The Association Between Hematological Indices and Type 2 Diabetes Mellitus in Iranian Population

authors:

avatar Mehdi Shahmoradi ORCID 1 , avatar Ladan Hajiabdolrrasouli 1 , avatar Masoumeh Kheirandish ORCID 1 , * , avatar Shideh Rafati ORCID 2 , avatar Seyyed Mohammad Hashemi 3 , avatar Yasmin Moradi 3 , avatar Ebrahim Eftekhar ORCID 4 , avatar Vahide Jamshidi 4 , avatar Mohammad Hosein Sheybani Arani ORCID 1

Endocrinology and Metabolism Research Center, Hormozgan University of Medical Sciences, Bandar Abbas, Iran
Social Determinants in Health Promotion Research Center, Hormozgan University of Medical Sciences, Bandar Abbas, Iran
Student Research Committee, Faculty of Medicine, Hormozgan University of Medical Sciences, Bandar Abbas, Iran
Molecular Medicine Research Center, Hormozgan Health Institute, Hormozgan University of Medical Sciences, Bandar Abbas, Iran

how to cite: Shahmoradi M, Hajiabdolrrasouli L, Kheirandish M, Rafati S, Hashemi S M, et al. The Association Between Hematological Indices and Type 2 Diabetes Mellitus in Iranian Population. Shiraz E-Med J. 2024;25(11):e145464. https://doi.org/10.5812/semj-145464.

Abstract

Background:

Hematological alterations have been observed in diabetes, with some studies showing controversial associations between specific hematologic parameters and type 2 diabetes mellitus (T2DM).

Objectives:

This study aims to determine the association between hematological indices, specifically white blood cell (WBC) count, red cell distribution width (RDW), and platelet distribution width (PDW), and the presence of T2DM in an Iranian population, using data from the Bandare-Kong non-communicable diseases (BKNCD) cohort.

Methods:

Data from the BKNCD cohort, which includes 4063 individuals aged 35 - 70 years, was used in this study. After excluding participants with conditions that could interfere with the analysis, 2318 subjects remained for final evaluation.

Results:

Among the 2318 individuals, T2DM was present in 530 (22.9%). Binary logistic regression analysis revealed that the odds of T2DM increased by approximately 7% for every 109/L increase in WBC count, after adjusting for variables such as occupation, age, body mass index, sex, place of residence, education, smoking, marital status, systolic and diastolic blood pressure (DBP), and physical activity (adjusted odds ratio (aOR) = 1.066, 95% confidence interval (CI) = 1.003; 1.133, P = 0.039). Additionally, elevated PDW was associated with a 63% increase in the odds of T2DM (aOR = 1.625, 95% CI 1.159; 2.279, P = 0.005), while increased RDW was associated with decreased odds of T2DM (aOR = 0.801, 95% CI 0.716; 0.895, P < 0.001).

Conclusions:

Elevated PDW and WBC counts in T2DM patients in this study suggest an inflammatory state and hypercoagulability. However, the paradoxically decreased RDW may be linked to poor glycemic control in these patients.

1. Background

Diabetes mellitus is a chronic illness characterized by elevated blood glucose levels due to the body's inability to produce enough insulin or effectively use it (1). As the global prevalence of type 2 diabetes mellitus (T2DM) continues to rise, it presents significant challenges to healthcare systems worldwide. By 2030, an estimated 7,079 cases of T2DM per 100,000 individuals are expected globally, with increases anticipated in all regions (2).

T2DM is a leading cause of cardiovascular disease (CVD) and is associated with dyslipidemia, oxidative stress, thrombophilia, endothelial dysfunction, inflammation, hemostatic disorders, and atherogenic lipoprotein production (3). Hematological changes, including abnormalities in red blood cells (RBCs), white blood cells (WBCs), platelets, and the coagulation system, are observed in T2DM patients, affecting their structure, function, and metabolism (4).

