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Original Research (Original Article) 


Hosam Talal Mashrah et al, 2019;3(11):926–932.

International Journal of Medicine in Developing Countries

Prevalence of Thyroid disorders among patients with Type One Diabetes Mellitus

Hosam Talal Mashrah1*, Raed Saeed Alghamedi1, Abdulaziz Amin Faydh1, Nawaf Eidhah Althobaiti1, Faisal Sultan Alosaimi1, Mona Modhef Algurashi2, Hameed Khashiban Alswat3, Gamal Mohamed Elnemr4

Correspondence to: Hosam Talal Mashrah

*Medical Student, Medical College, Taif University, Saudi Arabia.

Email: Hosam-T-M [at] hotmail.com

Full list of author information is available at the end of the article.

Received: 25 August 2019 | Accepted: 04 September 2019


ABSTRACT

Background:

According to the World Health Organization, up to 18% of the whole population in Saudi Arabia have DM (diabetes mellitus). Thyroid disorders are the most common endocrinal diseases among Type 1 diabetic (T1D) patients. This study aims to investigate the prevalence of thyroid disorders among T1DM patients.


Methodology:

A retrospective study was conducted on 239 patients with T1DM and data on the levels of HgA1c, thyroid stimulating hormone (TSH), T3, and T4 were collected from patients’ files.


Results:

Abnormal levels of HbA1c, TSH, T3, and T4 were present in 99.6%, 11.3%, 69.5%, and 12.1% of patients, respectively. The mean HgA1C was 9.781 ± 2.12, and for TSH it was 3.71± 10.67 uU/ml. The mean value for free T3 level was 6.42 ± 1.320 pmol/l, and for T4 levels it was 11.30 ± 2.486 pmol/l. No statistically significant relationship was found between the levels of HgA1c, TSH, T3, or T4, and both age groups and gender of the participants. T3 levels were significantly higher among pump users compared to multiple daily injections users.


Conclusions:

This study calls for the assessment of thyroid profile in all type 1 diabetic patients in their routine evaluation to allow early detection and management of any thyroid dysfunction among those patients.


Keywords:

Thyroid disorders, type one diabetes mellitus, endocrine disorders, prevalence, Saudi Arabia.


Introduction

Diabetes mellitus (DM) is a widely prevalent disease that may affect any individual at any age [1]. The incidence of DM has risen globally from 108 million in 1980 to 422 million in 2014, according to World Health Organization [1]. Also, the global prevalence of DM among adults over 18 years of age has risen from 4.7% in 1980 to 8.5% in 2014 [1].

Saudi Arabia, as mentioned in a report published in Diabetes UK (January 2013) is the third country in the world rate of type-1 diabetes (T1D) in children aged 14 years and below [2]. Type1 DM is an autoimmune disease that affects children and adolescents [2]. This disease is characterized by the inability of the body to produce insulin due to autoimmune destruction of beta cells in the islets of Langerhans of the pancreas [3]. Therefore, insulin is needed as daily continual replacement therapy to obtain an optimal blood sugar level and so grow properly and healthy [3]. Insulin is a protein that breaks down and digested when taken by mouth and becomes useless [4]. Therefore, it needs to be injected subcutaneously either by a special syringe (insulin pen) or by insulin pump, in which a cartridge stores the insulin as either regular or fast-acting insulin analogues [4].

Thyroid disorders are the most common endocrine diseases among type 1 diabetic patients, especially autoimmune thyroid disorders [3]. The autoimmune thyroid disorders and T1DM have similar pathogenesis and inherited by families. Hence, they may have genetic factors [3]. Generally, the two most common endocrine disorders found in clinical practice are thyroid disorders and DM. These two diseases are found in different populations and different ages [5].

The autoimmune thyroid disorder also called Hashimoto's disease is a condition in which the immune system attacks the thyroid gland [6]. The thyroid gland is a part of the endocrine system, which produces hormones that coordinate many functions of the body [6]. Inflammation from Hashimoto's disease, also known as chronic lymphocytic thyroiditis, often leads to an underactive thyroid gland (hypothyroidism). Signs and symptoms of hypothyroidism include fatigue and sluggishness, increased sensitivity to cold, constipation, pale, dry skin, puffy face, brittle nails, hair loss, enlargement of the tongue, weight gain, muscle aches, tenderness, stiffness, joint pain, muscle weakness, excessive or prolonged menstrual bleeding (menorrhagia), and depression. [7]

Hashimoto's disease is an autoimmune disorder, with unknown cause, in which the immune system creates antibodies that damage the thyroid gland. Some scientists think a virus or bacterium might trigger the response, while others believe a genetic flaw may be involved. A combination of factors, including heredity, sex and age may determine the likelihood of developing the disorder [8]. There is an association between DM and thyroid disorders, and both of them may affect each other [9].

