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Связь фактора роста фибробластов 21 с метаболическим фенотипом и жировыми депо у лиц молодого возраста с абдоминальным ожирением
Связь фактора роста фибробластов 21 с метаболическим фенотипом и жировыми депо у лиц молодого возраста с абдоминальным ожирением
Железнова Е.А., Жернакова Ю.В., Шария М.А. и др. Связь фактора роста фибробластов 21 с метаболическим фенотипом и жировыми депо у лиц молодого возраста с абдоминальным ожирением. Consilium Medicum. 2020; 22 (12): 23–30. DOI: 10.26442/20751753.2020.12.200560
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Аннотация
Фактор роста фибробластов 21 (FGF21) – гормоноподобный белок, участвующий в регулировании энергетического баланса и гомеостаза глюкозы и липидов. Исследование ассоциации данного фактора с метаболическим фенотипом – метаболически здоровым (МЗАО) и метаболически нездоровым абдоминальным ожирением (АО) и разными жировыми депо (висцеральным, подкожным, эпикардиальным, периваскулярным) у лиц молодого возраста представляет несомненный научный и практический интерес.
Цель. Определить уровень FGF21 в сыворотке крови и сопоставить с распределением жировой ткани у лиц молодого возраста с АО.
Материалы и методы. В исследование включены 132 человека (средний возраст 37,59±6,35 года). Сформированы 3 группы: 0-я – 16 условно здоровых добровольцев; 1-я – 46 человек 40 лет [34; 43] с МЗАО; 2-я – 70 человек с метаболическим синдромом (МС) 40 лет [35; 44]. Всем исследуемым проведены измерение роста, массы тела, окружности талии, расчет индекса массы тела. Оценивались уровень FGF21 (ELISA KIT, BCM Diagnostics, Германия), липидный профиль, глюкоза, 2-часовой тест толерантности к глюкозе, инсулин, лептин, адипонектин, HOMA-IR. Выполнено суточное мониторирование артериального давления. Определены объемы подкожного, висцерального, периваскулярного, эпикардиального жира, отношение подкожного жира к висцеральному по данным компьютерной томографии. Дополнительно для субанализа, в зависимости от наличия АО и количества факторов риска (ФР), все пациенты (132 человека, средний возраст 37,59±6,35 года) были распределены на 6 групп: АО-0/ФР-0 (n=16); АО-1/ФР-0 (n=3); АО-1/ФР-1 (n=40); АО-1/ФР-2 (n=37); АО-1/ФР-3 (n=14); АО-1/ФР-4 (n=5). В каждой группе оценивался уровень FGF21.
Результаты. Уровень FGF21 был достоверно выше в группах лиц с МЗАО (294,4 пг/мл) и МС (245,7 пг/мл) в сравнении с контрольной группой (110,2 пг/мл); p=0,04 и p=0,05 соответственно. По результатам корреляционного анализа были выявлены достоверные слабые связи FGF21 c возрастом (r=0,22, p≤0,05), окружностью талии (r=0,18, p≤0,05), окружностью бедер (r=0,26, p≤0,05), индексом массы тела (r=0,3, p≤0,01). Выявлена связь FGF21 с висцеральным (r=0,2, p≤0,05) и подкожным (r=0,2, p≤0,05) жировыми депо. Зарегистрирована достоверная связь FGF21 c триглицеридами (r=0,21, p≤0,05) и лептином (r=0,24, p≤0,05). Уровень FGF21≥345,8 пг/мл отражал увеличение риска МС у лиц молодого возраста в 3 раза (AuROC 0,74, чувствительность 78,6%, специфичность 75,0%, p<0,0001). Уровень FGF21≥294,4 пг/мл был маркером риска МЗАО (AuROC 0,70, чувствительность 67,4%, специфичность 75,0%, p<0,0001). По результатам субанализа выявлено достоверное (p<0,01) повышение концентрации FGF21 в группах с увеличением количества компонентов МС.
Заключение. Уровень FGF21 увеличивается с ухудшением метаболического фенотипа, его повышение наблюдается задолго до формирования МС (у лиц с МЗАО). FGF21 у лиц молодого возраста ассоциирован с висцеральным и подкожным жировыми депо, с уровнем триглицеридов и лептином. Уровень FGF21≥345,8 пг/мл может быть рассмотрен в качестве предиктора МС у лиц молодого возраста, однако требуются дальнейшие исследования.
Ключевые слова: фактор роста фибробластов 21, FGF21, ожирение, метаболический синдром, абдоминальное ожирение, висцеральное ожирение, жир, жировые депо, висцеральный жир, подкожный жир, периваскулярный жир, периаортальный жир, компьютерная томография, адипонектин, лептин, инсулин.
Aim. To determine serum FGF21 levels and match it with the distribution of adipose tissue in young people with AO.
