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Asia Pacific J Clin Nutr (1996) 5(4): 211-216

Body composition and disease: is there anything new to be learned?

Noel W Solomons MD and Manolo Mazariegos MD

Center for Studies of Sensory Impairment, Aging and Metabolism, the research branch for the Committee for the Blind and Deaf of Guatemala, "Dr. Rodolfo Robles V." Eye and Ear Hospital, Guatemala

Plenary lecture presented at an APCNS Satellite Meeting of the Asian Congress of Nutrition on "Nutrition, Body Composition and Ethnicity" in Tianjin, China on 5th October 1995.

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The observation that disease has an effect on the tissues of the human body is as old as medicine, itself, and was not lost on preliterate and pre-technological societies. Primary changes in the amount, proportions or quality of total body mass, specific organs and specific tissues constitute pathologies; conversely, changes in body composition secondary to and conditioned by diseases are myriad. The classification of most of the associations has been roughly addressed. Nutritional and dietetic therapeutics allows us to intervene to change proportions of fat and lean, while surgery provides some leverage to modify and reconstruct organs and appendages and also to remove excess fat. With respect to these secondary changes due to illness, however, one must determine whether they are generally detrimental or adaptive/accommodative before deciding to intervene. In the context of diet, body composition and ethnicity, ethnic groups differ with respect to their susceptibility to certain diseases and to the severity of their expression. Moreover, differences among different races in body composition are being documented systematically. The future holds in store the ability to analyse the molecular and chemical composition of the body. And we shall be able to focus not merely at the whole-body level, but at regional, segmental and even cellular loci. What must be kept in perspective is ensuring accessibility of the emerging technology to developing nations, as that is where the greatest diversity of both pathology and ethnicity is to be found.

Key words: body composition, ethnicity, pathology, fat tissue, lean tissue, nuclear magnetic resonance, bioelectrical impedance analysis, DEXA, neutron activation analysis

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Classification

To begin this inquiry, we shall exhaust the classificatory position to see if we can make the subtle differentiation between:

• Pathology in which the disease, itself, is a change in body composition
• Pathology in which the disease produces a reactive response by the body

Table 1. Primary body composition changes in disease.

In the category of the disease, itself, being a change in body composition we have a series of examples in Table 1. In general, however, the changes in body composition are secondary to disease. Tables 2 to 6 present an exemplary -- but not exhaustive -- series of the secondary or reactive changes in fluids, fat, lean tissue and bony tissues, respectively, that result from traumatic or pathological conditions. When one combines body composition and disease in a reactive sense, morbid obesity logically comes to mind. As pointed out by Bray1, obesity is not just the accumulation of excess fat. The carriage of the extra weight obligates additional development of musculature; hence, obesity is correctly classified as a combined gain of both fat and lean tissue. On the other hand, in diseases with a cytokine mediated inflammatory component, lean mass is lost disproportionately. At a somewhat more localised (micro) basis, infiltrates are also involved (Table 7). It is not to say anything challenging or original to point out the self-evident association of disease with changes in body composition, primary or secondary.

Prader-Willi Syndrome Acromegaly Gigantism Hypopituitary dwarfism Achondroplastic dwarfism Phocomelia Marfan’s syndrome Post-menopausal osteoporosis Paget’s disease Cleft palate

The quantity of tissue: The word "mass" would be the generic consideration for issues related to the quantity of tissue. In a further generic composition, we would want to know the total amount of fat, lean tissue, and bone. We might also be interested in total amounts of skeletal muscle, solid viscera, intracellular water, extracellular water, and intravascular volumes. The technological transition has been from very indirect methods, many of which were extrapolations of assumptions based on the hydration of tissue, to ever more direct approaches. Dilution methods and scanning techniques are running parallel routes to allow us more directly to assess the masses of various tissue components.

Bioelectrical impedance is a potentially promising tool for the measurement of total-body water, and its definition of TBW allows both the lean tissue and the fat tissue to be calculated using assumptions about the hydration of fat-free mass to estimate the former, and the latter is determined by subtracting the former from total body mass. BIA’s sensitivity to detecting and monitoring changes in mass in the context of wasting diseases has been the subject of commentary².

