lo
urna f Ger
Jo
Researc
h
tric
ia
gy & G
er
tolo
on
ISSN: 2167-7182
Journal of
Gerontology & Geriatric Research
Piccirilli, et al., J Gerontol Geriatr Res 2014, 3:5
DOI: 0.4172/2167-7182.1000183
Research Article
Open Access
Can Muscular Impairment be the “Key” for Femoral Fracture?
Piccirilli E, Gasbarra E, Baldi J, Pistillo P and Tarantino U*
Department of Orthopaedics and Traumatology, PTV Foundation, “Tor Vergata” University of Rome, Rome, Italy
*Corresponding
author: Umberto Tarantino, Department of Orthopaedics and Traumatology, “Tor Vergata” University of Rome, Italy, Tel: +390620903465; E-mail:
umberto.tarantino@uniroma2.it
Rec date: Jul 25, 2014; Acc date: Oct 29, 2014; Pub date: Oct 31, 2014
Copyright: © 2014 Piccirilli E, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted
use, distribution, and reproduction in any medium, provided the original author and source are credited.
Abstract
Background: Osteoporosis and osteoarthritis are the most common diseases of musculoskeletal system.
Osteoporosis is characterized by low bone mass and microarchitetural deterioration of bone tissue. This disease is
associated with sarcopenia and muscular impairment, while osteoarthritis seems to be independent of muscle
quality.
In the elderly, sarcopenia is characterized by an histological deterioration and by an important functional
impairment. The aim of the present work is to show how bone weakening is associated with muscle aging in terms of
fiber atrophy and physical activity reduction, producing disability and risk of fall and fractures.
Methods: A functional evaluation of muscular performance status in twenty osteoporotic women with a femoral
fracture and in twenty osteoarthritic women with a Total Hip Arthroplasty (THA) in progress was realized through the
PASE test (Physical Activity Scale for the Elderly). DeXa was performed and the T-score values were considered to
classify osteoporotic and osteoarthritic patients. As a part of a multiparametric model of evaluation, biopsies of
vastus lateralis muscle were analyzed to find a correlation with functional index.
Results: In osteoporotic patients, the PASE test showed a low or moderate level of physical activity before
occurring the fracture while osteoarthritic patients had more intensive physical performances. Hystological analysis
showed that osteoporosis is characterized by a type II fiber prevalent atrophy and data correlation showed that lower
scores of PASE test are associated with a lower type II fiber diameter. No correlation was found between BMD
values and PASE test.
Conclusion: We demonstrated that osteoporosis is closely related to sarcopenia. Infact, bone remodeling is
related to both muscle morphological and functional impairment and sarcopenia is considered one of the major
responsible factors for functional limitations and motor dependency in elderly osteoporotic persons. According to our
study, physical activity should be strongly recommended in osteoporotic patients at diagnosis.
Keywords: Sarcopenia; Osteoporosis; Physical activity
Introduction
Osteoporosis (OP) is a chronic progressive disease which causes a
reduction in bone mineral density and in Bone Quality with a resulting
imbalance in the regulation of the hormonal, cellular and metabolic
system that normally governs the skeletal tissue [1-4].
This gap can lead to an increase in osteoclastic activity to the
detriment of the appositive action of osteoblasts (postmenopausal
osteoporosis) or to a normal osteoclasts activity together with reduced
bone formation by osteoblastic cells (senile osteoporosis).
Instead, the main actor in the process of osteoarthritis’s (OA)
physiopathology is the cartilage. In fact, the arthritic articular cartilage
is characterized by an imbalance between matrix synthesis and
degradation. When the cartilage is damaged, it is replaced by a mixture
of immature and disarranged collagen fibers. The subchondral bone
loses its coating and is directly subjected to abnormal stress which can
lead to microfractures [5] and formation of reparative sclerotic bone
with a widely disorganized trabecular pattern.
J Gerontol Geriatr Res
ISSN:2167-7182 JGGR, an open access journal
The systemic tissutal “aging” is a multifactorial process related to a
natural decline of physiological functions, including the decrease in
bone mineral density (BMD) [6], of muscle mass and muscle strength
[7]. Sarcopenia is due to an important imbalance between synthesis
and deterioration of muscle proteins and cells, with a resulting poor
muscular quality. This depletion strongly influence bone trophism and
affects mobility and skeletal features during OP and OA.
