Changes in metacarpal mineral content and density in normal male and female subjects with age

Clin. Radiol. (1969) 20, 23-31 CHANGES IN METACARPAL MINERAL NORMAL MALE AND FEMALE

CONTENT SUBJECTS

AND DENSITY WITH AGE

IN

D. A. SMITH, J. B. A N D E R S O N , J. SHIMMINS, C. F. SPEIRS and E. BARNETT

From the University Department of Medicine, Gardiner Institute, Western Infirmary, the Regional Physics Department, 9 West Graham Street and the Department of Radiology, Western Infirmary, Glasgow

Using their own previously described technique, the authors measured the bone m;neral from the third metacarpal of 312 male and 317 female volunteers. Two measurements were used. Firstly, the Standardised Aluminium Equivalent (S.A.E.) is a measurement of the amount of mineral in the path of the X-ray beam divided by the external diameter of the bone - thus allowing for variations in size of the subjects. Secondly, the density (L) is quantitated. This is the amount of mineral per unit volume of cortical bone. The S.A.E. rises rapidly with age in both sexes to reach a peak at 36 years in male and 34 years in females. Thereafter the S.A.E. falls in both sexes especially in women after the age of 50 years, and the greatest fall is found within ten years of the menopause. The density (~,) rises rapidly in both sexes up to about 25 years of age. Thereafter a slow but steady rise occurs in men up to the age of 75. In women L continues to rise up to the age of 40 and gradually falls after then. The external diameter of the third metacarpal increases rapidly in both sexes between the ages of 5 and 30, but does not significantly change thereafter.

TIrE accurate measurement of the amount of mineral in bone is of great importance in the diagnosis of metabolic bone disease and in the assessment of the response to therapy. Many attempts have been made to quantitate the mineral content of bone. These range from simple anatomical measurements in peripheral bone and the spine (Barnett and Nordin 1960; Meema 1963) to the estimation of the density of various bones in the skeleton (Nordin et al. 1962; Keane et al. 1959; Doyle 1961; Meema et al. 1964; Mayo 1961; Bywaters 1948; Koch and Kaplan 1961). We have reported elsewhere (Anderson et al. 1966) a technique for measuring bone density and mineral content. The method is both simple to use and reproducible. Wesuggested at that time that the technique might be used in large surveys. In the present paper we report the changes in bone mineral and density with age in 312 male and 317 female subjects. They have been related to the menopause in women, and the values obtained for both the male and female subjects have been compared. Changes in total metacarpal diameter in relation to age have also been described.

carpal has been fully described in a previous communication (Anderson et al. 1966). The aluminium standard and third metacarpal of the right hand are X-rayed in air. The hand is placed on the film, the film focal distance being 50 ins. The hand and step-wedge are so positioned that the metacarpal is parallel to, and the step-wedge at right angles to the long axis of the X-ray tube to correct for the 'heel' effect. The aluminium wedge is in line with the midpoint of the third metacarpal. The X-ray exposure factors are 350 mAs and 42 kV. Standard screen films are used without screens and are processed automatically in an X-Omat M3 automatic processing unit. The Joyce Loebl chromoscan double beam recording densitometer is used to scan the films. All measurements are carried out on the third metacarpal. The cortical and total widths of the metacarpal are measured on the X-ray film with a pair of calipers. From the scan, the aluminium equivalent of the mineral of the metacarpal in the X-ray beam is measured (Fig. 1). This is a measure of the amount of mineral (a q- b) in the path of the X-ray beam. This value is then divided by the diameter of the metacarpal to allow for variations in size between individuals. The derived value is termed the Standardised Aluminium Equivalent (S.A.E.). METHODS The density (k) is a measure of the amount of The method used for measuring the X-ray mineral per unit volume of bone tissue in the density and mineral content of the third meta- cortex (a + b) (Fig. 1). 23

CLINICAL

24 t

RADIOLOGY

Path of X - r a y b e a m

= A b s o r p t i o n equivalent in A1 o f ( a + b.)

Aluminium Equivalent (A. E. ) Cross -section through metacarpal

A ° E .

~k = L i n e a r attenuation coefficient of the X - r a d i a t i o n in(a + b.)

FIG. 1 To show the derivation of (1) the Aluminium Equivalent (A.E.); (2) the Standardised Aluminium Equivalent (S.A.E.) ; (3) the density of the cortex (~.).

N O R M A L FEMALES Standardised Aluminium Equivalent

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FIG. 2 The variation in the S.A.E. with age in normal female subjects. The m e a n and two standard error range within 5 year age groups is illustrated.