Table 2. Reactive change in fluid space.	Table 3. Reactive fat-mass changes.	Table 4. Reactive lean-mass changes.
Loss: Diabetes mellitus Diabetes insipidus Secretory Diarrhoea Addison’s disease Acute Haemorrhage Accumulation: Renal Failure Advanced Cirrhosis (any cause) Protein - Energy Malnutrition Congestive Heart Failure Toxaemia of Pregnancy	Gains: Cushing’s disease Losses: Hyperthyroidism	Gains: Turner’s Syndrome Losses: Progeria Testicular feminisation

In the context of the prognosis of disease and prediction of mortality, the loss of mass of the two types of tissue can be indicative. Spontaneous "experiments" of human misfortune, including observations made by physicians within the Warsaw Ghetto and the voluntary monitoring of Northern Irish activists protesting through terminal hunger strikes, have revealed that a critical loss of lean mass and/or the catabolic arrival at a critical level of percent body fat are accurate harbingers of imminent demise³.

Table 5. Reactive mixed (fat plus lean) tissue changes.	Table 6. Reactive skeletal and hard-tissue changes	Table 7. Accumulation of abnormal tissues and infiltrates
Gains: Exogenous morbid obesity Losses: Anorexia nervosa Bulimia Acquired Immune Deficiency Syndrome Tuberculosis Schistosomiasis Rheumatoid arthritis Secondary cachexias	Losses: Osteomalacia Bony metastases Scurvy Spinal-cord injury Neuromuscular diseases Copper deficiency Dental caries	Malignant tumours Neurofibromas Lipomas Leiomyomas Tays-Sachs disease Amyloidosis Myxedema

The quality of tissue: The term "density" with respect to certain chemicals is the basis for the concept of the quality of tissue. The most acute thinking and writing on this topic of "quality" of tissue has come from the Body Composition Unit at Columbia University in New York⁴. From a vast array of sensitive 40K determinations associated with other measures of body water compartments, Pierson and Wang⁴ derived the quality index choosing as a numerator for their density ratio potassium or extra-cellular water and as a denominator intracellular or total-body water. With respect to our overall topic of body composition and disease, the quality of lean tissue findings are provocative. The groups with pathological diagnoses compared and contrasted were: 1) anorexia nervosa; 2) exogenous obesity; 3) acquired immunodeficiency syndrome; 4) alcoholic cirrhosis; 5) muscular dystrophy; and 6) affective disorders. As controls, the authors used their healthy, normal weight population as well as a group of marathon runners and body-builders. Expected associations were found in the quantity of tissue findings, that is with more or less fat and lean tissue as proportions of total body mass. Intriguing findings were documented in the quality domain. When the ECW/ICW ratio was used as a proxy for quality, abnormalities were found in all categories of pathology, except affective disorders. When potassium/ICW was the ratio used to assess quality of lean tissue, all of the pathologies (including affective disorders) except for muscular dystrophy showed marked deviations. For the quality indicators, the two athletic groups were identical to the general healthy population. The authors venture to speculate that the quality ratios might serve as somewhat "nonspecific" markers of the presence or absence of disease. Put another way, disease has a universal distorting effect on the quality of tissue.

In more recent years (Pierson RN: personal communication), on the basis of an expanding pool of total-body nitrogen determinations by instrumental neutron activation analysis, a potentially superior approximation of lean tissue quality, the potassium/nitrogen ratio, can be assessed in a clinical population. Especially in the context of disease, there is a theoretical premise that not only the mass of a tissue may be altered, but that the composition of the tissue may also be changed. It remains to be seen whether it will bear the same differentiation of healthy and unhealthy states.

Finally, viewed another way, to the extent that water is one of the constituents altered, the validity of the classical assumptions about the hydration of lean tissue is also altered. False estimations of true lean-body mass will result from over- or underhydration of lean tissue.

Where can current technology and paradigms take us?

Having documented that diseases and body composition have associations that are well known (even part of the nomenclature and classification reflect explicitly body composition concepts), we might ask where current technology and paradigms can take us.

The "original" technology for body composition was anthropometry, hydrodensitometry and plain X-rays. Delany et al⁵ have commented on the developments in the last two decades, sta 1000 ting: "new methods have been applied to body composition in the last twenty years including: (1) neutron activation; (2) dual energy photon absorptiometry; (3) dual energy x-ray absorptiometry; (4) body conductivity; (5) impedance measurements; (6) computed tomography; and (7) magnetic resonance imaging." Deurenberg⁶ has reviewed an even more exhaustive list and has provided a commentary on their cost, complexity, invasiveness and reliability. However, despite advancing technology, the ability to separate normal from abnormal is important, not only in a philosophical sense (below), but in a practical sense. Pierson et al⁷ have written a thoughtful treatise entitled "Biological homogeneity and precision of measurement. The boundary conditions for normal in body composition" providing an eloquent point of departure for the combination of technology with biology, and ultimately with pathology. To cite one example, dual energy x-ray absorptiometry (DEXA) is versatile insofar as its imaging applications, and it has been embraced in clinical medicine, such that much experience is being accumulated with defining the soft and hard tissue volumes of patients⁸. Caution with regard to the validity and accuracy of this method as a gold standard for body composition tissue components has been voiced, however⁹.

