Journal of Orthopaedic Science 28 (2023) 1279e1284

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Original Article

Bone mineral density, limb muscle mass, muscle strength, andexercise capacity are reduced in female patients with distal radius
fractures when the unaffected side grip strength is less than 18 kg
Kazushige Maeda a, *, Junya Imatani b, Shinji Narazaki b, Toshifumi Ozaki cabc

Maeda Orthopedic and Surgery Clinic, Japan
Department of Orthopedics, Okayama Saiseikai General Hospital, Japan
Department of Orthopedics, Okayama University Medical School, Japana r t i c l e i n f o

a b s t r a c t

Article history:
Received 9 May 2022
Received in revised form
19 July 2022
Accepted 3 September 2022
Available online 28 September 2022

Background: Prevention of domino effects after distal radius fractures is important for improving life
expectancy. Fragility fractures secondary to falls are associated with decreased bone mineral density,
muscle strength, and exercise capacity. Grip strength is one of the simplest and most useful tests tocomprehensively judge muscle strength. The purpose of this study was to examine whether grip strength
is associated with bone mineral density, limb muscle mass, muscle strength, and exercise capacity, bycomparing patient backgrounds based on the presence or absence of grip weakness in female patientswith distal radius fractures.
Methods: This study included women with distal radius fractures who visited our orthopedics outpatient
department between April 2015 and April 2020. Bone mineral density, limb muscle mass, skeletal muscle
mass index, muscle strength (grip strength on unaffected side and quadriceps muscle strength), theTimed Up and Go test, and the Two-Step test were evaluated six to eight weeks after injury. Patients weredivided into two groups according to the cutoff value of grip strength (18e21 kg), and 90 age-adjusted
and matched participants were compared and examined.
Results: At the cutoff value of 18 kg, a signiﬁcant decrease in lumbar spine and total proximal femur bonemineral density (p < 0.05, p < 0.05), limb muscle mass and skeletal muscle mass index (p < 0.01,
p < 0.05), quadriceps femoris muscle strength (p < 0.01), the Timed Up and Go test (p < 0.05), and the
Two-Step test (p < 0.01), was observed in the grip-weakness group compared to that in the no-gripweakness group.
Conclusions: In women with distal radius fracture and grip strength <18 kg on the unaffected side, bonemineral density, limb muscle mass, quadriceps femoris strength, and exercise capacity may be reduced.
These results suggest reduced grip strength may be an indicator for further testing to prevent domino
effects.
© 2022 The Japanese Orthopaedic Association. Published by Elsevier B.V. All rights reserved.

Keywords:
Distal radius fracture
Grip strength
Domino effects
Bone mineral density
Limb muscle mass
Exercise capacity

1. Introduction
The chain of fragility fractures caused by osteoporosis is referred
to as the domino phenomenon of fractures (domino effect). Amongthese fragility fractures, the distal radius fracture is often the ﬁrst
fragility fracture; its incidence increases in women in their late 50s
and peaks for those in their 60s and 70s, and this fracture is said tooccur in a relatively active age group [1]. In addition, because* Corresponding author.
E-mail address: kazushi_chick30@yahoo.or.jp (K. Maeda).

individuals with distal radius fractures are at a 3.3-,1.9-, and 1.7
times higher risk of forearm bone fractures, hip bone fractures, andvertebral bone fractures, respectively [2], the risk of domino effects
increases. Therefore, preventing domino effects after fractures ofthe distal radius is considered a critical issue for orthopedic
surgeons.
The causes of distal radius fractures and secondary fragility
fractures in older adults include bone fragility owing to decreasedbone mineral density and bone quality, and falling due to decreased
muscle mass, muscle strength, and exercise capacity. Approximately 90% of distal radius fractures in older adults are attributed tofalls, and most hip fractures are also said to be caused by falls [3,4];

https://doi.org/10.1016/j.jos.2022.09.001
0949-2658/© 2022 The Japanese Orthopaedic Association. Published by Elsevier B.V. All rights reserved.

