- Email: [email protected]
Assessment of the skeletal health of healthy Nigerian men and women using quantitative ultrasound
Bone 35 (2004) 387 – 394 www.elsevier.com/locate/bone
Assessment of the skeletal health of healthy Nigerian men and women using quantitative ultrasound D.J. VanderJagt, a,* L.A. Damiani, a T.M. Goodman, a I.O.A. Ujah, b M.O. Obadofin, b G.E. Imade, b D.R. Shatima, c and R.H. Glew a,* a
Department of Biochemistry and Molecular Biology, University of New Mexico School of Medicine, Albuquerque, NM 87131, USA b Jos University Teaching Hospital, Jos, Nigeria c National Hospital Abuja, Abuja, Nigeria Received 22 December 2003; revised 5 March 2004; accepted 1 April 2004
Abstract The dietary intake of calcium by African populations, particularly in sub-Saharan Africa, is relatively low compared to the recommended intake for US adults. However, the rate of osteoporotic fractures in West African women is reported to be less than that for Caucasian populations. Because there is little published data regarding the skeletal status of African men and women, we used quantitative ultrasound (QUS) to assess the bone density of 435 Nigerian women and 321 Nigerian men between 16 and 89 years of age. A progressive decline in bone quality was observed beginning at about 40 years of age for both men and women. The mean stiffness index (SI) for the women between 20 and 35 years of age (n = 186) in this study was 102 F 17. The equation that best described the age versus SI relationship for women was SI = 79.7 + 1.887 (age) + 0.043 (age)2 + 0.00020 (age)3. For Nigerian men, the peak SI of 115 F 17 was seen in the 20- to 29-year-old age group. For men, the SI values remained above 100 until about age 60 years when a significant decline in SI was then observed. The best-fit curve of SI versus age for men was SI = 134.9 1.27 (age) + 0.019 (age)2 0.00014 (age)3. The broadband ultrasound attenuation (BUA), speed of sound (SOS), and SI values for the Nigerian men and women were comparable to or higher than those reported for Caucasian and Asian populations. These data should serve as reference values for adult men and women in sub-Saharan Africa. D 2004 Elsevier Inc. All rights reserved. Keywords: Bone density; Quantitative ultrasound (QUS); Broadband ultrasound attenuation (BUA); Speed of sound (SOS); Stiffness index (SI); Nigeria; Men; Women
Introduction Osteoporosis is characterized by low bone density and deterioration of bone microarchitecture resulting in increased bone fragility and fracture risk. Although osteoporosis is an important cause of debility and morbidity in the elderly, the incidence of age-related osteoporotic fractures varies widely between different populations and ethnic groups [1]. The fact that hip fracture rates for Caucasian populations in the United States and Europe have been reported to be higher than those in Africa, Asia, and South America [2] has led to the questionable assumption that osteoporosis is not a significant problem in these less developed regions of the * Corresponding authors. Department of Biochemistry and Molecular Biology, University of New Mexico School of Medicine, Room 245, BMSB, Albuquerque, NM 87131-5221. Fax: +1-505-272-3518. E-mail address: [email protected] (R.H. Glew). 8756-3282/$ - see front matter D 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.bone.2004.04.001
world. However, projected demographics suggest that over the next 50 years, three fourths of the world’s elderly will reside in Africa, Asia, and Latin America, and these trends are likely to result in a significant increase in the number of fractures reported in these populations [2]. Bone density at any age is dependent on peak bone density attained in early adulthood, usually by age 30 years, and the subsequent rate of bone loss with age. Adequate dietary calcium intake over a lifetime is important in the accrual of bone mass during growth and the conservation of bone mass thereafter [3]. The indigenous people of West Africa and other parts of sub-Saharan Africa are subject to a variety of factors which can lead not only to a decrease in the maximum bone mass that an individual attains but also an accelerated age-related bone loss. First, diets in West Africa generally contain relatively low amounts of calcium [4,5]. For example, it was estimated that pregnant and lactating women in rural Gambia have a dietary calcium intake of 400
388
D.J. VanderJagt et al. / Bone 35 (2004) 387–394
mg/day [4]. In a recent dietary study conducted in northern Nigeria, we reported the mean dietary calcium intakes for urban men and women were 551 and 447 mg/day, respectively [5]. These intakes are substantially below the US recommended dietary intakes of 1000 mg/day for adults [6]. Second, in addition to low-calcium diets, many populations in sub-Saharan Africa place a heavy reliance on cereal staples which contain oxalates and other divalent metal cation chelators that decrease the bioavailability of calcium as well as other trace minerals [7]. Third, African women are under the additional calcium-depleting stress of extended breastfeeding of 2 years or more for each child, a condition which is exacerbated by high parity [8]. Fourth, estrogen replacement therapy is generally not widely available for post-menopausal women in most parts of Africa, primarily for economic reasons. Collectively, these factors place most Africans, particularly post-menopausal women, at an increased risk for osteoporosis and bone fracture. Despite these risk factors, the few published reports regarding fracture rates for African women suggest that bone fractures may be relatively uncommon in populations in West Africa [1,9 – 11]. In a study of fracture rates in 360,000 Nigerian women over 50 years of age, the incidence of hip and forearm fractures was reported to be 100 times lower for Nigerian women than for Caucasian women of comparable age in England [10]. The low fracture rate for Nigerian women is unexpected since we had shown in a previous study of 218 Nigerian women that they had significantly higher levels of NTx, a marker of bone turnover, than Caucasian women matched for age and body mass index [12]. There are no comparable data for African men. Bone strength or quality is determined by bone mineral density, bone architecture, and elasticity. Because there is currently no direct measure of bone strength, bone mineral density is the accepted surrogate for bone strength. Dualenergy X-ray absorptiometry (DXA) is considered the gold standard for the determination of bone density and estima-
tion of fracture risk. However, QUS of the calcaneus has been shown to be as reliable as DXA in predicting fracture risk in postmenopausal women [13 – 15]. In addition, QUS has the added advantages of relatively low cost and portability compared to DXA, thereby making it suitable for use in a developing country such as Nigeria. In this report, we describe the results of a cross-sectional study of the bone status of healthy Nigerian men and women using QUS and have compared these results with those reported for American, European, and Asian populations using the same ultrasound instrument.
Materials and methods Subjects Men and women were recruited from among hospital staff and visitors at the outpatient clinics of the National Hospital Abuja, Abuja, Nigeria, and the Jos University Teaching Hospital in Jos, Nigeria. Abuja is a metropolitan center and the capital of Nigeria, whereas Jos is a smaller city with a mix of ethnic groups who have traditional as well as urban lifestyles. Exclusion criteria for both the men and women included prolonged immobility, malignancy, renal or endocrine disease, recent surgery, or bone fracture. Information regarding age, previous fractures, and current medications was obtained for each subject. Women who were nursing or pregnant were excluded from the study. Measurements of height, weight, triceps skin-fold thickness, and mid-arm circumference were obtained for all subjects. For women, parity and menstrual status were recorded. Informed consent was obtained from each subject and this study was approved by the Ethics Review Committees of the Jos University Teaching Hospital, Jos, Nigeria and National Hospital, Abuja, Nigeria and by the Human Research Review Committee of the University of New Mexico, Albuquerque, New Mexico, USA.