It is important that the five component model of body composition proposed by Wang et al¹⁰ be emphasised. The various measures can be used to examine the composition of the body at five levels: 1) the atomic (elemental); 2) molecular (chemical); 3) tissue; 4) organ systems and 5) whole organism. Recently, an even higher conceptual and mathematical development of the multicompartmental has been offered by the same group from Columbia University¹¹.

With respect to the paradigms, there are two sequential questions that would present themselves; these are included in Table 8. These are based on a somewhat teleological concept that not all change is necessarily injurious, and that some can represent the best adaptation of the organism. When one talks of adaptation or accommodation, it is generally in the context of potentially harsh and adverse circumstances for human function or survival. When applied to populations, evolutionary theory tells us that Nature operates to diversify species and assure the survival of the species. The collective good for immediate and future fecundity -- rather than the life of any given individual within a species -- is the mandate¹². In an evolutionary sense, adaptation could mean selective mortality for those least suited for the environmental; Nature might want to eliminate certain individuals that would produce less fit offspring. When applied to individuals, the sense is different. It is related to the survival of the specific affected individual. The Medical Ethic dating back to Hippocrates relates to efforts from practitioners to benefit the comfort, well-being and survival of individual patients¹³.

Table 8. The "meaning" of body composition responses	Table 9. Interaction of body composition, and disease with ethnic differences.	Table 10. Priorities for continued application of body composition research to diseases.
Do the body-composition changes contribute to the adverse consequences ( such that retarding or opposing them would represent rational therapy) or do body-composition changes represent adap 1000 tive or accommodative compensation ( such that they should be encouraged, not opposed)? How can monitoring of body-composition changes aid in monitoring of the response to therapy or in the refining of emerging prognosis?	differential body composition by ethnicity differential prevalences of diseases by ethnicity differential manifestations of the same diseases by ethnicity transfer of technology to developing countries	The disease has been studied but new facets can be explored due to the emergence of new technology. The technology has been in existence but the disease entity is only recently identified. Both the pathology is new and the technology is novel.

It is in the latter context of medical humanism that we must interpret adaptation and accommodation. We must not treat all altered body composition as undesirable just because it is deviant. To the extent that a change in body composition in reaction to a disease process favours the function and/or the afflicted party, it should be respected, rather than reversed. It is obvious that the massive losses of water attendant to the diuresis of hyperglycaemia in uncontrolled diabetes should be replaced. However, it is not inherently evident whether preserving lean-body mass as progeria advances would enhance or impoverish the quality and duration of a person afflicted by this aberration of premature and accelerated aging. A classic example of body composition adaptation has been documented for the red cell mass during severe, clinical protein-energy malnutrition (PEM) of the oedematous type (kwashiorkor)¹⁴. Children with this state are "anaemic," with an anaemia that does not respond to iron. What it does respond to is the recuperation of protein status, and it has been interpreted to signify a re-prioritisation of protein resources from a function, that is. oxygen transport, which is less urgent in PEM, to more essential tissues. Hence. in this situation, neither the provision of red blood cell transfusions (nor of therapeutic iron) would be merited. In fact, given the possible involvement of free-radicals in the proximal origins of the oedematous transformation¹⁵, iron is a problematic nutrient in the context of protein deficiency.

As the tools of managing body composition, at least at a macro sense, are honed, we must develop the wisdom to know when and how much to apply it to maintain or reverse the body composition changes being caused by the disease. This wisdom only begins by holding the possibility that changes may represent favourable adaptation and are not "bad" just because they are part of the constellation of the present illness.

Interaction with ethnicity

Given that the theme of this Workshop relates to ethnicity, it is important to reflect the considerations of body composition and disease (above) with the particulars and peculiarities of different ethnic groups. The specific points of consideration are listed in Table 9. It is important to realise that ethnic groups are generally associated with specific geographic locations. The Thai tribal peoples live in the highlands of the north. Fiji islanders live on Fiji. Thus, one cannot easily separate the genetic factors from the dietary a 1000 nd environmental ones, in explaining any relationships or peculiarities relating to such groups.