During the last 40 years, investigators have collected considerable
information demonstrating that altered loading states play a crucial
role in modulating muscle fiber size as well as the contractile and
metabolic phenotypes with a consequent reduction of the
biomechanical stimulation on bone [8]. In particular, we know that in
osteoporotic patients there is a preferential loss of type II muscle fibers
(fast ones) [9]: this progressive loss of motor units leads to a rapid
progressive decline of muscle power needed to perform even the
simplest daily activities like rising from a chair, climbing the stairs or
recovering the right position after an imbalance. This results in a
reduction of bone stimulation and in an increased risk of fragility
femoral fractures [10].
Volume 3 • Issue 5 • 183
Citation:
Piccirilli E, Gasbarra E, Baldi J, Pistillo P and Tarantino U (2014) Can Muscular Impairment be the “Key” for Femoral Fracture?. J
Gerontol Geriatr Res 3: 1000183. doi:10.4172/2167-7182.1000183
Page 2 of 5
Muscle changes produced by the aging process can also partly
encourage the development of osteoarthritis as they make the joints
more susceptible to the effects of other risk factors including abnormal
biomechanical stimulation, trauma, genetic alterations and
comorbilities [11,12]. The differences in osteoporotic patients’
sarcopenia compared to arthritic one are highlighted at a microscopic
level, in rate and type of muscle fibers’ atrophy.
The OP, as already said, is characterized by type II fibers preferential
atrophy while in OA muscular atrophy appears more homogeneous in
relation to fiber type of and more attenuated, although it is always
connected to the functional deficit caused by the disease.
Sarcopenia in the elderly is characterized not only by an histological
deterioration but also by an important functional impairment:
physical inactivity or a reduction in exercise level are a part of the
mechanisms that underlie sarcopenia and therefore physical activity
can be seen as an important factor to reverse or modify the
development of this condition [13]. Exercise is believed to be the most
effective intervention proposed to improve the quality of life and
functionality in older adults, improving muscular and skeletal
trophism and reducing the risk of injuries [14].
The aim of our study was to show the presence and the degree of
muscle atrophy in female patients with osteoporosis and osteoarthritis
and to evaluate if sarcopenia, detected by morphometric analysis, is
related to reduced levels of physical activity and muscular disuse in
these two groups.
Materials and Method
A functional evaluation of muscle efficiency was performed in
twenty osteoporotic women with a cervical femoral fracture and in
twenty osteoarthritic women with a Total Hip Arthroplasty (THA) in
progress using PASE test questionnaire (Physical Activity Test for the
Elderly).
cycling, mild, moderate and heavy sports activities) and domestic
activities (washing dishes, going to the supermarket, washing the
floors, doing home repairs or gardening work, caring for someone).
Each of these actions corresponds to a set value (I) that is
proportional to the "weight" that they could have in the life of each
individual.
Each patient is asked how many hours in a day he/she spends in
these activities (Q) for how many days per week (G). For each activity
is calculated a score achieved by the operation (QXG/7) x I.
The sum of the individual scores set the patient into one of four
categories related to the degree of physical activity:
•
•
•
•
inactivity (total score <42);
lacking physical activity (43-105);
moderate physical activity (106-145);
intense physical activity (>146).
We chose the PASE because it is a brief, easily scored, reliable and
valid instrument for the assessment of physical activity in
epidemiologic studies of older people [15].
Bone mineral density evaluation
DeXa was performed with a Lunar GE apparatus and lumbar spine
(L1-L4) and femoral neck scans were analyzed to evaluate BMD (in
grams per square centimetres): this evaluation is expressed as absolute
values and as T-scores. For the OA group the measurements were
performed on the non-dominant site, while for the OP group the
measurements were performed on the limb opposite the fracture site.
Each measurement was acquired with the patients laying in a supine
position and after the removal of any metal object. Women with
fragility hip fracture, a T-score ≤−2.5 SD, and a negative radiographic
framework for hip OA were included in the OP group.
Personal data and case histories of patients were collected and
patients were included in the two groups (OP and OA) after
performing DeXA, T-score, MHarris Hip Score and after radiographic
assessment by Kellgren-Lawrence scale.
