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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONPREVIOUS HYDRATION STUDIESAREAS IN NEED OF...SUMMARY AND CONCLUSIONREFERENCES |
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0.73 in mammals and this constancy provides a means of estimating total body fat in vivo. This review examines both in vitro and in vivo data that support the hydration constancy hypothesis and provides a critique of applied methodology. Biological topics of interest are then examined and critical areas in need of future research are identified. These are important issues because water dilution is the only method currently available for estimating body fat in all mammals, which range in body mass by a factor of 104.
Key Words: Hydration • fat-free body mass • total body water • body composition • mammals • dual-energy X-ray absorptiometry
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONPREVIOUS HYDRATION STUDIESAREAS IN NEED OF...SUMMARY AND CONCLUSIONREFERENCES |
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Water, the largest chemical component in mammals, plays a central role in nutrient transport, waste removal, maintenance of cell volume, and thermal regulation. The water content or hydration of fat-free body mass (FFM) is among the best known and most widely applied of the body-composition constants. More than 5 decades ago, Pace and Rathbun (2) first proposed that total body water (TBW) is a constant fraction of FFM (
± SD: 0.724 ± 0.021) on the basis of experiments in guinea pigs. Subsequent chemical analysis of mature animals supported a hydration magnitude of 0.73 with a range of between 0.70 and 0.76 for several mammal species that range in body size from that of mice to cattle—a body mass difference of 104 (3). Additional strong support for the observed FFM hydration magnitude in mammals is provided by whole-body chemical analysis of 9 human cadavers with a mean TBW:FFM of 0.737 ± 0.036 and a range of between 0.684 and 0.808 (Table 1
).
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| (1) |
The importance of the TBW-based method of body-composition measurement led Sheng and Huggins in 1979 (3) to critically review available literature on methodology. Since then, many additional FFM hydration studies have been published, although no synthetic review summarized their findings. This report provides an overview and critique of existing FFM hydration studies. Our aim is to appraise investigators of both strengths and shortcomings in the TBW method of estimating fat mass in mammals.
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PREVIOUS HYDRATION STUDIES |
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TOPABSTRACTINTRODUCTIONPREVIOUS HYDRATION STUDIESAREAS IN NEED OF...SUMMARY AND CONCLUSIONREFERENCES |
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40 major components in humans and other mammals can be organized into atomic, molecular, cellular, tissue-organ, and whole-body levels (1). When examining previous publications on FFM hydration, we found that the studies can be divided into 2 main categories: in vitro and in vivo. Studies can then be organized according to the body-composition level evaluated.
In vitro
In vitro analysis, based on direct chemical assays of entire animal cadavers or isolated tissues and organs, is a classical approach used to investigate hydration of FFM. In vitro studies can be examined at 2 body-composition levels, whole body and tissue-organ.
Whole-body level
Most in vitro FFM hydration studies were carried out at the whole-body level, for which the entire animal cadaver was thoroughly homogenized. Aliquot samples were then used for chemical analysis to determine the contents of various molecular compounds. One can reasonably assume that the chemical composition of aliquot samples are identical to that of the whole body. FFM hydration can thus be calculated as follows:
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| (2) |
Pace and Rathbun (2) were the first authors to review chemical analytic data from several mammals. They calculated a mean TBW:FFM of 0.724 for 50 guinea pigs, whereas the widely quoted mean of 0.732 comes from combining available data for guinea pigs with limited data at that time for rats, rabbits, cats, dogs, and monkeys. Since then, many mammals have been investigated and there is substantial literature on this subject. We reviewed in vitro studies in 15 mammals (Table 2). Unfortunately, some investigators analyzed the animal's eviscerated carcass and their results may not be taken as indicative of whole-body FFM hydration. We review this concern in a later section. Only 9 mammals in this table were therefore considered, including mice, rats, hamsters, rhesus monkeys, baboons, goats, sheep, gray seals, and humans. A very strong correlation (r = 0.9999, P < 0.001) between TBW (kg) and FFM (kg) was observed across mammals (Figure 1):
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| (3) |
± SE: 0.724 ± 0.003) is significantly different from one (P = 7.89 x 10-17) and the intercept (0.255 ± 0.131) is not significantly different from zero (P = 0.088). The mean TBW:FFM for the 9 mammals is 0.739 ± 0.015 with a CV of 2.0%, indicating hydration stability between species. Note in Figure 2 that FFM hydration constancy applies to various mammals from 0.04-kg mice to 214-kg gray seals. The correlation between TBW:FFM and body mass for the 9 mammals is not significant (r = 0.18, P > 0.50).
