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The Journal of Nutrition Vol. 128 No. 9 September 1998,
pp. 1543-1549
,
, and
Departments of * Anesthesiology and Intensive Care, Nutrition and ** Orthopedics, Uppsala University, University Hospital, S-751 85 Uppsala, Sweden and Departments of Meat Sciences and Clinical Radiology, Swedish University of Agricultural Sciences, Ultuna S-750 07, Uppsala, Sweden
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ABSTRACT |
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Abstract
Introduction
Methods
Results
Discussion
References
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To evaluate the use of dual-energy X-ray absorptiometry (DXA) and underwater weighing (UWW) for body-composition measurements, the carcasses of eight piglets (12-wk old, 15-22 kg in weight) were dissected into muscle, fat and bone. Thereafter, the components were homogenized and chemically analyzed for fat and bone mineral mass. Body components as measured by DXA correlated closely to the carcass analysis (r = 0.90-1.0). However, DXA still overestimated significantly the bone mineral mass, lean mass and total weight, and underestimated fat mass. The reproducibility of measurements, expressed as the CV for fat mass was 13.5%, whereas for total weight, lean mass and bone mineral mass, the CV was 0.74-1.9%. Fat mass was overestimated by UWW using the equations of Siri or Kraybill (r = 0.77), but not by the equation of Lohman et al. (r = 0.69). The difference between the estimation of fat by chemical analysis and estimations by DXA and UWW was significantly affected by the amount of water in lean mass and fat-free mass.
KEY WORDS: body composition · pigs · underwater weighing · dual energy X-ray absorptiometry · dissection
The knowledge of body composition is of great clinical and scientific interest when studying metabolic diseases and nutritional disorders. Various indirect and noninvasive methods for the estimation of body composition have been developed (Johansson et al. 1993 DXA measures the differences in the attenuation of X-rays between fat, lean and bone mineral mass. The calculations are based on several assumptions, including constant hydration of the lean mass (Roubenoff et al. 1993 DXA has been evaluated against the chemical analysis of whole carcasses that have been homogenized (Lander Svendsen et al. 1993). There are at least three flaws with this procedure: 1) representative samples from the homogenate may be difficult to obtain (Ellis et al. 1994 Various three- and four-compartment equations based on UWW, DXA and bioimpedance have been described (Forslund et al. 1996 Eight, 12-wk-old, Swedish Landrace × Yorkshire pigs (Medical Innovation AB, Almunge, Uppsala, Sweden) (4 females and 4 castrated males, 26.3 ± 3.3 kg, mean weight ± SD) were used. The pigs were premedicated intramuscularly with ketamine 20 mg/kg and anesthetized intravenously with 500 mg of thiopentone. The animals were killed by means of intravenous potassium, exsanguinated and decapitated between the atlas and the skull. Through a sternal split and an abdominal incision, the thoracic and abdominal organs were removed. The mean carcass weight was 17.7 ± 2.93 kg. Use of experimental animals was approved by the ethical committee of Uppsala. The composition of carcasses was studied in the following order.
Dual energy X-ray absorptiometry, DXA.
The equipment used (DPX-L, Lunar, Madison, WI) utilizes a constant X-ray source at 78 kVp and K-edge filter (cerium) to achieve a congruent beam of stable, dual-energy radiation with effective energies of 40 and 70 keV. The detector system collects data from 120 pixels during each traverse as the scanner proceeds rectilinearly over the scanned object. The software used (Pediatric 1.5 b, DPX-L, Lunar) is designed for calculation of pediatric total body composition; its pixel size of 4.8 × 9.6 mm is optimal for body weights between 15 and 35 kg. Each carcass was placed in a prone position and the total body scan was performed in <10 min; the investigated object was exposed to a total irradiation dose of ~0.021 µSv, which is about two to three orders of magnitude lower than common radiological examinations (Njeh et al. 1997 Underwater weighing (UWW).