Subjects Studied.---The subjects in this survey were volunteers approached while visiting relatives and friends in the wards of the Western Infirmary, Glasgow. With their permission, an X-ray of the right hand was taken and a standard questionnaire completed. This questionnaire was designed to elicit any history of disease which may have affected the skeleton.

RESULTS The data were first analysed in terms of the mean and two standard error range in the 5 year age groups. In the female group, the mean S.A.E. rose from 20-9 between the ages of 5 and 9 to a value of 36.5 between 25 and 29 years of age (Fig. 2). The mean S.A.E. fell slowly thereafter to a value of 34.7 between 45 and 49 years, and then

CHANGES

IN

METACARPAL NORMAL

MINERAL

25

CONTENT

FEMALES

PRE-MENOPAUSAL

POST-MENOPAUSAL

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Years since Menopause

Fxo. 3 T h e effect of the m e n o p a u s e on the S.A.E. T h e age is s h o w n in p r e - m e n o p a u s a l w o m e n , a n d the years since the onset o f the m e n o p a u s e in the subjects in w h o m m e n s t r u a t i o n has stopped.

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FIG. 4 T h e v a r i a t i o n in the S.A.E. with age in n o r m a l m a l e subjects. T h e m e a n a n d two s t a n d a r d e r r o r range within 5 year age groups is illustrated.

much m o r e rapidly, to a value o f 24.1 between 70 a n d 74 years. The S.A.E. has also been related to the m e n o p a u s e (Fig. 3). There is an a b r u p t fall 5 years after the onset o f the m e n o p a u s e a n d a slower fall thereafter. I n the male group, the m e a n

S.A.E. rose f r o m a m e a n value o f 21.1 between 5 a n d 9 years to a value o f 35.5 between 30 a n d 3 4 years o f age (Fig. 4). Thereafter there was a g r a d u a l fall to a value o f 29.7 between the ages o f 70 a n d 74. There was n o a b r u p t fall in the S.A.E. o f the m a l e

26

CLINICAL

RADIOLOGY

group comparable with that seen in women between the ages of 50 and 54 years. The differences between the male and female subjects in the 5 year age groups have been tested for significance using the Student's 't' test, and the results are shown in Table 1. A third order polynomial has been fitted to the data, and the line of best fit and 95 ~ Confidence

limits are shown in Fig. 5. The values obtained from both the male and female subjects are superimposed so that they can be compared. The values of S.A.E. taken from the line of best fit show a rapid rise from just above 20 at the age of 5 years fgr both male and female subjects. The value for the female subjects rises and remains above the value for the males until the age of 49, when a much

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FIG. 5 Third order polynomial fit showing the mean and 95 ~ Confidence limits of the S tandardised Aluminium Equivalent (S.A.E.) plotted against age comparing normal male and female subjects.

TABLE 1 COMPARISON BETWEEN NORMAL MALE AND FEMALE SUBJECTS OF STANDARDISED ALUMINIUM EQUIVALENT ( S . A . E . ) AND DENSITY ()~,) OF THE THIRD METACARPAL. DIFFERENCES BETWEEN MEANS ARE CONSIDERED NOT TO BE SIGNIFICANT (N.S.) UNLESS P < 0"05

L

S.A.E. Age group

Mean Female subjects

Mean Male subjects

't'

5-9 10-14 15-19 20-24 25-29 30-34 35-39 40-44 45-49 50-54 55-59 60-64 65-69 70-74 75-79 80 +

20'9 27-9 33-3 34-1 36"5 35-4 35-7 35-1 34-7 32-9 29.2 28.5 26.3 24-3 23-5 21-8

21.2 22-3 31.9 32-7 33-9 35-5 34.6 32.1 33.8 33-7 31-5 29'9 31.0 29.7 30.8 25-8

0-15 1'73 0'73 0'92 1'87 0.07 0-60 1"99 0-61 0-58 1'82 1"48 4"21 4-58 3-30 1"14

N.S.

N.S. N.S. N.S. N.S. N.S. N.S. N.S. N.S. N.S. N.S. N.S. < '001 < '001 < "001 N.S.

Mean Female subjects

Mean Male subjects

't'

4.41 5-73 5-40 5.55 5-74 5-80 5-95 5-72 5-78 5-73 5-74 5-75 5-65 5-70 5-54 5.58

4,78 4-61 5.25 5.32 5-59 5"45 5'47 5"50 5'56 5'79 5'53 5'65 5"71 5-72 6'38 6-37

1-29 2-83 0-65 1'27 1-05 1'93 2.52 1"53 1"34 0-38 1-31 0-58 0-33 0.12 2.39 0.72 r

N.S.