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). The chemical composition of adult human cadavers was reported by several investigators and a strong correlation (r = 0.987, P < 0.001) between TBW (in kg) and FFM (in kg) was observed (Figure 3):
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| (4) |
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Chemical analysis at the tissue-organ level provides valuable insights into the magnitude and variability in observed FFM hydration. Whole-body FFM hydration at this level is equal to the sum of individual tissue water contents (Wi) divided by the sum of individual tissue FFMs (FFMi):
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| (5) |
(fFFMi) = 1, whole-body FFM hydration can be expressed as
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| (6) |
There are few reported in vitro FFM hydration studies at the tissue-organ level. Mitchell et al (8) studied a male cadaver 35 y of age, and later in 1953 and 1956, Forbes et al (4) and Forbes and Lewis (5) reported anatomic and chemical analysis data for 2 male cadavers aged 46 and 60 y, respectively. Whole-body FFM hydration values calculated by these authors for the 3 cadavers were 0.778, 0.696, and 0.695 with a mean of 0.723 ± 0.038, a value close to the well-recognized value of 0.73.
In addition to whole-body FFM hydration, tissue-organ level studies provide information regarding hydration of individual tissues and organs. As an example of this approach, we calculated Hi and fFFMi values for 16 tissues and organs using reference man data (Table 3) (21). The sum of (Hi x fFFMi) for the 16 tissues and organs is 0.714 and the sum of fFFMi values is 0.975. According to equation 6, whole-body FFM hydration can be calculated as (Hi x fFFMi)/(fFFMi) = 0.714/0.975 = 0.732, which is equal to the well-recognized value (2). Note in Table 3 that no individual tissue or organ has an FFM hydration equal to 0.73. The observed whole-body FFM hydration value of 0.73 is the integrated result of low hydration components (eg, skeleton and skin) and high hydration components such as skeletal muscle and visceral organs.
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These observations can be explained by the tissue-organ level FFM hydration model summarized by equation 6. The entire body can be divided into viscera and carcass. Assume that HV and HC are FFM hydration of viscera and carcass, and fV and fC are the fractions of FFM as viscera and carcass, respectively. Because fV + fC = 1, equation 6 can be converted and simplified to be
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| (7) |
), entire-body FFM hydration is higher than that of the carcass alone. The difference between entire-body and carcass hydration (ie, TBW:FFM - HC) is mainly determined by the fraction of viscera removed. The larger the fraction of removed viscera, the larger the hydration difference between the entire body and the carcass. Equation 7 thus indicates that carcass FFM hydration data may not be applied to the entire body if the fraction of viscera removed is large.
Limitations of in vitro analysis
There is general agreement that in vitro chemical analysis is accurate and should be considered the criterion when studying FFM hydration. However, this technique is also prone to biological and measurement errors. First, human cadavers that were analyzed postmortem often suffered from severe illnesses before death (Table 1). It is difficult to judge the effects of terminal illness on FFM hydration, and the extent to which TBW:FFM measured in cadavers represents hydration in healthy adults remains uncertain.
Second, underestimates of FFM hydration may be caused by insensible water loss between the time of death and the chemical analysis of homogenate samples. Conversely, overestimates of FFM hydration can result from loss of volatile solids during drying of homogenate samples.
