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Overweight black adults with homozygous sickle cell disease.

Introduction

Sickle cell disease (SCD) is a major public health concern that has great impact on both individuals and the society. In the United States, one in every 375 African Americans has SCD (Sibinga, Shindell, Casella, Duggan & Wilson, 2006). Sickle cell disease is an incapacitating disease resulting in chronic hemolytic anemia and vaso-occlusion, in almost all organs, leading to significant morbidity and early mortality (Schnog et al., 2004). In 2004, there were over 113,000 related SCD hospitalizations. Adults accounted for more than three quarters of these hospitalizations. In the same year, the average length of stay among adults was five days. Its cost was approximately $500 million in 2004 (Steiner & Miller, 2006).

Sickle cell anemia (HbSS) is the most serious and common type of SCD. Among children and adults with HbSS the median age at death was 42 years for males and 48 years for females. Many patients with SCD are now surviving into their fifth and sixth decades. This could be partially due to the implementation of newborn screening and improved pediatric management. In individuals diagnosed with sickle cell-hemoglobin C disease, the median age at death was 60 years for males and 68 years for females (Platt, Brambilla, & Rosse, 1994).

Several studies have documented growth abnormalities in children and adolescents. For example, Barden, Kawchak, Ohene-Frempong, Stalling & Zemel (2002) conducted a study in children that revealed significantly lower height, weight, arm circumference, upper and lower arm fat and muscle measurements . These growth deficits may be due to the deficiency of the growth hormone (GH) as observed by Nunlee-Bland, Rana, Houston-Yu, & Odonkor (2004). At the American Society of Hematology Annual Meeting and Exposition (2008), it was reported than the trend of overweight and obesity were similar to those observed in the general pediatrics population (Halpern, Welch, Hirway, & Chawla, 2008). Ashcroft and Serjeant (1972) demonstrated, in studies conducted in Jamaica, that by adulthood, individuals with SCD attained normal height or had substantial height gain. In 2001, a study examined the body composition of 22 adult women using dual-energy X-ray absorptiometry (DEXA) and a standard seven-day physical activity recall questionnaire to determine the resting energy expenditure. The percentage of body fat was 32.6% which indicated obesity; however, body mass index (BMI) was within the acceptable range at 22.6 (Woods et al., 2001). No significant difference was observed between the individuals with SCD and the controls.

Although major steps have been taken to understand the etiology of the disease, there are few successes in the treatment and management of SCD. Despite the increasing awareness that nutritional factors play a crucial role in the expression of a variety of chronic diseases, their role in SCD pathophysiology and treatment has not been fully examined. Only a relatively small number of studies have examined the nutritional status of children and adolescents with SCD, and the literature is even sparser for adults. It is expected that by investigating the anthropometric measurements, body composition, and energy expenditure of individuals with SCD, some explanation may be found for the wide clinical variation observed in the course of the disease.

The purpose of the study was to assess the anthropometric measurements, body composition, and energy expenditure of adults with sickle cell disease and healthy controls. Also, it is possible that by investigating these parameters new approaches and therapy for the treatment and management of SCD will emerge.

Materials and Method

A healthy control group of 14 (ten females and four males) with HbAA was randomly recruited from the Howard University community--hospital and university. Eight participants were African American adults (six females and two males) ages 18 - 69 years diagnosed with sickle cell anemia (SCA) homozygous HbSS disease. Subjects with SCD were recruited from the Howard University Sickle Cell Clinic. Participants were identified and characterized by ion-exchange high performance liquid chromatography (HPLC) of hemoglobins which is routinely used for HBSS screening (Wilson, Headlee, & Huismann, 1983). Only healthy controls and sickle cell patients in a steady state for a minimum of two weeks were selected for the study. All participants were given medical clearance for participation by a physician. Individuals who were transfused within the last 30 days, requiring oxygen supplementation, had vaso-occlusion within the last two weeks, diagnosed with HIV/AIDS, diabetes, cancer, and end stage renal disease--dialysis dependent were excluded from the study.