The whole-body density was determined according to Archimedes' principle. If one measures carcass mass in air and in water, the differences, corrected for the water density, represent the body volume. The carcass density (CD) can then be calculated as follows:
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
). Two of these, underwater weighing (UWW)3 and dual-energy X-ray absorptiometry (DXA), have frequently been used as reference methods. UWW is based on a two-compartment model [fat and fat-free mass (FFM)]; DXA is based on a three-compartment model (fat, lean and bone mineral mass). Underwater weighing measures body density and calculates the percentage of fat through an equation that assumes that fat and FFM have constant densities (Behnke 1959, Siri 1961). However, it has been shown that the density of FFM is not constant because it is influenced by the amount of water (Forslund et al. 1996) and bone mineral (Martin and Drinkwater 1991) contained. To our knowledge, none of the studies on FFM density and its influence on body composition calculations used direct methods (i.e., dissection and chemical analysis).
). It is possible for DXA to calculate only two compartments at a time, i.e., the fraction between fat and lean mass in soft tissue. If bone is present, DXA calculates the fraction of bone mineral and soft tissue (Jebb 1997). The fraction of fat-to-lean is extrapolated from non-bone area. This means, for example, that mineral outside the bones and fat in the bone marrow is measured as soft tissue.
, Lander Svendsen et al. 1993); 2) the ash obtained from the analysis of homogenized carcasses contains both bone and non-bone mineral (Ellis et al. 1994, Heymsfield et al. 1989a, Lander Svendsen et al. 1993); and 3) whole carcasses also include bone marrow fat. It would be more accurate, therefore, when evaluating DXA, to do a dissection followed by a homogenization of the separate tissues and thereafter analyze the mineral mass in the skeleton and the fat mass in the soft tissue.
, Heymsfield et al. 1989b), but they have not yet been validated by dissection followed by chemical analysis. The aims of this study were to evaluate the accuracy of body composition estimations by the indirect methods DXA and UWW, compared with dissection followed by chemical analysis of fat in soft tissue and bone mineral mass in the skeleton, and if possible to explain the differences in estimation of the two indirect methods.
MATERIALS AND METHODS
Abstract
Introduction
Methods
Results
Discussion
References
).
where Wair denotes carcass weight in air, Wwater the weight under water and Dwater the density of water corrected for the temperature when the measurements were performed.
(1)
Dissection, chemical fat analyses and ashing of the skeleton. After UWW, the carcasses were split along the midline. The right side of each carcass was stored at 4oC until the following morning and then dissected by meat scientists of the Swedish University of Agricultural Sciences. Carcasses were separated into dermis, lean meat, fat and bone. The forefoot was removed by a cut between the distal portion of the radius and ulna and the radial carpal bone, and the hind foot was removed by sawing through the tibia and fibula near the proximal tip of the calcaneus. The total amount of dermis, muscle and fat for each carcass was pooled, ground and analyzed for the quantity of chemical fat. The fat content of each sample was determined once or twice according to NMKL No 131 (Nordic Committee on Food Analysis 1989). The samples were treated with hydrochloric acid over a boiling water-bath. After cooling, ethanol, diethyl ether and light petroleum were successively added and mixed. After separation of the phases, the organic layer was withdrawn. The aqueous layer was extracted twice with a diethyl ether/light petroleum mixture and the extracts combined. Fat content was determined after evaporating the organic solvents and drying (Nordic Committee on Food Analysis 1989).
Calculations of body composition. General equation for the two-compartment model (fat and FFM) . The equation is as follows:
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(2) |
). Siri (1961) assumed a fat density of 0.9 g/cm3 and a FFM density of 1.1 g/cm3 in adult humans, corresponding to a = 4.95 and b = 4.5. Kraybill et al. (1953) assumed a fat density of 0.914 g/cm3 and a FFM density of 1.1 g/cm3 in pigs, corresponding to a = 5.405 and b = 4.914. Lohman (1984) assumed a fat density of 0.9 g/cm3 and a FFM density of 1.084 g/cm3 in prepubescent children, corresponding to a = 5.30 and b = 4.89.
(3)
(4)
(5)
The assumptions behind the three-compartment model and its equations have been described in detail previously (Forslund et al. 1996
(6)
). Equations 3-6 were based on the assumption that FFM minus bone has a density of 1.06 g/cm3 and fat mass has a density of 0.914 g/cm3. The bone mineral volume (Equation 3) was calculated using the density of 3.15 g/cm3 (Weast 1983). CD minus bone (Equation 4) stands for the density of the carcass minus bone mineral (i.e., fat and lean mass).
