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Submit a Manuscript: https://www.f6publishing.com World J Clin Cases 2020 September 26; 8(18): 4010-4016

DOI: 10.12998/wjcc.v8.i18.4010 ISSN 2307-8960 (online)

ORIGINAL ARTICLE
Case Control Study
Effects of different doses of metformin on bone mineral density and
bone metabolism in elderly male patients with type 2 diabetes
mellitus

Lin-Xia Wang, Guang-Ya Wang, Na Su, Jie Ma, Yu-Kun Li

ORCID number: Lin-Xia Wang 0000- Lin-Xia Wang, Yu-Kun Li, Department of Endocrinology, The Third Hospital of Hebei Medical
0002-7733-0089; Guang-Ya Wang University, Shijiazhuang 050051, Hebei Province, China
0000-0003-0646-6170; Na Su 0000-
0003-1112-0756; Jie Ma 0000-0001- Lin-Xia Wang, Guang-Ya Wang, Na Su, Jie Ma, Second Department of Endocrinology, Cangzhou
8108-9657; Yu-Kun Li 0000-0002- Central Hospital, Cangzhou 061001, Hebei Province, China
4005-9715.
Yu-Kun Li, Key Orthopaedic Biomechanics Laboratory of Hebei Province, Shijiazhuang
Author contributions: Wang LX, Li 050051, Hebei Province, China
YK, Su N, Ma J and Wang GY
collected the data and wrote and Corresponding author: Yu-Kun Li, PhD, Professor, Department of Endocrinology, The Third
edited the manuscript; all the Hospital of Hebei Medical University, No. 139 Ziqiang Road, Shijiazhuang 050051, Hebei
authors approved the publication Province, China. lykun1962@163.com
of the manuscript.

Institutional review board Abstract

statement: The study was
BACKGROUND
approved by Ethics Committee of
Diabetes is a chronic disease, which may cause various complications. Patients
Cangzhou Central Hospital.
with diabetes are at high risk of bone and joint disorders, such as osteoporosis and
Informed consent statement: All
bone fractures. In addition, it became widely accepted that diabetes has an
patients gave informed consent.
important impact on bone metabolism. Metformin is a commonly used and
effective first-line treatment for type 2 diabetes. Some glucose-lowering agents
Conflict-of-interest statement: The have been found to have an effect on bone metabolism. The present study
authors declare that there is no explored if different doses of metformin have an effect on bone mineral density
conflict of interest. (BMD) and bone metabolism in type 2 diabetes.

Data sharing statement: No AIM

additional data available. To investigate the effects of different doses of metformin on BMD and bone
metabolism in elderly male patients with type 2 diabetes mellitus.
STROBE statement: The
manuscript has been prepared and
METHODS
revised according to the STROBE
A total of 120 elderly male outpatients with type 2 diabetes mellitus who were
statement.
admitted to our hospital were included in the study from July 2018 to June 2019.
They were randomly assigned to an experimental group and a control group with
Open-Access: This article is an 60 patients in each group. Patients in the experimental group were given high
open-access article that was dose metformin four times a day 0.5 g each time for 12 wk. Patients in the control
selected by an in-house editor and group were given low dose metformin orally twice a day 0.5 g each time for 12
wk. The changes in bone mineral density and bone metabolism before and after

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 Wang LX et al. Is high dose of metformin good for BMD?

fully peer-reviewed by external treatment and the efficacy rate of the treatment were compared between the two
reviewers. It is distributed in groups.
accordance with the Creative
RESULTS
Commons Attribution
There was no significant difference in the efficacy rate between the two groups (P
NonCommercial (CC BY-NC 4.0)
> 0.05). Before the treatment, there was no significant difference in BMD and bone
license, which permits others to
metabolism between the two groups (P > 0.05). However, after the treatment,
distribute, remix, adapt, build
BMD and bone metabolism were improved in the two groups. Moreover, BMD
upon this work non-commercially,
and 25-hydroxyvitamin D were significantly higher in the experimental group
and license their derivative works
than in the control group, and N-terminal/midregion and β-isomerized C-
on different terms, provided the
terminal telopeptides were significantly lower in the experimental group than in
original work is properly cited and
the control group (all P < 0.05). There was no significant difference in the
the use is non-commercial. See: htt
incidence of adverse reactions between the two groups (P > 0.05).
p://creativecommons.org/licenses
/by-nc/4.0/ CONCLUSION
Both high and low dose metformin can effectively control the blood glucose levels
Manuscript source: Unsolicited in elderly male patients with type 2 diabetes mellitus. However, the benefits of
manuscript high dose metformin in improving BMD and bone metabolism level was more
obvious in patients with type 2 diabetes mellitus.
Received: June 5, 2020
Peer-review started: June 5, 2020
First decision: July 25, 2020 Key Words: Dosages; Metformin; Type 2 diabetes mellitus; Elderly male patients; Bone
Revised: August 12, 2020 mineral density; Bone metabolism
Accepted: August 22, 2020
Article in press: August 22, 2020 ©The Author(s) 2020. Published by Baishideng Publishing Group Inc. All rights reserved.
Published online: September 26,
2020 Core Tip: In the last two decades, metformin has been a widely used medicine in the
treatment of diabetes. It has been proven to have additional benefits in anticancer and
P-Reviewer: Georgescu EF, antiaging beyond glycemic control. To answer whether it has a positive effect on bone
Johansen S, Sato H mineral density and bone metabolism, the present study compared the outcomes of bone
S-Editor: Wang JL mineral density and bone metabolism between different doses of metformin in patients
L-Editor: Filipodia with type 2 diabetes. The results supported that a comparatively higher dose of metformin
P-Editor: Zhang YL helped to improve bone mineral density and bone metabolism levels in patients with type 2
diabetes.