K. Maeda, J. Imatani, S. Narazaki et al.

Journal of Orthopaedic Science 28 (2023) 1279e1284

thus, preventing falls might contribute to the prevention of domino
effects after distal radius fractures.
Grip strength is one of the simplest and most convenientmethods to measure muscle strength. A prospective cohort study
found that reduced grip strength predicted an increased risk offragility fractures of 1.57 times [5]. Grip weakness is also correlatedwith mortality [6]. Based on these studies, grip weakness may befactorial when evaluating fall and fracture etiology.
Therefore, this study aimed to investigate the background of
women with distal radius fractures, including bone mineral density,
limb muscle mass and muscle strength, and exercise capacity to
examine whether grip weakness is an indicator of these factors bycomparing them based on grip weakness on the unaffected side.
2. Materials and Methods
Between April 2015 and April 2020, all patients with distal
radius fractures who visited the orthopedic surgery outpatient
department of the City General Hospital were evaluated. Women
over 40 years of age with distal radius fractures who had sustained
injuries due to a fall and could walk independently were includedin this study. Exclusion criteria were injury not related to falls;
patients with thyroid disease, metabolic bone diseases, ureteralcalculus, renal dysfunction, Cushing's syndrome, use of glucocorticoid hormone actives; previous treatment for malignancy; previous upper extremity fracture on the unaffected side;
hemoglobinA1c  7.0, or diabetes. Patients who met the inclusion
criteria provided written informed consent prior to participating inthe study. This study was approved by the ethics committee of theCity General Hospital.
Prior to the fracture treatment, patient's information was obtained via questionnaire comprising age, sex, body mass index(BMI; weight divided by height squared), and medical history,
speciﬁcally fragility fracture history (including proximal femoral
fracture, vertebral fracture, and six non-vertebral fractures, namely
those of the distal radius, proximal humerus, rib, pelvic, clavicle,
and lower leg, as well as a family history of proximal femoral
fracture). Patients with distal radius fractures were treatedconservatively with a cast or surgically with a volar locking plate,based on the 2012 and 2017 revised clinical practice guidelines for
distal radius fractures [7,8]. At 6e8 weeks post-injury, bone mineraldensity was measured in the lumbar spine and total proximal femur, along with the limb muscle mass and skeletal muscle massindex (SMI) [9]. For muscle strength, the grip strength on the unaffected side and the strength of the quadriceps in the thigh were
measured, whereas for exercise capacity, the Timed Up and Go(TUG) and Two-Step tests (2ST), which are the criteria for locomotive syndrome [10], were measured.
Measurements of bone mineral density in the lumbar spine andtotal proximal femur and of muscle mass in the limb were performed using dual-energy X ray absorptiometry (DXA) with a bonedensitometer (PROGIDY FUGA, General Electric Health Care, Japan).
Bone mineral density was expressed as the young adult mean value(YAM). Lumbar spine bone mineral density was measured in the 1st
to 4th lumbar vertebra. Regarding the total proximal femoral bonemineral density, the bone mineral density of both left and rightproximal femurs were measured and the average was calculated.
Limb skeletal muscle mass was calculated by determining the bodyfat mass and the lean body mass using the DXA method andcombining the values of the lean mass of the upper limbs and of thelower limbs. The SMI was corrected for limb muscle mass divided
by the height squared. To evaluate muscle strength, grip strength
was measured using a Grip-D T.K.K 5401 (Takei Scientiﬁc Instrument Co., Ltd., Tokyo, Japan). Grip strength of the unaffected side

Fig. 1. Using an Isoforce GT330, the patient sits on the seat and is secured with lumbar
and thigh belts. The quadriceps femoris strength is then measured while the patient
performs the isotonic, open kinetic chain exercise of knee extension.

