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The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 59:M249-M254 (2004)
© 2004 The Gerontological Society of America

Hemoglobin Levels and Skeletal Muscle: Results From the InCHIANTI Study

Matteo Cesari1,2,, Brenda W. J. H. Penninx1, Fulvio Lauretani3, Cosimo R. Russo3, Christy Carter1, Stefania Bandinelli3, Hal Atkinson1, Graziano Onder2, Marco Pahor1 and Luigi Ferrucci4

1 Sticht Center on Aging, Wake Forest University School of Medicine, Winston-Salem, North Carolina.
2 Department of Geriatrics, Catholic University of Sacred Heart, Rome, Italy.
3 Laboratory of Clinical Epidemiology, Italian National Research Council on Aging Geriatric Department, Florence, Italy.
4 Longitudinal Studies Section, Clinical Research Branch, National Institute on Aging, Baltimore, Maryland.

Address correspondence to Matteo Cesari, MD, Sticht Center on Aging, Wake Forest Health Sciences, 1 Medical Center Boulevard, Winston Salem NC 27157. E-mail: mcesari{at}wfubmc.edu


   Abstract
Top
 Abstract
Methods
 Results
 Discussion
 References
 
Background. Anemia is associated with reduced physical performance and muscle strength. The aim of the study was to explore whether anemia and hemoglobin levels are associated with differences in quantitative and qualitative measures of muscle and fat.

Methods. The study sample consisted of 909 participants 65 years and older enrolled in the "Invecchiare in Chianti" (InCHIANTI) study, a prospective population-based study of older people aimed at identifying risk factors for late-life disability. All the analyses were performed considering continuous hemoglobin levels as well as the dichotomous anemia variable (defined according to World Health Organization criteria as hemoglobin <12 g/dL in women and <13 g/dL in men). A peripheral quantitative computed tomography (pQCT) scan was performed in all participants to evaluate total, muscular, and fat cross-sectional areas of the calf and relative muscle density. Ankle extension strength was measured using a hand-held dynamometer. Linear regression analyses were used to assess the multivariate relationship of pQCT and skeletal muscle strength measures with hemoglobin levels and anemia after adjustment for demographics, chronic conditions, medication use, and other biological variables.

Results. Participants were aged 74.8 ± 6.8 years. In our sample, 94 participants (10.3%) were anemic. Hemoglobin levels were significantly associated with muscle density (ß = 0.225 [SE, standard error 0.098], p =.02), muscle area/total area ratio (ß = 0.778 [SE 0.262], p =.003), fat area/total area ratio (ß = -0.869 [SE 0.225]; p <.001). Skeletal muscle strength and muscle density were highly associated with anemia (ß = -3.266 [SE 1.173], p =.005 and ß = -0.816 [SE 0.374], p =.03, respectively). Results did not change when analyses were rerun in a restricted sample of participants not affected by major medical conditions.

Conclusion. The present study shows that hemoglobin levels are associated with the parameters of body composition obtained by pQCT, and that decreases in muscular strength measures occur in the presence of anemia.

ANEMIA is one of the major clinical problems in older persons, affecting approximately 12% of persons aged 60 years and older (1). It has been defined by the World Health Organization (WHO) as a hemoglobin level lower than 12 g/dl for women and 13 g/dl for men (2). Anemia has been associated with mortality (3), disability (4,5), decline in physical performance (6), and poorer quality of life in elderly people (7). Moreover, anemia is often found in frail older persons, and it has been suggested that anemia is a typical feature of the frailty syndrome.

The aging process has been associated with a decrease in hemoglobin concentrations for several reasons, such as a lower erythropoietin secretion (8) and a reduced hematopoietic reserve (9). It has also been demonstrated that anemia is strongly related to diseases, and hemoglobin levels below normal ranges should always be investigated in clinical practice (3).

Several papers have documented the negative effects that chronic hypoxia in association with anemia exerts on homeostasis, resulting in pathophysiological modifications that could worsen health status (10–12). In fact, it has been demonstrated that lower hemoglobin levels have been associated with structural and functional changes in capillarity (13) and muscular fibers (14), as well as fatigue (15) and physical performance (5,6), and muscle strength (6) impairment. However, to our knowledge, no one has explored whether lower hemoglobin levels and anemia are associated with muscle and fat mass and strength differences in elderly people.

We hypothesized that anemia and hemoglobin levels would be associated with muscle mass, fat mass, and skeletal muscle strength, which would provide a more in-depth explanation for the higher prevalence of disability observed in anemic individuals (4,5,16). This study, using a large sample of community-dwelling older persons, explores muscle and fat mass measures (assessed by calf peripheral quantitative computed tomography [pQCT]) and ankle extension strength measures in their association with hemoglobin levels and anemia.