These hematological abnormalities in diabetes may result from increased reactive oxygen species (ROS) production and advanced glycation end products (AGEs) due to chronic hyperglycemia, leading to tissue damage, oxidative stress, and dysfunction in the vascular and hematological systems (5, 6). In T2DM patients, these alterations can exacerbate or contribute to conditions such as anemia, hypercoagulability, and CVD (7). Moreover, insulin resistance accelerates vascular complications through endothelial dysfunction, inflammation, and platelet hyperactivity (6).

2. Objectives

This study aims to explore the correlations between T2DM and hematological indices in the Iranian coastal city of Bandare-Kong.

3. Methods

3.1. Participants and Study Design

This study utilized data from the Bandare-Kong non-communicable diseases (BKNCD) cohort, which is part of the larger Prospective Epidemiological Research Studies in IrAN (PERSIAN) initiative. Bandare-Kong non-communicable diseases collected data from 4063 individuals aged 35 - 70 years in Bandare-Kong, Hormozgan province, southern Iran, between November 2016 and November 2018. The cohort's methodology has been thoroughly described elsewhere (8). After excluding individuals with conditions that could interfere with the study, 2318 participants remained for analysis, including 530 with diabetes. Exclusion criteria included pregnancy, thyroid disorders, autoimmune diseases, inflammatory bowel disease, malignancies, liver diseases, chronic obstructive pulmonary disease, thalassemia, and hormonal disorders. Those undergoing chemotherapy or taking statins, anticoagulant, oral contraceptives, supplements, or alcohol were also excluded.

3.2. Data Collection, Variable Definition, and Laboratory Methods

Sociodemographic information, including age, occupation, sex, marital status, education, place of residence, and smoking status, was collected through in-person interviews. Body weight was measured using a mechanical scale with a 0.5 kg accuracy, while subjects wore minimal clothing and no shoes. Heights were measured with bare feet, standing with shoulders relaxed, using a stretch-resistant tape accurate to 0.5 cm. Body mass index was calculated to the nearest 0.01 by dividing weight (in kilograms) by the square of height (in meters).

After five minutes of rest, a trained nurse measured blood pressure (BP) with the subjects seated, feet flat, and arms at heart level. A standard mercury sphygmomanometer was used, with the cuff size adjusted for arm circumference. The average of two BP readings, taken five minutes apart, was recorded. If the systolic BP (SBP) differed by more than 10 mmHg or diastolic BP (DBP) by more than 5 mmHg, a third measurement was taken, and the closest two values were averaged.

Following a 10 to 12-hours fast, blood samples were collected and centrifuged at 1000 g for 10 minutes. Serum was separated and stored at -80°C until analysis. A chemistry autoanalyzer (BT1500) was used to measure total cholesterol (TC), triglycerides (TG), high-density lipoprotein cholesterol (HDL-C), and fasting plasma glucose (FPG) using a colorimetric method and standard kits (Pars Azmoon, Tehran, Iran) (Biotechnical Instruments, Rome, Italy). The Friedewald equation (LDL-C = TC - HDL-C - TG/5) was used to calculate low-density lipoprotein cholesterol (LDL-C), and for individuals with TG levels above 300 mg/dL, LDL-C was directly measured using a kit (Pars Azmoon, Tehran, Iran).

Whole blood samples were analyzed for complete blood count (CBC) using a Mindray BC 3000 automatic hematology analyzer (Mindray Corporation, China). Parameters measured included WBC count, hemoglobin (Hb), RBC count, hematocrit (HCT), mean corpuscular hemoglobin (MCH), mean corpuscular volume (MCV), mean corpuscular hemoglobin concentration (MCHC), platelet count, red cell distribution width (RDW), mean platelet volume (MPV), platelet crit (PCT), platelet distribution width (PDW), platelet-to-lymphocyte ratio (PLR), and neutrophil-to-lymphocyte ratio (NLR).

Diabetes was defined by the American Diabetes Association (ADA) as having an FPG of 126 mg/dL or higher, confirmed by a second test, and/or the use of glucose-lowering medication. Additionally, individuals who self-reported having diabetes were classified as diabetics.