A stadiometer was used to measure height. Heights are accurate to 1 mm. A beam balance was used to determine the participants' weights. Weight was accurate to 0.1 kg. Body mass index (BMI) was calculated using the standard formula--weight (kg) divided by [height.sup.2]/m. Measurement of the waist circumference was done at a level midpoint between the lower rib margin and iliac crest. Hip measurement was taken from the maximum circumference of the hip. Waist to hip ratio was derived by dividing waist measurement by hip measurement (Seidel, 2001).

The participants' body composition was measured using the Tanita Body Composition Analyzer; Model TBF-300 (Arlington Heights, IL.). Maximum weight of the analyzer is 200 kg, fat ratio 0.1% increments, and range of fat ratio 1% - 75%. Body composition was determined by using bioelectrical impedance analysis. An electrical impedance of total body water is used to calculate fat-free mass and body fat. A frequency of 50 kHz is passed from the analyzer through foot to foot contact with the analyzer and the individual. Percent body fat was calculated from body fat.

The Vmax (SensorMedics, Yorba Linda, CA) machine was used to measure the participants' energy expenditure. Resting energy expenditure (REE) was measured by having the participant at rest in a bed in a supine position for 30 minutes. The participants were required not to move arms and legs; but not sleeping. The participant did not eat for at least three hours before starting the test. The participants were attached to an indirect calorimetry system that collected respiratory gases, and measured oxygen consumption (V[O.sub.2]) and carbon dioxide production (VC[O.sub.2]). Resting energy expenditure was measured at steady state during a five minute period when V[O.sub.2] and VC[O.sub.2] changes by less than 10%, and the average respiratory quotient (RQ) changes by less than 5%. Respiratory quotient (RQ) was calculated by using the standard formula - VC[O.sub.2] divided by V[O.sub.2].

This research was conducted according to the policies and procedures of Howard University Institutional Review Board (IRB) and the General Clinical Research Center (GCRC) at Howard University Hospital. Informed consent forms were obtained from all participants.

Statistical Analysis

The data were analyzed using the Statistical Package for the Social Sciences (SPSS) for Windows, Version15.0 (SPSS Inc., Chicago, IL). Descriptive and inferential statistics were used to analyze the data. Data were presented as means + standard errors of the mean (SEM). Independent sample t-test was used to assess differences between groups. Pearson's correlation coefficient and linear regression were calculated to determine relationship among resting energy expenditure, body composition, and anthropometric measurements. Statistical significance was determined at the 5% level.

Results

Linear regression was used to determine the relationships of age and gender to the anthropometric measurements. No significant differences were identified (p>0.05); therefore, the data was not adjusted for these factors (age and gender). Height, weight, BMI, waist, and hip measurements were comparable in both groups (Table 1). No significant difference was obtained with body fat percentage (p>0.05) but the acceptable range was exceeded by 53% in the control group and by 29% in the sickle cell group. There was a statistically significant difference between the groups' waist to hip ratio (p< 0.01). Although the BMI were similar (p>0.05) (p>0.05) they were above the acceptable range of 18.5 - 24.9. Females in the control and sickle cell groups both exceeded the recommended value of 0.7 for a healthy waist to hip ratio and waist measurement of 88.9 cm. The males' waist to hip ratio was below the recommended value of 101.6 cm, in both the control and sickle cell groups (0.86 and 0.87 respectively).

Table 2 provides the correlations among the anthropometric measurements. There were positive relationships among weight, BMI, waist, hip, fat mass measurements (p=0.000), body fat percent (p=0.001) and waist to hip ratio (p=0.013). Body mass index had positive association with waist, hip, fat mass measurements, body fat percent (p=0.000), and waist to hip ratio (p=0.003). There were positive associations among waist, hip, fat mass measurements, waist to hip ratio and body fat percent (p=0.000). Hip measurement had positive association with fat mass, body fat percent (p=0.000) and waist to hip ratio (p=0.016). Waist to hip ratio had positive relationships with fat mass (p=0.012) and body fat percent (p=0.010). There was also a positive association between fat mass and body fat percent (p=0.000).

