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JOURNAL OF CLINICAL MEDICINE OF KAZAKHSTAN
Озык, Макала / Оригинальная Статья / Original Article DOI: 10.23950/1812-2892-JCMK-00690
Frequency and independent risk factors of sarcopenia in type 2 diabetes
Bahar Ozdemir1, Pinar Karakaya2, Bulent Yaprak1, Hakan Kocoglu1
Abstract
Background: Diabetes is a growing public health problem with the increasing obesity prevalence, and aging world population. Many comorbidities, frailty, and deteriorations in both quality of life and the health status of these patients are associated with a compound outcome of increased body mass index, aging and sarcopenia. Sarcopenia has particular importance, since it is both a cause and an outcome in these patients.
Aim: The aim of this study is to evaluate the sarcopenia frequency, and to determine the independent predictors of sarcopenia in patients with type 2 diabetes.
Methods: Patients between 18 to 65 years of age that followed-up at the Endocrinology Department of Istanbul Bakirkoy Dr. Sadi Konuk Education and Research Hospital with a diagnosis of type 2 diabetes mellitus were evaluated retrospectively.
Results: A total of 86 patients (F/M 60/26) with a mean age of 52.9±12.4 years were included. Fifty-four patients (62.8%) had sarcopenia (70% of females and 46.2% of males; p=0.040), and albumin levels were significantly higher in those patients (p=0.037). Multivariate analyses revealed that females (OR: 3.9; p=0.020), and increased BMI (OR: 1.1 per unit increase; p=0.040), albumin (OR: 2.7 per unit increase; p=0.028) and LDL (OR: 1.02 per unit increase; p=0.016), and decreased Tg (OR: 1.01 per unit decrease; p=0.004) levels were independent determinants of sarcopenia.
Conclusion: Results of this current study confirmed the previous knowledge on the subject, moreover contributes to the available evidence with reporting the increased albumin as a novel risk factor for the sarcopenia. Keywords: sarcopenia, diabetes, frequency, risk factors
2 ТИП1 ^АНТ ДИАБЕТ1МЕН АУЫРАТЫН ПАЦИЕНТТЕРДЕ САРКОПЕНИЯ КЕЗДЕС1 ЖИ1Л1Г1 ЖЭНЕ ПАЙДА БОЛУ ЦАУПШЩ ТЭУЕЛС1З ФАКТОРЛАРЫ
Б. Оздемир1, П. Каракайя2, Б. Япрак1, Х. Кокоглу1
Чшю медицина бeлiмi, дэртер Сади Конук атындагы Ыстамбул Бакыркёй гылыми-зерттеу клиникасы, Ыстамбул, ТYркия
2Эндокринология бeлiмi, дэртер Сади Конук атындагы Ыстамбул Бакыркёй гылыми-зерттеу клиникасы, Ыстамбул, Туркия
Т¥ЖЫРЫМДАМА
Кiрiсnе: Диабет — бул элем халкыныц семiруi мен картаюын кец таратып келе жатырган когамдык денсаулык сактаудыц ^н сайын KYPделенiп келе жаткан проблемасы болып табылады. Бул аурумен ауыратын пациенттердщ кептеген iлеспе аурулары, элаздИ жэне вмiр сапасы мен денсаулык жагдайыныц нашарлауы агза салмагыныц кебеюiмен, картаюмен жэне саркопениямен байланысты. Саркопения ерекше мацызга ие, вйткенi ол осы пациенттер ауруыныц себебi де, нэтижес де болып табылады.
Максаты: Осы зерттеудщ максаты саркопенияныц кездесу жшлИн багалау жэне 2 типт диабетпен ауыратын пациенттерде тэуелсiз болжамдык факторларды айкындау болып табылады.
Эдютерк Дэрiгер Сади Конук атындагы Ыстамбул Бакыркёй гылыми-зерттеу клиникасыныц Эндокринология белiмiнде 2 типтi кант диабетi диагнозымен емделген 18 жэне 65 жас аральиындагы пациенттер осы ретроспективтi зерттеуге енгiзiлдi.
Нэтижелерi: Зерттеуге барлшы 86 пациент енпз^ (э/е:60/26), орташа жастары 52.9±12.4 жас курады. Елу терт пациентте (62.8%) саркопения болды (70% эйелдер жэне 46.2% ерлер; р=0.040), сондай-ак бул пациенттерде альбумин децгеш айтарлыктай жогары болды (р=0.037). Кеп факторлы талдау саркопенияныц тэуелсiз керсеташп^ мыналар болганын кврсеттi: эйелдер (OR: 3.9; р=0.020), дене салмагыныц улгайган индексi (OR: 1.1 бiрлiкке улгаю; р=0.040), альбумин децгейлерi (OR: 2.7 бiрлiкке улгаю; р=0.028) жэне ЛПНП (OR: 1.02 бiрлiкке улгаю; р=0.016), жэне Тг темендеген децгеш OR: 1.01 бiрлiкке улгаю; р=0.004).