Physical activity was defined as a combination of work, exercise, and leisure activities, measured as weekly metabolic equivalents of tasks (METs). Smoking status was self-reported, with current smokers defined as those having smoked at least 100 cigarettes in their lifetime, and ex-smokers defined as those who had smoked at least 100 cigarettes but had quit for at least six months.

3.3. Ethical Considerations

All participants provided written informed consent after being fully informed of the study's purpose. The study protocol was approved by the Hormozgan University of Medical Sciences Ethics Committee in accordance with the principles of the Helsinki Declaration (ethics code: IR.HUMS.REC.1398.473).

3.4. Data Analysis

Data were analyzed using SPSS version 25.0. Categorical variables were compared between diabetic and non-diabetic individuals using the chi-squared test, while continuous variables were compared using the independent t-test. Multivariable binary logistic regression was conducted to assess the relationship between hematological indices and T2DM, adjusting for relevant covariates. Odds ratios (ORs) and 95% confidence intervals (CIs) were reported, with a P-value of less than 0.05 considered statistically significant.

4. Results

Overall, 2318 participants from the BKNCD cohort were evaluated in this study. The general characteristics of individuals with and without T2DM are compared in Table 1. Participants with T2DM were significantly older (mean age 53.77 vs. 46.38 years, P < 0.001), had a higher BMI (mean 27.73 vs. 26.24 kg/m², P < 0.001), and exhibited higher systolic (125.72 vs. 115.87 mmHg, P < 0.001) and diastolic blood pressure (DBP) (79.80 vs. 75.77 mmHg, P < 0.001) compared to those without T2DM. The T2DM group also had higher mean total cholesterol (204.34 vs. 199.19 mg/dL, P = 0.036) and triglyceride levels (167.89 vs. 125.77 mg/dL, P < 0.001), as well as lower physical activity levels (mean weekly metabolic equivalent of task (MET) 271.08 vs. 285.59, P < 0.001).

Table 1.

Comparison of General Characteristics Between Individuals with and Without Type 2 Diabetes Mellitus a, b, c

Socio-demographicsDiabetes (n = 530)No Diabetes (n = 1788)P-Value b
Age (y) 53.77 (8.60)46.38 (8.97)< 0.001
Sex
Male226 (42.6)898 (50.2)0.002 c
Female304 (57.4)890 (49.8)
Marital status
Single54 (10.2)133 (7.4)0.041 c
Married476 (89.8)1655 (92.6)
Residence
Urban432 (81.5)1594 (89.1)< 0.001 c
Rural98 (18.5)194 (10.9)
Occupation
Unemployed337 (63.6)870 (48.7)< 0.001 c
Employed193 (36.4)918 (51.3)
Education (y) 4.14 (4.35)6.46 (4.74)< 0.001
Smoking 177 (33.4)527 (29.5)0.085 c
Anthropometrics
BMI (kg/m2) 27.73 (4.88)26.24 (4.92)< 0.001
Blood pressure
SBP (mmHg) 125.72 (18.28)115.87 (15.79)< 0.001
DBP (mmHg) 79.80 (17.74)75.77 (10.04)< 0.001
Lipid profile (mg/dL)
Total cholesterol204.34 (52.31)199.19 (39.00)0.036
TG167.89 (143.39)125.77 (69.72)< 0.001
LDL124.58 (38.43)126.98 (32.68)0.770
HDL 47.23 (10.77)47.38 (10.39)0.192
Physical activity
Weekly activity 271.08 (39.20)285.59 (46.24)< 0.001

Regarding hematological indices, the T2DM group had significantly higher WBC counts (mean 7.60 vs. 6.85 × 10⁹/L, P < 0.001), higher PDW (mean 15.50 vs. 14.40%, P < 0.001), and lower RDW (mean 13.10 vs. 13.30%, P = 0.043) compared to non-diabetic individuals (Table 2).