No statistically significant differences were determined between the two groups for measured resting energy expenditure (REE), predicted REE, oxygen consumption (V[O.sub.2]), carbon dioxide production (VC[O.sub.2]) and respiratory quotient (RQ). The measured REE for both groups was above the predicted REE (Table 3).

The correlations between REE and weight, BMI, waist, and hip are shown in Table 4. Strong positive associations were observed among the variables, with the relationship between weight and REE being highly significant (p=0.001).

Discussion

Several important, new and unexpected findings have been made in this study of adult sickle cell patients. Current available literature on the body composition, anthropometric measurements, and energy expenditure of adults with sickle cell is very limited. All the sickle cell participants were in a steady-state prior to the start and the duration of the study. Participants in both the control and sickle cell groups had sedentary lifestyles.

Gender and age both have been well-documented to have impacts on anthropometric measurements and body composition (Plowman and Smith 2003). Females have a higher percentage of body fat, which increases as one gets older. The data from the study were comprised of both genders of various ages. The data were tested using linear regression (SPSS; version 15.0) to determine if gender and age had a statistical significance on the results. No statistical difference was observed; therefore, the data were analyzed without adjusting for age and gender.

Although weight, BMI, waist, hip measurements and body fat percentage were similar in both groups, the findings revealed that the subjects were overweight in both the control and sickle cell groups. Woods et al., (2001) reported findings of obesity in women with sickle cell disease with high levels of body fat and body fat percentage, with an acceptable range of BMI. Pells et al., (2005) also reported overweight and obesity in adult sickle cell subjects. This study however found a high percentage of body fat and BMI values above the healthy range of 18.5 - 24.9 (Table 1). All the anthropometric measurements and body composition data (BMI, weight, waist, and hip measurements, waist to hip ratio, fat free mass, and body fat percent) gleaned in this study indicate overweight (Table 1). Body mass index is a common marker used to define overweight and obesity as an indicator for risk for chronic diseases (e.g. hypertension, type 2 diabetes mellitus, and certain types of cancer).Therefore overweight HBSS individuals may be at a higher risk for chronic diseases.

The findings of overweight adult sickle cell individuals and normal height is of particular interest. It has been well established that children with sickle cell disease have low body weight and retarded height compared to healthy subjects (Barden, et al., 2002). However, Ashcroft & Serjeant (1972) argued that adults with sickle cell disease do attain normal height or had substantial height gain by adulthood. It is generally perceived that sickle cell disease individuals are underweight. This study provided evidence that people with sickle cell disease were above their healthy weight range, and that women are at greater risk for chronic diseases associated with overweight and obesity, as evidenced in increased waist to hip ratio and waist measurement.

The World Health Organization (WHO) estimates that approximately one billion people are overweight globally (WHO, 2000). The negative impact of excessive body fat has been well documented (Fontana and Klein, 2007; Ghosh and Bandyopadhyay, 2007; Pedersen, 2007). The findings of this study are consistent with other anthropometric measurements and body composition studies that show a steady and consistent upward trend in the incidence of overweight and obesity. The Centers for Disease Control and Prevention (CDC) estimated that 79.6 % and 67% of Blacks or African Americans (females and males respectively) are overweight between the years of 1999 - 2004 (ages 20 - 74 years); compared to 66.5 % in females and 58.2 % in males during the period of 1988 -1984 (CDC, 2007).

As expected, this study established a strong positive relationship between the various anthropometric measurements and body composition data that were collected (Table 2).

An individual's weight is usually related to his/her BMI, waist and hip measurements, waist to hip ratio, fat free mass and body fat percent and vice versa. However, this may not always hold true; for example, high body fat may not result in above normal BMI. This finding has been reported by Woods, et al. (2001).

It is generally accepted and well documented that age and gender influence resting energy expenditure (REE) (Plowman and Smith, 2003). Resting energy expenditure usually decreases with age and males have a higher REE than females. Larger muscle tissues in males contribute primarily to this difference seen in males and females. Linear regression was used to determine the effect of age and gender on REE. Again, no statistical differences were observed. This may be due to the sample size.