was measured three times with the patient in a standing positionand elbow extended, and the average value was considered. The
quadriceps femoris muscle strength was also quantitatively
measured using Isoforce GT330 (OG Wellness Technologies Co., Ltd.,
Okayama, Japan), which is an automatic exercise training device
coupled with a measurement device (Fig. 1), and was calculated as
the average value of the left and right quadriceps femoris muscle
strength. In the TUG, the time (s) taken by each patient to stand up
from an armchair, walk 3 m, turn, walk back, and sit on the chair
was measured [11]. In the 2ST, the patients stood with their toesaligned at the standing line, took two steps as far as possible, andthen aligned their feet to complete the test [12].
The cutoff value of the grip strength on the unaffected side wasestimated by the following procedure. We divided the womenparticipants (n ¼ 124) with distal radius fracture before adjusting
for age based on the presence or absence of osteoporosis according
to the diagnostic criteria for primary osteoporosis (bone mineraldensity &70% YAM for lumbar or total proximal femur) [13]; theestimated grip value (19.6 kg) was calculated by the receiver
operating characteristic curve (speciﬁcity: 0.702, sensitivity: 0.652,
area under the curve: 0.687) (Fig. 2). After the cutoff value of grip
strength was set from 18 to 21 kg based on the estimated grip
strength of 19.6 kg, each parameter was compared between the
age-adjusted and age-matched grip-weakness (n ¼ 45) and nogrip-weakness (n ¼ 45) groups.
2.1. Statistical analysis
A per-protocol set analysis was used in this study. In the statistical test, propensity score matching using logistic regression
analysis was used to adjust for age. Fisher's exact tests were used tocompare the contingency table of gender and the occurrence rate ofeach event; BMI was compared by Student's t-test, because it followed a normal distribution. ManneWhitney U tests were used tocompare the other measured values, such as bone mineral density.
All statistical analyses were performed using the modiﬁed graphical user interface of R (version 2.13.2., The R Foundation for Statistical Computing, Vienna, Austria), known as EZR (Saitama
Medical Center, Jichi Medical University, Saitama, Japan). This
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Journal of Orthopaedic Science 28 (2023) 1279e1284

modiﬁed version of R Commander (version 1.8e4) was designed to
add statistical functions that are frequently used in biostatistics. We
considered p < 0.05 to indicate statistical signiﬁcance.
3. Results
Signiﬁcant differences were found in all parameters of bonemineral density, limb muscle mass, lower limb muscle strength,and exercise capacity at the cutoff value of 18 kg. The patients’backgrounds are shown in Table 1. There were no signiﬁcant differences in BMI between the two groups at this cutoff value. In
addition, there were no signiﬁcant differences in the history offragility fractures, vertebral compression fractures, parental hip
fractures, or osteoporosis treatment. However, the rate of treatments history was low in both groups.
Lumbar and total proximal femoral bone density were signiﬁcantly lower in the grip-weakness group (no-grip-weakness groupvs. grip-weakness group: median, 86% vs. 78%, and 78% vs. 70%,
respectively; both p < 0.05) (Fig. 3). Limb muscle mass and SMI
were also signiﬁcantly lower in the grip-weakness group comparedto those in the no-grip-weakness group (no-grip-weakness groupvs. grip-weakness group: median, 13,656 g vs. 12,694 g, and 5.89 g/
m2 vs. 5.52 g/m2, respectively; p < 0.01, p < 0.05) (Fig. 4A).
Regarding muscle strength, the quadriceps femoris muscle strength
was signiﬁcantly lower in the grip-weakness group compared tothat in the no-grip weakness group (no-grip-weakness group vs.

Fig. 2. Receiver operating characteristic curve that estimates the cutoff value of grip
strength.

Table 1Comparison of patient background data.

Age (year)
Body mass index (kg/m2)
Grip strength
Smoking history
Drinking history
History of fragile fractures
History of vertebral compression fractures
History of fracture treatments
Parental hip fractures

Mean ± SD
Mean ± SD
Mean ± SD
yes
yes
yes
yes
yes
yes

No-grip-weakness group (n ¼ 45)

Grip-weakness group (n ¼ 45)

p-value

71.4 ± 8.6
22.8 ± 3.8
22.2 ± 3.3
2 (4.4%)8 (17.8%)
14 (31.1%)
8 (17.8%)
3 (6.7%)2 (4.5%)71.5 ± 8.7
26.1 ± 30.1
14.2 ± 2.9
4 (8.9%)11 (24.4%)
18 (40%)11 (24.4%)
4 (8.9%)8 (17.8%)

p ¼ 0.942
p ¼ 0.144
p < 0.01**
p ¼ 0.677
p ¼ 0.477
p ¼ 0.509
p ¼ 0.606
p¼1
p ¼ 0.0897

Data are presented as numbers and percentages, unless otherwise stated. SD, standard deviation.