   METHODS
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 Abstract
 Methods
Results
 Discussion
 References
 
The present study is based on data from the "Invecchiare in Chianti" (Aging in the Chianti area, InCHIANTI) study, a prospective population-based study of older people, designed by the Laboratory of Clinical Epidemiology of the Italian National Research Council on Aging (INRCA), Florence, Italy. The InCHIANTI study is aimed at identifying risk factors for the onset of disability in elderly people, studying physiologic subsystems critical for walking, and defining critical ranges for tests evaluating the integrity of the physiologic subsystems important for walking.

The study population for these analyses included 1156 participants aged between 65 and 102 years, randomly selected from residents in two towns of the Chianti geographic area (Greve in Chianti and Bagno a Ripoli, Tuscany, Italy). The data collection started in September 1998 and was completed in March 2000. A detailed description of the sampling procedure and data collection method has been previously published (17). The INRCA Ethical Committee approved the entire study protocol.

The present analyses were performed on 909 participants. We excluded participants in whom hemoglobin levels, pQCT measures, and ankle extension strength were not assessed (n = 247). The only sociodemographic characteristic in which excluded participants differed from those considered for the present analyses was older age (80.3 years vs 74.8 years, p <.001).

Anemia
Blood samples were obtained from participants after a 12-hour fast, and after the participant had been sedentary in a sitting or supine position for at least 15 minutes. Hemoglobin levels were analyzed using the hematology autoanalyzer Dasit SE 9000 (Sysmex Corp., Kobe, Japan). For the present study we used 1) a continuous hemoglobin level variable and 2) a dichotomous anemia indicator, defined as the gender-specific definition used by the WHO (2): hemoglobin levels lower than 12 g/dL for women and 13 g/dL for men.

pQCT Measures
A right leg pQCT scan was performed in all participants by a recent generation device (XCT 2000; Stratec, Pforzheim, Germany) to evaluate the total, muscular, and fat cross-sectional areas of the calf. Data presented here was derived from standard 2.5 mm thick transverse scans obtained at 66% of the tibial length starting from the tibiotarsal joint. Previous studies demonstrated that this is the region with the largest outer calf diameter, with a small variability across individuals (18). The muscle density (in mg/cm3), the muscle area (in cm2), the fat area (in cm2), and the total area (in cm2) were calculated using the BonAlyse software version 3.1 (BonAlyse, Ltd., Jyväskylä, Finland). Different tissues in the analyses were separated according to different density thresholds, using the "soft tissue" algorithm: a density value of 15 mg/mm3 was used to separate fat from muscle tissue, and 180 mg/mm3 to separate muscle from bone tissue. For the present study, we considered the muscular density and ratios (expressed as percentages) of the muscle area and fat area to total calf area as outcomes.

Ankle Extension Strength
Ankle extension strength was measured with a hand-held dynamometer (Nicholas Muscle Tester, Sammon Preston, Inc., Chicago, IL). Participants, lying in lateral decubitus (opposite to the examined limb) with the hip and the knee extended and the ankle in neutral position, were asked to perform the task twice with the right foot. The average of the results obtained was used for the present analyses. This measure has been used as a muscular strength parameter of the lower limb (19). In our sample, this measure is highly correlated with other performance measures, such as hand-grip strength or knee extension strength (Spearman's correlation r =.647 and r =.790, respectively; both p <.001), which have been shown to predict mortality and subsequent disability in elderly people (20,21).

Covariates
Covariates included sociodemographic variables (age, gender, study site, smoking habit, Mini Mental State Examination [MMSE] score, education), body mass index (BMI; computed as weight in kg/height in meter squared), comorbidity (adjudicated diagnoses of hypertension, angina, myocardial infarction, stroke, cancer, diabetes, congestive heart failure, chronic obstructive pulmonary disease), physical activity (defined as moderate-to-high intensity exercise performed for at least 1–2 hours per week or light intensity exercise performed for more than 4 hours per week), as well as biological parameters (albumin, creatinine, total cholesterol, HDL [high-density lipoprotein] cholesterol, and triglycerides). Adjudicated disease diagnoses were based on self-reported history, clinical documentation, and medication use. Serum lipids were measured from fresh samples drawn after an overnight fast. Commercial enzymatic tests (Roche Diagnostics, Mannheim, Germany) were used for determining serum total and HDL cholesterol concentrations. The interassay coefficient of variation was less than 3.8% for total cholesterol and less than 5.0% for HDL cholesterol. Serum creatinine was detected by a standard creatinine Jaffe' method (Roche Diagnostics); interassay coefficient was less than 2.5%. Serum albumin (%) was detected by electrophoresis (mean interassay coefficient 0.8%) and its concentration was calculated from serum total proteins (interassay coefficient <1%).

