ภาวะขาดวิตามินดีในคนไข้เบาหวานชนิดที่ 2
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เบาหวานชนิดที่ 2, ภาวะขาดวิตามินดี, ภาวะดื้ออินซูลินบทคัดย่อ
Introduction Current evidence suggests that vitamin D deficiency may contribute to an increased
risk of type 2 DM.
Objective The aim of this study is to explore the relationship between vitamin D status and
type 2 DM.
Material and Methods A cross-sectional study was conducted on 360 patients at the outpatient
diabetes clinic of Burapha University Hospital. Patients were prospectively recruited, physically
examined, submitted to laboratory investigations as well as given a vitamin D level assessment.
Results The mean level of 25(OH)D was 25.0 ± 7.7ng/ml. 26.6% of the patients had vitamin
D deficiency; 48.8% had vitamin D insufficiency. After making adjustments for all variables,
we found that body mass index (BMI) (r = -0.123, p-value = 0.02), waist circumference (WC)
(r = -0.0565, p-value=0.28), and Homeostatic Model Assessment for Insulin Resistance (HOMA-IR)
(r = -0.006, p-value = 0.91) had an inverted correlation to vitamin D levels. In terms of ALT levels,
about 10.56% of the population had nonalcoholic fatty liver disease (NAFLD). In addition, we
found that diastolic blood pressure (DBP) (r = 0.159, p-value = 0.002) and fasting blood sugar
levels (FBS) (r = 0.127, p-value = 0.016) correlated with the presence of NAFLD. In contrast,
insulin sensitivity (r = -0.186, p-value < 0.001), triglycerides (r = 0.138, p = 0.009), and Time to
DM (r = -0.182, p = 0.001), had inversely correlated with NAFLD.
Conclusion High prevalence of vitamin D deficiency was observed in our diabetic type 2 patients.
After multivarious adjustments for all variables, high WC, high BMI, and high HOMA-IR were
associated with an increased risk of vitamin D deficiency; while high FBS, low insulin sensitivity
and short duration of a type 2 DM were associated with an increased risk of NAFLD.
References
1. Eckel RH, Grundy SM, Zimmet PZ. The
metabolic syndrome. Lancet. 2005; 365:
1415-28.
2. Chiu KC, Chu A, Go VL, Saad MF.
Hypovitaminosis D is associated with insulin
resistance and beta cell dysfunction. Am J
Clin Nutr. 2004; 79: 820-5.
3. Boucher BJ, Mannan N, Noonan K, Hales
CN, Evans SJ. Glucose intolerance and
impairment of insulin secretion in relation
to vitamin D deficiency in east London
Asians. Diabetologia. 1995; 38: 1239-45.
4. Ford ES, Ajani UA, McGuire LC, Liu S.
Concentrations of serum vitamin D and the
metabolic syndrome among U.S. adults.
Diabetes Care. 2005; 28: 1228-30.
5. Pittas AG, Lau J, Hu FB, Dawson-Hughes B.
The role of vitamin D and calcium in type
2 diabetes. A systematic review and metaanalysis.
J Clin Endocrinol Metab. 2007; 92:
2017-29.
6. Hypponen E, Laara E, Reunanen A, Jarvelin
MR, Virtanen SM. Intake of vitamin D and
risk of type 1 diabetes: a birth-cohort study.
Lancet. 2001; 358: 1500-3.
7. Mitri J, Muraru MD, Pittas AG. Vitamin D and
type 2 diabetes: a systematic review. Eur J
Clin Nutr. 2011; 65: 1005-15.
8. Pittas AG, Sun Q, Manson JE, Dawson-
Hughes B, Hu FB. Plasma 25-hydroxyvitamin
D concentration and risk of incident type
2 diabetes in women. Diabetes Care. 2010;
33: 2021-3.
9. C h a i l u r k i t L O , A e k p l a k o r n W ,
Ongphiphadhanakul B. The association
between vitamin D status and type 2
diabetes in a Thai population, a crosssectional
study. Clin Endocrinol (Oxf). 2012;
77: 658-64.
10. Kim MK, Il Kang M, Won Oh K, Lee JH,
Lee WC, Yoon KH, et al. The association
of serum vitamin D level with presence
of metabolic syndrome and hypertension
in middle-aged Korean subjects. Clin
Endocrinol (Oxf). 2010; 73: 330-8.