Citation: Wang LX, Wang GY, Su N, Ma J, Li YK. Effects of different doses of metformin on
bone mineral density and bone metabolism in elderly male patients with type 2 diabetes
mellitus. World J Clin Cases 2020; 8(18): 4010-4016
URL: https://www.wjgnet.com/2307-8960/full/v8/i18/4010.htm
DOI: https://dx.doi.org/10.12998/wjcc.v8.i18.4010

INTRODUCTION
The incidence of chronic diseases has increased due to the improvements in people’s
living conditions. Type 2 diabetes, as one of the common chronic diseases, is
threatening people’s health to a considerable degree[1,2]. It may raise the risk of
osteoporosis, which is mainly caused by the decreased insulin sensitivity or lack of
insulin production in elderly male patients. Accordingly, interests of clinical studies
are focused on exploring optimum therapies to control the blood glucose levels and
meanwhile improve osteoporosis in elderly male patients with type 2 diabetes
mellitus[3,4]. Currently, metformin is widely used in the treatment of type 2 diabetes.
However, there is a contradiction in the statements on different dosages of metformin
on bone mineral density (BMD) and bone metabolism in elderly male patients with
type 2 diabetes mellitus[5]. On this account, the present study analyzed the effects of
different dosages of metformin on BMD and bone metabolism in 120 patients with
type 2 diabetes.

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Wang LX et al. Is high dose of metformin good for BMD?

MATERIALS AND METHODS

Participants
A total of 120 elderly male patients with type 2 diabetes mellitus who visited The
Third Hospital of Hebei Medical University’s outpatient clinics were included from
July 2018 to June 2019. All of them meet the diagnostic criteria for type 2 diabetes and
received necessary examinations including routine blood test, coagulation test,
transcranial Doppler test and head computed tomography scan. According to the
sequences of hospitalization admission, they were assigned to an experimental group
and a control group with 60 patients in each group. The age range was 61 to 83 (72.12 ±
5.68) years for the experimental group and 62 to 84 (72.57 ± 5.63) years for the control
group. Patients in the experimental group had 2 to 15 years (8.84 ± 2.35) of disease
duration, and patients in the control group had 3 to 16 years (8.99 ± 2.15) of disease
duration. There was no significant difference in general information in patients
between the two groups (P > 0.05).

Inclusion criteria
Patients who meet any of the following diagnostic criteria were included in the study:
Fasting blood sugar ≥ 7.0 mmol/L; two-hour postprandial glucose ≥ 11.1 mmol/L;
normal random glucose ≥ 11.1 mmol/L based on 2017 Guideline for the Prevention
and Management of Type 2 Diabetes[6]. Additional criteria included patients without
previous history of cerebral hemorrhage or cerebral infarction complicated with
hemiplegia. Patients who were diagnosed with tumors were excluded from the study.
All the participants signed an informed consent statement, and the study was
approved by our hospital ethics committee.

Methods
Metformin (0.5 g, Cat. # H32021625, Suzhong Pharmaceutical Group Co., Ltd.,
Taizhou, China) was administrated to patients in both groups. In the experimental
group, metformin was dosed at 0.5 g four times daily with 2 g total daily dose. In the
control group, metformin was initially dosed 0.5 g twice daily with or after meals and
the maximum daily dose was 1 g. The treatment lasted for 12 wk in both groups.

