Section of Medicine, Experimental Medicine & Therapeutics
vironment. As clinical investigations continue it is becoming apparent that the problems of malnutrition are even more diverse than was at first thought and that other nutritional deficiency states must now be considered as important associated features of protein-energy malnutrition. The availability of essential fatty acids, iron and folic acid may all be limited and deficiencies of these nutrients deserve greater consideration. Attempts on a national or an international level to increase the protein and/or energy supply to the diet have had little success in reducing the prevalence of malnutrition and it would seem, therefore, that continued study of the condition is warranted. Public health measures depend upon an accurate understanding of the nutritional as well as social and economic factors involved in the development of protein-energy malnutrition. The role of intestinal infections and jejunal bacterial overgrowth may prove a key to further developments in understanding the prevalence of malnutrition. REFERENCES Ashworth A, Bell R, James W P T & Waterlow J C (1968) Lancet ii, 600 Autret M & Behar M (1954) Food and Agriculture Organization Nutritional Studies No. 13 Brock J F, Hansen J D L, Howe E E et al. (1955) Lancet ii, 355 Brunser 0, Reid A, Monckeberg F et al. (1966) Pediatrics 38, 605 Chandra R K (1975) British Medical Journal ii, 583 Chandra R K & Saraya A K (1975) Journal of Pediatrics 86, 899 Cooper W C, Good R A & Mariani T (1974) American Journal of Clinical Nutrition 27, 647 Coovadia H M, Parent M A, Loening W E K et al. (1974) American Journal of Clinical Nutrition 27, 665 Coward W A (1975) British Journal of Nutrition 34, 459 Dammin G J (1965) Federation Proceedings 24, 35 Edelman R, Suskind R, Sirisinha S & Olson R (1973) Lancet ii, 506 Fagundes Neto U, Toccalino H & Dujovney F (1967) Acta PAdiatrica Scandinavica 65, 609 Gopalan C (1968) In: Calorie Deficiencies and Protein Deficiencies. Ed. R A McCance & E M Widdowson. Churchill, London; p 49 Gracey M, Suharpono, Sunoto & Stone D F (1973) American Journal of Clinical Nutrition 26, 1170 Gross R L, Reid J V 0, Newberne P M et al. (1975) American Journal of Clinical Nutrition 28, 225 Heyworth B & Brown J (1975) Archives of Disease in Childhood 50, 27 Holman R T (1971) In: Progress in the Chemistry of Fats and other Lipids, vol 9. Ed. R T Holman. Pergamon, Oxford; p 275 James W P T (1971) Archives of Disease in Childhood 46, 218 James W P T, Drasar B S & Miller C (1972) American Journal of Clinical Nutrition 25, 564 James W P T & Hay A M (1968) Journal of Clinical Investigation 47, 1958 Jelliffe D B
(1959) Journal of Pagdiatrics 54, 227 Mats L J, Jimenex F, Cord6n M et al. (1972) American Journal of Clinical Nutrition 25, 1118
McCance R A (1968) In: Calorie Deficiencies and Protein Deficiences. Ed. R A McCance & E M Widdowson. Churchill, London; p 1 Naismith D (1973) British Journal of Nutrition 30, 567 Press M, Hartop P J & Prottey C (1974) Lancet ii, 597 Reddy V, Jagadeesen V, Ragharamulu N et al. (1976) American Journal of Clinical Nutrition 29, 3 Rossing N, Parying H-H & Lassen N A (1976) In: Plasma Protein Turnover. Ed. R Bianchi, G Mariani & A S McFarlane. Macmillan, London; p 357 Rutishawser I H E & Whitehead R G (1972) British Journal ofNutrition 28, 145 Schneider R E & Viteri F E (1974) American Journal of Clinical Nutrition 27, 788 Scrinmshaw N S, Taylor C E & Gordon J E (1968) WHO Monograph Series No. 57. World Health Organization, Geneva Smythe P, Schonland M, Brereton-Stiles G G et at. (1971) Lancet ii, 939 Troll V & Rittmeyer P (1974) Infusionstherapie 3, 230 Waterlow J C (1968) Lancet ii, 1091 Waterlow J C, Cravioto J & Stephen J M L (1960) Advances in Protein Chemistry 15, 131 Whitehead R G (1971) In: Proceedings of the XIII International Congress of Pediatrics, Vienna, vol. 2 part 1. Wiener Medizinischen Akademie, Vienna; p 231 Williams C D (1933) Archives of Disease in Childhood 8, 423
Professor A N Exton-Smith (University College Hospital Medical School, London WCJ) Malnutrition in the Elderly
The individual dietary patterns in the majority of old people remain similar to those which have been acquired by habits established at a younger age. Nevertheless, there are many factors which begin to operate more frequently with advancing age and these may lead to nutritional deficiencies. Some of these factors are related to decline in bodily health with difficulty in obtaining and preparing food; to changed economic circumstances resulting from retirement; to depression and organic mental deterioration; to social isolation and loneliness, especially following bereavement; and to ignorance of what constitutes a balanced diet, particularly in the widower who must often cater for himself for the first time. The primary and secondary causes of malnutrition in old age are summarized in Table 1. In any one individual malnutrition is often multifactorial in origin, especially in the housebound old person who, in addition to physical illhealth, may suffer from social isolation, straitened financial circumstances and impaired appetite due