11. Soontrapa S SS, Chailurkit L.The prevalence
and the calcidiol levels of vitamin D
deficiency in the elderly Thai women
in municipality of Khon Kaen province,
Thailand. Srinagarind Med J. 2002; 17:
231-8.
12. Athisakul S SS, Buddhari W. Prevalence of
hypovitaminosis D in heart failure patients
at King Chulalongkorn Memorial hospital.
Thai Heart Journal. 2010; 23: 154-63.
13. Elizabeth H. Harris M. Elevated Liver
Function Tests in Type 2 Diabetes. Clinical
Diabetes. 2005; 23: 115-9.
14. Trombetta M, Spiazzi G, Zoppini G, Muggeo
M. Review article: type 2 diabetes and
chronic liver disease in the Verona diabetes
study. Aliment Pharmacol Ther. 2005; 22
Suppl 2: 24-7.
15. Takero KAIDO YH, Kuniaki KITAMURA
Association between Liver Dysfunction and
Hyperglycemia in Japanese Male Workers at
Printing and Papermaking Plants. J Occup
Health. 2002; 44: 301-6.
16. Al-Faris EA. The prevalence of abnormal
results of annual investigations among
diabetic patients with different risk factors.
Ann Saudi Med. 2000; 20: 206-10.
17. Alavian SM, Hajarizadeh B, Nematizadeh F,
Larijani B. Prevalence and determinants of
diabetes mellitus among Iranian patients
with chronic liver disease. BMC Endocr
Disord. 2004; 4: 4.
18. Marchesini G, Bugianesi E, Forlani G,
Marzocchi R, Zannoni C, Vanni E, et al.
Non-alcoholic steatohepatitis in patients
cared in metabolic units. Diabetes Research
and Clinical Practice. 2004; 63.
19. Gupte P, Amarapurkar D, Agal S, Baijal
R, Kulshrestha P, Pramanik S, et al. Nonalcoholic
steatohepatitis in type 2 diabetes
mellitus. J Gastroenterol Hepatol. 2004;
19: 854-8.
20. Sanyal AJ, American Gastroenterological
A. AGA technical review on nonalcoholic
fatty liver disease. Gastroenterology. 2002;
123: 1705-25.
21. Jansen PL. Nonalcoholic steatohepatitis.
Neth J Med. 2004; 62: 217-24.
22. Ono M, Saibara T. Clinical features of
nonalcoholic steatohepatitis in Japan:
Evidence from the literature. J Gastroenterol.
2006; 41: 725-32.
23. West J, Brousil J, Gazis A, Jackson L, Mansell
P, Bennett A, Aithal GP.Elevated serum
alanine transaminase in patients with type
1 or type 2 diabetes mellitus. QJM. 2006;
99: 871-6.
24. Gonem S WA, De P. Prevalence of abnormal
liver function tests in patients with diabetes
mellitus. Endocrine Abstracts. 2007; 13:
157.
25. Holick MF, Binkley NC, Bischoff-Ferrari HA,
Gordon CM, Hanley DA, Heaney RP, et al.
Evaluation, treatment, and prevention of
vitamin D deficiency: an Endocrine Society
clinical practice guideline. J Clin Endocrinol
Metab. 2011; 96: 1911-30.
26. Grundy SM, Cleeman JI, Daniels SR, Donato
KA, Eckel RH, Franklin BA, et al. Diagnosis and
management of the metabolic syndrome:
an American Heart Association/National
Heart, Lung, and Blood Institute Scientific
Statement. Cardiol Rev. 2005; 13: 322-7.
27. C h a i l u r k i t L O , A e k p l a k o r n W ,
Ongphiphadhanakul B. Regional variation
and determinants of vitamin D status in
sunshine-abundant Thailand. BMC Public
Health. 2011; 11: 853.
28. NR. Pinelli LJ, MB. Brown, WH. Herman.
Serum 25-Hydroxy vitamin D and insulin
resistance, metabolic syndrome, and
glucose intolerance among Arab Americans
Diabetes Care. 2010; 235: 1373-75.
29. Nongluk P, Nakarin S, Supakit W, Sarinee
K. Prevalence of vitamin D deficiency and
association of serum vitamin D level with
anthropometric and metabolic factors
in metabolic syndrome patients. Asian
Biomedicine. 2013; 7: 227-35
30. Rahman SA, Chee WS, Yassin Z, Chan SP.
Vitamin D status among postmenopausal
Malaysian women. Asia Pac J Clin Nutr.