A third concern is that investigators differ in their choice of lipid extraction solvent. The type of solvent used has a large effect on the amount of material extracted. Fat or triacylglycerols are bound in tissues by weak van der Waal's forces or hydrophobic bonds and are usually extracted with nonpolar solvents such as ethyl ether or petroleum ether. The residual lipids, including phospholipids and sphingolipids, may form hydrogen bonds and electrostatic associations with proteins that require polar solvents such as methanol and acetone for disruption and tissue extraction (22). Many in vitro studies of FFM hydration used nonpolar solvents, hence, the extracted lipid consisted primarily of triacylglycerol or fat. Some other studies, however, were based on total lipid extraction protocols that used mixtures of nonpolar and polar solvents such as chloroform:methanol (2:1, by vol) or 45% chloroform, 10% methanol, and 45% heptane (7). Dobush et al (23) pointed out that although chloroform:methanol removes total lipid, under some conditions it also extracts a substantial amount of nonlipid compounds. For example, Dobush et al measured the percentage fat of homogenate samples of snow geese. The measured mean (±SE) percentage fat was 29.1 ± 0.27% with petroleum ether and 30.1 ± 0.22% with diethyl ether, respectively. Compared with nonpolar solvents, polar solvents such as chloroform:methanol extracted relatively large amounts of material (34.6 ± 0.6%, P < 0.05 compared with the other 2 methods). When combinations of nonpolar and polar solvents are used, therefore, the observed hydration of FFM will be higher than that when a nonpolar solvent is used (23, 24). Comparisons among studies must be interpreted cautiously.
Last, appropriate chemical analyses of entire animals or isolated tissues is difficult and requires substantial resources for completion. Accordingly, FFM hydration information from in vitro studies is limited, especially from humans and large animals.
In vivo
Whole-body level
Compared with in vitro studies, in vivo analysis avoids difficult homogenization and chemical analyses and can be carried out on a large scale in well-characterized and clinically stable living humans and animals. In vivo studies are thus widely used in FFM hydration investigations, especially when biological factors that may influence hydration such as age and adiposity are examined.
Inspection of published hydration studies often reveals contradictory findings with respect to hydration magnitude and stability. For example, in vivo data suggest that the aging process may or may not influence FFM hydration. Some authors report that FFM hydration does not change significantly in old adults (25–27). However, studies of very old adults (
84 y old) show a significantly higher (P < 0.01) TBW:FFM than that observed in young adults (28). In contrast, an opposite effect was reported by Virgili et al (29), who found that hydration steadily decreases with age in men from the seventh decade (0.702 ± 0.077) to the 10th decade (0.659 ± 0.082). These discrepant results may be caused by population differences, the sample size analyzed, or the measurement methods applied.
The principle of studying in vivo hydration is simple: TBW and FFM are measured separately and the ratio of TBW to FFM is then calculated. The accuracy of observed hydration is closely related to the quality of the TBW and FFM measurements.
Total body water measurement
Although several methods are available for estimating TBW, the accuracy of these methods differ. For example, TBW is sometimes estimated by anthropometric and bioimpedance analysis methods in field studies (30). The validity of observed FFM hydration values by these methods is obviously questionable because of their high measurement error. Antipyrine was used in the past as a dilution tracer but because of conflicting results, its use was discontinued in favor of labeled water isotopes (31).
TBW can be accurately measured by using tritium (3H2O) and deuterium (2H2O) dilution and in some laboratories by 18O-labeled water (H218O) (10). Each isotope measures a specific dilution volume. For tritium and deuterium the dilution volume is larger than actual TBW volume because the labeled hydrogen atoms exchange with hydrogen atoms associated with carboxyl, hydroxyl, and amino groups (32, 33). Similarly, 18O exchanges with labile oxygen atoms in carboxyl and phosphate groups (34, 35). The overexchange rate is 4–5% for tritium and deuterium and 0–1% for H218O. The usual approach today is to assume a 4% and 1% TBW overestimate for tritium and deuterium and 18O-labeled isotopes, respectively (10). This is a critical assumption because, for example, selecting 4% or 5% for tritium TBW overestimation correspondingly affects hydration by 1% (eg, 0.73 compared with 0.72). With correction for overexchange and careful attention to detail, TBW can be measured with a precision and accuracy of 1–2% (10). Even a measurement error of this magnitude may influence the observed TBW:FFM, particularly when small populations are studied.