Outcomes and methods. The study enrolled 132 people (mean age 37.59±6.35 years). 3 groups were formed: 0th – 16 conditionally healthy volunteers; 1st – 46 people of 40 years [34; 43] with MHAO; 2nd – 70 people of 40 years [35; 44] with metabolic syndrome (MS). All subjects underwent measurement of height, body weight, waist circumference, calculation of body mass index. The FGF21 levels (ELISA KIT, BCM Diagnostics, Germany), lipid profile, 2-hour glucose tolerance test, glucose, insulin, leptin, adiponectin levels and HOMA-IR were assessed. Daily monitoring of blood pressure was performed. The volumes of subcutaneous, visceral, perivascular, epicardial fat, as well as subcutaneous fat to visceral fat ratio were determined with computed tomography. Additionally, for subanalysis, all patients (132 people, mean age 37.59±6.35 years) were divided into 6 groups depending on the presence of AO and the number of risk factors (RF): AO-0/FR-0 (n=16); AO-1/FR-0 (n=3); AO-1/FR-1 (n=40); AO-1/FR-2 (n=37); AO-1/FR-3 (n=14); AO-1/FR-4 (n=5). In each group, FGF21 levels was assessed.
Results. The FGF21 levels was significantly higher in the groups of persons with MHAO (294.4 pg/ml) and MS (245.7 pg/ml) compared with the control group (110.2 pg/ml); p=0.04 and p=0.05, respectively. According to the correlation analysis data, there was significant weak association of FGF21 with age (r=0.22, p≤0.05), waist circumference (r=0.18, p≤0.05), hip circumference (r=0.26, p≤0.05), body mass index (r=0.3, p≤0.01). FGF21 was found to be associated with visceral (r=0.2, p≤0.05) and subcutaneous (r=0.2, p≤0.05) fat depots. A significant association of FGF21 with triglycerides (r=0.21, p≤0.05) and leptin (r=0.24, p≤0.05) was registered. The FGF21 level ≥345.8 pg/ml reflected a 3-fold increase in the risk of MS in young people (AuROC 0.74, sensitivity 78.6%, specificity 75.0%, p<0.0001). The FGF21 levels ≥294.4 pg/ml was a risk marker for MHAO (AuROC 0,70, sensitivity 67.4%, specificity 75.0%, p<0.0001). According to the results of subanalysis, a significant (p<0.01) increase in the FGF21 concentration was revealed in the groups with an increase in the number of MS components.
Conclusions. The FGF21 levels increases with the worsening of the metabolic phenotype; its increase is seen long before the formation of MS (in persons with MHAO). FGF21 in young people is associated with visceral and subcutaneous fat depots, triglyceride levels and leptin. FGF21≥345.8 pg/ml can be considered a predictor of MS in young people, but further research is required.
Key words: fibroblast growth factor 21, FGF21, obesity, metabolic syndrome, abdominal obesity, visceral obesity, fat, fat depots, visceral fat, subcutaneous fat, perivascular fat, periaortic fat, computed tomography, adiponectin, leptin, insulin.
Цель. Определить уровень FGF21 в сыворотке крови и сопоставить с распределением жировой ткани у лиц молодого возраста с АО.
Материалы и методы. В исследование включены 132 человека (средний возраст 37,59±6,35 года). Сформированы 3 группы: 0-я – 16 условно здоровых добровольцев; 1-я – 46 человек 40 лет [34; 43] с МЗАО; 2-я – 70 человек с метаболическим синдромом (МС) 40 лет [35; 44]. Всем исследуемым проведены измерение роста, массы тела, окружности талии, расчет индекса массы тела. Оценивались уровень FGF21 (ELISA KIT, BCM Diagnostics, Германия), липидный профиль, глюкоза, 2-часовой тест толерантности к глюкозе, инсулин, лептин, адипонектин, HOMA-IR. Выполнено суточное мониторирование артериального давления. Определены объемы подкожного, висцерального, периваскулярного, эпикардиального жира, отношение подкожного жира к висцеральному по данным компьютерной томографии. Дополнительно для субанализа, в зависимости от наличия АО и количества факторов риска (ФР), все пациенты (132 человека, средний возраст 37,59±6,35 года) были распределены на 6 групп: АО-0/ФР-0 (n=16); АО-1/ФР-0 (n=3); АО-1/ФР-1 (n=40); АО-1/ФР-2 (n=37); АО-1/ФР-3 (n=14); АО-1/ФР-4 (n=5). В каждой группе оценивался уровень FGF21.
Результаты. Уровень FGF21 был достоверно выше в группах лиц с МЗАО (294,4 пг/мл) и МС (245,7 пг/мл) в сравнении с контрольной группой (110,2 пг/мл); p=0,04 и p=0,05 соответственно. По результатам корреляционного анализа были выявлены достоверные слабые связи FGF21 c возрастом (r=0,22, p≤0,05), окружностью талии (r=0,18, p≤0,05), окружностью бедер (r=0,26, p≤0,05), индексом массы тела (r=0,3, p≤0,01). Выявлена связь FGF21 с висцеральным (r=0,2, p≤0,05) и подкожным (r=0,2, p≤0,05) жировыми депо. Зарегистрирована достоверная связь FGF21 c триглицеридами (r=0,21, p≤0,05) и лептином (r=0,24, p≤0,05). Уровень FGF21≥345,8 пг/мл отражал увеличение риска МС у лиц молодого возраста в 3 раза (AuROC 0,74, чувствительность 78,6%, специфичность 75,0%, p<0,0001). Уровень FGF21≥294,4 пг/мл был маркером риска МЗАО (AuROC 0,70, чувствительность 67,4%, специфичность 75,0%, p<0,0001). По результатам субанализа выявлено достоверное (p<0,01) повышение концентрации FGF21 в группах с увеличением количества компонентов МС.