2004; 13: 255-60.
31. Grammatiki M, Rapti E, Karras S, Ajjan RA,
Kotsa K. Vitamin D and diabetes mellitus:
Causal or casual association? Rev Endocr
Metab Disord. 2017; 18: 227-41.
32. Husemoen LL, Thuesen BH, Fenger M,
Jørgensen T, Glümer C, Svensson J, et
al. Serum 25(OH)D and type 2 diabetes
association in a general population: a
prospective study. Diabetes Care. 2012;
35: 1695-700.
33. Das G. Vitamin D and type 2 diabetes.
PRACTICAL DIABETES. 2017; 34: 19-24.
34. Kostoglou-Athanassiou I, Athanassiou P,
Gkountouvas A, Kaldrymides P. Vitamin D
and glycemic control in diabetes mellitus
type 2. Ther Adv Endocrinol Metab. 2013;
4: 122-8.
35. Bourlon PM, Billaudel B, Faure-Dussert A.
Influence of vitamin D3 deficiency and
1,25 dihydroxyvitamin D3 on de novo
insulin biosynthesis in the islets of the rat
endocrine pancreas. J Endocrinol. 1999;
160: 87-95.
36. Zeitz U, Weber K, Soegiarto DW, Wolf
E, Balling R, Erben RG. Impaired insulin
secretory capacity in mice lacking a
functional vitamin D receptor. FASEB J.
2003; 17: 509-11.
37. Afsaneh Talaei MM, Zahra Adgi. The effect
of vitamin D on insulin resistance in
patients with type 2 diabetes. Diabetology
& Metabolic Syndrome. 2013; 5: 8-12.
38. Maestro B, Campion J, Davila N, Calle C.
Stimulation by 1,25-dihydroxyvitamin D3
of insulin receptor expression and insulin
responsiveness for glucose transport in
U-937 human promonocytic cells. Endocr
J. 2000; 47: 383-91.
39. Fan JG, Saibara T, Chitturi S, Kim BI, Sung
JJ, Chutaputti A, et al. What are the risk
factors and settings for non-alcoholic fatty
liver disease in Asia-Pacific? J Gastroenterol
Hepatol. 2007; 22: 794-800.
40. Fan JG, Farrell GC. Epidemiology of nonalcoholic
fatty liver disease in China. J
Hepatol. 2009; 50: 204-10.
41. Farrell GC. Non-alcoholic steatohepatitis:
what is it, and why is it important in the
Asia-Pacific region? J Gastroenterol Hepatol.
2003; 18: 124-38.
42. Adolph TE, Grander C, Grabherr F, Tilg H.
Adipokines and Non-Alcoholic Fatty Liver
Disease: Multiple Interactions. Int J Mol Sci.
2017; 18.
43. Carlberg C. Genome-wide (over)view on
the actions of vitamin D. Front Physiol.
2014; 5: 167.
44. Sanyal AJ, Campbell-Sargent C, Mirshahi F, et
al. Nonalcoholic steatohepatitis: association
of insulin resistance and mitochondrial
abnormalities. Gastroenterology. 2001; 120:
1183-92.
metabolic syndrome. Lancet. 2005; 365:
1415-28.
2. Chiu KC, Chu A, Go VL, Saad MF.
Hypovitaminosis D is associated with insulin
resistance and beta cell dysfunction. Am J
Clin Nutr. 2004; 79: 820-5.
3. Boucher BJ, Mannan N, Noonan K, Hales
CN, Evans SJ. Glucose intolerance and
impairment of insulin secretion in relation
to vitamin D deficiency in east London
Asians. Diabetologia. 1995; 38: 1239-45.
4. Ford ES, Ajani UA, McGuire LC, Liu S.
Concentrations of serum vitamin D and the
metabolic syndrome among U.S. adults.
Diabetes Care. 2005; 28: 1228-30.
5. Pittas AG, Lau J, Hu FB, Dawson-Hughes B.
The role of vitamin D and calcium in type
2 diabetes. A systematic review and metaanalysis.
J Clin Endocrinol Metab. 2007; 92:
2017-29.
6. Hypponen E, Laara E, Reunanen A, Jarvelin
MR, Virtanen SM. Intake of vitamin D and
risk of type 1 diabetes: a birth-cohort study.
