Impact of serum levels of vitamin D on lipid profiles, glycemic indices, and insulin resistance in obese type 2 diabetes patients: An observational study

Mohanad Faris Raheem; Shatha H. Ali; Laith G. Shareef

doi:10.12688/f1000research.125191.1

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Research Article

Impact of serum levels of vitamin D on lipid profiles, glycemic indices, and insulin resistance in obese type 2 diabetes patients: An observational study

[version 1; peer review: awaiting peer review]

Mohanad Faris Raheem¹, Shatha H. Ali¹, Laith G. Shareef ²

PUBLISHED 06 Sep 2022

Author details Author details

¹ Department of Clinical Laboratory Science, College of Pharmacy, University of Baghdad, Baghdad, 10011, Iraq
² Department of Pharmacy, Al-Esraa University College, Baghdad, 10011, Iraq

Mohanad Faris Raheem
Roles: Conceptualization, Data Curation, Formal Analysis, Investigation, Methodology, Software, Writing – Original Draft Preparation

Shatha H. Ali
Roles: Conceptualization, Formal Analysis, Methodology, Supervision, Validation, Visualization, Writing – Review & Editing

Laith G. Shareef
Roles: Methodology, Software, Validation, Visualization, Writing – Review & Editing

OPEN PEER REVIEW

REVIEWER STATUS AWAITING PEER REVIEW

Abstract

Background: Diabetes patients have a higher chance of developing dyslipidemia and increased release of free fatty acids, which participate in developing insulin-resistant fat cells. On the other hand, vitamin D insufficiency is linked to the evolution of type 2 diabetes mellitus (T2DM). This study examines the impact of vitamin D serum levels on lipid profiles and insulin resistance concerning glycemic indices in obese T2DM patients.

Methods: During the data collecting stage, 47 diabetes patients were chosen from the out-patient clinic. The control individuals were selected from the general population and were equivalent to the matching patients, with a total of 43 healthy participants. After an overnight fast, a venous blood sample was collected from each individual to test insulin and vitamin D3 levels using particular ELISA kits. In addition, by colorimetric test, serum was used to estimate total cholesterol, triglyceride, and high-density lipoprotein cholesterol. Aside from that, fasting serum glucose levels were measured (FSG).

Results: Fasting serum glucose (FSG), homeostatic model assessment-insulin resistance (HOMA-IR), total cholesterol, and triglycerides, all of these values were significantly elevated in people with diabetes as compared to controls (p-value <0.05) when the serum level of vitamin D was markedly low. In contrast, insulin and high-density lipoprotein values had decreased significantly in the diabetic population compared to controls (p-value <0.05) and were not correlated to vitamin D levels.

Conclusions: Diabetes patients had higher FSG, HOMA-IR, hemoglobin A1c (HbA1c), fasting insulin, triglycerides, total cholesterol to high-density lipoprotein cholesterol ratios (TC: HDL-C), triglyceride to high-density lipoprotein cholesterol ratios (TG: HDL-C), and low-density lipoprotein cholesterol to high-density lipoprotein cholesterol ratios (LDL-C: HDL). In obese diabetic individuals, vitamin D levels had a significant impact on total cholesterol, LDL-C, and the TC:HDL-C ratio.

Keywords

diabetes mellitus, triglyceride, cholesterol, insulin, vitamin D

Corresponding author: Laith G. Shareef

Competing interests: No competing interests were disclosed.

Grant information: The author(s) declared that no grants were involved in supporting this work.

Copyright: © 2022 Faris Raheem M et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

How to cite: Faris Raheem M, H. Ali S and G. Shareef L. Impact of serum levels of vitamin D on lipid profiles, glycemic indices, and insulin resistance in obese type 2 diabetes patients: An observational study [version 1; peer review: awaiting peer review]. F1000Research 2022, 11:1002 (https://doi.org/10.12688/f1000research.125191.1) First published: 06 Sep 2022, 11:1002 (https://doi.org/10.12688/f1000research.125191.1) Latest published: 06 Sep 2022, 11:1002 (https://doi.org/10.12688/f1000research.125191.1)

Expression of Concern

Expression of Concern (20^th October 2023): We, the Publisher and Editor of F1000Research, are issuing an Expression of Concern for the following article:

Faris Raheem M, H. Ali S and G. Shareef L. Impact of serum levels of vitamin D on lipid profiles, glycemic indices, and insulin resistance in obese type 2 diabetes patients: An observational study [version 1; peer review: awaiting peer review]. F1000Research 2022, 11:1002 (https://doi.org/10.12688/f1000research.125191.1).