Differential body composition by ethnicity

Even when the issues are not strictly genetic, there are ways in which ecological and environmental situations associate with different ethnic groups. The climatic challenges of the arctic are generally shared only by the Eskimo and Inuit peoples. To the extent that evolutionary adaptation to arctic cold involves redistribution and deposition of fat, one might expect variance in these groups. An interesting observation has been made in contrasting Caucasian and Asian-American adults using various putative indicators of fatness. For height-matched Asians and whites, the latter had higher body mass indices, but the former had more total body fat, explained by a greater subcutaneous deposition of adipose tissue in the Asian volunteers¹⁶.

Undernutrition, especially short-stature, is common among all poor nations, but it is differentially more common in Latin America and Asia than in Africa¹⁷. Moreover, among short children, the mixture of fat and fat-free mass on the frame can differ by ethno-geographic situation. The short preschool children of Peru, an Andean country, have a high weight for their stature composed of additional lean tissue^18,19, whereas those in MesoAmerican countries such as Mexico or Guatemala have the same weight-for-stature that the NCHS reference population has²⁰.

In terms of skeletal mineralisation, African blacks and Afro-Americans have greater bone density than do whites^21,22. These considerations frame the question of how a person who is shorter, or heavier, or lighter, or denser-boned than the normative standard will change when afflicted by a disease that is a body composition-mutating process or that provokes one.

Differential prevalences of diseases by ethnicity

Genetics and environment play determinant roles in the prevalence of diseases. The secondary wasting of cystic fibrosis is likely only to be seen in Caucasian populations, as this gene is most frequent in whites, and rare in other races. Tays-Sachs disease is even more localised, to Jews of Ashkenazi heritage. Osteoporosis is more common among whites as compared to blacks²². Hypertension is more common among blacks than whites²³. In the reactive body composition domain, it has been observed for three decades that rates of obesity and overweight differed by ethnic origin²⁴. Over that era, obesity prevalence has been increasing among all of the ethnic groups represented in the North American population (white, black, Asian, Hispanic, Native American), but it is among the Afro-Americans that the prevalences are highest based on the National Health and Nutrition Examination Surveys²⁵. Thus, the need to apply body composition tools will vary from race to race based on the type of disease of interest.

Differential manifestation of the same disease by ethnicity

Whether it be ethnicity per se, or the geography correlated with the ethnic groups that inhabit a given region, different ethnic groups often exhibit different manifestations of the same disease. The classic example of an ethnicity - disease interaction is that of different virulences of malaria in relation to the sickle-cell anaemia trait; this genetic constitution mitigates the infection. The latter is found almost exclusively in persons of African descent. Another example is cretinism, the most severe result of in utero iodine deficiency disease. It manifests itself in the so-called myxedematous form among the black populations of central Zaire, whereas the neurological deficits predominate in ot 1000 her populations within "goitre belt" regions. Much discussion, possibly a mixture of fact and lore, has emerged with the AIDS epidemic regarding differential responses to the disease depending on geography²⁶. This could be due in part to the varieties such as HIV I versus HIV III, but the degree of wasting may differ between African and North American populations.

Transfer of technology to developing countries

Any additional discoveries among the myriad of possibilities of differential body composition and disease interactions will remain moot unless the most powerful and appropriate technology for assessing body composition is made accessible to the populations of interest. In practical terms this means the developing and transitional nations where the majority of non-white persons live. Some of these groups inhabit the polar north. The remainder would be divided equally between the temperate Far East (China, Japan, Korea) and the tropical regions of South and Southeast Asia, Saharan and sub-Saharan Africa and Latin America. With the exception of Japan, Korea, and some of the smaller Southeast Asian nations (Singapore, Brunei), financial resources, to easily fund the most modern body composition, are limited. However, we cannot dismiss the fact that advances in technology for assessing body composition has advanced in recent years, and applications for the issues of ethnic groups living in their native countries abound.

The sagacious words of Nevin Scrimshaw²⁷ on the topic should be heeded: "Whatever technology is economically, socially and politically feasible as well as effective for relieving malnutrition in developing countries is ‘appropriate,’ regardless of the degree of sophistication or lack of it." Any tool or technology, no matter how sophisticated, can be mastered by the Third World partners.

Instruments like bioimpedance spectroscopy units are quite feasible for Third World uses, but the instrumentation for determining stable-isotopic ratios, and sophisticated DEXA and magnetic resonance imaging (MRI) equipment has yet to penetrate developing countries. As these might be relatively cost-ineffective for any given country, regional facilities should be considered. Our group in Guatemala has commented on the possibilities and limitations of using low-cost methodologies to advance body composition research in the context of laboratories in developing countries²⁸.