Корытынды: Осы зерттеу нэтижелерi пэн бойынша бурын алган бiлiмдердi тиянактады, одан белек альбуминнщ жогарылаган децгей саркопенияныц кауiп факторы болып табылатынына дэлел кел^ру Yшiн Yлес косады.
Непзп свздер: саркопения, кант диабетi, кездесу жиiлiгi, кауiп факторлары
'Department of Internal Medicine, Bakirkoy Dr. Sadi Konuk Education and Research Hospital, Istanbul, Turkey 2Department of Endocrinology and Metabolic Diseases, Bakirkoy Dr. Sadi Konuk Education and Research Hospital, Istanbul, Turkey
© ®
This work is licensed under a Creative Commons Attribution 4.0 International License
Received: 2019-06-01 Accepted: 2019-06-13 UDC: 616.1
J Clin Med Kaz 2019;3(53):16-20
Corresponding Author: Hakan Kocoglu, MD, Department of Internal Medicine, Bakirkoy Dr. Sadi Konuk Education and Research Hospital, Istanbul, Turkey. Tel.: +90-506-3809215 E-mail: [email protected]
ЧАСТОТА ВСТРЕЧАЕМОСТИ И НЕЗАВИСИМЫЕ ФАКТОРЫ РИСКА САРКОПЕНИИ У ПАЦИЕНТОВ С САХАРНЫМ ДИАБЕТОМ 2 ТИПА Б. Оздемир1, П. Каракайя2, Б. Япрак1, Х. Кокоглу1
'Отделение внутренней медицины, Стамбульская научно-исследовательская клиника Бакыркёй имени доктора Сади Конук, Стамбул, Турция Ютделение эндокринологии, Стамбульская научно-исследовательская клиника Бакыркёй имени доктора Сади Конук, Стамбул, Турция
РЕЗЮМЕ
Введение: Диабет — это растущая проблема общественного здравоохранения с увеличивающейся распространенностью ожирения и старения населения мира. Многие сопутствующие заболевания, уязвимость и ухудшения как в качестве жизни, так и состоянии здоровья этих пациентов связаны со сложным исходом увеличенного индекса массы тела, старения и саркопении. Саркопения имеет особое значение, так как это является и причиной и исходом заболевания данных пациентов.
Цель: Целью данного исследования является оценка частоты встречаемости саркопении, и определение независимых прогностических факторов саркопении у пациентов с диабетом 2 типа.
Методы: Пациенты в возрасте от 18 до 65 лет, которые наблюдались в отделении эндокринологии Стамбульской научно-исследовательской клиники Бакыркёй имени доктора Сади Конук с диагнозом сахарный диабет 2 типа были включены в данное ретроспективное исследование.
Результаты: В исследование было включено всего 86 пациентов (ж/м: 60/26), средний возраст которых составил 52.9±12.4 года. У пя-тидесяти-четырех пациентов (62.8%) была саркопения (70% женщин и 46.2% мужчин; p=0.040), а также у этих пациентов уровень альбумина был значительно выше ф=0.037). Многофакторный анализ показал, что независимыми показателями саркопении оказались следующие: женщины (OR: 3.9; p=0.020), увеличенный индекс массы тела (OR: 1.1 увеличение на единицу; p=0.040), уровни альбумина (OR: 2.7 увеличение на единицу; p=0.028) и ЛПНП (OR: 1.02 увеличение на единицу; p=0.016), и сниженный уровень Тг (OR: 1.01 снижение на единицу; p=0.004).
Заключение: Результаты настоящего исследования подтвердили ранее полученные знания по предмету, более того они вносят вклад в имеющиеся доказательства, сообщая о том, что увеличенный уровень альбумина является новым фактором риска саркопении.
Ключевые слова: саркопения, сахарный диабет, частота встречаемости, факторы риска
Introduction
Excessive muscle loss and associated functional deteriorations are defined as sarcopenia [1]. Muscle loss is related with many diseases, but it can occur naturally due to aging, which is associated with deteriorated muscle functions. Under physiologic conditions, approximately 1% of the total muscle mass losses each year after 30 years-of-age [2]. With recent modifications, sarcopenia definition now includes decreased walking speed and grip strength along with the decreased muscle mass [3-5].