Several studies have measured resting energy expenditure in children and adolescents with sickle cell disease, but these findings have been contradictory (Woods, et al., 2001; Borel, Buchowski, Turner, Goldstein & Flakoll, 1998; Badaloo, Jackson & Jahoor, 1989). The studies have reported hypermetabolism, normal metabolism, and hypometabolism. This study however, found no statistical difference between the control and sickle cell groups' resting energy expenditure (REE) measurements (Table 3). Both groups' measured REE was above the predicted (calculated) REE. This result was not unexpected as most individuals are above their predicted REE. It is estimated that 85% of all healthy persons' measured REE will be 10% above their predicted REE. The remaining 15% may be higher than 20% as reported by Plowman and Smith (2003).

Although the sickle cell group had less oxygen consumption (VO2) it was not statistically different from the control group. Oxygen consumption was 20% less in the sickle cell group compared to the control group (Table 3). It could be theorized that the sickle cell participants' uptake of oxygen was less due to the pathophysiology of the disease as individuals with sickle cell disease have less normal hemoglobin because the red blood cells lose hemoglobin when the cells become rigid, thus affecting the transport of oxygen to be utilized at a cellular level.

The quantity of oxygen used and the carbon dioxide expired is indicative of the oxidation of fat, protein and carbohydrate. Based on the volume of oxygen consumed and carbon dioxide produced the respiratory quotient (RQ) was calculated (Table 3). No significant difference was seen in the RQ, but a value of 0.82 in the control suggests a balanced diet for all three macronutrients. In the sickle cell group the RQ was 0.80. Again, this indicates a fairly well mixed diet with maybe a slightly higher reliance on fat oxidation than in the control group. There is direct relationship between REE and an individual's weight (Table 4). Resting energy expenditure is related to body surface area (Plowman and Smith, 2003). The body surface area or weight of a person influences the amount of energy utilized. The strong correlation between REE and weight observed in this study has been previously documented (Das et al., 2003). This study earlier discussed that weight had a strong positive association with waist and hip measurements. Therefore, the positive relationship between REE and waist and hip measurements are within the general trends of findings for this study.

Conclusion

The findings revealed above healthy range BMI, waist circumference measurement and waist to hip ratio in the sickle cell group. This is indicative of overweight and obesity in the subjects. The study has provided evidence that the trends of obesity adults within the United States and globally is consistent in sickle cell anemia subjects. This indicates the need for nutrition education for weight management and improved nutritional status with sickle cell patients. Additional studies are required to determine the association among body composition, anthropometric measurements, vaso-occlusion and other complications associated with sickle cell disease.

References

Ashcroft, M.T., & Serjeant, G.R. (1972). Body habitus of Jamaican adults with sickle cell anemia. Southern Medical Journal, 65, 579 - 82.

Badaloo, A., Jackson, A.A., & Jahoor, F. (1989). Whole body protein turnover and resting metabolic rate in homozygous sickle cell disease. Clinical Science, 77, 93 - 97.

Barden, E.M., Kawchak, D.A, Ohene-Frempong, K., Stalling, V.A. & Zemel, B.S. (2002). Body composition in children with sickle cell disease. American Journal of Clinical Nutrition, 76, 218 - 225.

Borel, M.J., Buchowski, M.S., Turner, E.A., Goldstein, R.A. & Flakoll, P.J. (1998). Protein turnover and energy expenditure increase during exogenous nutrient availability in sickle cell disease. American Journal of Clinical Nutrition, 68, 607 - 614

Centers for Disease Control. (2007). Centers for Disease Control and Prevention National Health and Nutrition Examination Survey. Retrieved from http://www.cdc.gov/nchs/data/hus/hus04trend.pdf#069

Das, S.K., Roberts, S.B., McCrory, M.A., Hsu, L.K., Shikora, S.A., Kehayias, J.J. & Dallal, G.E. (2003). Long-term changes in energy expenditure and body composition after massive weight loss induced by gastric bypass surgery. American Journal of Clinical Nutrition, 78, 22 - 30.