Table 2

. Comparison of Hematological Indices Between Individuals with and Without Type 2 Diabetes Mellitus a, b

VariablesDiabetes (n = 530)No Diabetes (n = 1788)P-Value b
WBC count6.82 (1.86)6.42 (1.89)< 0.001
RBC count4.93 (0.66)4.86 (0.65)0.024
Hb (g/dL)13.02 (1.94)12.93 (1.99)0.360
HCT (%)39.47 (5.48)39.02 (5.38)0.096
MCV (fL)80.47 (8.26)80.94 (9.10)0.262
MCH (pg)26.52 (3.27)26.75 (3.56)0.170
MCHC (g/dL)32.93 (1.74)33.07 (1.95)0.129
RDW (%)14.17 (1.45)14.34 (1.72)0.043
Plt count (×109/L)258.50 (83.94)261.84 (74.30)0.379
MPV (fL)9.19 (0.80)9.04 (0.82)< 0.001
PDW (%)15.50 (0.50)15.42 (0.40)< 0.001
PCT (%)0.24 (0.07)0.23 (0.06)0.705
PLR112.44 (42.91)122.66 (43.65)< 0.001
NLR1.68 (0.62)1.71 (0.72)0.300

Binary logistic regression analysis (Table 3) showed that after adjusting for age, sex, education, marital status, place of residence, occupation, smoking, BMI, SBP, DBP, and physical activity, each 10⁹/L increase in WBC count was associated with a 7% higher odds of T2DM (aOR = 1.066, 95% CI 1.003; 1.133, P = 0.039). Additionally, each one percent increase in RDW decreased the odds of T2DM by approximately 20% (aOR = 0.801, 95% CI 0.716; 0.895, P < 0.001). Moreover, each one percent increase in PDW increased the odds of T2DM by 63% (aOR = 1.625, 95% CI 1.159; 2.279, P = 0.005).

Table 3.

Binary Logistic Regression Analysis for the Association of Hematological Indices with Type 2Diabetes Mellitus

Independent VariablescOR (95% CI)P-ValueaOR (95% CI)P-Value
Age (y)1.088 (1.076; 1.100)< 0.0011.076 (1.061; 1.092)< 0.001
Sex
Male1.000
Female1.357 (1.116; 1.650)0.0021.566 (1.072; 2.287)0.020
Education (y)0.888 (0.867; 0.910)< 0.0010.978 (0.949; 1.008)0.144
Marital status
Single1.412 (1.013; 1.968)0.0420.836 (0.561; 1.246)0.380
Married1.000
Residence
Rural1.000
Urban0.537 (0.412; 0.699)< 0.0010.519 (0.380; 0.708)< 0.001
Occupation
Unemployed1.000
Employed0.543 (0.444; 0.663)< 0.0011.123 (0.813; 1.551)0.481
Smoking1.200 (0.975; 1.476)0.0851.167 (0.900; 1.514)0.245
BMI (kg/m2)1.061 (1.041; 1.082)< 0.0011.073 (1.048; 1.099)< 0.001
SBP (mmHg)1.034 (1.028; 1.040)< 0.0011.022 (1.011; 1.033)< 0.001
DBP (mmHg)1.039 (1.029; 1.049)< 0.0010.985 (0.968; 1.003)0.095
Weekly activity (METs)0.991 (0.988; 0.993)< 0.0010.995 (0.992; 0.998)0.002
WBC count (× 109/L)1.110 (1.057; 1.167)< 0.0011.066 (1.003; 1.133)0.039
RBC count (× 1012/L)1.186 (1.023; 1.375)0.0240.586 (0.173; 1.866)0.352
HCT (%)1.015 (0.997; 1.034)0.0971.096 (0.945; 1.272)0.227
MCH (pg)0.982 (0.955; 1.009)0.1900.814 (0.649; 1.021)0.074
MCHC (g/dL)0.963 (0.915; 1.014)0.1541.131 (0.939; 1.362)0.195
RDW (%)0.937 (0.879; 0.998)0.0430.801 (0.716; 0.895)< 0.001
MPV (fL)1.251 (1.112; 1.406)< 0.0011.071 (0.923; 1.244)0.364
PDW (%)1.713 (1.293; 2.270)< 0.0011.625 (1.159; 2.279)0.005
PLR0.994 (0.992; 0.997)< 0.0010.997 (0.994; 1.000)0.096

5. Discussion

This population-based study revealed that, after controlling for potential confounders, WBC count, RDW, and PDW were significantly associated with T2DM. The association with WBC count and PDW was positive, while the correlation with RDW was negative.

