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The Journal of Clinical Endocrinology & Metabolism Vol. 85, No. 12 4657-4662
Copyright © 2000 by The Endocrine Society

Original Studies

The Role of Insulin-Like Growth Factor I in Age-Related Changes in Calcium Homeostasis in Men1

D. Fatayerji, E. B. Mawer and R. Eastell

Bone Metabolism Group (D.F., R.E.), University of Sheffield, Sheffield S5 7AU; and Department of Medicine (E.B.M.), University of Manchester, M13 9PL Manchester, United Kingdom

Address correspondence and requests for reprints to: Prof. Richard Eastell, Bone Metabolism Group, Clinical Science Center, Northern General Hospital, Herries Road, Sheffield S5 7AU, United Kindgom. E-mail: r.eastell{at}sheffield.ac.uk


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
The aim of this study was to evaluate hormonal influences on age-related changes in calcium homeostasis in men.

We recruited 178 healthy men, ages 20–79 (about 30 per decade). We measured serum calcium, phosphate, urinary calcium, and creatinine clearance. Dietary calcium intake and use of fish oils were determined by questionnaire. Fractional calcium absorption was estimated using the stable strontium technique in a subgroup of 60 men. PTH, 1,25-dihydroxyvitamin D [1,25(OH)2D], 25-hydroxyvitamin D (25OHD), serum insulin-like growth factor I (IGF-I), and testosterone were measured in all men.

There was no change in serum calcium with age. There were decreases in serum phosphate, urinary calcium, and creatinine clearance with age (P < 0.02). Dietary calcium was unchanged. Strontium absorption decreased (P < 0.01), and PTH increased (P < 0.001) with age. The data for 1,25OH2D were biphasic, reaching a peak at age 55 yr (P = 0.003). There was a linear increase in 25OHD with age (P = 0.009) that persisted after correcting for seasonal variation and was positively associated with fish oil use, therefore, the age-related changes in 25OHD were masked by self medication. There were log-linear decreases in IGF-I and testosterone with age (P < 0.0001).

Strontium absorption was not related to 25OHD or 1,25(OH)2D, but was positively correlated with IGF-I. 1,25(OH)2D correlated negatively with serum phosphate and calcium, but not PTH or creatinine clearance. IGF-I was positively associated with creatinine clearance, serum calcium, and phosphate and negatively associated with PTH (P < 0.001).

In this cross-sectional study of otherwise healthy, normally aging men, age-related decreases in IGF-I seem to have a greater impact on mineral absorption than does vitamin D status.


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
IN WOMEN THERE is evidence that the ability to adapt to decreased dietary calcium intake is impaired with age, resulting in an increase in serum PTH levels. However, it remains unclear whether the impairment in calcium absorption is related to vitamin D deficiency.

Studies in women are complicated by the dominating influence of estrogen. By studying men, age-related changes in calcium homeostasis can be studied free from the hormonal changes that accompany the menopause.

In men, as in women, calcium absorption has been reported to decrease with age (1, 2, 3, 4), PTH has been reported to increase with age (5, 6, 7, 8, 9), insulin-like growth factor I (IGF-I) has been shown to decrease with age (10, 11, 12, 13), and plasma 25-hydroxyvitamin D (25OHD) has been reported to decrease with age (6, 14, 15, 16, 17, 18). The effect of age on 1,25-dihydroxyvitamin D [1,25(OH)2D] remains controversial in both sexes because some studies have reported a decrease with aging, especially after age 65 yr (1, 19), whereas others have reported unchanged or increased levels with aging (6, 20).

The gold standard for determining calcium absorption is the dual-tracer technique, in which separate calcium isotopes are given orally and iv. The strontium absorption test has been successfully validated against this the dual-tracer technique (21) and is more suitable for use in healthy volunteers since it does not involve radiation.

The aims of this study were to: 1) describe the changes in calcium homeostasis, calcitropic hormones, IGF-I, and testosterone with age in men; and 2) to relate the changes in hormones to those in calcium homeostasis in men.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Subjects

We studied 178 men, ages 20–79 yr (~30 per decade; mean, 49.9 yr), who were recruited from a general practitioner register. The study was approved by the North Sheffield Local Research Ethics Committee, and all subjects gave written informed consent.