Measurements
Clinical effectiveness was compared between the two groups according to the levels of
blood glucose. The effectiveness was defined as stabilization of fasting and
postprandial blood glucose levels to the normal range without complications. Effective
blood glucose control was defined as blood glucose levels close to the normal range
without severe complications. Ineffectiveness was defined as blood glucose levels that
were still high[7,8]. BMD for lumbar vertebra of L1-4 and hip was measured by dual-
energy X-ray absorptiometry (Horizon DXA system, Manufacturer: Hologic, Inc., USA,
Model: Discovery A) before and after the treatment. Bone metabolic markers were
compared between the two groups. Levels of N-terminal midfragment of osteocalcin,
β-isomerized C-terminal telopeptides and 25-hydroxyvitamin in the blood were
measured by Infinite F50 ELISA reader. The incidence of complications was observed
in the duration of medication.

Data processing
Data that were counted or measured in the study were statistically analyzed using
SPSS19.0. The χ2 test was used to evaluate a relationship between two categorical
variables, and the counted data was expressed as a percentage. Student t test was used
for measured data. A P value < 0.05 was considered statistically significant.

RESULTS
Efficacy of treatment
There was no significant difference in the treatment efficacy between the two groups
(Table 1).

Changes in BMD and bone metabolic markers

There was no significant difference in the levels of BMD and bone metabolic markers
between the two groups before the treatment (P > 0.05). After the treatment, levels of
BMD and bone metabolic markers were improved. To be specific, levels of BMD and

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 Wang LX et al. Is high dose of metformin good for BMD?

Table 1 Comparison of efficacy between the two groups, n (%)

Groups Well-controlled Effectively-controlled Ineffective Overall efficacy

Control group 38 19 3 57 (95.00)

Experimental group 40 18 2 58 (96.67)

χ2 0.349

P value > 0.05

25-hydroxyvitamin D were higher in the experimental group than in the control group
(all P < 0.05). However, levels of N-terminal midfragment and β-isomerized C-
terminal telopeptides were lower in the experimental group than in the control group
(all P < 0.05, Table 2).

Complications in the two groups

Complications occurred in three patients in the control group during the
administration of medication including nausea in one patient, dizziness in one patient
and gastrointestinal reactions in one patient. Comparatively, complications were
reported in two patients in the experimental group during the administration of
medication including dizziness in one patient and nausea in one patient. These
complications disappeared after discontinuation of the study medicines, which did not
have an effect on the treatment efficacy. Therefore, there was no significant difference
in the incidence of complications between the two groups (P > 0.05).

DISCUSSION
Risk of osteoporosis is increased with the development of type 2 diabetes. Os-
teoporosis may occur in patients with type 2 diabetes for a variety of reasons. First,
type 2 diabetes makes blood glucose higher than normal for a long time, which means
a large amount of glucose is excreted in the urine, and islet function is influenced
gradually. Furthermore, a large amount of calcium and phosphate ions in serum is
excreted out of the body by osmotic diuretics. In that, the decreased blood calcium and
phosphate concentrations may lead to osteocyte dysfunction[9,10]. Second, the poor
blood glucose control may cause accumulation of glycosyl compound that may further
promote oxidative stress and then lead to osteopenia and myelosuppression. All of
this may have adverse effects on osteoblast and bone formation[11,12]. In another way,
physical activity is not low in elderly male patients. Microstructure impairment at
subchondral bone is more likely to occur resulting from bone disorders where the
bone remodeling process occurs too frequently. This increases the possibility of
fracture. Metformin as the first-line treatment for type 2 diabetes shows good efficacy
in lowering blood glucose. Meanwhile, it greatly improves BMD in patients with type
2 diabetes, and its role in bone tissues is now increasingly being mentioned and
discussed[13].
The present study examined the effect of different dosages of metformin on BMD
and bone metabolism in elderly male patients with type 2 diabetes mellitus. The
results showed that there was no significant difference in the treatment efficacy
between the two groups (P > 0.05). Before the treatment, there was no significant
difference in BMD and levels of bone metabolism markers between the two groups (P
> 0.05). However, BMD and levels of bone metabolism markers were improved in the
two groups after the treatment. To be specific, BMD and levels of 25-hydroxyvitamin
D were higher in the experimental group than in the control group and levels of N-
terminal midfragment and β-isomerized C-terminal telopeptides were lower in the
experimental group than in the control group (all P < 0.05). It revealed that a high
dosage of metformin can help to improve osteoporosis as well as control blood glucose
in elderly male patients with type 2 diabetes mellitus.
Metformin can promote the osteogenic differentiation and mineralization of
induced mesenchymal stem cells, which are derived from pluripotent stem cell and
can differentiate into many cell types such as adipocytes, osteoblasts and
chondrocytes. Its effect on differentiation can be regulated by cellular transcription
factors[14,15]. Several animal experiments reported that metformin may enhance and
induce osteogenic differentiation of mesenchymal stem cells. In vitro studies revealed
that metformin may increase type I collagen synthesis, alkaline phosphatase activity,

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Wang LX et al. Is high dose of metformin good for BMD?