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Table 1 Primary and secondary causes of malnutrition Primary Ignorance
Physical disability Mental disorder Iatrogenic Poverty
Secondary Impaired appetite Inefficient mastication Intestinal malabsorption Alcoholism Drugs Increased requirements
to physical inactivity. The housebound have been found to have nutrient intakes which are substantially lower than those of active people matched for age (Exton-Smith et al. 1972). Approximately 10 % of the elderly population are housebound (Sheldon 1948) and this section of the population represents the largest single group vulnerable to malnutrition. Thus, disability in old age not only affects the mode of living of those afflicted, but it also has an adverse effect on dietary intakes and nutritional
Occurrence of Nutritional Deficiencies In a recent nutrition survey of the elderly population, sponsored by the Department of Health and Social Security (DHSS 1972), a diagnosis of malnutrition was made in 3 % of old people living at home. It included protein-calorie malnutrition, iron deficiency and specific vitamin deficiencies, but rarely could a primary cause that was related to social and economic factors be discovered and in the majority of cases an underlying medical condition was responsible. Nevertheless, in the absence of overt malnutrition, socioeconomic factors may be of importance since it was found that men aged 75 years and over who were living alone fared worse than those living with a relative or spouse in respect of a large number of nutrients. This was in some measure reflected in the proportion having biochemical levels below certain arbitrary limits; for example, four times as many men in this age group living alone had leukocyte ascorbic acid levels below 7 pg/108 white cells compared with those living in the company of others. Several recent surveys have shown that the nutritional status of the elderly is often inferior to that of younger people. A few of these findings will be mentioned in order that their significance can be discussed.
Protein-calorie malnutrition: In the DHSS survey 88 of the 879 subjects had low energy intakes (less than 6.3 MJ/day for men and 5.0 MJ/day for women) and it was considered that 8 of these subjects could have protein-calorie malnutrition on the basis of the clinical assessment and the
findings of a serum pseudo-cholinesterase activity of less than 150 units. There was a correlation between low serum albumin levels and low serum cholinesterase activity and the clinician's assessment of health. Low activity of pseudocholinesterase was also correlated with skinfold thickness. When the serum albumin level was less than 35 g/l, 40 % of the subjects had cedema; 22 % had oedema when the albumin was 35 to 44.9 g/l and 13 % when it was above 45 g/l. It is considered that a possible explanation lies in the effects of stress; in this case the stress is non-nutritional disease (mainly cardiac failure) superimposed on levels of serum albumin which, in the majority of instances, would have been unassociated with cedema had it not been for the additional burden. The significance of subclinical protein deficiency is difficult to assess, but it may be of greater importance in the elderly than at other ages since homeostatic mechanisms are impaired and stress due to a variety of pathological processes in old age may upset the precarious physiological balance. It is not known to what extent the failure to maintain the body pool of albumin in older subjects, due to age-related alterations in the regulating mechanisms, can be influenced by a higher dietary intake of protein. Iron deficiency: In the DHSS survey the overall frequency of anamia was 7.3 % and the commonest single cause was iron deficiency. There was a significant correlation between hemoglobin concentration and serum iron levels when all the subjects were grouped together, and those living alone had a higher incidence of anaemia (P < 0.01) compared with those living with their spouse or relative. Overt iron deficiency, as measured by a serum iron concentration of less than 10.74 ,mol/l and total iron building capacity higher than 71.60 ,umol/l, was found in 4.7 % of the elderly men and 13.2 % of the elderly women. The most likely explanation of this difference is the lower iron intake of most groups of women compared with that of men. Thus, in the six areas surveyed only one group of women (the age group 65-74 in one area in Scotland) was found in which the mean intake was greater than the recommended allowance of 10 mg/day, whereas, by contrast, only one group of men (the over-75 age group in Sunderland) failed to meet the recommended intake of iron. B group vitamins: A high incidence of changes in the mucous membranes of the tongue and lips in elderly hospital patients has been reported and these have been attributable to deficiency of B vitamins (Griffiths et al. 1967, Brocklehurst et al. 1968). When single vitamin supplementation was given for one year, riboflavin produced an im-