The volunteers were healthy, ambulatory Caucasian men who lived in their own homes. They were not taking medication known to affect bone or calcium metabolism. Potential volunteers completed a questionnaire on health status and medication. Individuals treated with corticosteroids, diuretics, T4, chemotherapy, or with a history of epilepsy, diabetes, or stroke were excluded from the study. Spine radiographs of men over 50 yr enabled those with vertebral fractures to be excluded. The use of vitamin and mineral supplements was not an exclusion criterion.

Recruitment was carried out from June 1994 to April 1995, with an approximately even distribution of ages across the time period. All volunteers completed a lifestyle questionnaire, including use of nutritional supplements, and a dietary calcium food frequency questionnaire. Fasting blood and 24-h urine samples were obtained. The blood samples were collected between 0900 and 1000 h after an overnight fast. On a subset of 10 men per decade, calcium absorption was determined by the stable strontium method. All samples were stored at -80 C. Monthly hours of sunshine were obtained from the Weston Park Weather Station, Sheffield, for the study duration. The food frequency questionnaire was based on common foods eaten by British subjects. It was validated by comparison with 7-day weighed intake (dietary diary) within 30 subjects to which it correlated significantly (r = 0.68).

PTH was determined by immunoradiometric assay (Allegro, Nichols Institute Diagnostics, San Juan Capistrano, CA; intra-assay variation 9.7%, and interassay variation 15.3%, at 28 pg/ml).

1,25(OH)2D and 25OHD were determined by standard methods in the Department of Medicine (Manchester Royal Infirmary, Manchester, UK). Metabolites were separated by automated high-performance liquid chromatography (Waters Associates, Watford, UK) (22). 25OHD was quantified by competitive protein-binding assay (23) using normal human serum as the source of vitamin D-binding protein at a dilution of 1:20,000. A level of less than 12 ng/mL was taken as indicating vitamin D insufficiency (24). 1,25(OH)2D was measured by RIA using monoclonal antibody 5F2 (25).

IGF-I was measured by RIA after acid-ethanol extraction at the Department of Clinical Chemistry (Royal Hallamshire Hospital, Sheffield, UK) (Medgenex, Fleuraus, Belgium; intra-assay variation 7%, and interassay variation 5.6%, at 170 µg/L).

Total testosterone was determined by RIA (Coat-A-Count; DPL Division, EURO/DPC Ltd., Gwynedd, UK; with an intra-assay variation of 4.6% and an interassay variation of 5.6%).

Fractional strontium absorption was measured using strontium as the tracer with a breakfast containing 7.8 mmol calcium (21). A subgroup of 60 men (10 per decade) was provided with a test meal (100 mL milk with 35 g cornflakes and 10 g sugar; 10 mL lemon barley water with 100 mL water) that was consumed within 10 min. Immediately after the meal, strontium chloride (2.5 mmol) was administered in 30 mL milk and 20 mL water. The glass containing the drink was rinsed with a further 20 mL milk and 10 mL water. Serum samples were obtained exactly 3 h after the strontium was administered.

Serum strontium was measured in duplicate by electrothermal atomic absorption spectrophotometry (Pye Unicam PU 9400; at 460.7nm) at the Department of Chemical Pathology (St Thomas Hospital, London, UK) (intra-assay variation, 5%; interassay variation, 8%). The percentage of calcium absorbed was calculated from the administered dose (AD; 2.5 nmol or 219 mg), and extracellular fluid (ECF) volume was estimated as 15% of body weight:

where AD is the administered dose.

Urinary creatinine was determined by the Jaffe method, and urine calcium was determined by colorimetric assay. Measurements were performed by the Clinical Chemistry Department (Royal Hallamshire Hospital).

Serum creatinine, calcium, and phosphate were measured by standard colorimetric dry chemistry assay (Ecktachem 950; Johnson & Johnson, Rochester, NY) at the Clinical Chemistry Department (Northern General Hospital, Sheffield, UK).

Analysis

The relationship between variables relating to calcium homeostasis and age was evaluated by linear and multiple linear regression analysis (age, height, and weight). Regression with polynomial models (quadratic and cubic) was performed to examine for possible nonlinear relationships between the markers and age. Regression with sine curves were performed with a frequency of 1 yr to detect seasonal variation and Z-scores calculated from the regression equation to correct for season. The level of significance was taken as P < 0.05.