Table 1 Anthropometric characteristics of the Nigerian women by decade of age Age interval (years)
n
Age (years)
Weight (kg)
Height (cm)
BMI (kg/m2)
Mid-arm circumference (cm)
Triceps skin-fold (mm)
16 – 19 20 – 29 30 – 39 40 – 49 50 – 59 60 – 69 70 – 79 80 – 89
15 104 123 91 62 20 14 6
18.1 24.8 34.1 43.7 51.9 62.3 71.4 81.7
49.4 61.9 69.4 70.2 69.2 69.4 53.2 51.9
158.9 162.0 162.2 160.5 159.0 159.6 159.4 159.0
19.6 23.4 26.4 27.3 27.4 27.3 21.0 20.5
23.5 26.6 29.4 31.1 31.0 30.9 26.1 24.4
19.1 20.9 25.6 28.0 27.3 25.8 21.2 16.7
a
F F F F F F F F
1.0 2.8 2.8 3.0 2.7 2.7 2.2 2.6
F F F F F F F F
9.3 14.3 15.1a 15.0a 14.7b 15.0d 16.3d 9.7
Significantly different from 20- to 29-year-old group: P < 0.001. Significantly different from 20- to 29-year-old group: P = 0.003. c Significantly different from 20- to 29-year-old group: P = 0.002. d Significantly different from 20- to 29-year-old group: P = 0.03 – 0.05. e Significantly different from 20- to 29-year-old group: P = 0.01. b
F F F F F F F F
4.0 6.3 7.0 5.7 5.8c 5.3 3.6 2.9
F F F F F F F F
3.2 5.0 5.2a 5.9a 5.7a 6.0c 6.4 4.0
F F F F F F F F
4.8 4.9 4.4a 5.3a 5.3a 4.3a 5.0 5.0
F F F F F F F F
5.4 7.7 7.6a 8.0a 8.5a 9.4e 9.7 11.1
D.J. VanderJagt et al. / Bone 35 (2004) 387–394
389
Table 2 Anthropometric characteristics of Nigerian men by decade of age Age interval (years)
n
Age (years)
Weight (kg)
Height (cm)
BMI (kg/m2)
Mid-arm circumference (cm)
Triceps skin-fold (mm)
18 – 19 20 – 29 30 – 39 40 – 49 50 – 59 60 – 69 70 – 79 80 – 89
3 83 103 68 36 20 5 3
18.3 25.5 34.1 44.2 53.8 62.5 73.8 81.0
57.3 66.0 71.2 72.2 68.9 62.2 56.9 64.6
169 172 171 168 169 167 165 170
20.1 22.2 24.5 25.6 24.1 23.2 20.9 22.5
26.3 29.0 30.1 36.1 29.7 27.1 25.1 26.7
9.30 10.5 14.1 13.5 13.7 10.8 9.20 7.00
F F F F F F F F
0.6 2.8 2.9 3.0 2.9 2.3 2.4 1.0
F F F F F F F F
3.7 11 11 13a 12 13 14 3.4
F F F F F F F F
5.2 6.8 6.5 6.4a 5.7 6.8b 6.9c 1.8
F F F F F F F F
2.3 3.0 3.6a 3.5a 4.0 4.3 4.0 0.7
F F F F F F F F
2.0 3.0 3.4 4.4 3.2 4.0 3.6 1.2
F F F F F F F F
1.2 6.3 7.3a 6.6 6.6 7.4 6.3 2.6
a
Significantly different from the 20- to 29-year-old group: P < 0.001. Significantly different from the 20- to 29-year-old group: P = 0.002. c Significantly different from the 20- to 29-year-old group: P = 0.021. b
software were generated from healthy Caucasian women in the US. A separate T-score was calculated using SI data for the young African women in the study group who were between 20 and 35 years of age. Because reference data for men were not available, the T-scores for men were calculated using data for young Nigerian men 20 – 29 years old. Tscores were also calculated for Nigerian men using data obtained with the same model ultrasound instrument used for Italian and Japanese males between 20 and 29 years of age who served as the reference population [16,17].
Ultrasound measurement Ultrasound measurements of the calcaneus were obtained using the Achilles+ (Lunar Corporation, Madison, WI, USA) according to the manufacturer’s instructions. Each subject was seated with his or her right foot resting in the heel bath of the instrument. After introducing water into the heel bath, measurements of the speed of sound (SOS) transmission and the broadband ultrasound attenuation (BUA) were made. BUA is defined as the slope of the regression line derived from the ratio of the signal amplitude of the calcaneus to that of water (reference) at each frequency of ultrasound (dB/MHZ). SOS refers to the speed of the sound wave traveling through the calcaneus, measured in m/s. The stiffness index (SI) was calculated for each subject using the equation SI = (0.67 BUA) + (0.28 SOS) 420. Calibration of the instrument was monitored using a phantom heel. Reproducibility was validated by measuring the same control subject each day that measurements were made on the study subjects. For female subjects, the T-score was calculated as follows: T-score = (subject SI mean SI of the reference group) / (standard deviation of the reference group). The data for the reference population provided in the instrument
Statistical analysis Results are expressed as the mean F standard deviation. Statistical analysis was performed using the Number Crunching Statistical Software program (NCSS 2000, Kaysville, UT). Comparisons of parameters between decades of age were made using one-way ANOVA. Multiple regression analysis was used to determine the relation between anthropometric parameters and ultrasound variables. The regression equations of BUA, SOS and SI versus age were determined using the Table Curve 2D version of SPSS (SPSS 4.0, SPSS, Inc., Chicago, IL). A P value of 0.05 was considered statistically significant.
Table 3 Ultrasound parameters by decade of age for Nigerian women Age interval (years)
n
BUA (dB/MHz)
SOS (m/s) (mean F SD)
SI
16 – 19 20 – 29 30 – 39 40 – 49 50 – 59 60 – 69 70 – 79 80 – 89
15 104 123 91 62 20 14 6
128 F 130 F 131 F 126 F 120 F 116 F 98 F 93 F
1565 1556 1553 1549 1536 1515 1488 1492
103 102 102 97 90 81 62 60
a
14 13 14 15 20a 20a 13a 14a
F F F F F F F F
39 31 34 36 37a 36 27a 25a
T-score Caucasian reference (median (min, max)) F F F F F F F F
17 15 17 18 22a 21a 16a 15
0.21 0.13 0.13 0.16 0.66 1.2 2.1 2.5
( ( ( ( ( ( ( (
1.4, 3.3, 2.4, 3.2, 4.3, 3.8, 3.7, 3.9,
1.9) 2.0) 2.7) 2.3) 1.6) 1.6) 0.7) 0.9)
T-score Nigerian reference (median (min, max))
0.05 0.3 0.7 1.2 2.3 2.5
( ( ( ( ( (
– – 3.9, 3.1, 4.2, 3.7, 3.6, 3.8,
2.4) 2.1) 1.4) 1.4) 0.4) 1.0)
Significantly different from the 20- to 29-year-old group: P < 0.001; BUA, broadband ultrasound attenuation; SOS, speed of sound; SI, stiffness index*; T-score-C, based on data for Caucasian women; T-score-N, based on data for Nigerian women between 20 and 29 years of age in the present study group.
390
D.J. VanderJagt et al. / Bone 35 (2004) 387–394
Results Comments on the characteristics of the subjects Women A total of 435 women (301 premenopausal and 134 postmenopausal women) between the ages of 16 and 89 years were enrolled in the study. A summary of the characteristics of the female subjects by decade of age is given in Table 1. The majority of the women (87%) were between 20 and 59 years of age, with the lowest number of subjects being in the 16 – 19 (3.4%), 70– 79 (3.2%), and 80– 89 (1.4%) year age groups. There were progressive increases in weight, body mass index (BMI), mid-arm circumference and triceps skin-fold thickness for subjects over 30 years of age and these trends persisted until the seventh decade of age. Men A total of 321 Nigerian men aged 18 – 83 years participated in this study. A summary of the anthropometric measurements of the men is provided in Table 2. Eighty percent of men were between 20 and 50 years of age. The fewest number of subjects fell in the 18 –19 (0.93%) and the 80 – 89 (0.93%)-year-old age groups. For Nigerian men there was a progressive increase in weight, BMI, and midarm circumference after age 20 years, followed by a decline in each of these parameters after age 70 years to values that were comparable to those in the 18- to 19-year-old age group. Ultrasound parameters Women BUA, SOS, and SI parameters for the female subjects by decade of age are given in Table 3. Compared to the 20- to 29-year-old group, there was a decline in both BUA and SOS starting around 40 years of age; however, the decrease did not reach statistical significance until after 50 years of age (Figs. 1A and B). The mean SI for the women between 20 and 35 years of age (n = 186) in this study was 102 F 17. Compared with the 20- to 29-year-old group, a significant difference in SI was found for the women beginning with the 50- to 59-year-old age group. The equation that best described the age versus SI relationship for women was SI = 79.7 + 1.887 (age) + 0.04 3 (age)2 + 0.00020 (age)3 (Fig. 1C). Multiple regression analysis revealed that age and weight were significant determinants of BUA and SI for women (P V 0.001), whereas age alone was related to SOS (P < 0.001). When adjusted for age, height was not a significant determinant of any of the ultrasound parameters for the female subjects. Separate T-scores for the Nigerian women based on reference data for Caucasian and Nigerian women were calculated (Table 2). The T-scores for the Nigerian women
Fig. 1. (A) The relation between age and BUA for Nigerian women, BUA = 121.9 + 0.638 (age) – 0.012 (age)2. (B) The relation between SOS and age for Nigerian women, SOS = 1530 + 2.49 (age) 0.062 (age)2 + 0.0003 (age)3. (C) The relation between age and SI for Nigerian women, SI = 79.7 + 1.88 (age) 0.043 (age)2 + 0.00021 (age)3.