Заключение. Уровень FGF21 увеличивается с ухудшением метаболического фенотипа, его повышение наблюдается задолго до формирования МС (у лиц с МЗАО). FGF21 у лиц молодого возраста ассоциирован с висцеральным и подкожным жировыми депо, с уровнем триглицеридов и лептином. Уровень FGF21≥345,8 пг/мл может быть рассмотрен в качестве предиктора МС у лиц молодого возраста, однако требуются дальнейшие исследования.
Ключевые слова: фактор роста фибробластов 21, FGF21, ожирение, метаболический синдром, абдоминальное ожирение, висцеральное ожирение, жир, жировые депо, висцеральный жир, подкожный жир, периваскулярный жир, периаортальный жир, компьютерная томография, адипонектин, лептин, инсулин.
________________________________________________
Aim. To determine serum FGF21 levels and match it with the distribution of adipose tissue in young people with AO.
Outcomes and methods. The study enrolled 132 people (mean age 37.59±6.35 years). 3 groups were formed: 0th – 16 conditionally healthy volunteers; 1st – 46 people of 40 years [34; 43] with MHAO; 2nd – 70 people of 40 years [35; 44] with metabolic syndrome (MS). All subjects underwent measurement of height, body weight, waist circumference, calculation of body mass index. The FGF21 levels (ELISA KIT, BCM Diagnostics, Germany), lipid profile, 2-hour glucose tolerance test, glucose, insulin, leptin, adiponectin levels and HOMA-IR were assessed. Daily monitoring of blood pressure was performed. The volumes of subcutaneous, visceral, perivascular, epicardial fat, as well as subcutaneous fat to visceral fat ratio were determined with computed tomography. Additionally, for subanalysis, all patients (132 people, mean age 37.59±6.35 years) were divided into 6 groups depending on the presence of AO and the number of risk factors (RF): AO-0/FR-0 (n=16); AO-1/FR-0 (n=3); AO-1/FR-1 (n=40); AO-1/FR-2 (n=37); AO-1/FR-3 (n=14); AO-1/FR-4 (n=5). In each group, FGF21 levels was assessed.
Results. The FGF21 levels was significantly higher in the groups of persons with MHAO (294.4 pg/ml) and MS (245.7 pg/ml) compared with the control group (110.2 pg/ml); p=0.04 and p=0.05, respectively. According to the correlation analysis data, there was significant weak association of FGF21 with age (r=0.22, p≤0.05), waist circumference (r=0.18, p≤0.05), hip circumference (r=0.26, p≤0.05), body mass index (r=0.3, p≤0.01). FGF21 was found to be associated with visceral (r=0.2, p≤0.05) and subcutaneous (r=0.2, p≤0.05) fat depots. A significant association of FGF21 with triglycerides (r=0.21, p≤0.05) and leptin (r=0.24, p≤0.05) was registered. The FGF21 level ≥345.8 pg/ml reflected a 3-fold increase in the risk of MS in young people (AuROC 0.74, sensitivity 78.6%, specificity 75.0%, p<0.0001). The FGF21 levels ≥294.4 pg/ml was a risk marker for MHAO (AuROC 0,70, sensitivity 67.4%, specificity 75.0%, p<0.0001). According to the results of subanalysis, a significant (p<0.01) increase in the FGF21 concentration was revealed in the groups with an increase in the number of MS components.
Conclusions. The FGF21 levels increases with the worsening of the metabolic phenotype; its increase is seen long before the formation of MS (in persons with MHAO). FGF21 in young people is associated with visceral and subcutaneous fat depots, triglyceride levels and leptin. FGF21≥345.8 pg/ml can be considered a predictor of MS in young people, but further research is required.
Key words: fibroblast growth factor 21, FGF21, obesity, metabolic syndrome, abdominal obesity, visceral obesity, fat, fat depots, visceral fat, subcutaneous fat, perivascular fat, periaortic fat, computed tomography, adiponectin, leptin, insulin.