Fontana, L. & Klein, S. (2007). Aging, adiposity, and calorie restriction. Journal of the American Medical Association, 297, 986 - 994.

Ghosh, J.R. & Bandyopadhyay, A.R. (2007). Comparative evaluation of obesity measures: relationship with blood pressures and hypertension. Singapore Medical Journal , 48, 232 - 5.

Halpern, A.B., Welch, J.G., Hirway, P. & Chawla, A. (2008) Prevalence and complications of obesity in sickle cell disease. (American Society of Hematology Annual Meeting, San Francisco, CA 2009). Abstracts, 112, 434

Nunlee-Bland, G., Rana, S.R., Houston-Yu, P.E. & Odonkor, W. (2004). Growth hormone deficiency in patients with sickle cell disease and growth failure. Journal of Pediatric Endocrinology Metabolism, 17, 601 - 606.

Pedersen, B.K. (2007). Body mass index-independent effect of fitness and physical activity for all-cause mortality. Scandinavian Journal of Medicine and Science in Sports, 17, 196 - 204

Pells, J.J., Presnell, K.E., Edwards, C.L., Woods, M., Harrison, M.O., DeCastro, L. & Robinson, E. (2005). Moderate chronic pain, weight and dietary intake in African-American adult patients with sickle cell disease. Journal of the National Medical Association, 97, 1622-1629

Platt, O.S., Brambilla, D.J., Rosse, W.F., Milner, P.F., Castro, Steinburg, M.H. & Klug, P.P. (1994). Mortality in sickle cell disease. Life expectancy and risk factors for early death. New England Journal of Medicine, 330, 1639 - 1644.

Plowman, S.A. & Smith, D.L. (2003). Body composition: Determination and Importance. In: Plowman SA, Smith DL (Ed.). Exercise Physiology (2nd ed.). San Francisco, CA: Benjamin Cummings.

Schnog, J.B., Duits, A.J., Muskiet, F.A., ten Cate, H., Rojer, R.A. & Brandjes, D.P. (2004). Sickle cell disease; A general overview. Journal of Medicine, 62, 364-374.

Seidel, J.C. (2001). Report from a CDC Preventation Workshop on Use of Adult Anthropometry for Public Health and Primary Care. American Journal of Clinical Nutrition, 73: 123 - 6

Sibinga, E.M., Shindell, D.L., Casella, J.F., Duggan, A.K. & Wilson, M.H. (2006). Pediatric patients with sickle cell disease: use of complementary and alternative therapies. The Journal of Alternative Complementary Medicine, 12, 291 - 298

Steiner, C.A. & Miller, J.L. (2006). Sickle cell disease patients in U.S. hospitals, 2004. Healthcare Cost and Utilization Project, 21

Wilson, J.B., Headlee, M.E. & Huismann, T.H. (1983). A new high-performance liquid chromatographic procedure for the separation and quantitation of various hemoglobin variants in adults and newborn babies. Journal of Laboratory and Clinical Medicine, 102, 174 - 86.

Woods, K.F., Ramsey, L.T., Callahan, L.A., Mensah, G.A., Litaker, M.S. Kutlar, A. & Gatlin, B. (2001). Body composition in women with sickle cell disease. Ethnicity & Disease, 11, 30 - 5.

World Health Organization. 2002. The 2002 WHO Consultation on Obesity. Obesity: Preventing and Managing the Global Epidemic. (WHO Technical Report Series 894) Geneva, Switzerland: World Health Organization.

Judith Camele Anglin, Ph.D., R.D.

Assistant Professor

College of Health and Human Services

California State University, Long Beach

James S. Adkins, Ph.D.

Professor, Director of Graduate Studies

Department of Nutritional Sciences

Howard University

Allan A. Johnson, Ph.D., L.N.