Lancet. 2001; 358: 1500-3.
7. Mitri J, Muraru MD, Pittas AG. Vitamin D and
type 2 diabetes: a systematic review. Eur J
Clin Nutr. 2011; 65: 1005-15.
8. Pittas AG, Sun Q, Manson JE, Dawson-
Hughes B, Hu FB. Plasma 25-hydroxyvitamin
D concentration and risk of incident type
2 diabetes in women. Diabetes Care. 2010;
33: 2021-3.
9. C h a i l u r k i t L O , A e k p l a k o r n W ,
Ongphiphadhanakul B. The association
between vitamin D status and type 2
diabetes in a Thai population, a crosssectional
study. Clin Endocrinol (Oxf). 2012;
77: 658-64.
10. Kim MK, Il Kang M, Won Oh K, Lee JH,
Lee WC, Yoon KH, et al. The association
of serum vitamin D level with presence
of metabolic syndrome and hypertension
in middle-aged Korean subjects. Clin
Endocrinol (Oxf). 2010; 73: 330-8.
11. Soontrapa S SS, Chailurkit L.The prevalence
and the calcidiol levels of vitamin D
deficiency in the elderly Thai women
in municipality of Khon Kaen province,
Thailand. Srinagarind Med J. 2002; 17:
231-8.
12. Athisakul S SS, Buddhari W. Prevalence of
hypovitaminosis D in heart failure patients
at King Chulalongkorn Memorial hospital.
Thai Heart Journal. 2010; 23: 154-63.
13. Elizabeth H. Harris M. Elevated Liver
Function Tests in Type 2 Diabetes. Clinical
Diabetes. 2005; 23: 115-9.
14. Trombetta M, Spiazzi G, Zoppini G, Muggeo
M. Review article: type 2 diabetes and
chronic liver disease in the Verona diabetes
study. Aliment Pharmacol Ther. 2005; 22
Suppl 2: 24-7.
15. Takero KAIDO YH, Kuniaki KITAMURA
Association between Liver Dysfunction and
Hyperglycemia in Japanese Male Workers at
Printing and Papermaking Plants. J Occup
Health. 2002; 44: 301-6.
16. Al-Faris EA. The prevalence of abnormal
results of annual investigations among
diabetic patients with different risk factors.
Ann Saudi Med. 2000; 20: 206-10.
17. Alavian SM, Hajarizadeh B, Nematizadeh F,
Larijani B. Prevalence and determinants of
diabetes mellitus among Iranian patients
with chronic liver disease. BMC Endocr
Disord. 2004; 4: 4.
18. Marchesini G, Bugianesi E, Forlani G,
Marzocchi R, Zannoni C, Vanni E, et al.
Non-alcoholic steatohepatitis in patients
cared in metabolic units. Diabetes Research
and Clinical Practice. 2004; 63.
19. Gupte P, Amarapurkar D, Agal S, Baijal
R, Kulshrestha P, Pramanik S, et al. Nonalcoholic
steatohepatitis in type 2 diabetes
mellitus. J Gastroenterol Hepatol. 2004;
19: 854-8.
20. Sanyal AJ, American Gastroenterological
A. AGA technical review on nonalcoholic
fatty liver disease. Gastroenterology. 2002;
123: 1705-25.
21. Jansen PL. Nonalcoholic steatohepatitis.
Neth J Med. 2004; 62: 217-24.
22. Ono M, Saibara T. Clinical features of
nonalcoholic steatohepatitis in Japan:
Evidence from the literature. J Gastroenterol.
2006; 41: 725-32.
23. West J, Brousil J, Gazis A, Jackson L, Mansell
P, Bennett A, Aithal GP.Elevated serum
alanine transaminase in patients with type
1 or type 2 diabetes mellitus. QJM. 2006;
99: 871-6.
24. Gonem S WA, De P. Prevalence of abnormal
liver function tests in patients with diabetes
mellitus. Endocrine Abstracts. 2007; 13:
157.
25. Holick MF, Binkley NC, Bischoff-Ferrari HA,
Gordon CM, Hanley DA, Heaney RP, et al.
Evaluation, treatment, and prevention of
vitamin D deficiency: an Endocrine Society
clinical practice guideline. J Clin Endocrinol
Metab. 2011; 96: 1911-30.