Another problem is that a considerable difference in TBW estimations is observed when in vivo and in vitro studies are compared (3). After estimating TBW in vivo with tritium, animals in 5 separate studies (9, 17, 31, 36, 37) were killed and TBW was also estimated by chemical analysis. Although in vivo and in vitro methods obtained approximately the same TBW values for rabbits, sheep, and goats (9, 17, 31), in vivo methods measured a TBW value significantly larger (4–15% of body mass) than that produced by in vitro methods for rats, pigs, dogs, and cattle (36, 37). Only 0.5–2.0% of the overestimation by in vivo methods can be explained by the exchange of hydrogen between tritiated water and tissue organic compounds (3). Although technical errors may influence the observed TBW estimate, the remainder of the difference between in vivo and in vitro studies is still not explained fully.
Fat-free body mass measurement
Accurate in vivo measurement of FFM may be even more difficult than that of TBW. Although FFM can be estimated by total body potassium, anthropometry, and bioimpedance methods (29, 30), their value in investigating FFM hydration is obviously limited because of their low accuracy. Streat et al (38), for example, estimated FFM by skinfold thickness anthropometry. The estimated TBW:FFM (0.690 ± 0.075) is much lower than that measured by the neutron activation method (0.739 ± 0.028, P < 0.001). Moreover, the range of FFM hydration estimated by anthropometry (0.52–0.90) is clearly outside of accepted biological limits.
Currently available methods for measuring FFM include 2-, 3-, and 4-compartment densitometry models based on summary equations 8–10. These approaches are derived from corresponding 2-, 3-, and 4-compartment models for measuring total-body fat mass (39, 40):
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| (8) |
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| (9) |
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| (10) |
It has been suggested that multiple-component methods can be used as the reference to assess FFM; however, these methods may not be ideal for the analysis of FFM hydration. As shown in equations 9 and 10, 3- and 4-compartment model approaches require TBW measurement so that water measurement error may be propagated to FFM estimation. Therefore, ideally, FFM should be estimated independently from water measurement in hydration studies. The 2-compartment densitometry model (equation 8) and DXA do not require water measurement. However, the 2-compartment densitometry model is based on an FFM density of 1.10 g/cm3, which was derived from an assumed FFM water fraction of 0.73. DXA also assumes a uniform hydration of 0.73 and electrolyte constancy of FFM (42). If the measurement of FFM is based on DXA or the 2-compartment densitometry model, with an assumed FFM hydration of 0.73, estimated TBW:FFM will be in error for subjects that deviate from assumed hydration. Hewitt et al (28) compared the values of FFM hydration estimated by 2-, 3-, and 4-compartment models. The TBW:FFM values from 3- and 4-compartment models were significantly less than TBW:FFM values from the 2-compartment model in prepubescent subjects and elderly adult females (P < 0.001). In young adults, however, TBW:FFM values from the 3- and 4-compartment models (0.714 ± 0.012 and 0.710 ± 0.010) were greater than that from the 2-compartment model (0.690 ± 0.026, both P < 0.01).
Pietrobelli et al (43) recently evaluated errors arising in DXA body-composition estimates as a result of soft tissue hydration changes. The magnitude of this error is small (ie, a percentage fat error of 1%) unless the relative amount of added water or electrolyte solution is large.
It has been suggested that FFM can be calculated from body mass, total body carbon (TBC), nitrogen (TBN), and calcium (TBCa, all in kg), which are measured by the neutron-activation method (44), as follows:
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| (11) |
An ideal approach, although one that is not always practical, is to apply TBW-independent FFM measurement methods in hydration studies. An example of the method is dilution of fat-soluble inert gases such as cyclopropane or 85Kr (45). However, the application of fat-soluble inert gas methods is limited because of expense and restricted access to instruments.
In summary, both in vitro and in vivo studies make major contributions to the investigation of FFM hydration. In vitro studies reveal that FFM hydration of 0.73 is a universal body-composition rule that applies widely in mammals. In vivo studies additionally identify various biological factors that influence FFM hydration. An important consideration for both in vitro and in vivo hydration research is selection of appropriate subjects in adequate numbers and application of carefully planned body-composition analysis methods. These are critical considerations when evaluating within- or between-group hydration differences because under normal conditions TBW:FFM varies by only a few percentage points.