Statistical Analyses
Plasma levels of triglycerides were not normally distributed; therefore analyses were performed using their log values. We tested the linearity of the association between hemoglobin levels with pQCT and strength measures assessing the unadjusted means of these latter according to hemoglobin quintiles (taking into account the gender differences).

Differences in proportions and means of covariates according to anemia status were assessed using chi-square and analysis of variance statistics, respectively. All variables found to be significantly different (p <.05) in univariate analyses were used as covariates to adjust subsequent multivariate analyses. Linear regression analyses were used to identify regression coefficients (with standard error) in calf pQCT and strength measures for continuous hemoglobin levels as well as for the dichotomous anemia variable.


   RESULTS
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 Abstract
 Methods
 Results
Discussion
 References
 
The mean age of participants in the present study was 74.8 ± 6.8 years. Participants were predominantly female (55.9%) and moderately overweight (BMI 27.4 ± 4.1 kg/m2). The hemoglobin levels distribution according to gender is reported in Figure 1. Mean hemoglobin levels were 14.4 g/dL (SD [standard deviation] 1.3) for men and 13.2 g/dL (SD 1.1) for women.



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  		Figure 1. Hemoglobin distribution for men and women in the study sample

 
In our sample, 94 participants (10.3%) had hemoglobin levels below the WHO anemia cutoff (Table 1). Anemic participants were older, with a higher prevalence of stroke and gastric ulcer, a larger use of medications, and increased serum creatinine levels. They also had lower BMI and education, as well as decreased levels of albumin, total cholesterol, and triglycerides. Muscle density and ankle extension strength were significantly lower in participants with anemia. No significant differences were found at the univariate analyses for muscle and fat area ratios.


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  		Table 1. Main Characteristics of the Population.

 
Linear regression analyses (adjusted for age, gender, site, BMI, education, stroke, gastric ulcer, albumin, creatinine, total cholesterol, triglyceride, number of medications) showed a significant association between hemoglobin levels and pQCT measures (muscle density: ß = 0.225 [SE 0.098], p =.02; muscle area/total area ratio: ß = 0.778 [SE 0.262], p =.003; fat area/total area ratio: ß = -0.869 [SE 0.225]; p <.001). No significant association was found for ankle extension strength and hemoglobin level.

Analyses were then rerun using the dichotomous anemia variable as an independent variable. Anemic participants compared with nonanemic participants presented a lower skeletal muscle strength (ß = -3.266 [SE 1.173], p =.005) and a lower muscle density (ß = -0.816 [SE 0.374], p =.03).

We also explored whether our findings were driven by the presence of diseases. We performed some restricted analyses from which we excluded persons with stroke, gastric ulcer, and evidence of renal failure (serum creatinine levels higher than 1.2 mg/dL). These analyses (57 anemic participants/762 participants) were consistent with previous findings, confirming the association between pQCT measures and hemoglobin levels (muscle density ß = 0.205 [SE 0.117], p = 0.08; muscle area/total area ß = 0.847 [SE 0.291], p =.004; fat area/total area ß = -1.105 [SE 0.264], p <.001), and between muscular strength and density with anemia (ß = -2.514 [SE 1.339], p =.06 and ß = -0.712 [SE 0.453] p =.11, respectively).

Finally, we graphically plotted the adjusted means of pQCT and strength measures in relation to hemoglobin groups (Figure 2). Higher levels of hemoglobin were associated with higher muscle density (participants with hemoglobin >2 g/dl above the cutoff vs anemic participants: 70.06 mg/cm3 vs 71.171 mg/cm3, p =.008; p for trend =.06), higher muscle area/total area ratio (participants with hemoglobin >2 g/dl above the cutoff vs anemic participants: 71.627% vs 69.466%, p =.05; p for trend =.02), lower fat area/total area ratio (participants with hemoglobin >2 g/dl above the cutoff vs anemic participants: 19.684 kg vs 22.276 kg, p =.007; p for trend =.001), and higher ankle extension strength (participants with hemoglobin >2 g/dl above the cut-off vs anemic participants: 28.032 kg vs 25.060 kg, p =.02; p for trend =.05).



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  		Figure 2. Adjusted* means of peripheral quantitative computed tomography and strength measures according to hemoglobin levels. *Adjusted for age, gender, site, body mass index, education, stroke, gastric ulcer, albumin, creatinine, total cholesterol, triglyceride (log value), and number of medications

 

   DISCUSSION
Top
 Abstract
 Methods
 Results
 Discussion
References
 
To our knowledge, this is the first study exploring the relationships between anemia and hemoglobin levels with muscle strength, quality, and quantity measures. Our study shows that lower hemoglobin levels are associated with lower ankle extension strength, lower muscle density, and less muscle mass. The lower muscle density found for lower levels of hemoglobin may be explained by the higher percentage of adipose tissue in the calf, responsible for intramuscular infiltrates of fat (22–25).