became progressively more negative with advancing age. The decline was similar to that seen in the T-scores for Caucasian women in the US [18]. No significant differences were found between T-scores calculated using Caucasian and Nigerian reference data. Men A summary of the BUA, SOS, and SI parameters for the male subjects by decade of age is shown in Table 4. Compared to the 20- to 29-year-old group, there was a progressive decline in both BUA and SOS with increasing age (Figs. 2A and B). In general, the men between 40 and 80 years of age had ultrasound parameters that were significantly lower than the younger males. For Nigerian men, the peak SI of 115 F 17 occurred in the 20- to 29-
D.J. VanderJagt et al. / Bone 35 (2004) 387–394
391
Table 4 BUA, SOS, and SI by decade of age for the Nigerian men Age interval (years)
n
BUA (dB/MHz)
SOS (m/s)
SI
18 – 19 20 – 29 30 – 39 40 – 49 50 – 59 60 – 69 70 – 79 80 – 89
3 83 103 68 36 20 5 3
131 F 137 F 135 F 130 F 129 F 123 F 110 F 118 F
1560 1584 1567 1552 1570 1551 1543 1567
104 F 115 F 108 F 102 F 105 F 96 F 86 F 94 F
13 13 12 12 19 19a 20a 14
F F F F F F F F
40 39 43 40a 45 45b 30c 50
T-score (Nigerian reference) 18 17 17 17a 22 23a 17a 19
0.94 ( 1.52, – 0.35 ( 3.40, 0.73 ( 3.47, 0.58 ( 3.76, 1.47 ( 4.29, 2.11 ( 2.6, 1.23 ( 2.29,
0.53) 1.53) 1.94) 2.23) 1.29) 0.41) 0.11)
T-score (Japanese reference) 0.56 0.73 0.25 0.27 0.072 1.28 2.16 0.95
( ( ( ( ( ( ( (
1.36, 2.70, 3.94, 4.02, 4.42, 2.57, 2.89, 2.41,
1.45) 4.80) 2.80) 3.39) 3.79) 2.50) 0.17) 0.57)
T-score (Italian reference) 1.63 0.068 0.65 1.29 1.04 2.51 3.59 2.09
( ( ( ( ( ( ( (
2.60, 4.28, 4.08, 4.38, 5.46, 4.08, 4.48, 3.89,
0.81) 4.93) 2.48) 3.10) 3.60) 2.08) 0.75) 0.26)
a
P < 0.001. P = 0.001. c P = 0.035. b
year-old age group. The SI values remained above 100 until about age 60 years when a significant decline in SI was then observed. The best-fit curve of SI versus age for men was SI = 134.9 1.27 (age) + 0.019 (age)2 3 0.00014 (age) (Fig. 2C). For the male subjects, age and weight were significant determinants of BUA and SOS ( P < 0.001). However, age was the only variable that was significantly related to SI in this male population. Although height was significantly correlated with SOS, it was not found to be a contributor to the SOS value when age and weight were included in the multiple regression analysis. T-scores based on the SI of the Nigerian men ages 20 –29 years are summarized in Table 4. Since ultrasound parameter data are not available for African-American or Caucasian men, we compared our data to that reported for Italian and Japanese men using the same model of the QUS instrument we used in the present study [16,17]. T-scores of the Nigerian men for all decades of age fell below those of Italian men after ages 20 –29 years. Relative to the young Italian reference group, Nigerian men had a T-score of 1.38 in the fourth decade of age and a T-score of 3.60 in the 70- to 79-year decade. Relative to the Japanese males, Nigerian males in the decade between 70 and 79 years had a Tscore of 1.64.
Discussion In this report, we describe the bone status of men and women in Nigeria based on data obtained using QUS. A progressive decrease in bone ultrasound parameters beginning at about 40 years of age occurred in both men and women. Nigerian women between 20 and 40 years of age had the highest mean BUA, SOS, and SI values and after 40 years of age, there was a precipitous decline in all parameters. This abrupt decline in the various bone parameters for the women may be accounted for by menopause since we found a significant relation between years-since-menopause and SI in a previous study of
Nigerian women we conducted using QUS [19]. The relation between SI and age for the Nigerian women we studied is similar to that of the US reference population in which the incidence of hip fracture after menopause is high [20]. For men, the highest values for BUA, SOS, and SI were seen in the 20- to 29-year-old age group. Although there was a decline in all ultrasound parameters with age, the decrease was not as rapid as that seen for the women. To our knowledge, there are no other reports documenting the changes in bone status with age for African men. In light of the low calcium intake throughout the life span of Nigerians, an unexpected finding of our study was that the ultrasound parameters for the Nigerian men and women were comparable to or higher than those reported for populations in more developed countries [16,17]. For purposes of comparison, we used data only from studies that used the same ultrasound instrument for measuring bone density. When the BUA, SOS, and SI values for the Nigerian women were compared to those of Italian women [16], the Nigerian women were found to have slightly higher ultrasound values at all age ranges. In the 20- to 29-year age group, BUA measurements for the Nigerian and Italian women were 128 F 14 dB/MHz vs. 125 F 8 dB/MHz, respectively. SOS and SI measurements were 1565 F 39 m/s vs. 1566 F 21 m/s and 103 F 17 vs., 102 F 10, respectively. When the 50 to 59 year age groups were compared, the Nigerian women had slightly higher BUA and SI values than Italian women of the same age: the mean BUA values were 120 F 20 dB/MHz vs. 115 F 7 dB/MHz, respectively, and the mean SI values were 90 F 22 and 86 F 10, respectively. The weights and BMI values for the Italian subjects were not reported. Even greater differences in ultrasound parameters were observed when the Nigerian women were compared to Japanese women [17]. For example, the mean BUA for Nigerian women between 20 and 29 years of age was 130 F 13 dB/MHz compared to 115 F 11 dB/MHz for Japanese women of the same age. For women in the 50- to 59-year age range, the difference between the Nigerian and Japanese women was much greater (120 F 20 dB/MHz vs. 104 F 10
392
D.J. VanderJagt et al. / Bone 35 (2004) 387–394
Fig. 2. (A) The relation between age and BUA for Nigerian men, BUA = 122.2 + 1.079 (age) 0.025 (age)2 + 0.00012 (age)3. (B) The relation between age and SOS for Nigerian men, SOS = 1669 5.64 (age) + 0.096 (age)2 0.00055 (age)3. (C) The relation between age and SI for Nigerian men, 134 1.27 (age) + 0.019 (age)2 0.00013 (age)3.
dB/MHz, respectively). The mean SI for the Nigerian women between 50 and 59 years of age was 90 F 22, whereas the mean SI for Japanese women was 71 F 22. It should be noted that across all age ranges, the weights and BMI values for the Nigerian women were considerably greater than those for Japanese women. These anthropometric variables have an effect on accumulation and retention of bone mass. In a study of Polish men and postmenopausal women, Pluskiewicz and Drozdzowska [21] reported mean BUA and SOS values of 109 F 10 dB/MHz and 1511 F 26 m/s, respectively, for normal postmenopausal women with a mean age of 56.3 F 4.8 years, values which are considerably lower than the corresponding ones we obtained for Nigerian women of the same age (120 F 20 dB/MHz and 1536 F 37 m/s, respectively).
Although osteoporosis and the associated fracture risks have been studied primarily in postmenopausal women, there is increasing interest in the bone quality and fracture risks of men. It has been estimated that 25% to 30% of all hip fractures worldwide occur in men [2,22,23]. Therefore, we examined the bone quality of Nigerian men as well as women. The Nigerian males in the present study had comparable or higher ultrasound variables relative to European and Asian males [16,17]. Although the BUA, SOS, and SI values for the Nigerian and Italian men between 20 and 29 years of age were approximately equal, the Nigerian men between 50 and 59 years of age had a markedly higher mean SI than the Italian men (105 F 22 vs. 94 F 17, respectively). This difference was more pronounced when the Nigerian men were compared to Japanese men [17]. For subjects between 20 and 29 years of age, the Nigerian men had mean BUA, SOS, and SI values of 137 F 13 dB/MHz, 1584 F 39 m/s, and 115 F 17, respectively. The mean values for the Japanese men of that age were 124 F 10 dB/MHz, 1583 F 31 m/s, and 106 F 12, respectively. At older ages (50 to 59 years), the Nigerian men had higher QUS values than the Japanese men, particularly their SI values (105 F 22 vs. 86 F 13). The greater QUS values of the Nigerian men could be attributed to their greater weights and BMI values compared to the Japanese subjects. The BUA and SOS values for the Nigerian men were also considerably higher than the corresponding values reported for healthy Polish men whose mean age was 56.2 years [21]: 129 F 19 dB/MHz and 1570 F 45 m/s vs. 114 F 13 dB/MHz and 1517 F 35 m/s. SI values were not reported for the Polish men. Lifestyle factors such as tobacco use, alcohol consumption, and physical activity contribute to the maintenance of bone mass. Among the Nigerian population, tobacco use and alcohol consumption are uncommon. Although physical activity data were not obtained for the subjects in the present study, it is generally recognized that many Nigerian adults, men as well as women, walk considerable distances each day. Women, in particular, from an early age, carry heavy loads such as water containers and market goods over long distances. In addition to lifestyle factors, bone mineral density is affected by nutrition, hormone status, and genetics. It is estimated that approximately 75% of peak bone mass is determined by genetic factors [24]. African-American women share considerable ancestry with Nigerian women [25,26] and studies have shown that African-American women have a greater peak bone mass than Caucasian women and that the bone mass of the former is maintained better with age [27 –30]. However, the rate of hip fractures for African-American women increases exponentially after age 70 years (30 –33). Hip geometry is also a determinant of fracture risk. African-American, Asian, and Nigerian women have shorter hip-axis lengths than Caucasians and lower fracture rates
D.J. VanderJagt et al. / Bone 35 (2004) 387–394
[34,35]. This anatomical difference could account for the relatively low fracture incidences among Nigerian women despite their similar ultrasound measurements when compared to American Caucasian females. T-scores for individuals are calculated using data for a healthy young reference population. The cut-offs set by the World Health Organization for osteopenia and osteoporosis are 1.0 and 2.5, respectively. These criteria were established using the relation between bone mineral density data measured at the hip and fracture risk for postmenopausal Caucasian women. Nevertheless, these criteria have been applied to other methodologies such as QUS, which may not be appropriate. Faulkner et al. [18] compared T-scores obtained using DXA to those obtained by QUS and found that a cut-off of 2.5 obtained by QUS underestimated the actual number of osteoporotic subjects when compared to the number identified using bone mineral density scores. Frost et al. [36] also reported finding differences in the prevalence of osteoporosis in healthy postmenopausal women when using the 2.5-T score cut-off based on DXA measurements of the spine and hip and QUS scores. They found that a T-score threshold of 1.8 gave the same percentage of postmenopausal women classified as osteoporotic as the WHO threshold of 2.5 for BMD measurements and concluded that the WHO threshold for diagnosing osteoporosis should be modified when applied to QUS measurements. Because an individual’s calcium intake important in maintaining their bone density over a lifetime, the low dietary intakes of the Nigerian men and women are of particular concern. In developed countries, dietary calcium intake can be enhanced by the consumption of calcium supplements. Although relatively inexpensive and widely available in developed countries, nutritional supplements are expensive relative to the average income in Nigeria. Therefore, finding a locally available and affordable dietary source of calcium would be a more practical solution to the problem. For example, we have previously analyzed a variety of indigenous food sources in sub-Saharan Africa and have determined that the leaves of the baobab tree (Adansonia digitata) contain much calcium (14.7 mg/g dry weight) [37]. The baobab tree is common in sub-Saharan Africa and baobab leaves are an ingredient of several recipes prepared routinely in Nigeria. However, the chemical form of calcium in baobab leaves and its bioavailability in this food has yet to be determined. In summary, we found that the bone quality of Nigerian men and women from the calcaneal ultrasound measurements, BUA, SOS, and SI, is similar to that of other populations. However, these populations are known to have a high risk for fracture with increasing age. Future studies should focus on the determination of fracture rates in the Nigerian population for men as well as women. Meanwhile, strategies to increase the calcium consumption of Nigerian men and women need to be developed.