After publication of this article, questions about the integrity of the ethical approval and methodology were brought to the attention of the F1000 Editorial Team. We have reached out to the authors requesting that they respond to the concerns raised and provide additional information to support the integrity of the content. However, despite multiple attempts to contact the authors, and their institution, they have not responded to our queries within the requested timeframe. Therefore, as we continue to work through the issues raised, we advise readers to interpret the information presented in the article with due caution. The authors have been sent notification about this Expression of Concern.

Editorial note

Editorial Note (13^th July 2023): Since publication, concerns have been raised to the Editorial Team regarding the ethical approval for this study, as well as overlap in the sample and methods to other papers by these authors. The Editorial Team requested explanations regarding the similarities on 19^th May and 6^th June 2023, and the institution was contacted on 21^st March, 6^th April and 25^th April 2023 to verify the ethical approval. Neither the author nor institution have provided responses to our requests. The Editorial Team will update this Editorial Note as the situation progresses. Peer review activity has been suspended for this article until we receive an explanation from the authors/institution.

Introduction

Diabetes mellitus (DM) is a metabolic disorder specified by persistent hyperglycemia with varying degrees of deterioration in the metabolism of carbohydrates, lipids, and proteins.¹^,² Thus, diabetes patients have a higher chance of developing dyslipidemia³ and increased release of free fatty acids, which participate in developing insulin-resistant fat cells. Meanwhile, high concentrations of free fatty acids stimulate the creation of triglycerides; this boosts the release of apolipoprotein B (ApoB) and very low-density lipoprotein (VLDL), both have been related to an elevated risk of cardiovascular disease (CVD).⁴ Furthermore, hyperglycemia also has a negative effect on lipoproteins (especially low-density lipoprotein (LDL) and VLDL) by elevating their glycation and oxidation, thereby promoting the progression of aggressive atherosclerosis.⁵

On the other hand, vitamin D insufficiency is linked to the evolution of T2DM.⁶ Therefore, mild vitamin D deficiency is linked to insulin resistance in several pathways, including low-grade inflammation caused by an unbalanced innate immune system, associated pro-inflammatory cytokines, and enhanced acute phase reactants.⁷

This research aims to investigate the effects of vitamin D serum level on glycemic indices in relation to lipid profile in Iraqi obese type 2 diabetics compared to healthy controls with comparable vitamin D levels.

Methods

Ethical consideration

On 5 January 2022, the ethics committee of the College of Pharmacy at the University of Baghdad formally approved the research proposal (approval code: 542). In addition, all study participants gave written informed consent before participating.

Study design

An observational, case-control study that compared adults with type 2 diabetes mellitus with healthy controls.

Setting

From April to July 2022, a case-controlled study was carried out at two facilities in Baghdad, Iraq, including the Diabetes Centers at The Medical City Complex and AL- Kadhimiya Teaching Hospital.

Study groups

A total of 47 diabetic patients aged (35–64) years (nine male and 38 female) were selected from the out-patient clinic. Diabetic patients were diagnosed according to the American Diabetes Association ADA.⁸ The control subjects were comparable to the corresponding patients, with a total number of 43 healthy subjects (nine male and 34 female), aged (37–65) years, and were chosen from the general population as follows:

Group-1: Type 2DM patients have normal serum vitamin D levels ≥ 22.5 ng/ml, including 22 patients (four male, 18 female).

Group-2: Type 2DM patients have low serum vitamin D levels < 22.5 ng/ml, included 25 patients (five male, 20 female).