Current literature suggests that diabetics have an increased risk for development of sarcopenia [6]. Previous research on this topic has provided evidence about the effects of diabetes on muscle mass [7, 8]. Particularly for the patients with type 1 diabetes, insulin deprivation is the major stimulant for the increased catabolism of skeletal muscles [9, 10]. Despite the fact that the mechanism in type 2 diabetes is not so apparent like this, previous cross-sectional studies found that older diabetic adults have altered body composition and low skeletal muscle strength, and lost their knee extensor strength more rapidly than their non-diabetic counterparts [11]. Also, multivariate analyses assessing the associations between diabetes and sarcopenia controlling for the body-mass index (BMI) revealed that the difference between diabetics and non-diabetics regarding muscle density was significantly attenuated after adjustment for the BMI, which suggests that the fat density in the muscle mass was an important factor for the muscle dysfunctionality [12]. The aim of this study was to evaluate the frequency of sarcopenia in diabetic patients and evaluating the independent risk factors in sarcopenia.
Material and methods
This study was conducted at the Endocrinology Department of Istanbul Bakirkoy Dr. Sadi Konuk Education and Research Hospital. Patients with Type-2 diabetes between 18 to 65 years of age were searched from the patient records retrospectively. Demographic data including age and sex; anthropometric evaluations including height, weight and body mass index (BMI); and, laboratory analyses including routine biochemistry, complete blood count, 25-OH-vitamin D levels, neutrophil/ lymphocyte and platelet/lymphocyte ratios, and hemoglobin
A1c levels were recorded from the patient files. Cases below 18 years of age and older than 65 years of age were not included in the analyses.
Sarcopenia was diagnosed in patients according to the definitions of The European Working Group on Sarcopenia in Older People (EWGSOP).
Statistical Analysis
Descriptive data were presented as frequency and percent for categorical variables, and mean and standard deviation for numerical variables. Comparisons of data between patients with and without sarcopenia were performed with Mann-Whitney U test, and Chi-Square test for numerical and categorical variables, respectively. Independent predictors of sarcopenia were evaluated by a logistic regression model, and Omnibus test and Hosmer-Lemeshow tests were used to evaluate the model fit. A p value <0.05 was considered as statistically significant. All analyses were performed with SPSS 21 (IBM Inc., Armonk, NY, USA).
Results
A total of 86 patients (F/M 60/26) with a mean age of 52.9±12.4 years were evaluated retrospectively. The comparisons of demographic, anthropometric, and laboratory analyses between males and females revealed that ages of patients were similar, but metabolic ages were significantly lower in males (p=0.009). Males were taller (p<0.001), and had lower BMIs than females (p=0.017). Laboratory analyses revealed that TSH (p=0.004), fT4 (p=0.011), urea (p=0.003), uric acid (p=0.044), and creatinine (p<0.001) levels were higher in males. All other parameters were found to be similar between sexes (Table1).
The measurements regarding muscle mass revealed that 54 patients (62.8%) had sarcopenia. For the sex distribution, 70% of females had sarcopenia, whereas this was 46.2% for males, and the difference was statistically significant (p=0.040). Comparisons of other demographic characteristics, anthropometric measurements, and laboratory analyses between patients with and without sarcopenia revealed that only albumin levels were significantly higher in sarcopenia group (p=0.037) (Table 2).