393
Acknowledgments This study was supported by a Minority International Research Training (MIRT) grant from the Fogarty International Center of the National Institutes of Health. References [1] Anderson JB, Pollitzer WS. Ethnic and genetic differences in susceptibility to osteoporotic fractures. Adv Nutr Res 1994;9:129 – 49. [2] Cooper C, Campion G, Melton LJ. Hip fractures in the elderly: a world-wide projection. Osteoporosis Int 1992;2:285 – 9. [3] Johnston Jr CC, Miller JZ, Slemenda CW, Reister TK, Hui S, Christian JC, et al. Calcium supplementation and increases in bone mineral density in children. N Engl J Med 1992;327:82 – 7. [4] Prentice A, Laskey MA, Shaw J, Hudson GJ, Day KC, Jarjou LMA, et al. The calcium and phosphorus intakes of rural Gambian women during pregnancy and lactation. Br J Nutr 1993;69:885 – 96. [5] Glew RH, Conn CA, VanderJagt TA, Calvin C, Obadofin M, Crossey M, et al. Cardiovascular disease risk factors and diet of urban and rural dwellers in northern Nigeria. J Health Popul Nutr [in press]. [6] Food and Nutrition Board. Recommended dietary allowances. Tenth ed. Washington (DC): National Academy Press; 1989. [7] Odumodo CU. Antinutrient content of some locally available legumes and cereals in Nigeria. Trop Geogr Med 1992;44:2260 – 3. [8] Bererhi H, Kolhoff N, Constable A, Nielsen SP. Multiparity and bone mass. Br J Obstet Gynaecol 1996;103:818 – 21. [9] Aspray TJ, Prentice A, Cole TJ, Sawo Y, Reeve J, Francis RM. Low bone mineral content is common but osteoporotic fractures are rare in elderly rural Gambian women. J Bone Miner Res 1996;11:1019 – 25. [10] Adebajo AO, Cooper C, Grimley Evans J. Fractures of the hip and distal forearm in West Africa and the United Kingdom. Age Ageing 1991;20:435 – 8. [11] Kellie SE, Brody JA. Sex-specific and race-specific hip fracture rates. Am J Public Health 1990;80:326 – 8. [12] Baca EA, Ulibarri VA, Scariano JK, Ujah I, Rabasa AI, VanderJagt DJ, et al. Increased serum levels of N-telopeptides (NTx) of bone collagen in postmenopausal Nigerian women. Calcif Tisssue Int 1999;65:125 – 8. [13] Schott AM, Weill-Engerer S, Hans D, Duboeuf F, Delams P, Meunier P. Ultrasound discriminates patients with hip fracture equally well as dual energy X-ray absorptiometry and independently of bone mineral density. J Bone Miner Res 1995;10:243 – 9. [14] Hans D, Dargent-Molina P, Schott AM, Sebert JL, Cormier C, Kotzki PO, et al. Ultrasonographic heel measurements to predict hip fracture in elderly women: the EPIDOS prospective study. Lancet 1996; 348:511 – 4. [15] Bauer DC, Gluer CC, Cauley JA, Vogt TM, Ensrud KE, Genant HK, et al. Broadband ultrasound attenuation predicts fractures strongly and independently of densitometry in older women. Arch Intern Med 1997;157:629 – 34. [16] Cepollaro C, Agnusdei D, Gonnelli S, Martini G, Pondrelli C, Borracelli D, et al. Ultrasonographic assessment of bone in normal Italian males and females. Br J Radiol 1995;68:910 – 4. [17] Takeda N, Miyake M, Tomomitsu T, Fukunaga M. Sex and age patterns of quantitative ultrasound densitometry of the calcaneus in normal Japanese subjects. Calcif Tissue Int 1996;59:84 – 8. [18] Faulkner KG, von Stetten E, Miller P. Discordance in patient classification using T-scores. J Clin Densitom 1992;2:343 – 50. [19] VanderJagt DJ, Bond B, Dulai R, Pickel A, Ujah IOA, Wadinga WW, et al. Assessment of the bone status of Nigerian women by ultrasound and biochemical markers. Calcif Tissue Int 2001;68:277 – 84. [20] Rosen C, McClung M, Ettinger M, Gallagher C, Baldwin D, Faulkner K, et al. Heel ultrasound reference data for Caucasian women in the
394
[21]
[22] [23] [24]
[25] [26] [27]
[28]
[29] [30]
D.J. VanderJagt et al. / Bone 35 (2004) 387–394 USA (abs) Bone ultrasonometry. 2nd International Symposium for Clinical Practitioners. J Clin Densitom, vol. 1; 1998. p. 107. Pluskiewicz W, Drozdzowska B. Ultrasonic measurement of the calcaneus in Polish normal and osteoporotic women and men. Bone 1999;24:611 – 7. Melton III LJ. The prevalence of osteoporosis: gender and racial comparison. Calcif Tissue Int 2001;69:179 – 81. Orwoll ES. Osteoporosis in men. Osteoporos Int 1992;27:349 – 67. Pocock NA, Eisman JA, Hopper JL, Yeates MG, Sambrook PN, Eberi S. Genetic determinants of bone mass in adults: a twin study. J Clin Invest 1987;80:706 – 10. Reed TE. Caucasian genes in American Negroes. Science 1969; 165:762 – 8. Excoffier L, Pellegrini B, Sanchez-Maza A. Genetics and history of sub-Saharan Africa. Yearb Phys Anthropol 1987;30:151 – 94. DeSimone DP, Stevens J, Edwards J, Shary J, Gordon L, Bell NH. Influence of body habitus and race on bone mineral density of the midradius, hip, and spine in aging women. J Bone Miner Res 1989;4:827 – 30. Lucky MM. A prospective study of bone loss in African-American and White women: a clinical research center study. J Clin Endocrinol Metab 1996;81:2948 – 56. Perry HM. Aging and bone metabolism in African-American and Caucasian women. J Clin Endocrinol Metab 1996;81:1108 – 17. Silverman SL, Madison RE. Decreased incidence of hip fracture in
[31] [32]
[33]
[34]
[35]
[36]
[37]
Hispanics, Asians and Blacks: California hospital discharge data. Am J Public Health 1988;78:1482 – 3. Turner LW, Wang MQ, Fu Q. Risk factors for hip fracture among Southern older women. South Med J 1998;91:533 – 40. Karagas MR, Lu-Yao GL, Barrett JA, Beach ML, Baron JA. Heterogeneity of hip fracture: age, race, sex, and geographic patterns of femoral neck and trochanteric fractures among the U.S. elderly. Am J Epidemiol 1996;143:677 – 82. Farmer ME, White LR, Brody JA, Bailey KR. Race and sex differences in hip fracture incidences. Am J Public Health 1984;74: 1374 – 80. Cummings SR, Cauley JA, Palermo L, Ross PD, Wasnich RD, Black D, et al. Racial differences in hip axis lengths might explain racial differences in rates of hip fractures. Study of the Osteoporotic Fractures Research Group. Osteoporos Int 1994;4:226 – 9. Theobold TM, Cauley JA, Gluer CC, Bunker CH, Ukoli FAM, Genant HK. Black – white differences in hip geometry. Osteoporosis Int 1998;8:61 – 7. Frost ML, Blake GM, Fogelman I. Can the WHO criteria for diagnosing osteoporosis be applied to calcaneal quantitative ultrasound? Osteoporos Int 2000;11:321 – 30. Sena LP, VanderJagt DJ, Rivera C, Tsin ATC, Muhamadu I, Mahamadou O, et al. Analysis of nutritional components of eight famine foods of the Republic of Niger. Plant Foods Hum Nutr 1998;52: 17 – 30.