We found that for every 109/L increase in WBC count, the odds of T2DM increased by approximately 7%. The mean WBC count was significantly higher in T2DM patients than in individuals without T2DM. Similar findings were reported by Ebrahim et al., although their results did not reach statistical significance, likely due to a smaller sample size and lack of adjusted analysis (9). Conversely, Twig et al. concluded that even within the normal range, WBC count was an independent risk factor for diabetes in young men (10). A systematic review and meta-analysis of 20 studies also indicated a higher risk of T2DM with elevated WBC, although the authors noted that the relationship may have been overestimated due to publication bias and incomplete adjustment for confounders (11). Other studies have also shown that WBC count independently predicts incident T2DM (12), though some, such as Mahdiani et al., found no association between elevated WBC count and insulin resistance (13). Despite some inconsistencies, many studies link elevated WBC count with glucose metabolism disorders and diabetes complications (14, 15).

The link between chronic inflammation and T2DM has been widely studied, with low-grade inflammation thought to contribute to insulin resistance and metabolic dysfunction (16). Elevated WBC count, a classic marker of inflammation, may reflect the pro-inflammatory state in T2DM patients due to metabolic stress and oxidative damage in insulin-sensitive tissues (17, 18). This could explain our study's positive correlation between WBC count and T2DM, though the magnitude of this effect was relatively small.

Our study also found that each one percent increase in RDW decreased the odds of T2DM by nearly 20%. RDW, which measures variability in RBC size, is typically elevated in conditions associated with impaired erythropoiesis and systemic inflammation (19, 20). Increased RDW has been linked to poor prognosis in various conditions, including T2DM, as systemic inflammation and deficiencies in iron and folate may interfere with RBC production (21, 22). Interestingly, our study found that T2DM patients had significantly lower RDW levels compared to non-diabetic individuals, which contrasts with other studies reporting elevated RDW in T2DM patients (23-25). These differences may be related to glycemic control, as suggested by Alamri et al., who found that lower RDW values were associated with worse glycemic control (26). Although we could not assess glycemic control in our cohort, the lower RDW levels observed may indicate that many of our T2DM patients had uncontrolled diabetes.

Additionally, we found that PDW values were significantly higher in T2DM patients, and each one percent increase in PDW was associated with a 63% higher odds of T2DM. This finding aligns with studies by Atak et al. and others, which reported higher PDW values in T2DM patients, particularly those with poor glycemic control (27, 28). Platelet distribution width reflects variability in platelet size and is considered a marker of platelet activation (29, 30). T2DM patients are prone to increased platelet reactivity due to metabolic abnormalities, oxidative stress, and insulin resistance, which heighten their risk for hypercoagulability and cardiovascular complications (31, 32).

5.1. Strengths and Limitations

A key strength of this study is its population-based design and large sample size. Additionally, we controlled for many potential confounders in assessing the association between hematological indices and T2DM. However, there are several limitations. First, although BKNCD is a cohort study, we analyzed cross-sectional data from the first phase, preventing us from establishing causality. Second, logistic regression analysis tends to overestimate ORs, so the results should be interpreted cautiously. Third, we did not have data on the glycemic control status of T2DM patients, which may have influenced the results. Lastly, there was an age mismatch between the diabetes and non-diabetes groups, which could affect hematological indices despite age adjustment in the regression models.

5.2. Conclusions

Type 2 diabetes mellitus patients in this study exhibited increased WBC count and PDW, reflecting inflammation and hypercoagulability, while their RDW was surprisingly lower, potentially due to poor glycemic control. Future longitudinal data from the BKNCD cohort will help clarify the relationship between hematological indices and the development of T2DM over time.