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Список литературы
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4. Hong ES et al. Plasma fibroblast growth factor 21 levels increase with ectopic fat accumulation and its receptor levels are decreased in the visceral fat of patients with type 2 diabetes. BMJ Open Diabetes Res Care 2019; 7 (1). DOI: 10.1136/bmjdrc-2019-000776
5. Bobbert T et al. Fibroblast growth factor 21 predicts the metabolic syndrome and type 2 diabetes in Caucasians. Diabetes Care 2013; 36 (1): 145–9. DOI: 10.2337/dc12-0703
6. Chen C et al. High plasma level of fibroblast growth factor 21 is an independent predictor of type 2 diabetes: A 5.4-year population-based prospective study in Chinese subjects. Diabetes Care 2011; 34 (9): 2113–5. DOI: 10.2337/dc11-0294
7. Zhang X et al. Serum FGF21 levels are increased in obesity and are independently associated with the metabolic syndrome in humans. Diabetes 2008; 57 (5): 1246–53. DOI: 10.2337/db07-1476
8. Tan BK, Hallschmid M, Adya R et al. Fibroblast growth factor 21 (FGF21) in human cerebrospinal fluid: Relationship with plasma FGF21 and body adiposity. Diabetes 2011; 60 (11): 2758–62. DOI: 10.2337/db11-0672
9. Akyildiz ZI et al. Epicardial fat, body mass index, and triglyceride are independent contributors of serum fibroblast growth factor 21 level in obese premenopausal women. J Endocrinol Invest 2015; 38 (3): 361–6. DOI: 10.1007/s40618-014-0185-3
10. Giannini C et al. Circulating levels of FGF-21 in obese youth: Associations with liver fat content and markers of liver damage. J Clin Endocrinol Metab 2013; 98 (7): 2993–3000. DOI: 10.1210/jc.2013-1250
11. Domouzoglou EM et al. Fibroblast growth factors in cardiovascular disease: The emerging role of FGF21. Am J Physiol Hear Circ Physiol 2015; 309: 1029–38. DOI: 10.1152/ajpheart.00527.2015
12. Lakhani I et al. Fibroblast growth factor 21 in cardio-metabolic disorders: a systematic review and meta-analysis. Metabolism 2018; 83: 11–7. DOI: 10.1016/j.metabol.2018.01.017
13. Zhang W, Chu S, Ding W, Wang F. Serum level of fibroblast growth factor 21 is independently associated with acute myocardial infarction. PLoS One 2015; 10 (6). DOI: 10.1371/journal.pone.0129791
14. Xu P et al. Efficacy of a combination of high and low dosage of PEGylated FGF-21 in treatment of diabetes in db/db mice. Biomed Pharmacother 2016; 84: 97–105. DOI: 10.1016/j.biopha.2016.09.019
15. Geng L, Lam KSL, Xu A. The therapeutic potential of FGF21 in metabolic diseases: from bench to clinic. Nat Rev Endocrinol Nat Res 2020. DOI: 10.1038/s41574-020-0386-0
16. Ritchie M, Hanouneh IA, Noureddin M et al. Fibroblast growth factor (FGF)-21 based therapies: A magic bullet for nonalcoholic fatty liver disease (NAFLD)? Exp Opin Investig Drugs 2020; 29 (2): 197–204. DOI: 10.1080/13543784.2020.1718104
17. Ye X et al. Pharmacological efficacy of FGF21 analogue, liraglutide and insulin glargine in treatment of type 2 diabetes. J Diabetes Complications 2017; 31 (4): 726–34. DOI: 10.1016/j.jdiacomp.2017.01.008
18. Ross R et al. Waist circumference as a vital sign in clinical practice: a Consensus Statement from the IAS and ICCR Working Group on Visceral Obesity. Nat Rev Endocrinol 2020; 16 (3): 177–89. DOI: 10.1038/s41574-019-0310-7
19. Fisher FM et al. Obesity is a fibroblast growth factor 21 (FGF21)-resistant state. Diabetes 2010; 59 (11): 2781–9. DOI: 10.2337/db10-0193
20. Hollstein T, Piaggi P. Metabolic Factors Determining the Susceptibility to Weight Gain: Current Evidence. Curr Obesity Rep 2020; 9: 121–35. DOI: 10.1007/s13679-020-00371-4
21. Markan KR. Defining ‘FGF21 Resistance’ during obesity: Controversy, criteria and unresolved questions version 1; referees: 1 approved, 2 approved with reservations. F1000Res 2018; 7. DOI: 10.12688/f1000research.14117.1
22. Tanajak P. Letter to the editor: Parameters, characteristics, and criteria for defining the term ‘fGF21 resistance. Endocrinology 2017; 158 (5): 1523–4. DOI: 10.1210/en.2017-00056
23. Britton KA et al. Prevalence, distribution, and risk factor correlates of high thoracic periaortic fat in the Framingham Heart Study. J Am Heart Assoc 2012; 1 (6). DOI: 10.1161/JAHA.112.004200
24. Sarin S et al. Clinical Significance of Epicardial Fat Measured Using Cardiac Multislice Computed Tomography. Am J Cardiol 2008; 102 (6): 767–71. DOI: 10.1016/j.amjcard.2008.04.058
25. Zhang X et al. Erratum: Serum FGF21 levels are increased in obesity and are independently associated with the metabolic syndrome in humans. Diabetes 2019; 68 (1): 235. DOI: 10.2337/db19-er01c
26. Shen Y et al. Additive relationship between serum fibroblast growth factor 21 level and coronary artery disease. Cardiovasc Diabetol 2013; 12 (1). DOI: 10.1186/1475-2840-12-124