Group-3: Control subjects have normal serum vitamin D levels ≥ 22.5 ng/ml. It included 20 healthy subjects (four male, 16 female).

Group-4: Control subjects have low serum vitamin D levels <22.5 ng/ml, including 23 healthy subjects (five male, 18 female).

Eligibility criteria

Adults (˃18 years), both sexes eligible, patients with an established diagnosis of type 2 DM according to the American Diabetes Association diagnostic criteria⁹ and not taking medication or on sulfonylureas only, subjects with BMI ≥ 30 (obese).

Exclusion criteria

Hepatic disease: liver disease accompanied by insulin resistance and hyperinsulinemia. Renal diseases: resulting in diminished 1,25(OH)2D (calcitriol) and elevated parathyroid hormone (PTH) levels occurring early in the course of renal function decline (patients with GFR ˂90). Malignancy, chronic autoimmune diseases, any history of the use of drugs such as insulin, metformin, antihyperlipidemic drugs, vitamin D, corticosteroids or hormone-containing drugs within the three months preceding the start of the study, and women who were pregnant.

Variables

The primary goal of this research was to assess the study groups' fasting serum glucose, HbA1c, insulin, HDL-C, triglyceride, total cholesterol, and LDL-C levels.

Bias

Prospective studies make it simpler to control selection bias since the target population or specimen specification may be precisely controlled to assure group homogeneity. One of the most effective ways to eliminate selection bias is randomization. It can potentially lessen the asymmetry of known and unknown characteristics among groups. As a result, it is effective in reducing random errors. In practice, this was accomplished using methods such as automated randomization services (GraphPad QuickCalcs (RRID:_SCR 000306)). However, the randomization sequence was unknown to the researchers. Therefore, discussing the results with our peers was also one method for eliminating reporting bias.

Sample size

The statistical tool G*Power (RRID:_SCR 013726) version 3.1.9.7 was utilized to determine the sample size. Using a 95% confidence level, the following were the calculated results: df = 88, non-centrality parameter = 3.66, critical t =1.98. The sample size must be 90 individuals (f).

Study procedure

A venous blood specimen (6 ml) was obtained from each subject after overnight fasting; one milliliter of this specimen was put into an ethylene diamine tetra acetic acid (EDTA) tube to be used for the analysis of HbA1c.⁹ The remaining blood sample was placed into a gel tube (no anticoagulant) and left for 30 minutes at room temperature to allow it to clot, then centrifuged for 10–15 minutes at 4400 revolutions per minute (rpm) to get the serum. The resulting serum was then divided with a micropipette into three Eppendorf tubes to be kept frozen (-20 °C) until the assay for insulin¹⁰ and vitamin D₃¹¹ by using specific ELISA kits. The remainder of the serum was utilized for measuring total cholesterol (TC)¹² triglyceride (TG),¹³ and high-density lipoprotein cholesterol (HDL-C)¹⁴ by colorimetric assay. Fasting serum glucose (FSG) was also measured.¹⁵ The homeostatic model assessment-insulin resistance (HOMA-IR) was obtained to estimate insulin resistance or sensitivity by using fasting serum glucose and insulin levels,¹⁶ using the formula: HOMA-IR = (Fasting Glucose (mg/ml) × Fasting Insulin (μU/ml))/405.

Materials and instruments

The purest materials were used for this study. Table 1 provides a summary of the chemical kits utilized in this investigation.

Table 1. Summary of the chemical kits utilized in this investigation.

Chemicals	Provider	Catalogue number	Reference
Vitamin D	MyBioSource (American)	MBS264661	NA
Fasting serum glucose	LINEAR chemicals (Spain)	NA	1129010
Human Insulin Elisa Kit	MyBioSource (American)	MBS704195	NA
Total cholesterol	Human Diagnostic (Germany)	NA	10028
Triglycerides	Human Diagnostic (Germany)	NA	10724
HDL-C	Human Diagnostic (Germany)	NA	10018

Statistical analysis

IBM SPSS version 23 (RRID:SCR_016479) was used in the statistical analysis process. First, the normality of data distribution was assessed because the dataset was smaller than the 2000 Shapiro-Wilk test used; the p-value was >0.05, which means the data is not normally distributed, and a non-parametric test must be used for analysis Descriptive statistics were expressed as (median (interquartile range (IQR))). Then, the not normally distributed variables were managed by the analysis of variance (Kruskal-Wallis) test to compare the four studied groups and determine their degree of significance. Pearson's chi-squared test was carried out for categorical variables. A value less than 0.05 was accepted as a significant difference.