(7)
(8)
(9)
(10)
(ash + fat) (Equation 9) stands for the density of the carcass minus ash and fat (i.e., water and protein). The constants in Equation (10) were calculated according to Equation (11). The weight fractions of two compartments (i.e., water and protein) with different densities can be calculated from total density using a hyperbolic equation:
In this equation, dw is the density of the water compartment and dp is the density of the second compartment, e.g., protein. We assumed that CD minus fat minus bone mineral and water (i.e., protein plus non-bone mineral plus glycogen) has a density of 1.39 g/cm3 (Allen et al. 1959
(11)
, Brozek et al. 1963) using water density at 37°C (0.99336 g/cm3).
Statistical analysis.
To compare the methods, a simple regression analysis was used for calculations of correlations, combined with a t test of regression coefficients (intercept and slope). The methods were also statistically compared using a paired two-tailed Student's t test. A P-value <0.05 was considered significant. Coefficient of variance was used to analyze the reliability of DXA measurements (Winer 1971). All statistical calculations were done with SAS statistical software package, version 6 (SAS Institute, Cary, NC).
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RESULTS |
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Abstract
Introduction
Methods
Results
Discussion
References
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The individual body composition data obtained from dissection and UWW are shown in Table 1. Comparisons between the carcass analysis and the various indirect methods as well as the reliability of DXA measurements expressed as coefficient of variation (CV) are shown in Table 2. Fat mass was significantly overestimated when UWW data were used in Siri's (1961) and Kraybill's (1953) two-compartment equations. However, fat mass estimated by Lohman's equation (1984) did not significantly differ from the carcass analysis. DXA significantly overestimated bone mineral mass and lean mass, and significantly underestimated fat mass. Three-compartment equations using UWW plus DXA significantly overestimated fat mass and underestimated lean mass.
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One way to evaluate whether DXA or UWW offers a reliable estimation of the body composition is to compare these indirect methods with a direct method such as dissection followed by analysis of chemical fat and bone mineral content.
Manuscript received 23 September 1997. Initial reviews completed 5 January 1998. Revision accepted 27 April 1998.
We thank Inger Winkler for secretarial help, Leif Hambraeus for his guidance and constructive criticism and Neale Mushet for language revision.
View this table:
Table 3.
Regression data for various indirect methods compared with chemical analysis of fat and bone mineral in pig carcasses1
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Fig 1.
Regression of differences between dual-energy X-ray absorptiometry (DXA) and carcass analysis of fat mass on percentage of water in lean mass in 8 pigs; (y = 7.4 - 0.095x, r = 0.86, P < 0.001).
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Fig 2.
Regression of differences between underwater weighing (UWW) (Siri 1961 ) and carcass analysis of fat mass on percentage of water in fat-free mass (FFM) in 8 pigs; (y = 15.2 + 0.21x, r = 0.95, P < 0.001).
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Fig 3.
Correlation between fat-free mass (FFM) density and percentage of water in FFM; (y = 1.33 0.003x, r = 0.99, P < 0.001).
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Fig 4.
Regression of differences between dual-energy X-ray absorptiometry (DXA) and carcass analysis of bone mineral mass on chemically analyzed fat in 8 pigs; (y = 0.0374 + 0.0336x, r = 0.8, P < 0.005).
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Fig 5.
Regression of differences between dual-energy X-ray absorptiometry (DXA) and carcass analysis of bone mineral mass on total carcass weight in 8 pigs; (y = 0.144 + 0.0104x, r = 0.97, P < 0.001).
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
, Lander Svendsen et al. 1993). Furthermore, the ash obtained by analysis of homogenized carcasses comes from both skeletal and non-skeletal mineral (Ellis et al. 1994, Heymsfield et al. 1989a). According to Heymsfield et al. (1989b) non-bone mineral is ~13% of the total amount of mineral in the human body.
, Haarbo et al. 1991).