27. Lee Y et al. Serum FGF21 concentration is associated with hypertriglyceridaemia, hyperinsulinaemia and pericardial fat accumulation, independently of obesity, but not with current coronary artery status. Clin Endocrinol (Oxf) 2014; 80 (1): 57–64. DOI: 10.1111/cen.12134
28. Shafaei Y, Khoshnia M, Marjani A. Serum level of fibroblast growth factor 21 in type 2 diabetic patients with and without metabolic syndrome. J Med Sci 2015; 15 (2): 80–6. DOI: 10.3923/jms.2015.80.86
29. Asrih M, Veyrat-Durebex C, Poher AL et al. Leptin as a potential regulator of FGF21. Cell Physiol Biochem 2016; 38 (3): 1218–25. DOI: 10.1159/000443070
30. Hanks LJ, Gutiérrez OM, Bamman MM et al. Circulating levels of fibroblast growth factor-21 increase with age independently of body composition indices among healthy individuals. J Clin Transl Endocrinol 2015; 2 (2): 77–82. DOI: 10.1016/j.jcte.2015.02.001
31. Matsui M et al. Relationship between physical activity and circulating fibroblast growth factor 21 in middle-aged and older adults. Exp Gerontol 2020; 141: 111081. DOI: 10.1016/j.exger.2020.111081
32. Woo YC et al. Serum fibroblast growth factor 21 is a superior biomarker to other adipokines in predicting incident diabetes. Clin Endocrinol 2017; 86 (1): 37–43. DOI: 10.1111/cen.13229
33. Li G et al. FGF21 deficiency is associated with childhood obesity, insulin resistance and hypoadiponectinaemia: The BCAMS Study. Diabetes Metab 2017; 43 (3): 253–60. DOI: 10.1016/j.diabet.2016.12.003
34. An SY et al. Serum fibroblast growth factor 21 was elevated in subjects with type 2 diabetes mellitus and was associated with the presence of carotid artery plaques. Diabetes Res Clin Pract 2012; 96 (2): 196–203. DOI: 10.1016/j.diabres.2012.01.004
35. Ferreira JP et al. Circulating plasma proteins and new-onset diabetes in a population-based study: Proteomic and genomic insights from the STANISLAS cohort. Eur J Endocrinol 2020; 183 (3): 285–95. DOI: 10.1530/EJE-20-0246
36. Lundsgaard AM et al. Circulating FGF21 in humans is potently induced by short term overfeeding of carbohydrates. Mol Metab 2017; 6 (1): 22–9. DOI: 10.1016/j.molmet.2016.11.001
37. Dushay JR, Toschi E, Mitten EK et al. Fructose ingestion acutely stimulates circulating FGF21 levels in humans. Mol Metab 2015; 4 (1): 51–7. DOI: 10.1016/j.molmet.2014.09.008
38. Laeger T et al. FGF21 is an endocrine signal of protein restriction. J Clin Invest 2014; 124 (9): 3913–22. DOI: 10.1172/JCI74915
39. Søberg S et al. FGF21 Is a Sugar-Induced Hormone Associated with Sweet Intake and Preference in Humans. Cell Metab 2017; 25 (5): 1045–53.e6. DOI: 10.1016/j.cmet.2017.04.009
2. Wang YS et al. Increased serum/plasma fibroblast growth factor 21 in type 2 diabetes mellitus: A systematic review and meta-analysis. Postgrad Med J 2019; 95 (1121). DOI: 10.1136/postgradmedj-2018-136002
3. Staiger H, Keuper M, Berti L et al. Fibroblast growth factor 21-metabolic role in mice and men. Endocrine Rev 2017; 38 (5): 468–88. DOI: 10.1210/er.2017-00016
4. Hong ES et al. Plasma fibroblast growth factor 21 levels increase with ectopic fat accumulation and its receptor levels are decreased in the visceral fat of patients with type 2 diabetes. BMJ Open Diabetes Res Care 2019; 7 (1). DOI: 10.1136/bmjdrc-2019-000776
5. Bobbert T et al. Fibroblast growth factor 21 predicts the metabolic syndrome and type 2 diabetes in Caucasians. Diabetes Care 2013; 36 (1): 145–9. DOI: 10.2337/dc12-0703
6. Chen C et al. High plasma level of fibroblast growth factor 21 is an independent predictor of type 2 diabetes: A 5.4-year population-based prospective study in Chinese subjects. Diabetes Care 2011; 34 (9): 2113–5. DOI: 10.2337/dc11-0294
7. Zhang X et al. Serum FGF21 levels are increased in obesity and are independently associated with the metabolic syndrome in humans. Diabetes 2008; 57 (5): 1246–53. DOI: 10.2337/db07-1476
8. Tan BK, Hallschmid M, Adya R et al. Fibroblast growth factor 21 (FGF21) in human cerebrospinal fluid: Relationship with plasma FGF21 and body adiposity. Diabetes 2011; 60 (11): 2758–62. DOI: 10.2337/db11-0672
9. Akyildiz ZI et al. Epicardial fat, body mass index, and triglyceride are independent contributors of serum fibroblast growth factor 21 level in obese premenopausal women. J Endocrinol Invest 2015; 38 (3): 361–6. DOI: 10.1007/s40618-014-0185-3
10. Giannini C et al. Circulating levels of FGF-21 in obese youth: Associations with liver fat content and markers of liver damage. J Clin Endocrinol Metab 2013; 98 (7): 2993–3000. DOI: 10.1210/jc.2013-1250