26. Grundy SM, Cleeman JI, Daniels SR, Donato
KA, Eckel RH, Franklin BA, et al. Diagnosis and
management of the metabolic syndrome:
an American Heart Association/National
Heart, Lung, and Blood Institute Scientific
Statement. Cardiol Rev. 2005; 13: 322-7.
27. C h a i l u r k i t L O , A e k p l a k o r n W ,
Ongphiphadhanakul B. Regional variation
and determinants of vitamin D status in
sunshine-abundant Thailand. BMC Public
Health. 2011; 11: 853.
28. NR. Pinelli LJ, MB. Brown, WH. Herman.
Serum 25-Hydroxy vitamin D and insulin
resistance, metabolic syndrome, and
glucose intolerance among Arab Americans
Diabetes Care. 2010; 235: 1373-75.
29. Nongluk P, Nakarin S, Supakit W, Sarinee
K. Prevalence of vitamin D deficiency and
association of serum vitamin D level with
anthropometric and metabolic factors
in metabolic syndrome patients. Asian
Biomedicine. 2013; 7: 227-35
30. Rahman SA, Chee WS, Yassin Z, Chan SP.
Vitamin D status among postmenopausal
Malaysian women. Asia Pac J Clin Nutr.
2004; 13: 255-60.
31. Grammatiki M, Rapti E, Karras S, Ajjan RA,
Kotsa K. Vitamin D and diabetes mellitus:
Causal or casual association? Rev Endocr
Metab Disord. 2017; 18: 227-41.
32. Husemoen LL, Thuesen BH, Fenger M,
Jørgensen T, Glümer C, Svensson J, et
al. Serum 25(OH)D and type 2 diabetes
association in a general population: a
prospective study. Diabetes Care. 2012;
35: 1695-700.
33. Das G. Vitamin D and type 2 diabetes.
PRACTICAL DIABETES. 2017; 34: 19-24.
34. Kostoglou-Athanassiou I, Athanassiou P,
Gkountouvas A, Kaldrymides P. Vitamin D
and glycemic control in diabetes mellitus
type 2. Ther Adv Endocrinol Metab. 2013;
4: 122-8.
35. Bourlon PM, Billaudel B, Faure-Dussert A.
Influence of vitamin D3 deficiency and
1,25 dihydroxyvitamin D3 on de novo
insulin biosynthesis in the islets of the rat
endocrine pancreas. J Endocrinol. 1999;
160: 87-95.
36. Zeitz U, Weber K, Soegiarto DW, Wolf
E, Balling R, Erben RG. Impaired insulin
secretory capacity in mice lacking a
functional vitamin D receptor. FASEB J.
2003; 17: 509-11.
37. Afsaneh Talaei MM, Zahra Adgi. The effect
of vitamin D on insulin resistance in
patients with type 2 diabetes. Diabetology
& Metabolic Syndrome. 2013; 5: 8-12.
38. Maestro B, Campion J, Davila N, Calle C.
Stimulation by 1,25-dihydroxyvitamin D3
of insulin receptor expression and insulin
responsiveness for glucose transport in
U-937 human promonocytic cells. Endocr
J. 2000; 47: 383-91.
39. Fan JG, Saibara T, Chitturi S, Kim BI, Sung
JJ, Chutaputti A, et al. What are the risk
factors and settings for non-alcoholic fatty
liver disease in Asia-Pacific? J Gastroenterol
Hepatol. 2007; 22: 794-800.
40. Fan JG, Farrell GC. Epidemiology of nonalcoholic
fatty liver disease in China. J
Hepatol. 2009; 50: 204-10.
41. Farrell GC. Non-alcoholic steatohepatitis:
what is it, and why is it important in the
Asia-Pacific region? J Gastroenterol Hepatol.
2003; 18: 124-38.
42. Adolph TE, Grander C, Grabherr F, Tilg H.
Adipokines and Non-Alcoholic Fatty Liver
Disease: Multiple Interactions. Int J Mol Sci.
2017; 18.
43. Carlberg C. Genome-wide (over)view on
the actions of vitamin D. Front Physiol.
2014; 5: 167.
44. Sanyal AJ, Campbell-Sargent C, Mirshahi F, et
al. Nonalcoholic steatohepatitis: association
of insulin resistance and mitochondrial
abnormalities. Gastroenterology. 2001; 120:
1183-92.
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