Results

The diabetics' groups had higher FSG, Insulin, HOMA-IR, and HbA1c levels compared to the control groups. However, for HOMA-IR, insulin, and HbA1c, there was no significant difference between the two diabetic groups or between the two control groups, The FSG patients with vitamin D level <22.5 ng/dl showed higher FSG level than patients with vitamin D level ≥22.5 ng/dl, as demonstrated in Table 2 and Figure 1.¹⁷

Table 2. Glycemic measures among studied groups.

Variables	DM with vitamin D ≥22.5 ng/dl (N = 22)	DM with vitamin D <22.5 ng/dl (N = 25)	Control with vitamin D ≥22.5 ng/dl (N = 20)	Control with vitamin D <22.5 ng/dl (N = 23)
FSG (mg/dL)	141(84)^b	182(67)^a	101(18)^c	102(12.4)^c
Insulin (U/ml)	7.889(6.79)^a	8.670(5.18)^a	5.0715(0.73)^b	4.287(0.85)^b
HOMA-IR	2.728(2.93)^a	3.7505(2.33)^a	1.233(0.24)^b	1.223(0.33)^b
HbA1c (%)	6.35(1.65)^a	7.7(2.95)^a	5.375(0.61)^b	5.210(0.7)^b

Figure 1. HOMA-IR levels in studied groups.

There were no marked differences in TC, and LDL-C levels between the two control groups and the DM group with vitamin D level ≥22.5 ng/dl, while the DM group with vitamin D level <22.5 ng/dl showed significantly higher TC and LDL-C levels than the other three groups. There was no marked difference in TG level between the two DM groups or between the two control groups. DM patients with vitamin D level ≥22.5 ng/dl showed no difference with DM patients with vitamin D level <22.5 ng/dl group or with the two control groups, while the DM group with vitamin D level <22.5 ng/dl showed a significantly higher TG level than the two control groups. No marked difference in HDL-C serum level between the two diabetic groups or between the two control groups was shown. However, both control groups had a higher significant HDL-C value than the patient groups. The diabetic group with vitamin D levels <22.5 ng/dl showed higher TC: HDL-C ratio and TG: HDL-C ratio levels than the diabetic group with vitamin D levels ≥ 22.5 ng/dl and the two control groups, while DM patients with vitamin D level ≥22.5 ng/dl showed significantly higher values than the control group with vitamin D level ≥22.5 ng/dl and showed an insignificant difference with the control group with vitamin D level <22.5 ng/dl. No marked difference in serum level of LDL-C: HDL-C ratiobetween the two diabetic groups nor between the two control groups was shown. The DM group with vitamin D level >22.5 ng/dl showed a non-significant difference in LDL-C: HDL-C ratio level with the control group with vitamin D level <22.5 ng/dl, while the DM group with vitamin D level <22.5 ng/dl showed a significantly higher LDL-C: HDL-C ratio level than the two control groups as shown in Table 3.¹⁷

Table 3. Lipid profile among the studied groups.