Table 1
Comparison of general characteristics of patients between sexes
General characteristics of patients with and without sarcopenia
Male Female p Sarcopenia (-) Sarcopenia (+) p
n=26 n=60 n=32 n=54
Age 52±15.9 53.3±10.7 1.000 Sex 0.040
Metabolic age 54.4±15.7 64.2±11.9 0.009 Male 14 (53.8) 12 (46.2)
Height 169.5±7.3 159.7±5.4 0.000 Female 18 (30) 42 (70)
Age 52.8±13.7 52.9±11.7 0.792
Weight 94.1±27 91.2±16.7 0.873
Metabolic age 59.1±15.5 62.5±12.8 0.472
BMI 32.8±9.1 35.4±6.6 0.017 Height 162.2±8.7 162.9±6.8 0.693
25-OH-VitD3 20.6±13.6 21.9±16.8 1.000
Weight 87.9±17 94.5±21.7 0.344
TSH 5.1±2.7 3.3±2.3 0.004
fT4 2.1±0.7 1.7±0.5 0.011 BMI 25-OH-VitD3 32.9±6.9 23.8±16 35.6±7.7 20.2±15.7 0.180 0.255
WBC 9.1±4.1 8.7±2.2 0.862 TSH 3.9±2.6 3.8±2.5 0.879
Hgb 13.4±1.5 13.5±1.4 0.573 fT4 1.8±0.5 1.8±0.7 0.671
Htc 40.6±4.7 41.4±4.6 0.557 WBC 8.9±1.9 8.8±3.3 0.456
MPV 8±2 7.9±1.6 0.873 Hgb 13.5±1.5 13.5±1.4 0.876
MCV 84.5±9.2 87±4.7 0.229 Htc 40.9±5.1 41.3±4.4 0.652
Plt 289.5±82.4 281.7±71 0.602 MPV 7.9±1.9 7.9±1.6 0.251
Urea 40.8±18.8 30.6±11.5 0.003 MCV Plt 87±4.3 292±89.3 85.8±7.4 279.3±64.1 0.802 0.549
Uric acid 6.3±1.3 5.5±1.9 0.044 Urea 34.3±16 33.4±14.2 0.876
Creatinine 1.1±0.4 0.8±0.2 0.000 Uric acid 5.7±1.6 5.8±1.9 0.932
Albumin 3.4±0.6 3.4±0.6 0.589 Creatinine 0.9±0.5 0.8±0.2 0.655
CRP 3.4±5.2 1.8±1.4 0.789 Albumin 3.2±0.6 3.5±0.6 0.037
Cortisol 11.8±4.6 11.5±5.7 0.299 CRP 2.3±2.8 2.3±3.4 0.491
HgbA1c 8.1±1.3 8±1.6 0.679 Cortisol 10.8±3.8 12±6.1 0.617
LDL 145.1±29.2 135.8±38.9 0.323 HgbA1c LDL 8.4±1.6 134.3±37.3 7.9±1.5 141.2±35.8 0.086 0.442
HDL 39.5±10.4 41.7±13.2 0.785 HDL 37.4±9.6 43.2±13.4 0.055
Tg 259.5±130.9 260.4±128.3 0.796 Tg 293.2±146.1 240.5±113.5 0.133
Homocysteine 39.6±29.2 51.2±36.9 0.165 Homocysteine 46.1±34.5 48.7±35.6 0.626
HOMA-IR 12.4±8.5 11.8±8.3 0.689 HOMA-IR 12.5±9.3 11.7±7.7 0.979
FBG 165.8±88.3 151.3±78.5 0.478 FBG 171.8±93.7 146.1±72.4 0.221
PLR 22.2±4.5 22.1±3.8 0.847 PLR 21.7±4.1 22.4±3.9 0.294
NLR 1.9±2.6 1.4±2.3 0.789 NLR 1.9±2.8 1.4±2.2 0.288
Fasting insulin 14.6±7.7 14.8±8.1 0.959 Fasting insulin 15.1±8.5 14.6±7.7 0.813
The independent determinants of sarcopenia were evaluated by a stepwise logistic regression model, with the possible prognostic factors from univariate analyses including sex, age, BMI, albumin, LDL, HDL, TG, TSH, 25-OH-and VitD3. Final model revealed that females (OR: 3.9; p=0.020), and increased BMI (OR: 1.1 per unit increase; p=0.040), albumin (OR: 2.7 per unit increase; p=0.028) and LDL (OR: 1.02 per unit increase; p=0.016), and decreased Tg (OR: 1.01 per unit decrease; p=0.004) levels were independent determinants of sarcopenia. The final model was found to be valid and fit (Omnibus test p<0.05; Hosmer-Lemeshow test p>0.05) (Table 3).
Discussion
In parallel to the increasing obesity prevalence and aging of the world population, the prevalence of type 2 diabetes is also increasing progressively. The Turkish Statistical Institute released the population statistics of 2016 recently, and reported that the proportion of population over 65 years is 8.3% in Turkey [13]. Another recent report by this institution was the recent health survey of Turkey in 2016, which revealed that the obesity prevalence is 19.6% over 15 years of age (23.9% for women, and 15.2% for men) [14]. For the same time period, Ministry
Independent predictors for sarcopenia
OR
95% CI
Initial model
Sex (female vs. male) 4.943 1.407 ■ ■ 17.366 0.013
Age 0.994 0.951 ■ ■ 1.04 0.807
BMI 1.089 0.996 ■ ■ 1.19 0.061
Albumin 2.224 0.874 ■ ■ 5.662 0.094
HDL 1.029 0.977 ■ ■ 1.083 0.283
LDL 1.021 1.003 ■ ■ 1.039 0.021
Tg 0.991 0.986 ■ ■ 0.997 0.004
TSH 1.179 0.918 ■ ■ 1.514 0.197
25-OH-VitD3 1.005 0.972 ■ ■ 1.039 0.772
Constant 0.008 - 0.015
model
Sex (female vs. male) 3.903 1.244 ■ ■ 12.242 0.020
BMI 1.090 1.004 ■ ■ 1.183 0.040
Albumin 2.656 1.112 ■ ■ 6.342 0.028
LDL 1.021 1.004 ■ ■ 1.039 0.016
Tg (per unit decrease) 1.008 1.003 ■ ■ 1.013 0.004
Constant 0.001 - 0.005
of Health reported that the prevalence of diabetes mellitus over 15 years of age was 9.1% (10.9% for females, and 7.1% for males) [15]. As can be seen from these figures, obesity and type 2 diabetes possess a significant health burden in Turkey, as in the rest of the World. The consequences of combination of aging, obesity, and diabetes may be debilitating for the patients. Some of these are deteriorated quality of life, decreased mobility, and increased rates of comorbidities associated with these health problems including sarcopenia. In this study, we have evaluated the independent determinants of sarcopenia in patients with diabetes, which is important for identification of preventive measures, particularly prior to the onset of the disease.