Professor and Dean

College of Allied Health Sciences

Howard University
TABLE 1
Weight, Height, Body Mass Index, Hip,
Waist Measurements and Waist to Hip Ratio

                   Control Group            Sickle Cell
Measurements         (n = 14)             Group (n = 13)       p value

Weight (kg)    82.59 [+ or -] 6.91     68.11 [+ or -] 5.44     0.235
Height (cm)    169.58 [+ or -] 2.70    164.03 [+ or -] 2.66    0.291
BMI            29.17 [+ or -] 2.38     25.92 [+ or -] 2.84     0.957
Waist (cm)     95.18 [+ or -] 5.26     90.25 [+ or -] 5.66     0.533
Hip (cm)       108.40 [+ or -] 4.25    102.22 [+ or -] 5.68    0.981
Waist to hip
  ratio        0.87 ** [+ or -] 0.02   0.88 ** [+ or -] 0.01   0.008
Body fat (%)   33.01 [+ or -] 3.54     28.71 [+ or -] 4.41     0.830

The present data are means [+ or -] SEM; p< 0.01

TABLE 2
Pearson's Correlation Coefficients (r) among
Anthropometric Measurements and Body Composition

Variable   Weight   BMI        Waist      Hip        W/HR (1)

Weight r            0.92 ***   0.88 ***   0.87 ***   0.52
p Value             0.000      0.000      0.000      0.013

BMI
r                              0.96 ***   0.96 ***   0.61 **
p Value                        0.000      0.000      0.003

Waist r                                   0.95 ***   0.73 ***
p Value                                   0.000      0.000

Hip r                                                0.51 *
p Value                                              0.016

W/HR
r
p Value

Fat mass
r
p Value

Variable   Fat mass   BF%

Weight r   0.69 ***   0.64 ***
p Value    0.000      0.001

BMI
r          0.82 ***   0.82 ***
p Value    0.000      0.000

Waist r    0.83 **    0.79 **
p Value    0.000      0.000

Hip r      0.85 ***   0.79 ***
p Value    0.000      0.000

W/HR
r          0.52 *     0.54 **
p Value    0.012      0.010

Fat mass
r                     0.79
p Value               0.000

The present data are means [+ or -] SEM; W/HR: waist to hip
ratio; BF: body fat; * p [less than or equal to] 0.05; ** p [less
than or equal to] 0.01; *** p [less than or equal to] 0.001

TABLE 3
Resting Energy Expenditure, Oxygen Consumption,
Carbon Dioxide Production, and Respiratory Quotient

Energy Measurements         Control Group
                              (n = 13)

Measured REE (kcal)    2088.31 [+ or -] 109.12
Predicted REE (kcal)   1677.23 [+ or -] 92.26
Predicted REE (%)      125.23 [+ or -] 3.94
V[0.sub.2] (L/min)     0.30 [+ or -] 0.02
VC[0.sub.2] (L/min)    0.25 [+ or -] 0.01
RQ                     0.82 [+ or -] 0.02

Energy Measurements       Sickle Cell Group      p Value
                               (n = 8)

Measured REE (kcal)    1870.13 [+ or -] 133.92   0.862
Predicted REE (kcal)   1463.50 [+ or -] 69.17    0.347
Predicted REE (%)      127.38 [+ or -] 5.89      0.798
V[0.sub.2] (L/min)     0.24 [+ or -] 0.04        0.292
VC[0.sub.2] (L/min)    0.19 [+ or -] 0.03        0.381
RQ                     0.80 [+ or -] 0.02        0.055

The present data are means [+ or -] SEM

TABLE 4
Pearson's Correlation Coefficients (r) between Resting Energy
Expenditure and Weight, Body Mass Index, Waist, and Hip Measurements

Measurements      REE (1)

Weight
r                 0.70 **
p Value           0.000

Body Mass Index
r                 0.56 *
p Value           0.008

Waist
r                 0.58 *
p Value           0.006

Hip
r                 0.56 *
p Value           0.009

REE: resting energy expenditure; * p [less than or
equal to] 0.01; ** p [less than or equal to] 0.001
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Author:Anglin, Judith Camele; Adkins, James S.; Johnson, Allan A.
Publication:Journal of the National Society of Allied Health
Article Type:Clinical report
Geographic Code:1USA
Date:Mar 22, 2011
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