Variables	Diabetic patients with vitamin D levels >22.5ng/dl (N = 22)	Diabetic patients with vitamin D levels <22.5 ng/dl (N = 25)	Control group with vitamin D levels >22.5 ng/dl (N = 20)	Control group with vitamin D levels <22.5 ng/dl (N = 23)
TC mg/dL	196(70.5)^b	226(64)^a	172.5(40.50)^b	170(41)^b
TG mg/dL	119(114.50)^ab	178(138.25)^a	103(53)^b	118(113.45)^b
HDL-C mg/dL	42.075(4.24)^b	42.03(10.33)^b	54.234(8.93)^a	47(12.8)^a
LDL-C mg/dl	118.527(69.73)^b	155.130(81.54)^a	91.219(42.81)^b	100(48.46)^b
TC: HDL-C Ratio	4.8245(1.91)^b	5.4521(3.43)^a	3.2905(0.95)^c	3.8655(1.51)^bc
TG: HDL-C Ratio	3.8816(2.81)^ab	4.1950(3.61)^a	1.8686(1.79)^c	2.37(2.61)^bc
LDL-C: HDL-C ratio	2.8270(1.83)^ab	3.6458(3.37)^a	1.8569(0.92)^c	2.1277(1.48)^bc

Discussion

For the current study, there were no marked differences in confounder (age, gender, BMI, and smoking) among the four studied groups. The diabetics' groups had higher FSG, fasting insulin, HOMA- IR, and HbA1c levels compared to the control groups due to the effect of diabetes. The findings in this study showed that vitamin D levels had no impact on the level of fasting insulin, HOMA-IR, and HbA1c as demonstrated in Table 2, and this finding highly agreed with Al- Shoumer et al. and Luo et al. who suggested in their research that there was no link between glycemic control and vitamin D when confounders like age, gender, and BMI were controlled.¹⁸^,¹⁹ This also agreed with research carried out by Olt S. et al. who suggested that vitamin D level wasn't correlated with glycemic control (For HbA1C correlation with vitamin D level, p = 0.33 (>0.05)).²⁰ While Al-Timimi et al. reported that deficiency in vitamin D levels in patients with T2DM was significantly associated with glycemic control.²¹ The correlation between vitamin D and HbA1c is controversial; many previously published studies have shown a significantly weak negative correlation between HbA1c and vitamin D levels.²²^,²³ Pittas et al., in a retrospective study, suggested that impaired B-cell activity and insulin resistance are among the pathophysiological factors associated with metabolic syndrome and type 2 diabetes (T2DM). Vitamin D levels may indirectly impact these factors by regulating calcium homeostasis or activating vitamin D receptors.²⁴ In this study, patients with vitamin D levels <22.5 ng/dl showed higher FSG levels than patients with vitamin D level ≥22.5ng/dl, which agreed with a study done by Scragg et al. who found an inverse relationship between vitamin D and FSG levels in their research.²⁵ While a Japanese study comparing DM type, two patients and healthy controls found that vitamin D insufficiency was present in 70% of cases without a difference in vitamin D levels between patients and controls.²⁶ Two US studies suggest an increase in the mean vitamin D level in T2DM and the corresponding controls.²⁷ The variation in outcome among studies indicates that vitamin D levels in patients with T2DM differ according to ethnicity or other unknown causes.²⁸ In the present study, levels of vitamin D showed a pronounced impact on TC, LDL-C, and TC: HDL-C ratio levels, but it didn’t show an effect on TG, HDL-C, TG: HDL-C ratio, and LDL-C: HDL-C ratio levels. DM in this study showed an impact on all lipid profiles. This finding agreed with many studies that reported dyslipidemia as an independent predictor of a decrease in vitamin D level. TC was reported to correlate inversely with serum levels of vitamin D even after controlling for confounders.²⁹

This study's results disagree with many cross-sectional studies, where serum vitamin D levels correlate directly with HDL-C. Many investigations also revealed an oppositional relationship between TG and blood vitamin D levels. Although some research found a link between TG and blood vitamin D levels, other investigations found an opposite correlation.³⁰ The current study findings are comparable to the research of John et al. on 170 Bangladeshi individuals born in the UK (101 female and 69 male) without a history of diabetes or other chronic illness. They found no link between vitamin D and HDL-C or TG levels.³¹ Due to enhancing intestinal calcium absorption, research considering lipid metabolism has found that vitamin D can decrease hepatic triglyceride production and boost uptake by peripheral tissues.³² Vitamin D boosts reverse cholesterol transport by increasing apo-lipoprotein A1, vitamin D also encourages the development of big HDL-C particles.³³ Due to the interdependence of the metabolism of carbohydrates and lipids, blood lipid levels can be influenced by various variables in people with diabetes. As a result, every issue in lipid metabolism causes a disorder in glucose metabolism and vice versa. The primary defect in most people with type two DM is insulin resistance. Insulin resistance and hyperinsulinemia have a good predictive value for the development of T2DM in non-diabetic people.³⁴ The TG: HDL ratio and other lipid profile ratios have been evaluated daily for many critical clinical uses.³⁵^,³⁶ Prior studies have suggested a positive correlation between metabolic syndrome, negative cardio-metabolic risk factor profiles, and the prediction of diabetes or its consequences. This can happen because of the link between insulin resistance and TG: HDL-C ratio.³⁵