Acknowledgements

References

  • 1.

    Sun H, Saeedi P, Karuranga S, Pinkepank M, Ogurtsova K, Duncan BB, et al. IDF Diabetes Atlas: Global, regional and country-level diabetes prevalence estimates for 2021 and projections for 2045. Diabetes Res Clin Pract. 2022;183:109119. [PubMed ID: 34879977]. [PubMed Central ID: PMC11057359]. https://doi.org/10.1016/j.diabres.2021.109119.

  • 2.

    Khan MAB, Hashim MJ, King JK, Govender RD, Mustafa H, Al Kaabi J. Epidemiology of Type 2 Diabetes - Global Burden of Disease and Forecasted Trends. J Epidemiol Glob Health. 2020;10(1):107-11. [PubMed ID: 32175717]. [PubMed Central ID: PMC7310804]. https://doi.org/10.2991/jegh.k.191028.001.

  • 3.

    Odegaard AO, Jacobs DJ, Sanchez OA, Goff DJ, Reiner AP, Gross MD. Oxidative stress, inflammation, endothelial dysfunction and incidence of type 2 diabetes. Cardiovasc Diabetol. 2016;15:51. [PubMed ID: 27013319]. [PubMed Central ID: PMC4806507]. https://doi.org/10.1186/s12933-016-0369-6.

  • 4.

    Antwi-Baffour S, Kyeremeh R, Boateng SO, Annison L, Seidu MA. Haematological parameters and lipid profile abnormalities among patients with Type-2 diabetes mellitus in Ghana. Lipids Health Dis. 2018;17(1):283. [PubMed ID: 30545361]. [PubMed Central ID: PMC6293632]. https://doi.org/10.1186/s12944-018-0926-y.

  • 5.

    Asmah RH, Yeboah G, Asare-Anane H, Antwi-Baffour S, Archampong TN, Brown CA, et al. Relationship between oxidative stress and haematological indices in patients with diabetes in the Ghanaian population. Clin Diabetes Endocrinol. 2015;1:7. [PubMed ID: 28702226]. [PubMed Central ID: PMC5471723]. https://doi.org/10.1186/s40842-015-0008-2.

  • 6.

    Kaur R, Kaur M, Singh J. Endothelial dysfunction and platelet hyperactivity in type 2 diabetes mellitus: molecular insights and therapeutic strategies. Cardiovasc Diabetol. 2018;17(1):121. [PubMed ID: 30170601]. [PubMed Central ID: PMC6117983]. https://doi.org/10.1186/s12933-018-0763-3.

  • 7.

    Hillson R. Diabetes and the blood – red cells. Practical Diabetes. 2015;32(4):124-6. https://doi.org/10.1002/pdi.1939.

  • 8.

    Poustchi H, Eghtesad S, Kamangar F, Etemadi A, Keshtkar AA, Hekmatdoost A, et al. Prospective Epidemiological Research Studies in Iran (the PERSIAN Cohort Study): Rationale, Objectives, and Design. Am J Epidemiol. 2018;187(4):647-55. [PubMed ID: 29145581]. [PubMed Central ID: PMC6279089]. https://doi.org/10.1093/aje/kwx314.

  • 9.

    Ebrahim H, Fiseha T, Ebrahim Y, Bisetegn H. Comparison of hematological parameters between type 2 diabetes mellitus patients and healthy controls at Dessie comprehensive specialized hospital, Northeast Ethiopia: Comparative cross-sectional study. PLoS One. 2022;17(7). e0272145. [PubMed ID: 35895700]. [PubMed Central ID: PMC9328522]. https://doi.org/10.1371/journal.pone.0272145.

  • 10.

    Twig G, Afek A, Shamiss A, Derazne E, Tzur D, Gordon B, et al. White blood cells count and incidence of type 2 diabetes in young men. Diabetes Care. 2013;36(2):276-82. [PubMed ID: 22961572]. [PubMed Central ID: PMC3554323]. https://doi.org/10.2337/dc11-2298.