11. Domouzoglou EM et al. Fibroblast growth factors in cardiovascular disease: The emerging role of FGF21. Am J Physiol Hear Circ Physiol 2015; 309: 1029–38. DOI: 10.1152/ajpheart.00527.2015
12. Lakhani I et al. Fibroblast growth factor 21 in cardio-metabolic disorders: a systematic review and meta-analysis. Metabolism 2018; 83: 11–7. DOI: 10.1016/j.metabol.2018.01.017
13. Zhang W, Chu S, Ding W, Wang F. Serum level of fibroblast growth factor 21 is independently associated with acute myocardial infarction. PLoS One 2015; 10 (6). DOI: 10.1371/journal.pone.0129791
14. Xu P et al. Efficacy of a combination of high and low dosage of PEGylated FGF-21 in treatment of diabetes in db/db mice. Biomed Pharmacother 2016; 84: 97–105. DOI: 10.1016/j.biopha.2016.09.019
15. Geng L, Lam KSL, Xu A. The therapeutic potential of FGF21 in metabolic diseases: from bench to clinic. Nat Rev Endocrinol Nat Res 2020. DOI: 10.1038/s41574-020-0386-0
16. Ritchie M, Hanouneh IA, Noureddin M et al. Fibroblast growth factor (FGF)-21 based therapies: A magic bullet for nonalcoholic fatty liver disease (NAFLD)? Exp Opin Investig Drugs 2020; 29 (2): 197–204. DOI: 10.1080/13543784.2020.1718104
17. Ye X et al. Pharmacological efficacy of FGF21 analogue, liraglutide and insulin glargine in treatment of type 2 diabetes. J Diabetes Complications 2017; 31 (4): 726–34. DOI: 10.1016/j.jdiacomp.2017.01.008
18. Ross R et al. Waist circumference as a vital sign in clinical practice: a Consensus Statement from the IAS and ICCR Working Group on Visceral Obesity. Nat Rev Endocrinol 2020; 16 (3): 177–89. DOI: 10.1038/s41574-019-0310-7
19. Fisher FM et al. Obesity is a fibroblast growth factor 21 (FGF21)-resistant state. Diabetes 2010; 59 (11): 2781–9. DOI: 10.2337/db10-0193
20. Hollstein T, Piaggi P. Metabolic Factors Determining the Susceptibility to Weight Gain: Current Evidence. Curr Obesity Rep 2020; 9: 121–35. DOI: 10.1007/s13679-020-00371-4
21. Markan KR. Defining ‘FGF21 Resistance’ during obesity: Controversy, criteria and unresolved questions version 1; referees: 1 approved, 2 approved with reservations. F1000Res 2018; 7. DOI: 10.12688/f1000research.14117.1
22. Tanajak P. Letter to the editor: Parameters, characteristics, and criteria for defining the term ‘fGF21 resistance. Endocrinology 2017; 158 (5): 1523–4. DOI: 10.1210/en.2017-00056
23. Britton KA et al. Prevalence, distribution, and risk factor correlates of high thoracic periaortic fat in the Framingham Heart Study. J Am Heart Assoc 2012; 1 (6). DOI: 10.1161/JAHA.112.004200
24. Sarin S et al. Clinical Significance of Epicardial Fat Measured Using Cardiac Multislice Computed Tomography. Am J Cardiol 2008; 102 (6): 767–71. DOI: 10.1016/j.amjcard.2008.04.058
25. Zhang X et al. Erratum: Serum FGF21 levels are increased in obesity and are independently associated with the metabolic syndrome in humans. Diabetes 2019; 68 (1): 235. DOI: 10.2337/db19-er01c
26. Shen Y et al. Additive relationship between serum fibroblast growth factor 21 level and coronary artery disease. Cardiovasc Diabetol 2013; 12 (1). DOI: 10.1186/1475-2840-12-124
27. Lee Y et al. Serum FGF21 concentration is associated with hypertriglyceridaemia, hyperinsulinaemia and pericardial fat accumulation, independently of obesity, but not with current coronary artery status. Clin Endocrinol (Oxf) 2014; 80 (1): 57–64. DOI: 10.1111/cen.12134
28. Shafaei Y, Khoshnia M, Marjani A. Serum level of fibroblast growth factor 21 in type 2 diabetic patients with and without metabolic syndrome. J Med Sci 2015; 15 (2): 80–6. DOI: 10.3923/jms.2015.80.86
29. Asrih M, Veyrat-Durebex C, Poher AL et al. Leptin as a potential regulator of FGF21. Cell Physiol Biochem 2016; 38 (3): 1218–25. DOI: 10.1159/000443070
30. Hanks LJ, Gutiérrez OM, Bamman MM et al. Circulating levels of fibroblast growth factor-21 increase with age independently of body composition indices among healthy individuals. J Clin Transl Endocrinol 2015; 2 (2): 77–82. DOI: 10.1016/j.jcte.2015.02.001
31. Matsui M et al. Relationship between physical activity and circulating fibroblast growth factor 21 in middle-aged and older adults. Exp Gerontol 2020; 141: 111081. DOI: 10.1016/j.exger.2020.111081
32. Woo YC et al. Serum fibroblast growth factor 21 is a superior biomarker to other adipokines in predicting incident diabetes. Clin Endocrinol 2017; 86 (1): 37–43. DOI: 10.1111/cen.13229
33. Li G et al. FGF21 deficiency is associated with childhood obesity, insulin resistance and hypoadiponectinaemia: The BCAMS Study. Diabetes Metab 2017; 43 (3): 253–60. DOI: 10.1016/j.diabet.2016.12.003
34. An SY et al. Serum fibroblast growth factor 21 was elevated in subjects with type 2 diabetes mellitus and was associated with the presence of carotid artery plaques. Diabetes Res Clin Pract 2012; 96 (2): 196–203. DOI: 10.1016/j.diabres.2012.01.004