13%), DXA correlated closely to the values from chemical analysis of the carcasses (r = 0.90-1.0). In a previous study, DXA was compared with chemically analyzed fat after homogenization (Ellis et al. 1994). The authors used similar DXA equipment, but software intended for adult body weight, and the pigs used in their study were heavier (35-95 kg) than ours (15-22 kg). As in this study, the correlations were high (r > 0.97).
) and 28% of the wet weight of the femur in pigs of market weight (Håkansson et al. 1989). Our lower estimations might be explained by the fact that our pigs were prepubertal and their total wet skeleton was not fully mineralized.
). We found (Fig. 1) that this assumption of a fixed quantity of water in lean mass could cause an error in the estimated fat mass. We also found that the amount of fat and the total weight influenced the estimated bone mineral mass. This is in agreement with Laskey et al. (1992) who used a phantom. They concluded that the estimated bone mineral mass was affected by the depth and composition of the subject and that it will be least accurate in obese subjects.
, Van Loan and Mayclin 1992), but these studies were performed on adult humans. Possible explanations of the higher correlation coefficient for DXA vs. UWW compared with dissection might be that with DXA we calculated three compartments and used pediatric software, whereas with UWW, we calculated two compartments and did not use a specific pediatric equation.
stated, this requires the tissue composition of the compartment to be fixed between subjects. Low density of the fat free compartment due to high amount of water and/or low amount of bone mineral will also lead to erroneous results (Forslund et al. 1996). In piglets, the bone mineral content of the growing skeleton is lower compared with the skeleton of the adult pig (Combs et al. 1991), resulting in a lower FFM density. The proportion of mineral (or ash) in the FFM differs notably in our pigs from that in humans. The FFM contains ~5% mineral in adult humans (Forslund et al. 1996); in our study, however, the FFM of carcasses of the pigs contained only 3.3% minerals. According to Heymsfield et al. (1990), the ash weight represents 55% of wet skeletal weight in adult humans, whereas in this study, in which the skull and feet were excluded, the ash weight represented only 15-16% of the wet skeletal weight. The FFM contained on average 78% water in our piglets, which is higher than the 73% assumed in adult humans (Pace and Rathbun 1945). However, the hydration in FFM was similar to the finding of Pintauro et al. (1996) in a study using pigs in the same weight range as ours.
and the 1.1 g/cm3 assumed in the equations of Siri (1961) and Kraybill et al. (1953). Lohman et al. (1984) estimated the average amount of bone mineral and water in FFM in children to be 5.4 and 76.6%, respectively. Brozek et al. (1963) estimated the average amount of bone mineral and water in FFM in adults to be 6.8 and 73.8%, respectively. The low amount of bone mineral and the high amount of water in FFM found in this study account for the lower FFM density and the overestimation of the amount of fat by UWW.
). However, in one study of pigs with weights between 35 and 90 kg using the DPX-L standard adult software, a precision of 0.6-2.6% for all body composition variables including percentage of fat was reported (Lander Svendsen et al. 1993).
, Gotfredsen 1986). However, these studies were performed on humans by using different indirect methods. In this study, we were able to show that the FFM density is not constant among piglets and that the variation is explained mainly by differing amounts of water in FFM. Furthermore, we have shown that these variations in FFM and lean mass can influence the calculated amount of fat. The three-compartment model using UWW and DXA together did not improve the calculation of the fat mass; the main reason (93%) was the influence of variations in the water content of the lean mass on the lean mass density.
1
The costs of publication of this article were defrayed in part
by the payment of page charges. This article must therefore be hereby marked "advertisement"
in accordance with 18 USC section 1734 solely to indicate this fact.
FOOTNOTES
2
To whom correspondence should be addressed.
3
Abbreviations used: BMD, bone mineral density; CD, carcass density; DXA, dual-energy X-ray absorptiometry; FFM, fat-free mass; UWW, underwater weighing.
ACKNOWLEDGMENTS
LITERATURE CITED
Abstract
Introduction
Methods
Results
Discussion
References
a comparison of dual-energy X-ray absorptiometry and hydrodensitometry.
Am. J. Clin. Nutr.
1993;
57:323-326
0022-3166/98 $3.00 ©1998 American Society for Nutritional Sciences
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