In the last decades, thoughts about anemia in elderly people have sensibly changed. The idea that the fall in hemoglobin that occurs with age represents a direct effect of senescence and may be a normal physiological response to aging (9) has been revised and attenuated. Izaks and colleagues (3) recently demonstrated that anemia in older persons is largely due to disease and not only to aging. Therefore, to avoid potential confounding diseases, we refined our analyses in a restricted sample without conditions clearly linked to anemia (stroke, gastric ulcer, and creatinine levels higher than 1.2 mg/dL). Our findings show that functional impairments and poorer health status related to lower hemoglobin levels and to anemia appear to be rather independent from disease status.

Several publications have suggested that anemia and hemoglobin levels might affect physical performance, and consequently quality of life, through various pathways generally involving decreased oxygenation of tissues (6,7,26,27). One of the most common symptoms of anemia is fatigue, an important burden to quality of life (15) and limitation to physical function (28). Some studies have demonstrated that lower levels of hemoglobin are able to influence oxygen delivery to skeletal muscle (29) and consequently negatively impact muscular strength (30). In fact, in chronic obstructive pulmonary disease and obstructive sleep apnea syndrome, structural, bioenergetic, and functional changes have been reported in skeletal muscle, possibly secondary to hypoxia (31,32). It has also been demonstrated that chronic hypoxia is responsible for several pathophysiological modifications (such as peripheral arterial vasodilatation, capillary angiogenesis, myocardial dysfunction, lower blood pressure, activation of the sympathetic and renin angiotensin aldosterone systems, and salt and water retention) that result in the onset or worsening of disabling diseases (10,33). Moreover, anemia has been associated with higher levels of inflammatory markers (34), which may negatively impact physical performance (35) and muscle mass (36,37).

A further explanation of our findings might be found in the influence that testosterone levels have on body composition and anemia. In fact, a direct relationship between serum testosterone levels and hematopoiesis has already been demonstrated (38,39). The use of androgenic steroids has been associated with an increase in hemoglobin concentration (39). Moreover, it has been shown that testosterone supplementation is associated with increased muscle mass and a decrease in body fat (40–42).

It could be argued that our findings might be the expression of the effect that physical activities play on the muscle mass and strength. In fact, it is very likely that participants with normal hemoglobin levels perform more daily physical activities and, therefore, retain higher muscle mass and strength. However, in our study, daily physical activity was not significantly different at the univariate analyses between anemic and nonanemic participants and, when this variable was added to the model as a potential confounder, it did not affect our results.

The cross-sectional design of our study cannot explain whether our findings are merely the expression of subclinical diseases, not yet diagnosed, impairing and modifying our outcome measures, or are indeed a causative factor in the pathway leading to frailty. Lower hemoglobin levels might enhance and accelerate age-related muscle and fat mass modifications leading to physical performance loss. In fact, changes in muscle and fat measures, which characterize our participants with lower hemoglobin levels, have already been indicated by Kyle and colleagues (43) as age-related modifications. Further longitudinal studies should explore this topic, evaluating whether hemoglobin levels and/or anemia are able to influence age-related muscle mass and strength modifications. Another limitation of our study is due to the small number of severely anemic participants in our sample, which did not allow us to explore more carefully what happens below the anemia cutoff.

Conclusion
Our study shows that hemoglobin levels are associated with muscle and fat mass changes, and that decreased muscular strength occurs in the presence of anemia. Further dedicated studies should investigate whether interventions aimed at correction of anemia prevent negative body composition and muscular strength changes.


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  		Table 2. Adjusted* Regression Coefficients (With SE) for the Association Between Hemoglobin Levels and Anemia With pQCT and Strength Measures.

 

   Acknowledgments
 
The InCHIANTI study was supported as a "targeted project" (ICS 110.1/RS97.71) by the Italian Ministry of Health (Rome, Italy) and in part by the U.S. National Institute on Aging (Contracts 263 MD 9164 13 and 263 MD 821336). Data analyses were supported by Bristol-Myers Squibb Company (Princeton, NJ) and by Ortho Biotech Products (Bridgewater, NJ).

The work of Dr. Cesari was supported by the Wake Forest University Claude D. Pepper Older Americans Independence Center (NIA grant P30-AG-021332-01).

Received August 19, 2003

Accepted August 22, 2003


   References
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 Abstract
 Methods
 Results
 Discussion
 References
 

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