Assessment of the skeletal health of healthy Nigerian men and women using quantitative ultrasound D.J. VanderJagt, a,* L.A. Damiani, a T.M. Goodman, a I.O.A. Ujah, b M.O. Obadofin, b G.E. Imade, b D.R. Shatima, c and R.H. Glew a,* a
Department of Biochemistry and Molecular Biology, University of New Mexico School of Medicine, Albuquerque, NM 87131, USA b Jos University Teaching Hospital, Jos, Nigeria c National Hospital Abuja, Abuja, Nigeria Received 22 December 2003; revised 5 March 2004; accepted 1 April 2004
Abstract The dietary intake of calcium by African populations, particularly in sub-Saharan Africa, is relatively low compared to the recommended intake for US adults. However, the rate of osteoporotic fractures in West African women is reported to be less than that for Caucasian populations. Because there is little published data regarding the skeletal status of African men and women, we used quantitative ultrasound (QUS) to assess the bone density of 435 Nigerian women and 321 Nigerian men between 16 and 89 years of age. A progressive decline in bone quality was observed beginning at about 40 years of age for both men and women. The mean stiffness index (SI) for the women between 20 and 35 years of age (n = 186) in this study was 102 F 17. The equation that best described the age versus SI relationship for women was SI = 79.7 + 1.887 (age) + 0.043 (age)2 + 0.00020 (age)3. For Nigerian men, the peak SI of 115 F 17 was seen in the 20- to 29-year-old age group. For men, the SI values remained above 100 until about age 60 years when a significant decline in SI was then observed. The best-fit curve of SI versus age for men was SI = 134.9 1.27 (age) + 0.019 (age)2 0.00014 (age)3. The broadband ultrasound attenuation (BUA), speed of sound (SOS), and SI values for the Nigerian men and women were comparable to or higher than those reported for Caucasian and Asian populations. These data should serve as reference values for adult men and women in sub-Saharan Africa. D 2004 Elsevier Inc. All rights reserved. Keywords: Bone density; Quantitative ultrasound (QUS); Broadband ultrasound attenuation (BUA); Speed of sound (SOS); Stiffness index (SI); Nigeria; Men; Women
Introduction Osteoporosis is characterized by low bone density and deterioration of bone microarchitecture resulting in increased bone fragility and fracture risk. Although osteoporosis is an important cause of debility and morbidity in the elderly, the incidence of age-related osteoporotic fractures varies widely between different populations and ethnic groups [1]. The fact that hip fracture rates for Caucasian populations in the United States and Europe have been reported to be higher than those in Africa, Asia, and South America [2] has led to the questionable assumption that osteoporosis is not a significant problem in these less developed regions of the * Corresponding authors. Department of Biochemistry and Molecular Biology, University of New Mexico School of Medicine, Room 245, BMSB, Albuquerque, NM 87131-5221. Fax: +1-505-272-3518. E-mail address: [email protected] (R.H. Glew). 8756-3282/$ - see front matter D 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.bone.2004.04.001
world. However, projected demographics suggest that over the next 50 years, three fourths of the world’s elderly will reside in Africa, Asia, and Latin America, and these trends are likely to result in a significant increase in the number of fractures reported in these populations [2]. Bone density at any age is dependent on peak bone density attained in early adulthood, usually by age 30 years, and the subsequent rate of bone loss with age. Adequate dietary calcium intake over a lifetime is important in the accrual of bone mass during growth and the conservation of bone mass thereafter [3]. The indigenous people of West Africa and other parts of sub-Saharan Africa are subject to a variety of factors which can lead not only to a decrease in the maximum bone mass that an individual attains but also an accelerated age-related bone loss. First, diets in West Africa generally contain relatively low amounts of calcium [4,5]. For example, it was estimated that pregnant and lactating women in rural Gambia have a dietary calcium intake of 400
388
D.J. VanderJagt et al. / Bone 35 (2004) 387–394
mg/day [4]. In a recent dietary study conducted in northern Nigeria, we reported the mean dietary calcium intakes for urban men and women were 551 and 447 mg/day, respectively [5]. These intakes are substantially below the US recommended dietary intakes of 1000 mg/day for adults [6]. Second, in addition to low-calcium diets, many populations in sub-Saharan Africa place a heavy reliance on cereal staples which contain oxalates and other divalent metal cation chelators that decrease the bioavailability of calcium as well as other trace minerals [7]. Third, African women are under the additional calcium-depleting stress of extended breastfeeding of 2 years or more for each child, a condition which is exacerbated by high parity [8]. Fourth, estrogen replacement therapy is generally not widely available for post-menopausal women in most parts of Africa, primarily for economic reasons. Collectively, these factors place most Africans, particularly post-menopausal women, at an increased risk for osteoporosis and bone fracture. Despite these risk factors, the few published reports regarding fracture rates for African women suggest that bone fractures may be relatively uncommon in populations in West Africa [1,9 – 11]. In a study of fracture rates in 360,000 Nigerian women over 50 years of age, the incidence of hip and forearm fractures was reported to be 100 times lower for Nigerian women than for Caucasian women of comparable age in England [10]. The low fracture rate for Nigerian women is unexpected since we had shown in a previous study of 218 Nigerian women that they had significantly higher levels of NTx, a marker of bone turnover, than Caucasian women matched for age and body mass index [12]. There are no comparable data for African men. Bone strength or quality is determined by bone mineral density, bone architecture, and elasticity. Because there is currently no direct measure of bone strength, bone mineral density is the accepted surrogate for bone strength. Dualenergy X-ray absorptiometry (DXA) is considered the gold standard for the determination of bone density and estima-
tion of fracture risk. However, QUS of the calcaneus has been shown to be as reliable as DXA in predicting fracture risk in postmenopausal women [13 – 15]. In addition, QUS has the added advantages of relatively low cost and portability compared to DXA, thereby making it suitable for use in a developing country such as Nigeria. In this report, we describe the results of a cross-sectional study of the bone status of healthy Nigerian men and women using QUS and have compared these results with those reported for American, European, and Asian populations using the same ultrasound instrument.
Materials and methods Subjects Men and women were recruited from among hospital staff and visitors at the outpatient clinics of the National Hospital Abuja, Abuja, Nigeria, and the Jos University Teaching Hospital in Jos, Nigeria. Abuja is a metropolitan center and the capital of Nigeria, whereas Jos is a smaller city with a mix of ethnic groups who have traditional as well as urban lifestyles. Exclusion criteria for both the men and women included prolonged immobility, malignancy, renal or endocrine disease, recent surgery, or bone fracture. Information regarding age, previous fractures, and current medications was obtained for each subject. Women who were nursing or pregnant were excluded from the study. Measurements of height, weight, triceps skin-fold thickness, and mid-arm circumference were obtained for all subjects. For women, parity and menstrual status were recorded. Informed consent was obtained from each subject and this study was approved by the Ethics Review Committees of the Jos University Teaching Hospital, Jos, Nigeria and National Hospital, Abuja, Nigeria and by the Human Research Review Committee of the University of New Mexico, Albuquerque, New Mexico, USA.
Table 1 Anthropometric characteristics of the Nigerian women by decade of age Age interval (years)
n
Age (years)
Weight (kg)
Height (cm)
BMI (kg/m2)
Mid-arm circumference (cm)
Triceps skin-fold (mm)
16 – 19 20 – 29 30 – 39 40 – 49 50 – 59 60 – 69 70 – 79 80 – 89
15 104 123 91 62 20 14 6
18.1 24.8 34.1 43.7 51.9 62.3 71.4 81.7
49.4 61.9 69.4 70.2 69.2 69.4 53.2 51.9
158.9 162.0 162.2 160.5 159.0 159.6 159.4 159.0
19.6 23.4 26.4 27.3 27.4 27.3 21.0 20.5
23.5 26.6 29.4 31.1 31.0 30.9 26.1 24.4
19.1 20.9 25.6 28.0 27.3 25.8 21.2 16.7
a
F F F F F F F F
1.0 2.8 2.8 3.0 2.7 2.7 2.2 2.6
F F F F F F F F
9.3 14.3 15.1a 15.0a 14.7b 15.0d 16.3d 9.7
Significantly different from 20- to 29-year-old group: P < 0.001. Significantly different from 20- to 29-year-old group: P = 0.003. c Significantly different from 20- to 29-year-old group: P = 0.002. d Significantly different from 20- to 29-year-old group: P = 0.03 – 0.05. e Significantly different from 20- to 29-year-old group: P = 0.01. b
F F F F F F F F
4.0 6.3 7.0 5.7 5.8c 5.3 3.6 2.9
F F F F F F F F
3.2 5.0 5.2a 5.9a 5.7a 6.0c 6.4 4.0
F F F F F F F F
4.8 4.9 4.4a 5.3a 5.3a 4.3a 5.0 5.0
F F F F F F F F
5.4 7.7 7.6a 8.0a 8.5a 9.4e 9.7 11.1
D.J. VanderJagt et al. / Bone 35 (2004) 387–394
389
Table 2 Anthropometric characteristics of Nigerian men by decade of age Age interval (years)
n
Age (years)
Weight (kg)
Height (cm)
BMI (kg/m2)
Mid-arm circumference (cm)
Triceps skin-fold (mm)
18 – 19 20 – 29 30 – 39 40 – 49 50 – 59 60 – 69 70 – 79 80 – 89
3 83 103 68 36 20 5 3
18.3 25.5 34.1 44.2 53.8 62.5 73.8 81.0
57.3 66.0 71.2 72.2 68.9 62.2 56.9 64.6
169 172 171 168 169 167 165 170
20.1 22.2 24.5 25.6 24.1 23.2 20.9 22.5
26.3 29.0 30.1 36.1 29.7 27.1 25.1 26.7
9.30 10.5 14.1 13.5 13.7 10.8 9.20 7.00
F F F F F F F F
0.6 2.8 2.9 3.0 2.9 2.3 2.4 1.0
F F F F F F F F
3.7 11 11 13a 12 13 14 3.4
F F F F F F F F
5.2 6.8 6.5 6.4a 5.7 6.8b 6.9c 1.8
F F F F F F F F
2.3 3.0 3.6a 3.5a 4.0 4.3 4.0 0.7
F F F F F F F F
2.0 3.0 3.4 4.4 3.2 4.0 3.6 1.2
F F F F F F F F
1.2 6.3 7.3a 6.6 6.6 7.4 6.3 2.6
a
Significantly different from the 20- to 29-year-old group: P < 0.001. Significantly different from the 20- to 29-year-old group: P = 0.002. c Significantly different from the 20- to 29-year-old group: P = 0.021. b
software were generated from healthy Caucasian women in the US. A separate T-score was calculated using SI data for the young African women in the study group who were between 20 and 35 years of age. Because reference data for men were not available, the T-scores for men were calculated using data for young Nigerian men 20 – 29 years old. Tscores were also calculated for Nigerian men using data obtained with the same model ultrasound instrument used for Italian and Japanese males between 20 and 29 years of age who served as the reference population [16,17].