There is a potent human leucocytic antigen (HLA) association between the type 1 diabetes and autoimmune thyroid disease with HLA-DQA and HLA-DQB genes linking [10]. At diagnosis, approximately 25% of the patients with type 1 diabetes have thyroid autoantibodies [11].

Many studies were done to determine the prevalence of thyroid disorders among diabetic patients. Recently, they found an association between autoimmune hypothyroidism and T1DM [12]. A study, on 233 Brazilian children and adolescents suffering from T1DM, found that 23% of them had thyroid disorders, and most of them were females [13]. Another study, on 382 Type 1 diabetic children and adolescents in Poland, found that14.4% of the participants had an elevation in antibodies against thyroid peroxidase [14].

Several studies were done in Saudi Arabia to assess the prevalence of thyroid disorders among patients with type-2 diabetes mellitus [15,16]. According to a careful literature review, only four studies were done in Saudi Arabia to assess the prevalence of thyroid disorders among type 1 diabetic patients.

The first study was done in 2015 on 305 children and adolescents having T1DM. This study reported a significant increase in the risk of developing thyroid dysfunction with a high prevalence of 21.3% [17]. The other study, which was done in 2015 by Al-Agha et al. [18] reported that thyroid dysfunctions due to autoimmune thyroiditis were found in 4.8% of the patients, whereas subclinical hypothyroidism was found in 9.4% of the patients. Another such study, on 200 individuals (100 Type1 and 100 Type2) admitted at the Diabetes Centre in Al Qurayyat Governorate, Al-Jouf, Saudi Arabia, found that 31% of the participants had thyroid dysfunction [19].

A case-control study, done in 2017 on 132 children, reported a higher distribution of anti-glutamic acid decarboxylase (GAD), thyroid autoantibodies antithyroid peroxidase (TPO), and anti-thyroglobulin (TG) among T1DM patients (56.8%, 36.4%, and 19.7%, respectively) compared to a lower prevalence among controls (5.6%, 9.7%, and 4.2%, respectively) [20].

As the studies done in Saudi Arabia on the prevalence of thyroid disorders among patients with type-1 diabetes mellitus are scarce, this study aimed to determine the incidence of thyroid disorders among those patients.


Methodology

The current study was a retrospective study that was conducted at the Diabetes Center of King Abdulaziz Specialist Hospital (KAASH) in Taif City, Saudi Arabia, from March to April 2019.

Electronic files of all the patients who attended the Diabetes Center at the time of the study were included in the study.

By reviewing the patients' files, serum samples were collected from all the participants, diagnosed with T1DM, of any age or sex either managed by multiple daily injections or by continuous subcutaneous insulin infusion. From these patients, a sample of 2 ml of blood was drawn randomly into plain tubes, i.e., without anticoagulants. They were left to clot in the incubator at 37°C and then centrifuged for ~ 15 minutes. This was followed by separation of the supernatant serum for thyroid function tests [thyroid stimulating hormone (TSH), free T4, and free T3] to determine the prevalence of thyroid disease among T1DM by using BECKMAN COULTER access 2 and for HbA1c by using SIEMENS dimension®.

The total number of patients included in the study were 239, 163 of them were using multiple daily injections (MDI) and 76 of them were using the insulin pump.

Normal value according to the lab:

HgA1c: from 5.7 to <6.5 (borderline), ≥6.5 (high).

TSH: 0.340–5.600 uU/l.

T3: 3.80–6.00 pmol/dl.

T4: 7.90–14.40 pmol/dl.

Table 1. Prevalence of normal and abnormal values of HbA1c, TSH, T3, and T4 levels.

Parameter Normal Abnormal
HbA1c level 1 (0.4%) 238 (99.6%)
TSH level 212 (88.7%) 27 (11.3%)
T3 level 37 (30.5%) 166 (69.5%)
T4 level 210 (87.9%) 29 (12.1%)

Table 2. Relationship between participants’ age groups and HbA1c, TSH, T3, and T4 levels.