35. Ferreira JP et al. Circulating plasma proteins and new-onset diabetes in a population-based study: Proteomic and genomic insights from the STANISLAS cohort. Eur J Endocrinol 2020; 183 (3): 285–95. DOI: 10.1530/EJE-20-0246
36. Lundsgaard AM et al. Circulating FGF21 in humans is potently induced by short term overfeeding of carbohydrates. Mol Metab 2017; 6 (1): 22–9. DOI: 10.1016/j.molmet.2016.11.001
37. Dushay JR, Toschi E, Mitten EK et al. Fructose ingestion acutely stimulates circulating FGF21 levels in humans. Mol Metab 2015; 4 (1): 51–7. DOI: 10.1016/j.molmet.2014.09.008
38. Laeger T et al. FGF21 is an endocrine signal of protein restriction. J Clin Invest 2014; 124 (9): 3913–22. DOI: 10.1172/JCI74915
39. Søberg S et al. FGF21 Is a Sugar-Induced Hormone Associated with Sweet Intake and Preference in Humans. Cell Metab 2017; 25 (5): 1045–53.e6. DOI: 10.1016/j.cmet.2017.04.009
________________________________________________
2. Wang YS et al. Increased serum/plasma fibroblast growth factor 21 in type 2 diabetes mellitus: A systematic review and meta-analysis. Postgrad Med J 2019; 95 (1121). DOI: 10.1136/postgradmedj-2018-136002
3. Staiger H, Keuper M, Berti L et al. Fibroblast growth factor 21-metabolic role in mice and men. Endocrine Rev 2017; 38 (5): 468–88. DOI: 10.1210/er.2017-00016
4. Hong ES et al. Plasma fibroblast growth factor 21 levels increase with ectopic fat accumulation and its receptor levels are decreased in the visceral fat of patients with type 2 diabetes. BMJ Open Diabetes Res Care 2019; 7 (1). DOI: 10.1136/bmjdrc-2019-000776
5. Bobbert T et al. Fibroblast growth factor 21 predicts the metabolic syndrome and type 2 diabetes in Caucasians. Diabetes Care 2013; 36 (1): 145–9. DOI: 10.2337/dc12-0703
6. Chen C et al. High plasma level of fibroblast growth factor 21 is an independent predictor of type 2 diabetes: A 5.4-year population-based prospective study in Chinese subjects. Diabetes Care 2011; 34 (9): 2113–5. DOI: 10.2337/dc11-0294
7. Zhang X et al. Serum FGF21 levels are increased in obesity and are independently associated with the metabolic syndrome in humans. Diabetes 2008; 57 (5): 1246–53. DOI: 10.2337/db07-1476
8. Tan BK, Hallschmid M, Adya R et al. Fibroblast growth factor 21 (FGF21) in human cerebrospinal fluid: Relationship with plasma FGF21 and body adiposity. Diabetes 2011; 60 (11): 2758–62. DOI: 10.2337/db11-0672
9. Akyildiz ZI et al. Epicardial fat, body mass index, and triglyceride are independent contributors of serum fibroblast growth factor 21 level in obese premenopausal women. J Endocrinol Invest 2015; 38 (3): 361–6. DOI: 10.1007/s40618-014-0185-3
10. Giannini C et al. Circulating levels of FGF-21 in obese youth: Associations with liver fat content and markers of liver damage. J Clin Endocrinol Metab 2013; 98 (7): 2993–3000. DOI: 10.1210/jc.2013-1250
11. Domouzoglou EM et al. Fibroblast growth factors in cardiovascular disease: The emerging role of FGF21. Am J Physiol Hear Circ Physiol 2015; 309: 1029–38. DOI: 10.1152/ajpheart.00527.2015
12. Lakhani I et al. Fibroblast growth factor 21 in cardio-metabolic disorders: a systematic review and meta-analysis. Metabolism 2018; 83: 11–7. DOI: 10.1016/j.metabol.2018.01.017
13. Zhang W, Chu S, Ding W, Wang F. Serum level of fibroblast growth factor 21 is independently associated with acute myocardial infarction. PLoS One 2015; 10 (6). DOI: 10.1371/journal.pone.0129791
14. Xu P et al. Efficacy of a combination of high and low dosage of PEGylated FGF-21 in treatment of diabetes in db/db mice. Biomed Pharmacother 2016; 84: 97–105. DOI: 10.1016/j.biopha.2016.09.019
15. Geng L, Lam KSL, Xu A. The therapeutic potential of FGF21 in metabolic diseases: from bench to clinic. Nat Rev Endocrinol Nat Res 2020. DOI: 10.1038/s41574-020-0386-0
16. Ritchie M, Hanouneh IA, Noureddin M et al. Fibroblast growth factor (FGF)-21 based therapies: A magic bullet for nonalcoholic fatty liver disease (NAFLD)? Exp Opin Investig Drugs 2020; 29 (2): 197–204. DOI: 10.1080/13543784.2020.1718104
17. Ye X et al. Pharmacological efficacy of FGF21 analogue, liraglutide and insulin glargine in treatment of type 2 diabetes. J Diabetes Complications 2017; 31 (4): 726–34. DOI: 10.1016/j.jdiacomp.2017.01.008
18. Ross R et al. Waist circumference as a vital sign in clinical practice: a Consensus Statement from the IAS and ICCR Working Group on Visceral Obesity. Nat Rev Endocrinol 2020; 16 (3): 177–89. DOI: 10.1038/s41574-019-0310-7
19. Fisher FM et al. Obesity is a fibroblast growth factor 21 (FGF21)-resistant state. Diabetes 2010; 59 (11): 2781–9. DOI: 10.2337/db10-0193