Future considerations

The rate of appearance of brand new diseases is relatively slow. Three notable examples, however, human infections caused by the human immunodeficiency, hiatha and Ebola viruses, have raised our attention. Lyme disease and Legionnaire’s disease are two additional infections that have only been recognised in recent years. Rates (prevalences and incidences) of diseases are constantly moving. This happens, in part, because of increased (or decreased) survival in a given affliction. Rates also change (reductions) because of effective preventive measures that can be either direct, for example, the vaccine for measles, or indirect, for example,. improved economic conditions in Southeast Asia that have diminished nutritional blindness incidence due to hypovitaminosis A. Rates also change (increase) due to the proliferation of adverse exposures. For some diseases, fluctuations from endemic to pandemic are seen; this was the characteristic of small-pox and bubonic plague in former eras, and is currently seen in the context of Vibrio cholerae and Mycobacterium infections in the resurgence of cholera morbus and tuberculosis. Pathologists and epidemiologists have the primary role in defining new diseases, and characterising the expression of diseases: old and new.

Priorities for inquiry are listed in Table 10. Basically, body composition specialists should rush to fill in the gaps when the opportunities of a new disease or a technique present themselves. Besides total or near-total ignorance of a disease or a disease relationship, a second tier of considerations would include: 1) the degree of death, suffering or decreased productivity due to a disease in a society; and 2) the relative importance of the most susceptible population sector(s) within the public health priorities of the society.

Finally, there is an emerging area of "body composition" that might be termed cellular composition. If we refocus on the multi-tier compartmental model for body composition¹⁰, elemental and chemical composition stand beside the levels of tissue and organ. Segmental and regional isolation is required to pursue questions at a localised, cellular and subcellular locus. Virchow was the pioneer in the objective, systematic evaluation and classification of pathology based on microscopic tissue examination. This required biopsy material, surgical specimens, or cadaveric samples. What the imaging techniques portend, in fact, is an approximation of an in vivo chemical and anatomic imaging/scanning "biopsy" of a tissue, in which the elemental composition, hydration, energetics, and oxidation status of the constituent cells can be determined with probes external to the body.

With regard to elemental composition, instrumental neutron activation analysis can define certain nutrients at the total-body level, but scanning techniques are honing in on elemental composition at the localised level. An example of this can be found in the work of Bartzokis et al²⁹, quantifying elemental iron in the brain of living subjects using MRI.

With regard to cellular hydration, the relationship of cellular hydration state to catabolism has been offered by Fürst and Stehle³⁰ when they state: "... an increase in cellular hydration (swelling) acts as an anabolic proliferative signal, whereas shrinkage is catabolic and antiproliferative." This is a fascinating observation on the micro anatomic level, consistent in general terms with the observations (above) of the obligate expansion of the ECW/ICW ratio with almost all pathological processes by Pierson and Wang⁴. Work currently going on in our Center in Guatemala (Mazariegos and Solomons: unpublished observations) is exploring the isolation of segments of limbs, and determining the sensitivity of multifrequency bioimpedance spectroscopy to define the average hydration of tissue over an extension of the arm or leg.

With regard to cellular energetics, D. Jacobs and his group at Harvard have pioneered the use of MRI coupled to radiophosphorus to determine the actual ATP dynamics in vivo within living cells³¹. The extension of this approach to actually "mapping" the fuel supply of the living body has limitless possibilities. Although a methodology does not come to mind, a final frontier in this line of in vivo cell diagnosis would be an approach to documenting either the fact of lipid peroxidation, in vivo, or the generation of free-radicals and oxygen-reactive species.

Although the relationship is long-standing, we can give an affirmative answer to the sub-title of this presentation. There is indeed more to be learned. In fact, there may be much to be learned. The priorities for the application of body composition research might be summarised as shown in Table 10. The additional judgement of how much of a practical contribution the elucidation of body-composition aspects will make on the management or control of the disease in individuals or groups. When those determinations 1000 are made, then the fundamentals discussed above will come into play. It is essential that investigators be trained and equipped, especially in the economically less privileged settings. Caveats and nuances related to ethnic differences must be taken into consideration in the design of studies and interpretation of data. Finally, once the relationships are sorted out, the final judgement as to what interventions to take directly to influence body composition should be based on critical assessment of whether these changes are detrimental or adaptive in nature.

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Body composition and disease: is there anything new to be learned?

Noel W Solomons and Manolo Mazariegos

Asia Pacific Journal of Clinical Nutrition (1996) Volume 5, Number 4: 211-216

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Copyright © 1996 [Asia Pacific Journal of Clinical Nutrition]. All rights reserved.
Revised: January 19, 1999 .

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