Parameter Toddlers Preschool Age School age Teenage Adult Pearson
Chi-Square
p-value
HbA1c
Normal
Low
High
0
0
2
0
0
1
0
1
9
1
5
162
0
1
57
2.57 0.958
TSH
Normal
Low
High
1
0
1
1
0
0
9
0
1
151
2
15
50
0
8
5.355 0.719
T3
Normal
Low
High
0
0
2
0
0
1
2
0
8
43
2
123
28
0
30
12.992 0.112
T4
Normal
Low
High
2
0
0
1
0
0
8
0
2
145
5
18
54
1
3
3.771 0.877

Table 3. Relationship between participants’ gender and HbA1c, TSH, T3, and T4 levels.

Parameter Gender Pearson
Chi-Square
p-value
Male Female
HbA1c
Normal
Low
High
1
3
109
0
4
122
1.170 0.557
TSH
Normal
Low
High
101
1
11
111
1
14
0.124 0.939
T3
Normal
Low
High
22
1
90
51
1
74
12.992 0.112
T4
Normal
Low
High
97
2
14
113
4
9
2.272 0.321

Data of this research were collected and analyzed using the Statistical Package of Social Sciences Version [23]. Quantitative data were expressed as mean and standard deviation (Mean ± SD), where the independent sample ‘t’ test was used to compare the values based on the normality of data. Qualitative data were expressed as numbers and percentages, and the Chi-square (χ2) analysis was used to test the relationship between variables. A p-value of <0.05 was considered as statistically significant. Spearman correlation test was done to assess the relationship between the non-parametric variables.


Results

In the present study, the sample size was 239, 126 (52.7%) of them were females and 113 (47.3%) were males. The mean age of all the participants was 16.65 ± 6.13. The mean HgA1C level in all the participants was 9.781 ± 2.12, and for TSH, it was 3.71 ± 10.67 uU/ml.

The mean value for T3 level was 0.42 ± 1.320 pmol/l, and for T4 levels it was 11.30 ± 2.486 pmol/l. The prevalence of normal and abnormal values of HbA1c, TSH, T3, and T4 levels are shown in Table 1. We categorized HgA1C levels based on the ranges given as High (≥6.5%), Borderline (5.7 - <6.5%), and Normal (<5.7%).

When the association of the HgA1C levels with age was done, there was no statistically significant association present (p > 0.05). The relationship of gender with HbA1c levels also had no statistically significant association (p > 0.05).

The TSH levels were categorized into three groups; Low (<0.34 uU/ml), Normal (0.34–5.6uU/ml), and High level (>5.6 uU/ml) groups. We found out that about 212 (88.7%) of the participants had ‘Normal’ TSH levels. The abnormality was seen in 27 (11.3%) participants. The levels were high in 25 number of participants (10.5%) and were low in only 2 (0.8%) participants. When TSH was related to age and gender, there was no statistically significant association (p > 0.05).

We also analyzed the T3 levels and then categorized them into high (>6.0 pmol/l), normal (3.8–5.6 pmol/l), and low (<3.8 pmol/l) based on their ranges. It was found that 73 (30.5%) participants were in the normal range. The abnormality was found in 166 (69.5%) number of participants. Among the participants, 164 (68.6%) had high T3 levels; only 2 (0.9%) had low T3 levels. When we associate T3 levels with different age groups, there was no statistically significant association (p > 0.05). The Relationship between participants’ age groups and HbA1c, TSH, T3, and T4 levels is shown in Table 2.

When the relationship of different levels of T3 was assessed for gender, it was found that no statistically significant difference was found between males and females. In the current study, the T4 levels were also categorized into three groups, namely, high (>14.5 pmol/l), low (<7.9 pmol/l), and normal (7.9–14.5 pmol/l) based on the ranges. We found that, among the participants, 209 (87.4%) were in the normal group. The abnormality was seen in 29 (12.1%) participants. Among the participants, 23 (9.6%) had “high” T4 levels, and only 6 (2.5%) had “low” levels. When T4 levels were related to different age categories and gender, it was found that no statistically significant association present (p > 0.05). Relationship between participants’ gender and HbA1c, TSH, T3, and T4 levels is shown in Table 3 and the Relationship between HbA1c levels T3, TSH, and T4 levels is shown in Table 4.

In our study, we had 163 (68.2%) participants on MDI and 76 (31.8%) on the pump. When the relationship of pump usage was associated with T3 levels, there were comparatively “high” levels of T3 in participants who were on the pump with a statistically significant association (p < 0.05). A statistically nonsignificant difference was found between patients on MDI and pump according to the TSH, HbA1c, and T4 levels (p < 0.05) (Table 5).