Section ofMedicine, Experimental Medicine & Therapeutics
provement in cheilosis (and possibly in angular stomatitis), and nicotinamide in the appearance of the dorsum of the tongue (Dymock & Brocklehurst 1973). Subsequent investigations (MacLeod 1972, Berry & Darke 1972) failed to confirm the benefits of single vitamin supplementation. Thurnham (1972 unpublished) measured the erythrocyte glutathione reductase activity (EGR) and the percentage stimulation of EGR by flavine adenine dinucleotide (FAD) in 128 old people living at home in the London Borough of Camden. A stimulation of greater than 30 % (often regarded as an indication of riboflavin deficiency in younger people) was found in 18 % of the men and 19 % of the women. Thus, marginal deficiency could exist in the elderly population but the true significance of these biochemical levels is unknown. Thiamine deficiency leads to a variety of cardiac and neurological manifestations including Wernicke's encephalopathy which is occasionally seen in old people; the clinical features include diplopia, nystagmus, ophthalmoplegia and the mental changes of Korsakoff's psychosis. The response to treatment with thiamine is usually dramatic. Hypothermia can complicate Wernicke's encephalopathy (Philip & Smith 1973) and is presumably due to lesions in the hypothalmic centres controlling temperature regulation. The possibility of thiamine deficiency associated with the poor natritional status of old people admitted with hypothermia needs to be investigated. Several studies have reported folate deficiency in old people. Read et al. (1965) found that 80% of entrants to old people's homes in Bristol had folate deficiency, which was taken as a serum level of less than 6 pg/l. Batata et al. (1967), working in Oxford and adopting a lower limit of 2.1 pg/l, found that 10 % of patients over the age of 60 had folate deficiency. The levels tended to be lowest in those with severe disability and there was a significant correlation between organic brain disease and low folate levels.
Vitamin C deficiency: Although overt manifestations of deficiency are rare, the body stores of vitamin C in many old people are diminished. Low levels of leukocyte ascorbic acid (LAA) have been reported by several observers; the levels are lower in the elderly than in younger subjects (Bowers & Kubik 1965, Andrews et al. 1966), lower in winter than in summer (Andrews et al. 1966), lower in men than in women (Milne et al. 1971) and smokers have lower LAA levels compared with non-smokers (Brook & Grimshaw 1968). Furthermore, diminished abscorbic acid levels have been reported in institutionalized old people (Kataria et al. 1965, Andrews & Brook 1966). The low levels of LAA in certain old people are not a natural accompaniment of ageing, since by feeding with
ascorbic acid they can be brought to levels seen in younger people (Andrews et al. 1966). In a study made in Edinburgh, Milne et al. (1971) found that LAA levels were significantly higher in July to December compared with the rest of the year. Slightly more than halfthe subjects had vitamin C intakes of less than 30 mg/day and a significantly greater proportion had low vitamin C intakes in the months October to March compared with the months April to September. Vitamin C intake was correlated with LAA level and it was found that LAA levels increased in parallel with, but lagged behind, seasonal increases in vitamin C intakes. Similar findings were reported in the DHSS survey (1972). Windsor & Williams (1970), by measuring total hydroxyproline excretion (THP) in response to vitamin C, found that THP increased when the initial LAA content was less than 15 pg/108 white cells, but when the LAA level was higher than this the response to vitamin C supplementation failed to occur. In an investigation of old people who participated in the Camden survey, Thurnham found that 28 % of the men and 10 % of the women had LAA levels of less than 15 pg/108 white cells (Thurnham 1972, personal communication). The higher proportion of men with deficiency is in keeping with the findings of clinicians that scurvy is more prone to occur in men than in women. Sublingual 'petechie' have been regarded by Taylor (1968) as an early sign of scurvy, but Andrews et al. (1969) have shown by histological examination that the lesions are small aneurysmal dilatations of the minute vessels under the tongue. It is highly unlikely, therefore, that they can be caused by acute vitamin C deficiency; moreover, they do not disappear when ascorbic acid intake is increased. Recently Eddy & Taylor (1977) have shown a much lower incidence of these sublingual lesions in a group of elderly people who were vegetarians for many years and who had high plasma and leukocyte ascorbic acid values compared with old people in general. They suggest that previous, perhaps recurrent, vitamin C deficiency may lead to irreversible changes in the vessel walls which cannot subsequently be reversed by vitamin