20. Hollstein T, Piaggi P. Metabolic Factors Determining the Susceptibility to Weight Gain: Current Evidence. Curr Obesity Rep 2020; 9: 121–35. DOI: 10.1007/s13679-020-00371-4
21. Markan KR. Defining ‘FGF21 Resistance’ during obesity: Controversy, criteria and unresolved questions version 1; referees: 1 approved, 2 approved with reservations. F1000Res 2018; 7. DOI: 10.12688/f1000research.14117.1
22. Tanajak P. Letter to the editor: Parameters, characteristics, and criteria for defining the term ‘fGF21 resistance. Endocrinology 2017; 158 (5): 1523–4. DOI: 10.1210/en.2017-00056
23. Britton KA et al. Prevalence, distribution, and risk factor correlates of high thoracic periaortic fat in the Framingham Heart Study. J Am Heart Assoc 2012; 1 (6). DOI: 10.1161/JAHA.112.004200
24. Sarin S et al. Clinical Significance of Epicardial Fat Measured Using Cardiac Multislice Computed Tomography. Am J Cardiol 2008; 102 (6): 767–71. DOI: 10.1016/j.amjcard.2008.04.058
25. Zhang X et al. Erratum: Serum FGF21 levels are increased in obesity and are independently associated with the metabolic syndrome in humans. Diabetes 2019; 68 (1): 235. DOI: 10.2337/db19-er01c
26. Shen Y et al. Additive relationship between serum fibroblast growth factor 21 level and coronary artery disease. Cardiovasc Diabetol 2013; 12 (1). DOI: 10.1186/1475-2840-12-124
27. Lee Y et al. Serum FGF21 concentration is associated with hypertriglyceridaemia, hyperinsulinaemia and pericardial fat accumulation, independently of obesity, but not with current coronary artery status. Clin Endocrinol (Oxf) 2014; 80 (1): 57–64. DOI: 10.1111/cen.12134
28. Shafaei Y, Khoshnia M, Marjani A. Serum level of fibroblast growth factor 21 in type 2 diabetic patients with and without metabolic syndrome. J Med Sci 2015; 15 (2): 80–6. DOI: 10.3923/jms.2015.80.86
29. Asrih M, Veyrat-Durebex C, Poher AL et al. Leptin as a potential regulator of FGF21. Cell Physiol Biochem 2016; 38 (3): 1218–25. DOI: 10.1159/000443070
30. Hanks LJ, Gutiérrez OM, Bamman MM et al. Circulating levels of fibroblast growth factor-21 increase with age independently of body composition indices among healthy individuals. J Clin Transl Endocrinol 2015; 2 (2): 77–82. DOI: 10.1016/j.jcte.2015.02.001
31. Matsui M et al. Relationship between physical activity and circulating fibroblast growth factor 21 in middle-aged and older adults. Exp Gerontol 2020; 141: 111081. DOI: 10.1016/j.exger.2020.111081
32. Woo YC et al. Serum fibroblast growth factor 21 is a superior biomarker to other adipokines in predicting incident diabetes. Clin Endocrinol 2017; 86 (1): 37–43. DOI: 10.1111/cen.13229
33. Li G et al. FGF21 deficiency is associated with childhood obesity, insulin resistance and hypoadiponectinaemia: The BCAMS Study. Diabetes Metab 2017; 43 (3): 253–60. DOI: 10.1016/j.diabet.2016.12.003
34. An SY et al. Serum fibroblast growth factor 21 was elevated in subjects with type 2 diabetes mellitus and was associated with the presence of carotid artery plaques. Diabetes Res Clin Pract 2012; 96 (2): 196–203. DOI: 10.1016/j.diabres.2012.01.004
35. Ferreira JP et al. Circulating plasma proteins and new-onset diabetes in a population-based study: Proteomic and genomic insights from the STANISLAS cohort. Eur J Endocrinol 2020; 183 (3): 285–95. DOI: 10.1530/EJE-20-0246
36. Lundsgaard AM et al. Circulating FGF21 in humans is potently induced by short term overfeeding of carbohydrates. Mol Metab 2017; 6 (1): 22–9. DOI: 10.1016/j.molmet.2016.11.001
37. Dushay JR, Toschi E, Mitten EK et al. Fructose ingestion acutely stimulates circulating FGF21 levels in humans. Mol Metab 2015; 4 (1): 51–7. DOI: 10.1016/j.molmet.2014.09.008
38. Laeger T et al. FGF21 is an endocrine signal of protein restriction. J Clin Invest 2014; 124 (9): 3913–22. DOI: 10.1172/JCI74915
39. Søberg S et al. FGF21 Is a Sugar-Induced Hormone Associated with Sweet Intake and Preference in Humans. Cell Metab 2017; 25 (5): 1045–53.e6. DOI: 10.1016/j.cmet.2017.04.009
Авторы
Е.А. Железнова*, Ю.В. Жернакова, М.А. Шария, Н.В. Блинова, М.О. Азимова, Т.В. Шарф, В.П. Масенко, И.Е. Чазова
ФГБУ «Национальный медицинский исследовательский центр кардиологии» Минздрава России, Москва, Россия
*katia.zheleznova@yandex.ru
National Medical Research Center for Cardiology, Moscow, Russia
*katia.zheleznova@yandex.ru
ФГБУ «Национальный медицинский исследовательский центр кардиологии» Минздрава России, Москва, Россия
*katia.zheleznova@yandex.ru
________________________________________________
National Medical Research Center for Cardiology, Moscow, Russia
*katia.zheleznova@yandex.ru
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