Fig. 3. Comparison of bone mineral density (lumbar spine and total proximal femur). Bone mineral density was expressed as the young adult mean value (YAM).
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Journal of Orthopaedic Science 28 (2023) 1279e1284

Fig. 4. Comparison of limb muscle mass, muscle strength and exercise capacity. A: Limb muscle mass and skeletal muscle mass index (SMI). B: Quadriceps muscle strength. C:
Timed Up and Go (TUG) and Two-Step tests (2ST).

4. Discussion

grip-weakness group: median, 317.5 N・m vs. 240.5 N・m;p < 0.01) (Fig. 4B). Furthermore, the TUG and 2ST as indicators of
exercise capacity were also signiﬁcantly lower in the grip-weakness
group compared to those in the no-grip-weakness group (no-gripweakness group vs. grip-weakness group: median, 8.5 s vs. 10.8 s
and 1.06 vs. 1.21, respectively; p < 0.05, p < 0.01) (Fig. 4C).

This study aimed to compare bone mineral density, limb muscle
mass, SMI, lower limb muscle strength, and exercise capacity, basedon the presence or absence of grip weakness, and examine whether
grip strength can be an indicator of decreases in these factors that1282

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Journal of Orthopaedic Science 28 (2023) 1279e1284

future locomotive syndrome. Consistent with the results of thesestudies, our ﬁndings suggest that grip strength is closely associatedwith quadriceps femoris strength and exercise capacity.
Bone mineral density, limb muscle mass, SMI, lower limb muscle
strength, and exercise capacity in women with distal radius fractureand grip weakness of less than 18 kg on the unaffected side werelower than in those without grip weakness. Bone mineral density is
one of the indicators of treatment interventions for fall reoccurrence and secondary fractures, but only certain facilities haveavailable devices for measuring bone mineral density. On the other
hand, measuring grip strength is one of the simplest tests that canbe performed anywhere. If the presence or absence of decreased
grip strength on the unaffected side of women with distal radius
fracture is an indicator for a decrease in bone mineral density, limb
muscle mass, lower limb strength, and exercise capacity, it might bepossible to implement effective treatment interventions to prevent
domino effects. In other words, if decreased grip strength on theunaffected side is present, it should be followed with a test for bonemineral density, limb muscle mass, lower limb muscle strength andbalance, to conﬁrm the diagnosis of locomotive syndrome. In cases
where a decrease in these parameters is observed, it is necessary toactively intervene with treatment to prevent falls and further
fractures.
This study has some limitations. First, the number of cases was
small, which may have affected the results of the study. It istherefore necessary to increase the sample size and continue theinvestigation in the future. Second, because the tests were not
performed directly after the injury but 6e8 weeks later, rehabilitation may have affected the results. However, the grip strength of
the hand on the unaffected side was measured, which was probably
less affected by rehabilitation than that on the affected side. Since
there is no speciﬁc guidance on rehabilitation or exercise for thetrunk or lower limbs, its inﬂuence on exercise capacity is likely
relatively low. Third, only the grip on the unaffected side wasmeasured; we did not factor in whether the grip was of thedominant or nondominant hand, the inﬂuence of which might be ofconcern. In general, 10% of all individuals are left-handed [25], andonly left-sided fractures were evaluated; thus, the unaffected side
was likely the dominant side in this study. However, it might benecessary to examine grip only on the dominant side as the numberof cases increase. Fourth, regarding the bone mineral density
measurement of the lumbar spine, collapsed vertebral body was
included in 3 no-grip-weakness and in 4 grip-weakness cases.
However, all vertebral bodies were only mildly collapsed, so theinﬂuence on lumbar spine bone mineral density is likely relatively
low.
In conclusion, if the grip strength on the unaffected side is below
18 kg in women with distal radius fractures, the bone mineraldensity, limb muscle mass, lower limb muscle strength, and exercise capacity might be decreased. Therefore, these ﬁndings suggest
reduced grip strength may warrant further testing and active
intervention with timely treatment, thereby preventing domino
effects by early examination after a distal radius fracture.