Women with a positive radiogram for hip OA and T-score ≥−2.5
SD were included in the OA group.
In the context of a multimodal model of evaluation, we analyzed
biopsies of vastus lateralis muscle performed during the surgical
operation.
Muscle biopsies were taken from the upper portion of the vastus
lateralis during open surgery for hip arthroplasty.
The patients were informed about the experimental procedures and
signed an informed consent form before the study. The study was
approved by the Ethical Committee of Tor Vergata University
Hospital.
There was no discrepancy for age, sex and comorbidities in the two
groups (women, mean age OP 76 ± 3.2 y OA 74 ± 4.1 y). We used
standard statistical procedures in order to calculate means and
standard deviation (SD) of age.
We calculated Pearson correlation coefficient in order to find
statistically significant correlation for p<0.05. We performed the
Student's t-test to compare statistically different data.
PASE test
A functional evaluation of their performance status was realized
through the PASE test (Physical Activity Scale for the Elderly). The
questionnaire assesses two main groups of activities: recreational
activities carried out during free-time (reading, watching TV, walking,
J Gerontol Geriatr Res
ISSN:2167-7182 JGGR, an open access journal
Morphometric analysis
Muscle specimen was frozen into RCL2 and histological evaluations
were performed on transverse cryostat sections (7 μm thick) stained
with hematoxylin–eosin, myosin-slow and Gomori trichrome. We
used a a semiautomatic image analysis system (QWin Standard V3,
Leica, Cambridge, UK) to obtain morphometric data. A minimum of
200 muscle fibers per biopsy have been evaluated, comparing type I
and type II fibers for their relative prevalence, minimum transverse
diameter, and cross-sectional area. We established as atrophic fibers
those with a diameter lower than 30 μm, which is the minimum value
of the normal range for women [16].
Results
Morphometric and structural subjects parameters have shown
differences in the two gropus (Table 1).
Parameters
OA
OP
Age (years)
74 ± 4.1
76 ± 3.2
Volume 3 • Issue 5 • 183
Citation:
Piccirilli E, Gasbarra E, Baldi J, Pistillo P and Tarantino U (2014) Can Muscular Impairment be the “Key” for Femoral Fracture?. J
Gerontol Geriatr Res 3: 1000183. doi:10.4172/2167-7182.1000183
Page 3 of 5
Menopausal age (years)
49.8 ± 2.36
45.8 ± 2.88
HHS (points)
38 ± 7.6
Not performed
Kellgren-Lawrence Scale (degree)
4-Mar
2-Jan
T score
-0.9 ± 1.9
-2.7 ± 0.9
Pase test (score)
100 ± 20.86
62.6 ± 33
Average diameter type I fibers (μm)
30.20
33.01
Average diameter type II fibers (μm)
26.08
24.93
Table 1: Morphometric and structural subjects parameters.
In osteoporotic patients, the PASE test showed a low or moderate
level of physical activity or inactivity before occurring the fracture.
These findings are sustained by the old age of the patients, but they are
further supported by the idea that osteoporosis is closely related to an
important decrease in muscular performance, despite associated
symptoms like pain are usually absent. On the contrary, osteoarthritis
is characterized by a strong pain and functional limitation related to
articular damage: this is the reason for the reduction in physical
activity, although this impairment is not so evident (Figure 1).
Figure 1: Trend of PASE test scores in OP and OA patients.
Histological analysis showed no signs of necrosis, inflammation and
regeneration in muscle biopsies. The mean value of type I fibers’
diameter in OP and OA was 33.01 μm (ranging between 57.13 μm to
11.27 μm) and 30.20 μm (ranging between 37.29 μm to 19.32 μm),
respectively; the mean value of type II fibers’ diameter in OP and OA
was 24.93 μm (ranging between 32.77 μm to 15.58 μm) and 26.08 μm
(ranging between 31.86 μm to 18.13 μm), respectively.
These data underline that fiber diameters in OP tend to deviation
from the normal distribution toward an atrophic range. This deviation
is prominent for type II fibers compared with type I fibers.
Correlation between fiber II type diameters and PASE test in OP
showed that lower scores of PASE test are associated with a lower type
II fiber diameter (Figure 2 and Table 2). To verify if there was a
correlation we performed the Pearson product–moment correlation
test (p<0.001).
