individuals with iron deficiency, b thalassemia trait, and suspected a thalassemia trait. Adolescent patients were subcategorized by age and sex to account for the effects of both maturation and sex on hemoglobin levels. Of the 3,000 samples collected, 839 were excluded because of patients’ nutritional history, iron deficiency, or the presence of thalassemia trait. Among the remaining 2,161 samples, this study found a statistically significant difference (P < 0.0001) in the mean hemoglobin value for each age group when compared to reference normative mean hemoglobin values. These findings were consistent with previous reports of significant racial differences in mean hemoglobin values. MATERIALS AND METHODS
To establish hematologic reference values for African American children and adolescents, we performed an analysis of two existing data sets. The first data was from our previous study of a sample of 2,161 healthy African American children between the ages of 2–18 years. The second and larger data set was American Journal of Hematology DOI 10.1002/ajh
obtained from the National Health and Nutrition Examination Surveys III (NHANES III) 1988–1994 [14], which contained data from 33,994 individuals 2 months old and older with subsamples of White (n ¼ 6,321), Mexican American (n ¼ 3,616), other Hispanic (n ¼ 313), and African American (n ¼ 3,593). The NHANES III data files were organized in a manner suitable for comparative analysis. We used the subsample of children and adolescents of ages 2–18 years from the NHANES III subsample. Of the 3,593 African American children, 2,878 were of the appropriate age for this analysis. The number of African American children from the NHANES III study, 2,878, was comparable to the 2,161 African American children in our study. Mean hemoglobin and hematocrit values for each ethnic group were extracted from the NHANES III data files with the appropriate statistical analysis software (SAS) code. The mean hemoglobin values for non-Hispanic Whites from the NHANES III subsample was compared to the mean hemoglobin values from the NHANES III African American subsample using Students T-test. These data files were sorted into groups as in our previous study: 2– 5 years, 6–10 years, 11–15 years, and 16–18 years, with data from those over the age of 10 years also sorted into male and female groups. We compared the NHANES III subsample of hemoglobin values for African American children and adolescents to the data from our earlier study. Because our data were collected from a single demographic area of the United States, they may not be representative of all African Americans. The NHANES III study, in contrast, was a cross-sectional study and is considered to be more representative of the United States population. RESULTS
Statistically significant differences in hemoglobin values were found between all age and sex groups (Table I). The mean hemoglobin values from the NHANES III subsample of non-Hispanic Whites were similar to the published reference standards currently available. Comparing the data for African Americans from the NHANES III study group and our own study group, we found no statistically significant differences in mean hemoglobin by age and sex group (Table II). This finding confirmed that African American children and adolescents have lower mean hemoglobin values than do Whites. The similarity in all age and sex groups of the mean hemoglobin values for the two study groups demonstrates that the samples used in our analysis were indeed representative of African American children and adolescents. We determined normative hemoglobin values based on the similar mean hemoglobin values of the two studies.
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TABLE I. NHANES III Hemoglobin Values for Non-Hispanic Whites and African Americans Aged 2–18 Years White non-Hispanic Age (yrs)
Mean
2 STD
Sample size
2–5 6–10 11–15 male 11–15 female 16–18 male 16–18 female
12.21 12.87 13.76 13.32 15.00 13.39
10.8 11.31 11.76 11.5 13.24 11.61
730 718 266 263 124 163
African American Mean
2 STD
Sample size
P Value
11.95 12.40 13.06 12.61 14.18 12.37
10.37 10.74 10.88 10.85 12.42 10.37
846 898 356 388 184 206
P ¼ 0.0006 P < 0.0001 P < 0.0001 P < 0.0001 P < 0.0001 P < 0.0001
Sample size is 5,142 (White, 2,264; African American, 2,878). TABLE II. NHANES III African American Hemoglobin Values and Robins 2004 African American Hemoglobin Values
Robins African American
NHANES African American
Age (yrs)
Mean
2 STD
Sample size
Mean
2 STD
Sample size
P Value
2–5 6–10 11–15 male 11–15 female 16–18 male 16–18 female
11.94 12.48 13.35 12.73 14.52 12.73
10.36 9.96 11.06 9.36 10.2 10.18
724 673 262 266 114 122
11.95 12.40 13.06 12.61 14.18 12.37
10.37 10.70 10.88 10.85 12.42 10.37
846 898 356 388 184 206
P ¼ 0.9005 P ¼ 1.000 P ¼ 0.1842 P ¼ 0.6524 P ¼ 0.914 P ¼ 0.1829
Sample size is 5,039 (NHANES, 2,878; Robins, 2,161). TABLE III. Normative Hematological Reference Values for African American Children and Adolescents Aged 2–18 Yearsa African American [Hb (g/dl)] Age (yrs) 2–5 6–10 11–15 male 11–15 female 16–18 male 16–18 female
African American [Hct (%)]
African American [MCV (fl)]
African American (mean WBC)
Mean
2 STD
Mean
2 STD
Mean
STD
7.33 6.74 6.32 6.58 5.91 6.92
11.94 12.44 13.2 12.67 14.35 12.55
10.37 10.3 10.97 10.1 11.30 10.27
35.98 37.27 39.29 37.95 43.50 37.39
31.54 32.71 32.91 33.41 37.62 31.87
79.81 81.44 83.20 83.60 86.02 85.26
74.65 76.45 77.99 78.01 80.85 79.43
Sample size is 5,039. a Mean values obtained from NHANES and Robins studies.