  • 11.

    Gkrania-Klotsas E, Ye Z, Cooper AJ, Sharp SJ, Luben R, Biggs ML, et al. Differential white blood cell count and type 2 diabetes: systematic review and meta-analysis of cross-sectional and prospective studies. PLoS One. 2010;5(10). e13405. [PubMed ID: 20976133]. [PubMed Central ID: PMC2956635]. https://doi.org/10.1371/journal.pone.0013405.

  • 12.

    Kashima S, Inoue K, Matsumoto M, Akimoto K. White Blood Cell Count and C-Reactive Protein Independently Predicted Incident Diabetes: Yuport Medical Checkup Center Study. Endocr Res. 2019;44(4):127-37. [PubMed ID: 30895902]. https://doi.org/10.1080/07435800.2019.1589494.

  • 13.

    Mahdiani A, Kheirandish M, Bonakdaran S. Correlation Between White Blood Cell Count and Insulin Resistance in Type 2 Diabetes. Curr Diabetes Rev. 2019;15(1):62-6. [PubMed ID: 29357806]. https://doi.org/10.2174/1573399814666180119143026.

  • 14.

    Jiang H, Yan WH, Li CJ, Wang AP, Dou JT, Mu YM. Elevated white blood cell count is associated with higher risk of glucose metabolism disorders in middle-aged and elderly Chinese people. Int J Environ Res Public Health. 2014;11(5):5497-509. [PubMed ID: 24852600]. [PubMed Central ID: PMC4053882]. https://doi.org/10.3390/ijerph110505497.

  • 15.

    Moradi S, Kerman SR, Rohani F, Salari F. Association between diabetes complications and leukocyte counts in Iranian patients. J Inflamm Res. 2012;5:7-11. [PubMed ID: 22334791]. [PubMed Central ID: PMC3278259]. https://doi.org/10.2147/jir.S26917.

  • 16.

    Akash MS, Rehman K, Chen S. Role of inflammatory mechanisms in pathogenesis of type 2 diabetes mellitus. J Cell Biochem. 2013;114(3):525-31. [PubMed ID: 22991242]. https://doi.org/10.1002/jcb.24402.

  • 17.

    Rehman K, Akash MS. Mechanisms of inflammatory responses and development of insulin resistance: how are they interlinked? J Biomed Sci. 2016;23(1):87. [PubMed ID: 27912756]. [PubMed Central ID: PMC5135788]. https://doi.org/10.1186/s12929-016-0303-y.

  • 18.

    Akash MSH, Rehman K, Liaqat A. Tumor Necrosis Factor-Alpha: Role in Development of Insulin Resistance and Pathogenesis of Type 2 Diabetes Mellitus. J Cell Biochem. 2018;119(1):105-10. [PubMed ID: 28569437]. https://doi.org/10.1002/jcb.26174.

  • 19.

    Montagnana M, Cervellin G, Meschi T, Lippi G. The role of red blood cell distribution width in cardiovascular and thrombotic disorders. Clin Chem Lab Med. 2011;50(4):635-41. [PubMed ID: 22505527]. https://doi.org/10.1515/cclm.2011.831.

  • 20.

    Ferreira JP, Girerd N, Arrigo M, Medeiros PB, Ricardo MB, Almeida T, et al. Enlarging Red Blood Cell Distribution Width During Hospitalization Identifies a Very High-Risk Subset of Acutely Decompensated Heart Failure Patients and Adds Valuable Prognostic Information on Top of Hemoconcentration. Medicine (Baltimore). 2016;95(14). e3307. [PubMed ID: 27057905]. [PubMed Central ID: PMC4998821]. https://doi.org/10.1097/md.0000000000003307.

  • 21.

    Al-Kindi SG, Refaat M, Jayyousi A, Asaad N, Al Suwaidi J, Abi Khalil C. Red Cell Distribution Width Is Associated with All-Cause and Cardiovascular Mortality in Patients with Diabetes. Biomed Res Int. 2017;2017:5843702. [PubMed ID: 29359154]. [PubMed Central ID: PMC5735623]. https://doi.org/10.1155/2017/5843702.