Statistical analyses were performed using Statgraphics for Windows version 1.4 (Manugistics, Rockville, MD) and GraphPad Prism (Intuitive Softwear for Science, San Diego, CA).


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
There was no change in serum calcium with age (Fig. 1Go and Table 1Go). There were decreases in serum phosphate (40%) and urinary calcium (30%), and the data for phosphate were best fitted by a quadratic, with a nadir at age 68 and 47 yr, respectively (Fig. 1Go). There was a linear decrease in creatinine clearance with age (40%; Fig. 1Go). There was no change in dietary calcium intake with age (mean, 990 mg/day; range, 358-2185 mg/day).



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  		Figure 1. Relationship between indices of calcium homeostasis and age. The data for PTH and AD of strontium in extracellular fluid were log transformed. There was a decrease in the percentage of the AD of strontium in extracellular fluid and creatinine clearance with age (r2 = 0.14, 0.41, and 0.23; P < 0.01). There was no change in serum calcium with age. The data for urine calcium and serum phosphate were best fit by a quadratic (r2 = 0.12 and 0.08, P < 0.002, respectively).

 

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  		Table 1. The median and range for PTH, IGF-I, testosterone, and absorbed does of strontium per 10-yr age group1

 
There was a weak seasonal variation for strontium absorption, but not for PTH. There was a log-linear decrease with age in fractional strontium absorption (32%; Fig. 1Go) and a log-linear increase in PTH (43% between ages 20 and 79; Fig. 2Go) with age.



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  		Figure 2. Relationship between age and calcitropic hormones. There was an increase in 25OHD with age, and the graph indicates vitamin D insufficiency (<12 ng/mL; dashed line). Split point analysis described the relationship between serum 1,25(OH)2D and age (r2 = 0.06, P = 0.003). For age less than 55 yr 1,25(OH)2D = 48.23 + 0.39 (age 55). For age more than 55 yr 1,25(OH)2D = 48.23 + (0.39 - 0.82)*(age 55). There was an increase in PTH with age (r2 = 0.09, P = 0.0001). Data for IGF-I were log transformed. There was a decrease in IGF-I with age, and the data were best fit by a quadratic (r2 = 0.41, P < 0.0001). There was a log-linear decrease in testosterone with age (r2 = 0.89, P = 0.0001).

 
There was a weak seasonal variation for 1,25(OH)2D (nadir in June). There was no overall change in 1,25(OH)2D with age. However, when we fit the model proposed by Epstein et al. (7), split point analysis was significant: there was a 40% increase between ages 20 and 55 yr, followed by a 22% decrease by age 80 yr (Fig. 2Go). The trends were similar after correcting for season (r2 = 0.07, P = 0.003). Use of cod liver oil was more common in the elderly (14% for men in their 3rd, 4th, or 5th decade compared with over 30% in men in their 6th, 7th, or 8th decade), and 1,25(OH)2D were 17% higher in fish oil users (P < 0.008).

There was a marked seasonal variation 25OHD (nadir in March). Vitamin D insufficiency was present in 11% of men (25OHD, <12 ng/mL) and was more common in young than in old men. There was a linear increase in 25OHD with age (35% between ages 20 and 79; Fig. 2Go), which persisted after correcting for season (r2 = 0.05, P = 0.003). 25OHD levels were 31% higher in fish oil users (P < 0.008).

IGF-I decreased with age (54%), and the data were best fit by a quadratic relationship after log-transformation, with the nadir at age 76 yr (Fig. 2Go and Table 1Go). There was a log-linear decrease in total testosterone (26%) with age (Fig. 2Go and Table 1Go).

IGF-I correlated positively with fractional strontium absorption, creatinine clearance, urinary calcium, serum calcium, and phosphate and negatively with PTH (Table 2Go). However, only the relationships between IGF-I and creatinine clearance, serum calcium, and phosphate were significant when all these factors were entered into a multiple linear regression model (P < 0.0001, P = 0.0001, and P = 0.005, respectively).