N.S. N.S. N.S. N.S. N.S. N.S. N.S. N.S. N.S. N.S. N.S. N.S. N.S. <0'05 N.S.

CHANGES

IN

METACARPAL

MINERAL

27

CONTENT

29.21 at 75 years. The peak value of the S.A.E. for the male subjects is reached at 36 years. The densities of the cortices in the two groups has been analysed in terms of the mean and two standard error range. The density of the cortex

more rapid fall in values again takes them below that for the male subjects to a value of 23.29 at 75 years. The highest value for the female subjects is 36-34 which occurs at 34 years of age. The males show a comparatively less rapid fall to a value of NORMAL

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FiG. 6 Bone density (~,) changes with age in n o r m a l w o m e n .

M e a n a n d two s t a n d a r d e r r o r r a n g e in 5 year ago groups.

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AGE (years) FZG, 7 Bone density (~.) changes with age in n o r m a l males. M e a n and two s t a n d a r d e r r o r r a n g e in 5 year age groups.

90

28

CLINICAL RADIOLOGY

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FIG. 8 Third order polynomial fit showing the mean and 95 ~ Confidence [imits of the density (~,) plotted against age comparing normal male and female subjects.

rises from a mean value of 4.4 in the female subjects (Fig. 6) to a peak of 5"8 between the ages of 30 and 34. In the male subjects, the mean density starts at 4.8 between 5 and 9 years (Fig. 7), rises rapidly to a value of 5.6 between 25 and 29 years, and thereafter it appears to rise more slowly until the age range 70-74 years. The values for the male and female subjects have been tested for significant differences in these 5 year age groups and the values are shown in Table 1. None of the differences reach significance when tested by Student's 't' test except between 75 and 79 years. These values have again been fitted to a third order polynomial (Fig. 8). This shows that the female group have a density of 4.49 at 5 years rising rapidly to 5-8 at 25 years, and thereafter more slowly to a maximum value of 5.84 between 37

and 42 years, and finally declines to a value of 5.65 at the age of 75. The male group showed a rapid rise from 4.76 at 5 years to a value of 5,40 at 25 years, followed by a slow, but steady rise to 5.93 at the age of 75. Both the male and female subjects showed a further small rise in density after the age of 75, but the significance of this is questionable as the numbers are small. The value of L for the female subjects rises above the value for the male subjects at 13 years of age (;~-~ 5.13), and falls below the level for the male subjects at the age of 61 (L -- 5.68). The percentage of patients in each of the five social classes as defined in Appendix B of the Registrar General's Classification of Occupations is shown in Table 2. There is a preponderance of subjects in social class (3). Since it might be

TABLE 2 NUMBER OF SUBJECTS IN EACH SOCIAL CLASS AS DEFINED IN APPENDI~ B OF TH~ REGISTRAR GENERAL'S CLASSIFICATION OF OCCUPATIONS

Number

Percentage of total

Social class (1) Professional etc. (2) Senior Executive (3) Skilled (4) Semi-skilled (5) Unskilled Unclassified

Female

Male

Female

Male

12 39 139 72 28 27

20 48 140 68 22 14

3-8 12-3 43.8 22.7 8.8 8-4

6-4 15.4 44.9 21-8 7-1 4-5

CHANGES

IN

METACARPAL

expected that differences in social class might result in differences in nutrition, the S.A.E. of social classes 1 and 2 have been compared with those subjects in social classes 4 and 5 in ten year ago groups (Table 3). No significant difference was TABLE 3 COMPARISON OF S . A . E . IN MALE AND FEMALE SUBJECTS IN SOCIAL CLASSES I q- 2 AND 4 + 5 IN RELATION TO AGE

Age group I 20-29 30-39 40-49 50--59 60-69 70 +

Social class 1 +2 4+5 1 +2 4+5 1+2 4+5 1 +2 4+5 1+2 4+5 1+2 4+5

M e a n S.A.E. Female Male 35-57 34-85 32-39 35-74 36,94 33,87 33-57 30-54 26,63 28.57 24.48 24.36

32-68 34.27 34.11 36-29 32-37 31.72 3-023 33-84 33-99 29.67 28-72 29.05

P Female

M ale

N.S. N.S.

N.S.

N.S.

N.S.

N.S.

N.S.

N.S.

< '01

N.S.