Ultrasound measurement Ultrasound measurements of the calcaneus were obtained using the Achilles+ (Lunar Corporation, Madison, WI, USA) according to the manufacturer’s instructions. Each subject was seated with his or her right foot resting in the heel bath of the instrument. After introducing water into the heel bath, measurements of the speed of sound (SOS) transmission and the broadband ultrasound attenuation (BUA) were made. BUA is defined as the slope of the regression line derived from the ratio of the signal amplitude of the calcaneus to that of water (reference) at each frequency of ultrasound (dB/MHZ). SOS refers to the speed of the sound wave traveling through the calcaneus, measured in m/s. The stiffness index (SI) was calculated for each subject using the equation SI = (0.67 BUA) + (0.28 SOS) 420. Calibration of the instrument was monitored using a phantom heel. Reproducibility was validated by measuring the same control subject each day that measurements were made on the study subjects. For female subjects, the T-score was calculated as follows: T-score = (subject SI mean SI of the reference group) / (standard deviation of the reference group). The data for the reference population provided in the instrument
Statistical analysis Results are expressed as the mean F standard deviation. Statistical analysis was performed using the Number Crunching Statistical Software program (NCSS 2000, Kaysville, UT). Comparisons of parameters between decades of age were made using one-way ANOVA. Multiple regression analysis was used to determine the relation between anthropometric parameters and ultrasound variables. The regression equations of BUA, SOS and SI versus age were determined using the Table Curve 2D version of SPSS (SPSS 4.0, SPSS, Inc., Chicago, IL). A P value of 0.05 was considered statistically significant.
Table 3 Ultrasound parameters by decade of age for Nigerian women Age interval (years)
n
BUA (dB/MHz)
SOS (m/s) (mean F SD)
SI
16 – 19 20 – 29 30 – 39 40 – 49 50 – 59 60 – 69 70 – 79 80 – 89
15 104 123 91 62 20 14 6
128 F 130 F 131 F 126 F 120 F 116 F 98 F 93 F
1565 1556 1553 1549 1536 1515 1488 1492
103 102 102 97 90 81 62 60
a
14 13 14 15 20a 20a 13a 14a
F F F F F F F F
39 31 34 36 37a 36 27a 25a
T-score Caucasian reference (median (min, max)) F F F F F F F F
17 15 17 18 22a 21a 16a 15
0.21 0.13 0.13 0.16 0.66 1.2 2.1 2.5
( ( ( ( ( ( ( (
1.4, 3.3, 2.4, 3.2, 4.3, 3.8, 3.7, 3.9,
1.9) 2.0) 2.7) 2.3) 1.6) 1.6) 0.7) 0.9)
T-score Nigerian reference (median (min, max))
0.05 0.3 0.7 1.2 2.3 2.5
( ( ( ( ( (
– – 3.9, 3.1, 4.2, 3.7, 3.6, 3.8,
2.4) 2.1) 1.4) 1.4) 0.4) 1.0)
Significantly different from the 20- to 29-year-old group: P < 0.001; BUA, broadband ultrasound attenuation; SOS, speed of sound; SI, stiffness index*; T-score-C, based on data for Caucasian women; T-score-N, based on data for Nigerian women between 20 and 29 years of age in the present study group.
390
D.J. VanderJagt et al. / Bone 35 (2004) 387–394
Results Comments on the characteristics of the subjects Women A total of 435 women (301 premenopausal and 134 postmenopausal women) between the ages of 16 and 89 years were enrolled in the study. A summary of the characteristics of the female subjects by decade of age is given in Table 1. The majority of the women (87%) were between 20 and 59 years of age, with the lowest number of subjects being in the 16 – 19 (3.4%), 70– 79 (3.2%), and 80– 89 (1.4%) year age groups. There were progressive increases in weight, body mass index (BMI), mid-arm circumference and triceps skin-fold thickness for subjects over 30 years of age and these trends persisted until the seventh decade of age. Men A total of 321 Nigerian men aged 18 – 83 years participated in this study. A summary of the anthropometric measurements of the men is provided in Table 2. Eighty percent of men were between 20 and 50 years of age. The fewest number of subjects fell in the 18 –19 (0.93%) and the 80 – 89 (0.93%)-year-old age groups. For Nigerian men there was a progressive increase in weight, BMI, and midarm circumference after age 20 years, followed by a decline in each of these parameters after age 70 years to values that were comparable to those in the 18- to 19-year-old age group. Ultrasound parameters Women BUA, SOS, and SI parameters for the female subjects by decade of age are given in Table 3. Compared to the 20- to 29-year-old group, there was a decline in both BUA and SOS starting around 40 years of age; however, the decrease did not reach statistical significance until after 50 years of age (Figs. 1A and B). The mean SI for the women between 20 and 35 years of age (n = 186) in this study was 102 F 17. Compared with the 20- to 29-year-old group, a significant difference in SI was found for the women beginning with the 50- to 59-year-old age group. The equation that best described the age versus SI relationship for women was SI = 79.7 + 1.887 (age) + 0.04 3 (age)2 + 0.00020 (age)3 (Fig. 1C). Multiple regression analysis revealed that age and weight were significant determinants of BUA and SI for women (P V 0.001), whereas age alone was related to SOS (P < 0.001). When adjusted for age, height was not a significant determinant of any of the ultrasound parameters for the female subjects. Separate T-scores for the Nigerian women based on reference data for Caucasian and Nigerian women were calculated (Table 2). The T-scores for the Nigerian women
Fig. 1. (A) The relation between age and BUA for Nigerian women, BUA = 121.9 + 0.638 (age) – 0.012 (age)2. (B) The relation between SOS and age for Nigerian women, SOS = 1530 + 2.49 (age) 0.062 (age)2 + 0.0003 (age)3. (C) The relation between age and SI for Nigerian women, SI = 79.7 + 1.88 (age) 0.043 (age)2 + 0.00021 (age)3.