  • 22.

    Ye Z, Smith C, Kullo IJ. Usefulness of red cell distribution width to predict mortality in patients with peripheral artery disease. Am J Cardiol. 2011;107(8):1241-5. [PubMed ID: 21296321]. [PubMed Central ID: PMC3209662]. https://doi.org/10.1016/j.amjcard.2010.12.023.

  • 23.

    Biadgo B, Melku M, Abebe SM, Abebe M. Hematological indices and their correlation with fasting blood glucose level and anthropometric measurements in type 2 diabetes mellitus patients in Gondar, Northwest Ethiopia. Diabetes Metab Syndr Obes. 2016;9:91-9. [PubMed ID: 27042134]. [PubMed Central ID: PMC4801204]. https://doi.org/10.2147/dmso.S97563.

  • 24.

    Knychala MA, Garrote-Filho MDS, Batista da Silva B, Neves de Oliveira S, Yasminy Luz S, Marques Rodrigues MO, et al. Red cell distribution width and erythrocyte osmotic stability in type 2 diabetes mellitus. J Cell Mol Med. 2021;25(5):2505-16. [PubMed ID: 33591627]. [PubMed Central ID: PMC7933938]. https://doi.org/10.1111/jcmm.16184.

  • 25.

    Farooqui R, Afsar N, Afroze IA. Role and Significance of Hematological parameters in Diabetes Mellitus. Ann Patholo Lab Med. 2019;6(3):A158-62. https://doi.org/10.21276/apalm.2355.

  • 26.

    Alamri BN, Bahabri A, Aldereihim AA, Alabduljabbar M, Alsubaie MM, Alnaqeb D, et al. Hyperglycemia effect on red blood cells indices. Eur Rev Med Pharmacol Sci. 2019;23(5):2139-50. [PubMed ID: 30915759]. https://doi.org/10.26355/eurrev_201903_17259.

  • 27.

    Atak BM, Duman TT, Aktas G, Kocak MZ, Savli H. Platelet Distribution Width is Associated with Type 2 Diabetes Mellitus and Diabetic Nephropathy and Neuropathy. Nat J Health Sci. 2018;3(3):95-8. https://doi.org/10.21089/njhs.33.0095.

  • 28.

    Jabeen F, Fawwad A, Rizvi HA, Alvi F. Role of platelet indices, glycemic control and hs-CRP in pathogenesis of vascular complications in type-2 diabetic patients. Pak J Med Sci. 2013;29(1):152-6. [PubMed ID: 24353529]. [PubMed Central ID: PMC3809177]. https://doi.org/10.12669/pjms.291.2592.

  • 29.

    Osselaer JC, Jamart J, Scheiff JM. Platelet distribution width for differential diagnosis of thrombocytosis. Clin Chem. 1997;43(6 Pt 1):1072-6. [PubMed ID: 9191563].

  • 30.

    Vagdatli E, Gounari E, Lazaridou E, Katsibourlia E, Tsikopoulou F, Labrianou I. Platelet distribution width: a simple, practical and specific marker of activation of coagulation. Hippokratia. 2010;14(1):28-32. [PubMed ID: 20411056]. [PubMed Central ID: PMC2843567].

  • 31.

    Ferreiro JL, Gómez-Hospital JA, Angiolillo DJ. Platelet abnormalities in diabetes mellitus. Diab Vasc Dis Res. 2010;7(4):251-9. [PubMed ID: 20921090]. https://doi.org/10.1177/1479164110383994.

  • 32.

    Kakouros N, Rade JJ, Kourliouros A, Resar JR. Platelet function in patients with diabetes mellitus: from a theoretical to a practical perspective. Int J Endocrinol. 2011;2011:742719. [PubMed ID: 21869886]. [PubMed Central ID: PMC3159301]. https://doi.org/10.1155/2011/742719.