contribute to domino effects in older women with distal radius
fractures.
Distal radius fractures in the older population are the third mostcommon fracture after vertebral compression and proximal femur
fractures, and are one of the most frequent fractures that occur
mainly because of osteoporosis [14]. They often precede proximal
humerus/femoral fractures among fragility fractures [1], andbecause they are likely to be the ﬁrst fragility fracture, this isconsidered an opportunity for therapeutic intervention to prevent
domino effects. Most patients with distal radius fractures have afalling mechanism of injury; in a study of 85 postmenopausal patients with distal radius fractures, 60% of the patients exhibitedbone loss and 22.3% experienced a recurring fall one year after thefracture [15]. Based on this result, it is considered that patients are
more likely to experience a secondary fracture from another fall
after an initial fracture of the distal radius.
The results of this study showed that the bone mineral density
in the lumbar spine and total proximal femur was signiﬁcantly
reduced in the grip-weakness group. Li et al. [16] reported that in astudy of 120 postmenopausal women, the grip-weakness group(less than 20 kg in the dominant arm) exhibited signiﬁcantly
reduced bone mineral density in the lumbar spine, total proximal
femur, and femoral neck. It has also been reported that grip
strength correlates with vertebral, total proximal femur, andfemoral neck bone density [17,18]. Based on the results of this study,
we suggest that when a decrease in grip strength on the unaffectedside is observed after a fracture of the distal radius, it is likely thatbone mineral density has decreased and that secondary fractures
might occur because of bone fragility. Therefore, bone mineraldensity should be actively measured in such patients. Additionally,
if bone mineral density has decreased on DXA, treatment intervention is necessary to prevent osteoporosis.
Limb muscle mass and SMI were signiﬁcantly decreased in the
grip-weakness group. Ho et al. [19] reported that in a study of 120
patients with a history of hip fractures, appendicular SMI was
positively correlated with hip bone mineral density. Pereira et al.
[20] also reported that in a study of 198 male patients over 60 years
old, patients with decreasing relative appendicular muscle mass
were approximately eight times more likely to receive a diagnosisof abnormal bone mineral density compared with that of normal
men. These results indicated that limb muscle mass and bonemineral density are correlated; patients with decreasing limb
muscle mass might fall and sustain fracture. Therefore, not onlybone mineral density but also limb muscle mass should be actively
measured, such that in case of adverse outcomes, timely rehabilitation and nutrition therapy can be considered to prevent falls.
The quadriceps femoris muscle strength, the TUG, which reﬂects
dynamic balance, and the 2ST, which comprehensively represents
walking ability, were signiﬁcantly decreased in the grip-weakness
group compared with the no-grip-weakness group. A study of
167 healthy men and women aged 18e82 years reported a correlation between grip strength and quadriceps strength [21]. Basedon the results of this study, it might be possible to predict muscle
weakness in the lower limbs by simply measuring the grip strengthof women after fractures of the distal radius. In addition, in a studyof 6766 older adults aged 67e93 years, Fragala et al. [22] reported
that decreased grip strength and quadriceps muscle strength weresigniﬁcantly associated with decreased walking speed. In a study
comparing 128 women with distal radius fractures and controls,
Fujita et al. [23] reported that patients with distal radius fractures
had reduced grip strength and dynamic balance, suggesting thatpatients with distal radius fractures had preexisting decreased
muscle strength and exercise capacity. Kobayashi et al. [24] also
surveyed 88 Japanese individuals over 40 years old and reported
that reduced grip strength could be a signiﬁcant risk factor for

5. Consent statement
All patients included in this study provided written informed
consent prior to participating in the study. This study was approvedby the ethics committee of the City General Hospital.
Funding statement
This research did not receive any speciﬁc grant from funding
agencies in the public, commercial, or not-for-proﬁt sectors.
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Journal of Orthopaedic Science 28 (2023) 1279e1284

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The authors declare that there are no conﬂicts of interest toreport.
Acknowledgements
We wish to thank Dr. Hayashi and Dr. Okazaki for the advice on
experimental design.
We would like to thank Editage (www.editage.com) for English
language editing.
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