DISCUSSION
According to the 2004 U.S. census, African Americans make up 12.3% of the country’s population. African American children represent an even higher proportion of the pediatric population in the United States, accounting, according to the 2004 census, for 16.5% of children less than 5 years of age [15]. The purpose of establishing the normative values for African American children and adolescents is not to create confusion for general pediatricians, but to emphasize the fact that hemoglobin values vary by ethnicity. With the ethnic diversity of the United States and its everchanging demographic patterns, practitioners need to be aware of how ethnicity and mixed ethnicity can influence what may be considered a normal hemoglobin value. These new reference values are intended to be used only
as guidelines; they are not designed to replace good clinical judgment and appropriate hematological workups. However, this newly developed reference table does provide documentation and a quick reference source for the racial differences in hemoglobin values between African American children and adolescents and non-Hispanic White children of the same ages. Although this information has been available in the NHANES database for years, and although the medical literature has, for decades, clearly demonstrated that normal hemoglobin values differ between African Americans and non-Hispanic Whites, a reference database for African Americans has never before been developed. Table III shows the normative hematological values for African American children of the ages of 2–18 years. American Journal of Hematology DOI 10.1002/ajh
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CONCLUSIONS
These guidelines presented here, which present mean hemoglobin concentrations and 2 std values for age and gender, will help pediatricians evaluate anemia in African American children. With the costs and restrictions of present-day health care, unnecessary anemia evaluation and treatment should be avoided. These guidelines will not only identify patients who need additional anemia evaluation, but also prevent the misdiagnosis of anemia in African American children and adolescents. REFERENCES 1. Dallman PR, Siimes M. Percentile curves for hemoglobin and red cell volume in infancy and childhood. J Pediatr 1979;94:26–31. 2. Nathan D, Oski F. Hematology of Infancy and Childhood, 5th ed. Philadelphia: W.B. Saunders; 1998. 3. Jackson RT. Separate hemoglobin standards for Blacks and Whites: A critical review of the case for separate and unequal hemoglobin standards. Med Hypothesis 1990;32:181–189. 4. Williams DM. Racial differences of hemoglobin concentration: Measurements of iron, copper, and zinc. Am J Clin Nutr 1981; 34:1694–1700. 5. Sherry BL, Mei Z, Yip R. Continuation of the decline in prevalence of anemia in low-income infants and children in five states. Pediatrics 2001;107:677–682.
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6. Garn SM, Ryan AS, Owen MD, Abraham S. Income matched Black–White hemoglobin differences after correction for low transferring saturations. Am J Clin Nutr 1981;34:1645–1647. 7. Castro O, Haddy TB, Rana SR. Age and sex related blood cell values in healthy Black Americans. Public Health Rep 1987;102: 232–237. 8. Summer L. National Academy on an Aging Society, Washington, DC. Retrieved January 6, 2005 from world wide web. http// www.agingsociety.org 9. Polhamus B, Dalenius K, Thompson D, Scanoln K, Borland E, Smith B, Grummer-Strawn L. Pediatric Nutrition Surveillance 2002 Report. Atlanta: U.S. Department of Health and Human Services, Center for Disease Control and Prevention; 2004. 10. Perry GS, Byers T, Yip R, Margen S. Iron nutrition does not account for the hemoglobin differences between Blacks and Whites. J Nutr 1992;122:1417–1424. 11. Nduka N, Aneke C, Maxwell-Owhochuku SM. Comparison of some haematological indicies of Africans and Caucasians resident in the same Nigerian environment. Haematologica 1988;2:57–63. 12. National Center for Health Statistics. Second National Health and Nutrition Examination Survey (NHANES II) Public-Use Data Files. 1982. Hyattsville, MD: NCHS. 13. Robins EB, Nichols E, Dwarka R. Hemoglobin concentrations in African American Children in NYC. Are separate normative values necessary for anemia evaluation. Presented at the American Academy of Pediatric Annual Meeting. Section of Epidemiology; 2004. 14. National Center for Health Statistics.Third National Health and Nutrition Examination Survey (NHANES III) Public-Use Data Files. 1999. Hyattsville, MD: NCHS. 15. U.S. Census Bureau. American Community Survey; 2004.