became progressively more negative with advancing age. The decline was similar to that seen in the T-scores for Caucasian women in the US [18]. No significant differences were found between T-scores calculated using Caucasian and Nigerian reference data. Men A summary of the BUA, SOS, and SI parameters for the male subjects by decade of age is shown in Table 4. Compared to the 20- to 29-year-old group, there was a progressive decline in both BUA and SOS with increasing age (Figs. 2A and B). In general, the men between 40 and 80 years of age had ultrasound parameters that were significantly lower than the younger males. For Nigerian men, the peak SI of 115 F 17 occurred in the 20- to 29-
D.J. VanderJagt et al. / Bone 35 (2004) 387–394
391
Table 4 BUA, SOS, and SI by decade of age for the Nigerian men Age interval (years)
n
BUA (dB/MHz)
SOS (m/s)
SI
18 – 19 20 – 29 30 – 39 40 – 49 50 – 59 60 – 69 70 – 79 80 – 89
3 83 103 68 36 20 5 3
131 F 137 F 135 F 130 F 129 F 123 F 110 F 118 F
1560 1584 1567 1552 1570 1551 1543 1567
104 F 115 F 108 F 102 F 105 F 96 F 86 F 94 F
13 13 12 12 19 19a 20a 14
F F F F F F F F
40 39 43 40a 45 45b 30c 50
T-score (Nigerian reference) 18 17 17 17a 22 23a 17a 19
0.94 ( 1.52, – 0.35 ( 3.40, 0.73 ( 3.47, 0.58 ( 3.76, 1.47 ( 4.29, 2.11 ( 2.6, 1.23 ( 2.29,
0.53) 1.53) 1.94) 2.23) 1.29) 0.41) 0.11)
T-score (Japanese reference) 0.56 0.73 0.25 0.27 0.072 1.28 2.16 0.95
( ( ( ( ( ( ( (
1.36, 2.70, 3.94, 4.02, 4.42, 2.57, 2.89, 2.41,
1.45) 4.80) 2.80) 3.39) 3.79) 2.50) 0.17) 0.57)
T-score (Italian reference) 1.63 0.068 0.65 1.29 1.04 2.51 3.59 2.09
( ( ( ( ( ( ( (
2.60, 4.28, 4.08, 4.38, 5.46, 4.08, 4.48, 3.89,
0.81) 4.93) 2.48) 3.10) 3.60) 2.08) 0.75) 0.26)
a
P < 0.001. P = 0.001. c P = 0.035. b
year-old age group. The SI values remained above 100 until about age 60 years when a significant decline in SI was then observed. The best-fit curve of SI versus age for men was SI = 134.9 1.27 (age) + 0.019 (age)2 3 0.00014 (age) (Fig. 2C). For the male subjects, age and weight were significant determinants of BUA and SOS ( P < 0.001). However, age was the only variable that was significantly related to SI in this male population. Although height was significantly correlated with SOS, it was not found to be a contributor to the SOS value when age and weight were included in the multiple regression analysis. T-scores based on the SI of the Nigerian men ages 20 –29 years are summarized in Table 4. Since ultrasound parameter data are not available for African-American or Caucasian men, we compared our data to that reported for Italian and Japanese men using the same model of the QUS instrument we used in the present study [16,17]. T-scores of the Nigerian men for all decades of age fell below those of Italian men after ages 20 –29 years. Relative to the young Italian reference group, Nigerian men had a T-score of 1.38 in the fourth decade of age and a T-score of 3.60 in the 70- to 79-year decade. Relative to the Japanese males, Nigerian males in the decade between 70 and 79 years had a Tscore of 1.64.
Discussion In this report, we describe the bone status of men and women in Nigeria based on data obtained using QUS. A progressive decrease in bone ultrasound parameters beginning at about 40 years of age occurred in both men and women. Nigerian women between 20 and 40 years of age had the highest mean BUA, SOS, and SI values and after 40 years of age, there was a precipitous decline in all parameters. This abrupt decline in the various bone parameters for the women may be accounted for by menopause since we found a significant relation between years-since-menopause and SI in a previous study of
Nigerian women we conducted using QUS [19]. The relation between SI and age for the Nigerian women we studied is similar to that of the US reference population in which the incidence of hip fracture after menopause is high [20]. For men, the highest values for BUA, SOS, and SI were seen in the 20- to 29-year-old age group. Although there was a decline in all ultrasound parameters with age, the decrease was not as rapid as that seen for the women. To our knowledge, there are no other reports documenting the changes in bone status with age for African men. In light of the low calcium intake throughout the life span of Nigerians, an unexpected finding of our study was that the ultrasound parameters for the Nigerian men and women were comparable to or higher than those reported for populations in more developed countries [16,17]. For purposes of comparison, we used data only from studies that used the same ultrasound instrument for measuring bone density. When the BUA, SOS, and SI values for the Nigerian women were compared to those of Italian women [16], the Nigerian women were found to have slightly higher ultrasound values at all age ranges. In the 20- to 29-year age group, BUA measurements for the Nigerian and Italian women were 128 F 14 dB/MHz vs. 125 F 8 dB/MHz, respectively. SOS and SI measurements were 1565 F 39 m/s vs. 1566 F 21 m/s and 103 F 17 vs., 102 F 10, respectively. When the 50 to 59 year age groups were compared, the Nigerian women had slightly higher BUA and SI values than Italian women of the same age: the mean BUA values were 120 F 20 dB/MHz vs. 115 F 7 dB/MHz, respectively, and the mean SI values were 90 F 22 and 86 F 10, respectively. The weights and BMI values for the Italian subjects were not reported. Even greater differences in ultrasound parameters were observed when the Nigerian women were compared to Japanese women [17]. For example, the mean BUA for Nigerian women between 20 and 29 years of age was 130 F 13 dB/MHz compared to 115 F 11 dB/MHz for Japanese women of the same age. For women in the 50- to 59-year age range, the difference between the Nigerian and Japanese women was much greater (120 F 20 dB/MHz vs. 104 F 10
392
D.J. VanderJagt et al. / Bone 35 (2004) 387–394
Fig. 2. (A) The relation between age and BUA for Nigerian men, BUA = 122.2 + 1.079 (age) 0.025 (age)2 + 0.00012 (age)3. (B) The relation between age and SOS for Nigerian men, SOS = 1669 5.64 (age) + 0.096 (age)2 0.00055 (age)3. (C) The relation between age and SI for Nigerian men, 134 1.27 (age) + 0.019 (age)2 0.00013 (age)3.
dB/MHz, respectively). The mean SI for the Nigerian women between 50 and 59 years of age was 90 F 22, whereas the mean SI for Japanese women was 71 F 22. It should be noted that across all age ranges, the weights and BMI values for the Nigerian women were considerably greater than those for Japanese women. These anthropometric variables have an effect on accumulation and retention of bone mass. In a study of Polish men and postmenopausal women, Pluskiewicz and Drozdzowska [21] reported mean BUA and SOS values of 109 F 10 dB/MHz and 1511 F 26 m/s, respectively, for normal postmenopausal women with a mean age of 56.3 F 4.8 years, values which are considerably lower than the corresponding ones we obtained for Nigerian women of the same age (120 F 20 dB/MHz and 1536 F 37 m/s, respectively).
Although osteoporosis and the associated fracture risks have been studied primarily in postmenopausal women, there is increasing interest in the bone quality and fracture risks of men. It has been estimated that 25% to 30% of all hip fractures worldwide occur in men [2,22,23]. Therefore, we examined the bone quality of Nigerian men as well as women. The Nigerian males in the present study had comparable or higher ultrasound variables relative to European and Asian males [16,17]. Although the BUA, SOS, and SI values for the Nigerian and Italian men between 20 and 29 years of age were approximately equal, the Nigerian men between 50 and 59 years of age had a markedly higher mean SI than the Italian men (105 F 22 vs. 94 F 17, respectively). This difference was more pronounced when the Nigerian men were compared to Japanese men [17]. For subjects between 20 and 29 years of age, the Nigerian men had mean BUA, SOS, and SI values of 137 F 13 dB/MHz, 1584 F 39 m/s, and 115 F 17, respectively. The mean values for the Japanese men of that age were 124 F 10 dB/MHz, 1583 F 31 m/s, and 106 F 12, respectively. At older ages (50 to 59 years), the Nigerian men had higher QUS values than the Japanese men, particularly their SI values (105 F 22 vs. 86 F 13). The greater QUS values of the Nigerian men could be attributed to their greater weights and BMI values compared to the Japanese subjects. The BUA and SOS values for the Nigerian men were also considerably higher than the corresponding values reported for healthy Polish men whose mean age was 56.2 years [21]: 129 F 19 dB/MHz and 1570 F 45 m/s vs. 114 F 13 dB/MHz and 1517 F 35 m/s. SI values were not reported for the Polish men. Lifestyle factors such as tobacco use, alcohol consumption, and physical activity contribute to the maintenance of bone mass. Among the Nigerian population, tobacco use and alcohol consumption are uncommon. Although physical activity data were not obtained for the subjects in the present study, it is generally recognized that many Nigerian adults, men as well as women, walk considerable distances each day. Women, in particular, from an early age, carry heavy loads such as water containers and market goods over long distances. In addition to lifestyle factors, bone mineral density is affected by nutrition, hormone status, and genetics. It is estimated that approximately 75% of peak bone mass is determined by genetic factors [24]. African-American women share considerable ancestry with Nigerian women [25,26] and studies have shown that African-American women have a greater peak bone mass than Caucasian women and that the bone mass of the former is maintained better with age [27 –30]. However, the rate of hip fractures for African-American women increases exponentially after age 70 years (30 –33). Hip geometry is also a determinant of fracture risk. African-American, Asian, and Nigerian women have shorter hip-axis lengths than Caucasians and lower fracture rates
D.J. VanderJagt et al. / Bone 35 (2004) 387–394
[34,35]. This anatomical difference could account for the relatively low fracture incidences among Nigerian women despite their similar ultrasound measurements when compared to American Caucasian females. T-scores for individuals are calculated using data for a healthy young reference population. The cut-offs set by the World Health Organization for osteopenia and osteoporosis are 1.0 and 2.5, respectively. These criteria were established using the relation between bone mineral density data measured at the hip and fracture risk for postmenopausal Caucasian women. Nevertheless, these criteria have been applied to other methodologies such as QUS, which may not be appropriate. Faulkner et al. [18] compared T-scores obtained using DXA to those obtained by QUS and found that a cut-off of 2.5 obtained by QUS underestimated the actual number of osteoporotic subjects when compared to the number identified using bone mineral density scores. Frost et al. [36] also reported finding differences in the prevalence of osteoporosis in healthy postmenopausal women when using the 2.5-T score cut-off based on DXA measurements of the spine and hip and QUS scores. They found that a T-score threshold of 1.8 gave the same percentage of postmenopausal women classified as osteoporotic as the WHO threshold of 2.5 for BMD measurements and concluded that the WHO threshold for diagnosing osteoporosis should be modified when applied to QUS measurements. Because an individual’s calcium intake important in maintaining their bone density over a lifetime, the low dietary intakes of the Nigerian men and women are of particular concern. In developed countries, dietary calcium intake can be enhanced by the consumption of calcium supplements. Although relatively inexpensive and widely available in developed countries, nutritional supplements are expensive relative to the average income in Nigeria. Therefore, finding a locally available and affordable dietary source of calcium would be a more practical solution to the problem. For example, we have previously analyzed a variety of indigenous food sources in sub-Saharan Africa and have determined that the leaves of the baobab tree (Adansonia digitata) contain much calcium (14.7 mg/g dry weight) [37]. The baobab tree is common in sub-Saharan Africa and baobab leaves are an ingredient of several recipes prepared routinely in Nigeria. However, the chemical form of calcium in baobab leaves and its bioavailability in this food has yet to be determined. In summary, we found that the bone quality of Nigerian men and women from the calcaneal ultrasound measurements, BUA, SOS, and SI, is similar to that of other populations. However, these populations are known to have a high risk for fracture with increasing age. Future studies should focus on the determination of fracture rates in the Nigerian population for men as well as women. Meanwhile, strategies to increase the calcium consumption of Nigerian men and women need to be developed.