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AREAS IN NEED OF ADDITIONAL RESEARCH |
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TOPABSTRACTINTRODUCTIONPREVIOUS HYDRATION STUDIESAREAS IN NEED OF...SUMMARY AND CONCLUSIONREFERENCES |
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Does body adiposity influence hydration?
It is often concluded that FFM hydration of adult animals is independent of adiposity and there is a sizable database in support of this view in humans and other mammals (5, 6, 8). In contrast, small and unimpressive increases in FFM hydration with greater body adiposity were reported for guinea pigs and rats (2). Lewis et al (16) tested 13 female baboons by chemical analysis and found a high correlation (r = 0.98, P < 0.01) between percentage body fat and FFM hydration. However, their conclusion is questionable because the FFM hydration values (0.85 and 0.92) observed in 2 animals are obviously beyond the upper limit of normal biological variation.
The influence of adiposity on FFM hydration may be explained with the aid of the tissue-organ level hydration model (equation 6). Body mass can be divided into adipose tissue (AT) and adipose tissue–free body mass (ATFM) on the tissue-organ level. Reference man, with whole-body TBW:FFM of 0.741, has an adipose tissue hydration (HAT) of 0.7667, which is higher than that of adipose tissue–free body mass (HATFM) at 0.7393 (21). The difference between HAT and HATFM (0.0274) indicates that the more adipose tissue an individual has, the higher the FFM hydration. If one assumes that fAT and fATFM are the fractions of FFM as fat-free AT and fat-free ATFM, respectively, and that fAT + fATFM = 1, the tissue-organ level hydration model (equation 6) can be rewritten as
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| (12) |
For example, reference man contains 56.7 kg FFM, 15 kg adipose tissue, and 3 kg nonfat adipose tissue, fAT = 3/56.7 = 0.053. Even though fAT doubles from 0.053 to 0.106, according to equation 11, FFM hydration only increases from 0.741 to 0.742. Therefore, although body adiposity theoretically influences FFM hydration, the change in TBW:FFM may be too small to identify using available in vivo methods. However, the model presented in equation 11 assumes a constant ATFM hydration at all levels of adiposity. Organ proportions may change with increasing body mass and, additionally, edema is often observed in very obese subjects. Hence, our estimates of adiposity effects on TBW:FFM based on equation 11 should only serve as a guide for planning future hydration studies.
Is there an association between age and hydration?
In vivo studies indicate that FFM hydration may be influenced by biological factors such as age. Moulton (46), in his classic investigation, summarized chemical analysis results of 9 mammals, including mice, rats, guinea pigs, rabbits, cats, dogs, pigs, cattle, and humans. At birth, all mammals show a high FFM hydration and low concentrations of protein and mineral. FFM hydration then rapidly declines and protein and mineral content increase from early life until chemical maturity is reached.
Although TBW:FFM decreases rapidly during growth and then stabilizes in young adults, it is not clear whether senescence influences FFM hydration and previous studies are contradictory on this important issue. For example, in vitro cadaver studies (Table 1) do not show a significant correlation (r = 0.15, P > 0.50) between FFM hydration and age. The number of cadaver analyses, however, is small (n = 9) and there are no subjects >67 y of age. Moreover, the subjects presented in Table 1 all died from illnesses or conditions that potentially alter FFM hydration.
FFM hydration change may not be identified by in vivo studies, particularly with small subject groups, because the expected change may be within the range of measurement error. Schoeller (25) suggested that there is little or no effect of aging on FFM hydration through the age of 70 y. Visser et al (47) studied the FFM hydration in a large cohort of individuals aged 20–94 y. No relation was observed between the FFM hydration and age. The correlation coefficients were -0.02 (P = 0.67) for women and -0.07 (P = 0.23) for men. Baumgartner et al (48) also did not observe an age-related change in FFM hydration in 98 subjects aged 65–94 y. Moreover, Goran et al (49) did not observe a significant difference in FFM hydration between young (0.716) and elderly (0.723) men. Mazariegos et al (50) compared FFM hydration between young and older women matched for body mass and height. The TBW:FFM value was similar in the young (0.735 ± 0.020) and older (0.725 ± 0.030) women.