therapy. Vitamin D deficiency: The state of vitamin D nutrition of two groups of elderly women has been assessed by Smith et al. (1964). For women living in Michigan (average age 60.6 years) the level of vitamin D in the blood as determined by the serum antirachitic activity was significantly lower in those subjects with low bone density compared with those having normal bones, and the level showed marked seasonal variation. By contrast, for a group of women of similar age living in Puerto Rico, where there is much greater exposure to sunlight and higher vitamin D content of food, the in-
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cidence of skeletal rarefaction was much lower, the serum vitamin D levels were much higher, and there was no seasonal variation. Using the more precise index of radiostereoassay of 25-hydroxycholecalciferol levels, Stamp & Round (1974) have shown similar seasonal variations in both young and old subjects. They conclude that summer sunlight is an important, and possibly the chief, determinant of vitamin D nutrition in Britain. In this respect, housebound old people (Exton-Smith et al. 1972) may be at the greatest disadvantage since they lack exposure to sunlight and often have very low dietary intakes; 48 % of housebound women aged 70 to 79 years had a dietary intake of less than 30 iu per day compared with 13% of active women of similar age. Clinical osteomalacia is not uncommon in certain sections of the elderly population. In Glasgow, Anderson et al. (1966) found that 16 % of elderly women admitted to a geriatric department had osteomalacia when there was a possible clinical indication; subsequently osteomalacia was found in 4 % of all elderly women admitted. The question has recently arisen whether vitamin D deficiency is of clinical importance in the absence of the usual features of osteomalacia. Aaron et al. working in Leeds, have shown by histological methods than 20-30% of women with fracture of the proximal femur and about 40 % of men had osteomalacia (Aaron, Gallagher, Anderson et al. 1974). Later they showed that the proportion with osteomalacia varied with the season (Aaron, Gallagher & Nordin 1974). The highest frequency of abnormal calcification fronts (43 %) was observed in February to April and the lowest (15 %) in August to October. The highest frequency of abnormal osteoid covered surfaces (47 %) was observed in April to June and the lowest (13 %) in October to December. They concluded that variation in hours of sunshine is responsible for a seasonal variation in osteomalacia in femoral neck fractures and, possibly, in the elderly population as a whole. The significance of vitamin D deficiency as an important factor in the pathogenesis of fracture of the femoral neck has been confirmed by the study of Faccini et al. (1976). The mean value of trabecular osteoid area in the fracture group was 4 % compared with 1 % in a control group. The difference was also striking in the proportion of trabecular surface covered by osteoid; the mean value for the fracture group was 24.5 % compared with 7.9 % for the control group. Brown et al. (1976) found significantly lower levels of 25-hydroxycholecalciferol in patients with fractures of the femoral neck compared with those in controls of similar age from whom blood samples were taken at the same time of year. This is believed to be a reflection of the decreased out-of-doors activity of the patients prior to their fracture.
Significance of Low Intakes and Tissue Levels of Nutrients The examples of nutritional deficiency which have been considered above have several features in common which can be summarized as follows: (1) A high proportion of old people have low dietary intakes, and many of these are well below the recommended nutrient intakes for the United Kingdom. In some instances there is an association between low intakes and socioeconomic factors (for example, living alone) and with physical disorders, especially those which render the individual housebound.
(2) Many old people have blood and tissue levels of nutrients which are below the arbitrarily defined limits adopted for younger people. The lowest levels are often found in those individuals with physical disorders.