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  		Table 2. Correlations for IGF-I and vitamin D metabolites with calcitropic hormones and indices of calcium homeostasis

 
25OHD was related only to PTH. 1,25(OH)2D was negatively correlated with serum calcium and phosphate but was not related to other determinants of calcium homeostasis. Neither 25OHD, 1,25(OH)2D, nor IGF-I were related to serum testosterone.


   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
The most interesting findings were that: 1) strontium absorption was not related to serum levels of vitamin D metabolites; and 2) strontium absorption was related to serum IGF-I.

In women, impaired calcium absorption with age has been attributed to: 1) a decrease in renal function, leading to a decrease in 1,25(OH)2D synthesis; 2) intestinal vitamin D resistance (11); 3) an increase in vitamin D-binding protein, resulting in a reduction in free 1,25(OH)2D index (26), although an increase in vitamin D binding protein with age is not a universal finding (27); and 4) a decrease in GH (12, 13) and IGF-I (28, 29, 30) with age.

Strontium absorption was not correlated with 25OHD or 1,25(OH)2D, therefore, changes in vitamin D with age cannot explain the change in strontium absorption. The correlation between strontium absorption and serum IGF-I supports a role for IGF-I in strontium absorption. This study cannot address the effect of changes in vitamin D binding protein with age.

A role for GH in calcium absorption has been proposed, and these effects may be mediated by IGF-I (28, 29, 30). GH has been proposed as an important determinant of both passive and active calcium absorption by maintaining structural integrity of the mucosa (12) and may further influence active, vitamin D-dependent transport by maintaining intestinal sensitivity to 1,25(OH)2D (12) and increasing synthesis of calcium binding protein (29). GH may also have an indirect role on calcium absorption via its action at the kidney where it increases 1,25(OH)2D synthesis and phosphate reabsorption (29). The positive correlations between IGF-I and both strontium absorption and serum phosphate in this study suggests that the action of IGF-I on the intestine and kidney may be important in determining strontium absorption; thus, the decrease in IGF-I with age may be responsible for the observed decrease in strontium absorption. This could be examined by observing the response of strontium absorption to IGF-I administration.

Decreased calcium absorption would tend toward a decrease in serum calcium, resulting in a compensatory increase in PTH; thus, the positive correlation between IGF-I and serum calcium and the negative correlation between IGF-I and PTH further supports a role for IGF-I in calcium absorption. In the kidney, PTH decreases urine calcium excretion, increases phosphate excretion, and increases 1,25(OH)2D production. The decrease in urine calcium and serum phosphate with age, the increase in 1,25(OH)2D with age, and the negative correlation between PTH and urine calcium supports its role in calcium conservation by the kidney. In bone, PTH increases net bone resorption to maintain serum calcium levels (Fig. 3Go).



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  		Figure 3. Proposed mechanism for changes in calcium homeostasis in men with aging. +, stimulation of 1,25(OH)2D synthesis.

 
Synthesis of 1,25(OH)2D is stimulated by PTH, by decreased serum phosphate, and by decreased serum calcium. The increase in 1,25(OH)2D with age, despite the decrease in IGF-I, is probably part of the calcium homeostatic response to compensate for the decreasing calcium absorption, and is driven by the rising PTH level. The observed negative correlation between 1,25(OH)2D and both serum calcium and phosphate supports this hypothesis. The small decrease in 1,25(OH)2D after age 55 may be related to impaired renal function, which is suggested by decreased creatinine clearance and phosphate excretion in the elderly.

The correlations between IGF-I and indices of calcium homeostasis are intriguing, but only the relationship with serum calcium and phosphate remained valid after adjusting for age. IGF-I stimulation studies in the elderly are necessary to determine the exact relationship between IGF-I and calcium homeostasis.

In this cross-sectional study of otherwise healthy, normally aging men, age-related decreases in IGF-I seem to have a greater impact on mineral absorption than does vitamin D status.


   Acknowledgments
 
We thank Prof. R. Swaminathan and the Department of Chemical Pathology (St. Thomas’ Hospital, London, UK) for serum strontium measurements.


   Footnotes
 
1 Funded by an Arthritis and Rheumatism Council Program Grant. This work was presented in part at the meeting of the Bone and Tooth Society in Oxford, United Kingdom, March 30 and 31, 1998. Back

Received December 2, 1999.

Revised August 2, 2000.

Accepted August 25, 2000.


   References
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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