However, a significantly higher TBW:FFM than in young adults (0.708 ± 0.012) was observed in elderly men age 84 y (0.725 ± 0.014, P < 0.01) (28). Bergsma-Kadijk et al (51) observed that FFM hydration was lower in young females (0.723 ± 0.010) than in elderly women aged 65–78 y (0.737 ± 0.025, P < 0.001). The contradictory observations reported by previous investigators on the relation between FFM hydration and the aging process may have been caused by varying population characteristics, including differences in subject body mass, physical activity level, and health status.
Fomon et al (52) and Ellis (53) reported TBW and FFM for children from birth (0.81) to age 10 y (0.75) and in adults from age 20 to 85 y, respectively. FFM hydration decreases markedly during growth and the "constancy" of FFM hydration can therefore only be assumed in nonelderly adults. Although FFM hydration may also change with senescence, the change is probably small and may be difficult to quantify by in vivo studies. Clarification of these issues awaits longitudinal studies with appropriately selected methods and adequate numbers of subjects (54).
Is hydration in nonmammals also stable at <0.73?
Previous studies show that FFM hydration is remarkably constant across mammal species. An interesting question thus arises: do nonmammal vertebrates have the same FFM hydration of 0.73? Up to now, to our knowledge, there are no chemical analysis reports that describe FFM hydration in lower vertebrates. Thorson (55–59), however, provided systematic reports on a related body-composition index, the ratio of TBW to body mass, in poikilothermous vertebrates (Table 4). The fraction of body mass as water in different species depends on habitat. In general, fresh water animals tend to have a higher ratio of water to body mass whereas the reverse applies in marine and terrestrial animals. Another important factor is evolutionary hierarchy. In general, lower animal classes tend to have higher ratios of water to body mass than higher animals. Note that the fractions of body mass as water are similar in animal species of the same class that share similar habitats.
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only provides data for the ratio of TBW to body mass, one can still appraise the FFM hydration of different species. Lower animals living in fresh water may have higher FFM hydration (>0.80) whereas higher animals living in sea water and on land have lower hydration (0.73). Therefore, even though chemical analysis is still lacking for individual species of lower animals, one can make a preliminary conclusion: FFM hydration of 0.73 may not be a characteristic of all vertebrates. |
SUMMARY AND CONCLUSION |
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TOPABSTRACTINTRODUCTIONPREVIOUS HYDRATION STUDIESAREAS IN NEED OF...SUMMARY AND CONCLUSIONREFERENCES |
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0.73 in humans and other mammal species? Does the constancy of FFM hydration of 0.73 reflect physiologic regulatory mechanisms? These are all important topics for future investigation.
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FOOTNOTES |
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2 Supported by National Institutes of Health grants RR00645 and NIDDK 42618.
3 Address reprint requests to ZM Wang, Weight Control Unit, 1090 Amsterdam Avenue, 14th Floor, Columbia University College of Physicians and Surgeons, New York, NY 10025. E-mail: ZW28{at}Columbia.edu.
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TOPABSTRACTINTRODUCTIONPREVIOUS HYDRATION STUDIESAREAS IN NEED OF...SUMMARY AND CONCLUSIONREFERENCES |
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K. J. Ellis Selected Body Composition Methods Can Be Used in Field Studies J. Nutr., May 1, 2001; 131(5): 1589S - 1595. [Abstract] [Full Text]
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G. W. Welch and M. R. Sowers The Interrelationship between Body Topology and Body Composition Varies with Age among Women J. Nutr., September 1, 2000; 130(9): 2371 - 2377. [Abstract] [Full Text]
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D. Gallagher, A. J. Kovera, G. Clay-Williams, D. Agin, P. Leone, J. Albu, D. E. Matthews, and S. B. Heymsfield Weight loss in postmenopausal obesity: no adverse alterations in body composition and protein metabolism Am J Physiol Endocrinol Metab, July 1, 2000; 279(1): E124 - E131. [Abstract] [Full Text] [PDF]
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