No correlation was found in OA or referring to type II fiber
diameter (p>0.05).
No correlation was found between BMD and PASE test (p>0.05),
while type II fiber prevalent atrophy correlates with low BMD
(p<0.05), suggesting that osteoporosis’s severity has a central role in
the pathogenesis of OP-related muscle atrophy.
Figure 2: Correlation between fiber II type diameters and PASE test
scores in OP patients.
Our data suggest that osteoporosis is a complex disease in which a
lot of factors may be associated with bone resorption and may
contribute to the reduction of patients’ physical skills, first of all a
sarcopenic status characterized by muscular decay and fiber atrophy.
Subgroups
Range of type I muscle fibers diameter
Range of type II muscle fibers diameters
Inactivity (<42 points)
19.32-24.73 μm
17.34- 22.46 μm
Lacking physical activity (43-105 points)
27.45-28.58 μm
22.93- 28.33 μm
Moderate physical activity (106-145 points)
26.47-31.46 μm
29.04- 30.02 μm
Intense physical activity (>146)
30.13-37.29 μm
31.86- 31.93 μm
Table 2: Subcategories of the osteoporotic patients according to PASE test scores and correlation with the average diameters of type I and type II
fibers (μm) in the four groups.
J Gerontol Geriatr Res
ISSN:2167-7182 JGGR, an open access journal
Volume 3 • Issue 5 • 183
Citation:
Piccirilli E, Gasbarra E, Baldi J, Pistillo P and Tarantino U (2014) Can Muscular Impairment be the “Key” for Femoral Fracture?. J
Gerontol Geriatr Res 3: 1000183. doi:10.4172/2167-7182.1000183
Page 4 of 5
Discussion
In this study, we compared from a morphological and functional
point of view two of the most common skeletal disease in the elderly,
osteoporosis and osteoarthritis.
We demonstrated that osteoporosis is closely related to sarcopenia:
in fact, bone weakening is associated with muscle aging in terms of
fiber atrophy and physical activity reduction, in a complex framework
of disability and high risk of fall and fractures.
Physical impairment does not correlate with BMD measured by
DeXa: this is to say that muscle functionality is not only associated
with the severity of osteoporosis disease. These data confirm the idea
that there is a large number of factors that influence skeletal
deterioration in addition to bone remodeling, as nutritional and
hormonal factors.
We selected patients that was homogeneous for age and sex so we
underlined that there is no correlation between type II fiber atrophy
and patients’ age. This could be explained by the idea that muscle
aging run faster in OP than in OA and leads to a greater state of
physical impairment at the same age.
The limitation of our study is that we selected only twenty female
patients. Maybe a larger sample of patients should be considered,
including male individuals in order to assess the impact of physical
activity according to a different genetic and hormonal substrate.
Sarcopenia is considered to be one of the major responsible factors
for functional limitations and motor dependency in elderly
osteoporotic persons [17].
It is important to emphasize that in OP morphological and
functional alterations proceed together toward a global weakening of
the musculoskeletal system.
All patients in the OP group were examined for the first time when
they were admitted to the hospital because of the cervical femoral
fracture and they referred important limitation in their physical daily
activity before the trauma. This leads to the hypothesis that OP muscle
atrophy could be enhanced by muscle disuse together with multiple
factors as the decrease of circulating hormones and reduced levels of
intracellular specific pathways.
On the contrary, osteoarthritis in is not linked to reduced physical
activity and selective fibers’ atrophy. Our data demonstrate that
muscle tissue is able to maintain a good trophism during OA.
A recent study [18] reported that in the initial stage of knee
osteoarthritis no accumulation of metabolic products and no
alteration of muscle proteins were found, maybe because during OA
muscle tissue is able to adapt itself to a new microenvironment in
order to avoid injury.
Muscle impairment is typical of osteoporotic condition.
According to our study, physical activity should be strongly
recommended in osteoporotic patients at diagnosis time because it
could be useful to delay muscle atrophy and bone loss thanks to the
biomechanical stimuli the muscle exerts on bone. In particular, multitask and balance exercises could improve fall-related self-efficacy, gait
speed and balance performance reducing the risk of falling [19].