(3) Only rarely are the low intakes and the abnormal biochemical findings associated with a disturbance of form or function that is required for the diagnosis of clinical malnutrition. (4) The significance of subclinical malnutrition and the extent to which the health of these old people would benefit from increased dietary intakes are unknown. Nevertheless, it would seem prudent to attempt to raise the levels of nutrients in order to make these individuals more resistant to the effects of stress due to non-nutritional diseases which become increasingly common with advancing years. Longitudinal Studies The relationship between health and nutrition in old age can be determined by longitudinal studies. Few studies of this kind have been undertaken, but the results of an investigation of the mortality in a five-year follow up of the participants in the 1967/68 DHSS nutrition survey have been described (Hodkinson & Exton-Smith 1976). Nutritional factors which were significant in predicting mortality were found to be a low vitamin C intake in men (P < 0.02) and a low serum pyridoxine level in women (P < 0.01). These findings must be interpreted with caution and further confirmatory studies are required to ascertain whether they represent true vitamin deficiencies. Another investigation has shown that leukocyte vitamin C level is a predictor of mortality in patients admitted to a geriatric department, but this was subsequently found to be an effect related to severity of illness and not an expression of deficiency of vitamin C, since supplementation had no influence on survival (Wilson et al. 1973). It is possible that the relationship
Section of Medirine, Experimental Medicine & Therapeutics
between vitamin C intake and mortality is an Department of Health and Social Security A Nutrition Survey of the Elderly epiphenomenon in that the fittest men may select (1972) Dymock S M & Brocklehurst J C diets which are particularly rich in vitamin C. (1973) Age and Ageing 2, 172 It would also be desirable to establish 'running Eddy T P & Taylor G F Age and Ageing 6, 6 indices' in a small group of elderly people by the (1977) Exton-Smith A N, Stanton B R & Windsor A C M continuous monitoring of dietary intakes and the (1972) Nutrition of Housebound Old People. King Edward's frequent assessment of nutritional status by Hospital Fund Faccini J M, Exton-Smith A N & Boyde A biochemical and clinical examinations (Whitehead (1976) i, 1089 1974, personal communication). Using this GrifithsLancet L L, Brocklehurst J C, Scott D L, Marks J & Blackley J method it should be possible to determine the (1967) Gerontologia Clinica 9, 1 Hodkinson H M & Exton-Smith A N efficiency of homeostasis and the extent to which (1976) and Ageing 5, 110 variations in biochemical values are a reflection of KatariaAge M S, Rao D B & Curtis R C changes in health and in nutrient intakes. Finally, (1965) Gerontologia Clinica 7, 189 MacLeod R D M there is sufficient evidence of a poor vitamin D (1972) Age and Ageing 1, 99 status in certain sections of the elderly population Milne J S, Lonergan M E, Williamson J, Moore F M L, to justify controlled trials of vitamin sup- McMaster R & Percy N British Medical Journal iv, 383 plementation. It is essential that such trials should (1971) Philip G & Smith J F be carried out to establish any benefits from (1973) Lancet ii, 122 increased intakes before recommendations are Read E A, Gough K R, Pardoe J L & Nicholas A British Medical Journal ii, 843 (1965) made for the fortification of foods with vitamin D. Sheldon JH REFERENCES Aaron J E, Gallagher J C, Anderson J, Stasiak L, Longton E B, Nordin B E C & Nicholson M (1974) Lancet i, 229 Aaron J E, Gallagher J C & Nordin B E C (1974) Lancet ii, 84 Anderson I, Campbell A E R, Dunn A & Runciman J B M (1966) Scottish Medical Journal 2, 429 Andrews J & Brook M (1966) Lancet i, 1350 Andrews J, Brook M & Allen M A (1966) Gerontologia Clinica 8, 257 Andrews J, Letcher M & Brook M (1969) British Medical Journal ii, 416 Batata M, Spray G H, Bolton F G, Higgins G & Wollner L (1967) British Medical Journal ii, 667 Berry W T C & Darke S (1972) Age and Ageing 1, 177 Bowers E F & Kubik M M (1965) Practitioner 19, 141 Brocklehurst J, Grittiths L L, Taylor G F, Marks J, Scott D L & Blackley J (1968) Gerontologia Clinica 10, 309 Brook J & Grinshaw J J (1968) American Journal of Clinical Nutrition 21, 1254 Brown I R F, Bakowska A & Millard P H (1976) Age and Ageing 5, 127
(1948) The Social Medicine of Old Age. Oxford University Press, London Smith R W, Rizek J, Frame B & Mansour J (1964) American Journal of Clinical Nutrition 14, 98 Stamp T C B & Round J M (1974) Nature (London) 247, 563 Taylor G F (1968) In: Vitamins in the Elderly. Ed A N Exton-Smith & D L Scott. John Wright, Bristol Wilson T S, Datta S B, Murrell J S & Andrews C T (1973) Age and Ageing 3, 163 Windsor A C M & Williams C B (1970) British Medical Journal i, 732
The following paper was also read: Epidemiology of Malnutrition in the World Professor J C Waterlow (Department of Human Nutrition, London School of Hygiene and Tropical Medicine, Keppel Street, London WCJ)