Table 2 Comparison of levels of bone mineral density and bone metabolic markers between the two groups

BMD, g/cm2
Groups n N-MID, ng/mL β-CTx, pg/mL 25(OH)D, ng/mL
Lumbar L1-4 Hip
Control group

Before the treatment 60 0.71 ± 0.13 0.62 ± 0.09 19.35 ± 8.14 498.57 ± 210.02 9.54 ± 3.67
a a
After the treatment 60 0.88 ± 0.17 0.76 ± 0.15 15.54 ± 5.23 376.27 ± 157.45 17.97 ± 5.74

Experimental group

Before the treatment 60 0.73 ± 0.11 0.64 ± 0.08 20.41 ± 8.13 504.74 ± 237.41 9.23 ± 2.84
ab ab ab ab
After the treatment 60 1.04 ± 0.25 0.93 ± 0.20 10.68 ± 4.24 310.64 ± 146.83 25.96 ± 6.91ab

a
P < 0.05 vs before the treatment;
b
P < 0.05 vs the control group after the treatment. 25(OH)D: 25-hydroxyvitamin D; β-CTx: β-isomerized C-terminal telopeptides; BMD: Bone mineral
density; N-MID: N-terminal midfragment.

extracellular calcium deposition and osteocalcin synthesis and may repair bone lesions
in rats with diabetes[16].
Moreover, metformin can inhibit osteoclast differentiation and reduce the activity of
C-terminal propeptides of type I collagen. Metformin’s effect on bone metabolism is
realized through several ways in patients with diabetes mellitus including activating
the extracellular signal-regulated kinase and AMP-activated protein kinase signaling
pathway, changing the expression of bone morphogenetic proteins and nitric oxide
and influencing osteoblasts[17]. When used at high doses, metformin can reduce blood
glucose, inhibit advanced glycation end product deposition, relieve injuries to the
thigh and induce the osteogenic differentiation[18,19]. Similarly, the present study
revealed that the relationship between osteoporosis and blood glucose levels should be
taken into consideration in addition to usage of osteogenic promoting agents in the
treatment of type 2 diabetes complicated with osteoporosis in elderly patients. In this
way, the treatment efficacy will be improved greatly in these population[20].

CONCLUSION
In conclusion, both high and low dose metformin can effectively control blood glucose
in elderly male patients with type 2 diabetes mellitus. Comparatively, a high dosage of
metformin may help to improve BMD and bone metabolism. However, the influence
of high metformin concentration in inhibiting bone formation should be cautioned.
Further studies are needed to assess the optimum dosage of metformin.

ARTICLE HIGHLIGHTS
Research background
Patients with diabetes mellitus may develop skeletal complications including
osteopenia, osteoporosis and even fracture. Although metformin is used as an
antidiabetic rather than an antiosteoporotic medicine, it is essential to examine the
effects of metformin on bone metabolism because it is a widely used medication to
treat diabetes in this population.

Research motivation
By comparing different doses of metformin on bone metabolism and bone mineral
density (BMD) in patients with type 2 diabetes, the optimal dose of metformin will be
estimated to achieve the benefits of bone protection beyond glycemic control.

Research objectives
The aim of this study is to compare the effects of a high dose vs low dose of metformin
on BMD and bone metabolism in patients with type 2 diabetes mellitus.

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 Wang LX et al. Is high dose of metformin good for BMD?

Research methods
One hundred and twenty patients with type 2 diabetes were enrolled in the study.
They were assigned to a high dose metformin group (2 g daily) and a low dose
metformin group (1 g daily) with 60 patients in each group for 12 wk. Changes in
BMD and bone metabolism as well as the efficacy of the treatment were compared
between the two groups before and after treatment.

Research results
The results showed that there was no significant difference in the treatment efficacy
between the two treatment groups. After the treatment, levels of BMD and bone
metabolic markers were improved. To be specific, levels of BMD and 25-
hydroxyvitamin D were higher in the high dose metformin group than in the low dose
metformin group. However, levels of N-terminal midfragment and β-isomerized C-
terminal telopeptides were lower in the high dose metformin group than in the low
dose metformin group.

Research conclusions
A high dosage of metformin can help to improve osteoporosis as well as control blood
glucose in elderly male patients with type 2 diabetes mellitus.

Research perspectives
The effects of metformin on BMD and bone metabolism should be further evaluated in
long-term observational studies with large sample sizes.

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