N.S.

found except in the group of male subjects between 60 and 69 years. In this group, the S.A.E. was significantly lower in subjects in social classes 4 and 5. The external diameter of the 3rd metacarpal has been measured in both the male and female subjects and a third order polynomial fitted to the measurements from each group. F r o m the polynomial fit, the external diameter was found to rise until 30 years of age in both groups. Between the ages of 30 and 70, the external diameter was constant. This steady value was 8-0 mm. for the female and 9.0 ram. for the male subjects. DISCUSSION The definition of disease is only possible if the limits of normality have first been defined. However, there are many definitions of normal, and where changes occur over many years in the general population and in patients with disease it is inevitable that the 'normal' will merge gradually into the a b n o r m a l In this paper we have defined as normal a group of male and female subjects who were approached while visiting patients in the wards of the Western Infirmary, Glasgow. The scope of the survey was explained to them, and they were asked if they would volunteer to have a medical questionnaire completed, and an X-ray taken of their hand. The method of selection of subjects is thus similar to that used by Nordin et al. (1966).

MINERAL

CONTENT

29

The distribution of the subjects within the social classes is similar to that found by Nordin et al. (1966), a slightly higher incidence of subjects appearing under social class 3 (skilled workers) than might be expected to occur from the population in general (Table 2). Since differences in nutrition might possibly affect the bone mineral measurements, this was tested for in the different social classes. A significant difference was found in only one group of male subjects between 60 and 69 years, and it seems unlikely on this evidence that there is any real difference in metacarpal mineral content between the different social classes. One of the difficulties encountered in attempting to compare the results of other authors is the precise understanding of what is measured by the technique used. We have used two measurements to determine the amount of mineral in bone. The first is the Standardised Aluminium Equivalent (S.A.E.). This is a measure of the amount of mineral in the path of the X-ray beam divided by the external diameter of the metacarpal. Dividing by the external diameter allows for differences in size so that the mineral content can be compared between individuals within one age group. It also makes it possible to compare the metacarpal mineral content between male and female subjects and between different age groups. The density (~.) is a measure of the mineral per unit volume of cortical bone. Both )~ and S.A.E. are, of course, found from the equivalent absorption of the X-rays in our standard aluminium step-wedge. There is a rapid rise in the mineral content (S.A.E.) in both the male and female subjects over the first 20 years, reaching a peak at the age of 36 years in the male and 34 years in the female subjects. Thereafter there is a steady decline in the S.A.E. in the male subjects up to 75 years. The female subjects show a similar slow decline up to the age of 50 when a more rapid decline in mineral content occurs. The S.A.E. in the female subjects remains above the value for males until the age of 49. It is interesting to note the results of Takahashi and Frost (1966) who measured the cortical and total areas in section of rib in normal male and female subjects. These specimens were obtained either during thoracotomy or at autopsy in cases of sudden death. The cortical and total areas were greatest in the male subjects throughout the age range from infancy to over 70 years of age. The ratios of the cortical area to the total area, however, showed a higher value in the female subjects except below 5 and over 70 years of age. A fall in the cortical width with age has, of course, been previously reported by a number of authors.

30

CLINICAL RADIOLOGY

Meema and Meema (1963) reported a fall in the width of the humeral cortex in both male and female subjects, the fall starting earlier and occurring more rapidly in the female subjects. Similar results were obtained by Fujita et al. (1966). Nordin et al. (1966) showed a fall in the metacarpal index, femoral index and the Relative Vertebral Density (R.V.D.) with age. They also showed that an abrupt change in the R.V.D. occurred in women 5 years after the onset of the menopause. The fall in the metacarpal index occurred 10 years after the onset of the menopause. We have found a similar change in the metacarpal mineral content in association with the menopause. The change in S.A.E. was found to occur 5 years after the menopause, that is five years earlier than in the metacarpal index but at the same time as in the R.V.D. Morgan et al. (1967) report changes in the metacarpal cortical width with age in men and women. They preferred this measurement as they were unable to demonstrate a relation between the marrow cavity and the total diameter. They showed changes in cortical width similar to those reported by other workers. They also employed a densitometry technique, but found it did not give any better results than the simple cortical width measurement. However, the technique used has two sources of error which may lead to a loss of precision. Firstly, no allowance was made for the 'heel' effect, and secondly, scatter from the water bath and the bone may not have been constant over the length of the aluminium step-wedge. This would almost certainly lead to unpredictable variation in density in the step-wedge. We have found a much greater reproducibility in our densitometric technique than in the simple measurement of cortical width (Anderson et al. 1966). Morgan et al. (1967) made an estimate of the calcium content of the metacarpal with age from X-ray density measurements. It is interesting to note that they also found no statistical difference between men and women, their results closely resembling our own. They found a continuing rise in density with age in the male subjects with the exception of those between 60 and 70 years of age. The female subjects showed a rise up to the fifth decade, then started to fall. The density measurements of the female subjects are persistently higher than those of the male subjects. A rise in bone mineral density up to the age of 20 would be expected. Young subjects have a higher proportion of young bone with a higher water and lower mineral content than mature bone. Dollerup (1964) measured the mineral content in samples taken from the iliac crest at post-mortem