393
Acknowledgments This study was supported by a Minority International Research Training (MIRT) grant from the Fogarty International Center of the National Institutes of Health. References [1] Anderson JB, Pollitzer WS. Ethnic and genetic differences in susceptibility to osteoporotic fractures. Adv Nutr Res 1994;9:129 – 49. [2] Cooper C, Campion G, Melton LJ. Hip fractures in the elderly: a world-wide projection. Osteoporosis Int 1992;2:285 – 9. [3] Johnston Jr CC, Miller JZ, Slemenda CW, Reister TK, Hui S, Christian JC, et al. Calcium supplementation and increases in bone mineral density in children. N Engl J Med 1992;327:82 – 7. [4] Prentice A, Laskey MA, Shaw J, Hudson GJ, Day KC, Jarjou LMA, et al. The calcium and phosphorus intakes of rural Gambian women during pregnancy and lactation. Br J Nutr 1993;69:885 – 96. [5] Glew RH, Conn CA, VanderJagt TA, Calvin C, Obadofin M, Crossey M, et al. Cardiovascular disease risk factors and diet of urban and rural dwellers in northern Nigeria. J Health Popul Nutr [in press]. [6] Food and Nutrition Board. Recommended dietary allowances. Tenth ed. Washington (DC): National Academy Press; 1989. [7] Odumodo CU. Antinutrient content of some locally available legumes and cereals in Nigeria. Trop Geogr Med 1992;44:2260 – 3. [8] Bererhi H, Kolhoff N, Constable A, Nielsen SP. Multiparity and bone mass. Br J Obstet Gynaecol 1996;103:818 – 21. [9] Aspray TJ, Prentice A, Cole TJ, Sawo Y, Reeve J, Francis RM. Low bone mineral content is common but osteoporotic fractures are rare in elderly rural Gambian women. J Bone Miner Res 1996;11:1019 – 25. [10] Adebajo AO, Cooper C, Grimley Evans J. Fractures of the hip and distal forearm in West Africa and the United Kingdom. Age Ageing 1991;20:435 – 8. [11] Kellie SE, Brody JA. Sex-specific and race-specific hip fracture rates. Am J Public Health 1990;80:326 – 8. [12] Baca EA, Ulibarri VA, Scariano JK, Ujah I, Rabasa AI, VanderJagt DJ, et al. Increased serum levels of N-telopeptides (NTx) of bone collagen in postmenopausal Nigerian women. Calcif Tisssue Int 1999;65:125 – 8. [13] Schott AM, Weill-Engerer S, Hans D, Duboeuf F, Delams P, Meunier P. Ultrasound discriminates patients with hip fracture equally well as dual energy X-ray absorptiometry and independently of bone mineral density. J Bone Miner Res 1995;10:243 – 9. [14] Hans D, Dargent-Molina P, Schott AM, Sebert JL, Cormier C, Kotzki PO, et al. Ultrasonographic heel measurements to predict hip fracture in elderly women: the EPIDOS prospective study. Lancet 1996; 348:511 – 4. [15] Bauer DC, Gluer CC, Cauley JA, Vogt TM, Ensrud KE, Genant HK, et al. Broadband ultrasound attenuation predicts fractures strongly and independently of densitometry in older women. Arch Intern Med 1997;157:629 – 34. [16] Cepollaro C, Agnusdei D, Gonnelli S, Martini G, Pondrelli C, Borracelli D, et al. Ultrasonographic assessment of bone in normal Italian males and females. Br J Radiol 1995;68:910 – 4. [17] Takeda N, Miyake M, Tomomitsu T, Fukunaga M. Sex and age patterns of quantitative ultrasound densitometry of the calcaneus in normal Japanese subjects. Calcif Tissue Int 1996;59:84 – 8. [18] Faulkner KG, von Stetten E, Miller P. Discordance in patient classification using T-scores. J Clin Densitom 1992;2:343 – 50. [19] VanderJagt DJ, Bond B, Dulai R, Pickel A, Ujah IOA, Wadinga WW, et al. Assessment of the bone status of Nigerian women by ultrasound and biochemical markers. Calcif Tissue Int 2001;68:277 – 84. [20] Rosen C, McClung M, Ettinger M, Gallagher C, Baldwin D, Faulkner K, et al. Heel ultrasound reference data for Caucasian women in the
394
[21]
[22] [23] [24]
[25] [26] [27]
[28]
[29] [30]
D.J. VanderJagt et al. / Bone 35 (2004) 387–394 USA (abs) Bone ultrasonometry. 2nd International Symposium for Clinical Practitioners. J Clin Densitom, vol. 1; 1998. p. 107. Pluskiewicz W, Drozdzowska B. Ultrasonic measurement of the calcaneus in Polish normal and osteoporotic women and men. Bone 1999;24:611 – 7. Melton III LJ. The prevalence of osteoporosis: gender and racial comparison. Calcif Tissue Int 2001;69:179 – 81. Orwoll ES. Osteoporosis in men. Osteoporos Int 1992;27:349 – 67. Pocock NA, Eisman JA, Hopper JL, Yeates MG, Sambrook PN, Eberi S. Genetic determinants of bone mass in adults: a twin study. J Clin Invest 1987;80:706 – 10. Reed TE. Caucasian genes in American Negroes. Science 1969; 165:762 – 8. Excoffier L, Pellegrini B, Sanchez-Maza A. Genetics and history of sub-Saharan Africa. Yearb Phys Anthropol 1987;30:151 – 94. DeSimone DP, Stevens J, Edwards J, Shary J, Gordon L, Bell NH. Influence of body habitus and race on bone mineral density of the midradius, hip, and spine in aging women. J Bone Miner Res 1989;4:827 – 30. Lucky MM. A prospective study of bone loss in African-American and White women: a clinical research center study. J Clin Endocrinol Metab 1996;81:2948 – 56. Perry HM. Aging and bone metabolism in African-American and Caucasian women. J Clin Endocrinol Metab 1996;81:1108 – 17. Silverman SL, Madison RE. Decreased incidence of hip fracture in
[31] [32]
[33]
[34]
[35]
[36]
[37]
Hispanics, Asians and Blacks: California hospital discharge data. Am J Public Health 1988;78:1482 – 3. Turner LW, Wang MQ, Fu Q. Risk factors for hip fracture among Southern older women. South Med J 1998;91:533 – 40. Karagas MR, Lu-Yao GL, Barrett JA, Beach ML, Baron JA. Heterogeneity of hip fracture: age, race, sex, and geographic patterns of femoral neck and trochanteric fractures among the U.S. elderly. Am J Epidemiol 1996;143:677 – 82. Farmer ME, White LR, Brody JA, Bailey KR. Race and sex differences in hip fracture incidences. Am J Public Health 1984;74: 1374 – 80. Cummings SR, Cauley JA, Palermo L, Ross PD, Wasnich RD, Black D, et al. Racial differences in hip axis lengths might explain racial differences in rates of hip fractures. Study of the Osteoporotic Fractures Research Group. Osteoporos Int 1994;4:226 – 9. Theobold TM, Cauley JA, Gluer CC, Bunker CH, Ukoli FAM, Genant HK. Black – white differences in hip geometry. Osteoporosis Int 1998;8:61 – 7. Frost ML, Blake GM, Fogelman I. Can the WHO criteria for diagnosing osteoporosis be applied to calcaneal quantitative ultrasound? Osteoporos Int 2000;11:321 – 30. Sena LP, VanderJagt DJ, Rivera C, Tsin ATC, Muhamadu I, Mahamadou O, et al. Analysis of nutritional components of eight famine foods of the Republic of Niger. Plant Foods Hum Nutr 1998;52: 17 – 30.