Limitations

Several selection criteria were used in the study to limit the confounding effect. Also, because the number of participants in our study was limited, we recommend increasing the number of patients in future research.

Conclusions

Elevated FSG, HOMA-IR, HbA1c, fasting insulin, triglycerides, TC: HDL-C ratio, TG: HDL-C ratio, and LDL-C: HDL-C ratio values were found in diabetes patients compared to healthy controls, with markedly diminished HDL-C levels in diabetes patients compared to healthy controls as a result of the diabetes effect. Vitamin D level significantly impacted total cholesterol, LDL-C, and TC: HDL-C ratio in obese diabetic patients.

Data availability

Underlying data

Zenodo: Underlying data for ‘Impact of serum levels of vitamin D on lipid profiles, glycemic indices, and insulin resistance in obese type 2 diabetes patients: An observational study’. ‘Laboratory findings’. https://doi.org/10.5281/zenodo.6989464.¹⁷

Data are available under the Creative Commons Attribution 4.0 International license (CC-BY 4.0).

Consent

Written informed consent for publication of the participants’ details was obtained from the participants.

Acknowledgments

The authors would like to acknowledge the participants, the Diabetes Centers at The Medical City Complex, and the AL- Kadhimiya Teaching Hospital team for their ongoing assistance throughout data collection.

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Author details Author details

¹ Department of Clinical Laboratory Science, College of Pharmacy, University of Baghdad, Baghdad, 10011, Iraq
² Department of Pharmacy, Al-Esraa University College, Baghdad, 10011, Iraq

Mohanad Faris Raheem
Roles: Conceptualization, Data Curation, Formal Analysis, Investigation, Methodology, Software, Writing – Original Draft Preparation

Shatha H. Ali
Roles: Conceptualization, Formal Analysis, Methodology, Supervision, Validation, Visualization, Writing – Review & Editing

Laith G. Shareef
Roles: Methodology, Software, Validation, Visualization, Writing – Review & Editing

Competing interests

No competing interests were disclosed.

Grant information

The author(s) declared that no grants were involved in supporting this work.

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Published: 06 Sep 2022, 11:1002

https://doi.org/10.12688/f1000research.125191.1

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© 2022 Faris Raheem M et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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Faris Raheem M, H. Ali S and G. Shareef L. Impact of serum levels of vitamin D on lipid profiles, glycemic indices, and insulin resistance in obese type 2 diabetes patients: An observational study [version 1; peer review: awaiting peer review]. F1000Research 2022, 11:1002 (https://doi.org/10.12688/f1000research.125191.1)

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Impact of serum levels of vitamin D on lipid profiles, glycemic indices, and insulin resistance in obese type 2 diabetes patients: An observational study

Abstract

Keywords

Expression of Concern

Editorial note

Introduction

Methods

Ethical consideration

Study design

Setting

Study groups

Eligibility criteria

Exclusion criteria

Variables

Bias

Sample size

Materials and instruments

Table 1. Summary of the chemical kits utilized in this investigation.

Statistical analysis

Results

Table 2. Glycemic measures among studied groups.

Figure 1. HOMA-IR levels in studied groups.

Table 3. Lipid profile among the studied groups.

Discussion

Limitations

Conclusions

Data availability

Underlying data

Consent

Acknowledgments

References

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