With the recent modifications in the definition of the sarcopenia, now it includes the decreased muscle mass, and the decreased strength and functionality [16]. Historically, aging-related functional deteriorations were thought to be associated with significantly decreased muscle mass, but research on the topic showed that functional decline is much more related with loss in muscle strength than the muscle mass [17]. These physiological changes may be monitored by routine evaluation methods including clinical and biochemical assessments, and may be accounted as independent determinants of sarcopenia. Our analyses for evaluating this hypothesis revealed that diabetic patients with sarcopenia were predominantly female, and had elevated albumin levels in the univariate analyses. Muscle loss with increasing age is more pronounced for males in the literature. For the situations like aging and/or other diseases, testosterone deficiency is more associated with a catabolic response, which also plays a major role for sarcopenia [18]. On the other hand, estrogen deficiency was found to be more related with sarcopenia particularly in postmenopausal women [17]. In our study, we have not evaluated if the women were pre- or post-menopausal, but our analyses revealed the female predominance in the sarcopenia group. This may also be associated with the nutritional status, obesity or body fat composition, and mobility and exercise status of the patients.
Secondly, we found that albumin levels were increased in patients with sarcopenia. The albumin levels in elderly patients are commonly measured for the assessment of nutritional status or disease severity [19]. The current evidence suggests that serum albumin levels may decrease in stress conditions, renal diseases, liver diseases, inflammation and following surgical interventions [20, 21]. Since it is biologically plausible for using this biomarker for assessment of muscle mass, the literature data
and currently available evidence do not suggest its utilization for this purpose [22]. Nevertheless, previous studies showed a decline in albumin levels in conditions with muscle loss. This is contradictory to our results that showed that patients with sarcopenia had elevated levels of albumin levels. But, despite the statistical significance between the albumin levels of patients with and without sarcopenia, the difference was not clinically meaningful.
The multivariate analyses for evaluating the independent determinants of sarcopenia showed that female gender, increased BMI, albumin, and LDL levels, and decreased triglyceride levels were associated with increased sarcopenia risk. BMI and increased fat levels were found to be associated with the muscle loss and sarcopenia in previous studies. Our patients were all diabetics, and diabetes itself is known as a major risk factor for functional disability, obesity, and immobility. The body fat composition significantly changes in these patients, and possess a risk for the muscle loss. Another mechanism is the insulin resistance, which also increases with aging, and defective insulin signaling can lead to reduced muscle synthesis and functioning [23]. Moreover, these patients are prone to increased oxidative stress, and this may also an underlying mechanism of the development of sarcopenia [24]. Other contributors of sarcopenia in this patient group may include sex hormone changes, [25] IGF-1 status [26], and aging-related functional loss in neuronal network and impaired re-innervation [27]. According to our results, elevated cholesterol levels and increased BMI are significant contributors to sarcopenia. But increased albumin levels as a risk factor is a striking finding, which has not been reported previously, and should be confirmed in prospective studies.
Conclusion
Results of this current study confirmed the previous knowledge on the subject, moreover contributes to the available evidence with reporting the increased albumin as a novel risk factor for the sarcopenia.
The major limitation of this study is the retrospective design, which constrains us to make further conclusions. Thus, our striking finding of albumin as a potential risk factor of sarcopenia in diabetic patients should need confirmation in prospective studies with large sample sizes.
Disclosures: There is no conflict of interest for all authors.
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How to cite this article: Bahar Ozdemir, Pinar Karakaya, Bulent Yaprak, Hakan Kocoglu. Frequency and independent risk factors of sarcopenia in type 2 diabetes. J Clin Med Kaz. 2019; 3(53):16-20