examination. He showed a rapid rise in rnil content up to 20-30 years of age. There w sharp peak at 40 years of age, but if this is ign there is a slow but steady rise with age in pat: up to and over 90 years. The density of bone tissue will be affected by the porosity, and degree of mineralisation of the bone. Jox (1963a) reported an increased intracortical port in the femur which would tend to cause a fa density. However, Epker et al. (1965) found little change in the porosity of the human rib, age. Furthermor6, Jowsey (1963b) reported increasing incidence of plugged and filled lacL with age. The plugged lacunae were hypermin~ ised when compared with the surrounding b~ the density being 1.63 gm./cc, in contrast to 1-44 gm./cc, in normal bone as shown by Rowl et al. (1958) using a quantitative microradiogral technique. This suggests the mechanism by wt the density could increase with age, but i~ obviously necessary for further post-mortem stu. to be carried out to assess changes in min, content and porosity changes with age in metacarpal. Smith and Rizak (1966) reported a rise in total width of the femur, but did not find significant increase in the external diameter of metacarpal between the ages of 45 and 75 ye Morgan et al. (1967) also reported that there was change in total width of the metacarpal with However, Garn et al. (1967) demonstrated significant increase in the external diameter of metacarpal in both male and female subje They studied two North American and three So American groups of subjects. In the combi groups they found an increase of 4 ~ in the felt and 3-2~ in the male subjects in the extel metacarpal diameter in six decades from the ag~ 25 years. In the present series we found no sigt cant increase in the total metacarpal diameter in male and female subjects between the ages of and 70 years. SUMMARY Using the X-ray technique previously descril by us (Anderson et al. 1966), we have reported results obtained in 312 male and 317 fern volunteers. Two values were derived from third metacarpal. Firstly, the Standardi Aluminium Equivalent (S.A.E.), which measu the amount of mineral in the path of the Xbeam divided by the external diameter of the b~ to allow for variations in size of individu~ Secondly, the density (~,), which is the amount mineral per unit volume of bone tissue in the cort

CHANGES IN METACARPAL MINERAL CONTENT The S.A.E. rises rapidly with age in b o t h the male and female subjects to a peak at the age of 36 in the males a n d 34 years in the females. Thereafter a fall occurs in b o t h groups, which is more marked in the female subjects after the age of 53, the greatest fall occurring within 5 years of the menopause. The S,A.E. in the female subjects is slightly though n o t significantly higher t h a n that of the males u p to the age of 49 years. The density (~,) rises rapidly in b o t h groups up to about 25 years of age. Thereafter a slow b u t steady rise occurs in the male subjects up to the age of 75. I n the female group, 3, continues to rise up to the age of 40 a n d gradually declines thereafter. The density of the b o n e of the female subjects is slightly b u t n o t significantly higher t h a n that of the males between the ages of 13 a n d 62 years. The external diameter of the third metacarpal increases rapidly in b o t h groups between 5 a n d 20 years, but there was n o significant change thereafter.

3I

BARNETT,E. and NORDIN,B. E. C. (1960). Clin. RadioL,

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NOTICE THE APPLICATION OF COMPUTERS IN RADIOLOGY Brussels 18-20 September, 1969 THIs Meeting will be organised on behalf of the European Association of Radiology by the Royal Belgian Society of Radiology. It will study the use of computers in all fields of radiology (diagnostic, therapeutic, nuclear medicine, etc,) including the wider aspects of medical history and bibliography relating to radiology. The Meeting should be of interest therefore to all those concerned in all radiological disciplines using computers, or considering their advantages. Simultaneous translation will be provided in English, French and German and those wishing to participate by presenting papers to the Meeting should send titles with approximately 200 word abstracts, preferably with a French translation, to Colloque de Radiologie, 64 chaussre de Haecht, Brussels 3, Belgium, as soon as possible and indicating the size of slides.