However, it is a good clinical practice to suggest physical activity
also in osteoarthritic patients. In fact, the pain could reduce their
physical performance leading to obesity and mechanical overload. It is
J Gerontol Geriatr Res
ISSN:2167-7182 JGGR, an open access journal
known that physical activity and changes in diet composition can
reverse the inflammatory resistance, reducing progression or
preventing the onset of osteoarthritis [20].
Then, exercise could be a valid instrument to improve bone and
muscle quality and it could be a good strategy to reduce fracture risk
and disability in the elderly population.
References
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
Gorka J, Taylor-Gjevre RM, Arnason T (2013) Metabolic and clinical
consequences of hyperthyroidism on bone density. Int J Endocrinol 2013:
638727.
Martin AC (2011) Osteoporosis in men: a review of endogenous sex
hormones and testosterone replacement therapy. J Pharm Pract 24:
307-315.
McLean RR (2009) Proinflammatory cytokines and osteoporosis. Curr
Osteoporos Rep 7: 134-139.
Goldring MB1, Goldring SR (2007) Osteoarthritis. J Cell Physiol 213:
626-634.
Burr DB, Radin EL (2003) Microfractures and microcracks in
subchondral bone: are they relevant to osteoarthrosis? Rheum Dis Clin
North Am 29: 675-685.
Lindsay R (1992) The growing problem of osteoporosis. Osteoporos Int
2: 267-268.
Maltais ML, Desroches J, Dionne IJ (2009) Changes in muscle mass and
strength after menopause. J Musculoskelet Neuronal Interact 9: 186-197.
Baldwin KM, Haddad F, Pandorf CE, Roy RR, Edgerton VR (2013)
Alterations in muscle mass and contractile phenotype in response to
unloading models: role of transcriptional/pretranslational mechanisms.
Front Physiol 4: 284.
Terracciano C, Celi M, Lecce D, Baldi J, Rastelli E, et al. (2013)
Differential features of muscle fiber atrophy in osteoporosis and
osteoarthritis. Osteoporos Int 24: 1095-1100.
Cooper C, Dere W, Evans W, Kanis JA, Rizzoli R, et al. (2012) Frailty and
sarcopenia: definitions and outcome parameters. Osteoporos Int 23:
1839-1848.
Verschueren S, Gielen E, O'Neill TW, Pye SR, Adams JE, et al. (2013)
Sarcopenia and its relationship with bone mineral density in middle-aged
and elderly European men. Osteoporos Int 24: 87-98.
Loeser RF (2010) Age-related changes in the musculoskeletal system and
the development of osteoarthritis. Clin Geriatr Med 26: 371-386.
Montero-Fernández N, Serra-Rexach JA (2013) Role of exercise on
sarcopenia in the elderly. Eur J Phys Rehabil Med 49: 131-143.
McDermott AY, Mernitz H (2006) Exercise and older patients:
prescribing guidelines. Am Fam Physician 74: 437-444.
Washburn RA, Smith KW, Jette AM, Janney CA (1993) The Physical
Activity Scale for the Elderly (PASE): development and evaluation. J Clin
Epidemiol 46: 153-162.
Dubowitz V, Sewry CA (2007) Muscle biopsy: a practical approach, 3rd
edn. Saunders, Elsevier, New York, pp 75–123
Tarantino U, Baldi J, Celi M, Rao C, Liuni FM, et al. (2013) Osteoporosis
and sarcopenia: the connections. Aging Clin Exp Res 25 Suppl 1: S93-95.
M S Serrão PR, Vasilceac FA, Gramani-Say K, Lessi GC, B M Reiff R, et
al. (2014) Expression of receptors of advanced glycation end product
(RAGE) and types I, III and IV collagen in the vastus lateralis muscle of
men in early stages of knee osteoarthritis, Connect Tissue Res 12:1-8.
Halvarsson A, Franzén E, Ståhle A (2014) Balance training with multitask exercises improves fall-related self-efficacy, gait, balance
performance and physical function in older adults with osteoporosis: a
randomized controlled trial. Clin Rehabil.
Sartori-Cintra AR, Aikawa P, Cintra DE (2014) Obesity versus
osteoarthritis: beyond the mechanical overload. Einstein (Sao Paulo) 12:
374-379.
Volume 3 • Issue 5 • 183