Table 6 shows that a non-significant positive correlation was found between the mean HgA1C level and the mean age of the participants (r = –0.126, p = 0.52), while a non-significant negative correlation was found between the HgA1C levels and TSH, T3, and T4 levels (r = –0.49, –0.205, and 0.027, respectively, and p = 0.45, 0.7, and 0.67, respectively).


Discussion

The present work aimed to know the prevalence of thyroid disorders among type-1 Diabetes in Taif city, Saudi Arabia. In the present study, patients with abnormal thyroid function represented 11.3% of all the participants. This figure is lower than that reported in a previous Saudi survey done in 2015, where 31% of patients had thyroid dysfunction [19]. This high figure could be explained by carrying out the previous study on diabetic patients with both types (type 1 and type 2).

Table 4. Relationship between HbA1c levels T3, TSH, and T4 levels.

Parameter T3 types Total Pearson
Chi-Square
p-value
HbA1c Levels High Low Normal
HbA1c High 158 2 71 231 0.539 0.969
Normal 1 0 0 1
Low 5 0 2 7
TSH types
High 24 0 205 229 0.990 0.294
Normal 0 0 1 1
Low 1 0 6 7
T4 types
High 23 6 202 231 1.143 0.887
Normal 0 0 1 1
Low 0 0 7 7

Table 5. Comparison between patients with and without pump usage according to HgA1C, TSH, T3, and T4 types.

Variable PUMP NON-PUMP Pearson
Chi-Square
p-value
Frequency Percent Frequency Percent
HgA1C levels High 75 98.7% 156 95.7% 1.504 0.471
Normal 0 0% 1 0.6%
Borderline 1 1.3% 6 3.7%
TSH levels High 11 14.5% 14 8.6% 2.775 0.249
Low 0 0% 2 1.2%
Normal 65 85.5% 147 90.2%
T3 levels High 122 74.8% 42 55.3% 11.179 0.004
Low 2 1.2% 0 0%
Normal 39 23.9% 34 44.7%
T4 levels High 4 5.3% 19 11.7% 2.436 0.296
Low 2 2.6% 4 2.5%
Normal 70 92.1% 140 85.9%

Table 6. Spearman correlation between HbA1c level and each of age, TSH, T3, and T4 levels.

Variable Ha1C level
r p-value
Age 0.126 0.052
TSH level 0.049 0.450
T3 level 0.025 0.700
T4 level 0.027 0.670

The prevalence of thyroid dysfunction reported in the present study is lower than that reported in the research done in 2017 on Saudi children and adolescents having T1DM, where the incidence of thyroid dysfunction was 21.3% [17]. It is also lower than that reported in another Saudi case-control study where the distribution of anti- GAD, thyroid autoantibodies anti-TPO, and anti-TG among T1DM patients was 56.8%, 36.4%, and 19.7%, respectively [20].

On the other hand, the prevalence of thyroid dysfunction observed in the current study is higher than that found in other Saudi studies [18]. This variability in the results of previous studies could be attributed to the different instruments used for measuring the studies laboratory variables and the different reference ranges of those variables.

In the present study, no significant difference was found between males and females participants. According to the presence of thyroid dysfunction, this result is in agreement with that observed in a previous Saudi study [19].

Thyroid hormones and insulin antagonize each other, and change in any one of them may affect the other directly or indirectly [21]. Previous studies have explained the association between diabetes and thyroid dysfunction by the disturbance of thyroid function by DM by affecting both the hypothalamic control of TSH production and the transformation of T4 to T3 in the peripheral tissue [22]. Diabetic medications were also found to increase the TSH level as they suppress the T3 and T4 levels and subsequently increases the TSH level [23]. Insulin also increases the T4 level and decreases the T3 level by suppressing the hepatic conversion of T4 to T3 [24]. Another cause is autoimmune diseases [25], or the presence of thyroid antibodies in diabetic patients [26].

The present study did not assess the level of the autoantibodies anti-TPO among the studied patients. However, the anti-TPO level was determined in a previous Saudi study and the distribution of anti-TPO, T1DM patients were 36.4% [20].

Other international studies measured the level of anti-TPO among type 1 DM patients. In a survey conducted in Ajou University Hospital, South Korea, a long term followup study showed there was a significant relationship between autoimmune thyroiditis among T1DM. Up to 30% of patients had high thyroid antibodies. This research investigated anti-TPO [27]. Our study lacked anti-TPO testing.

Another study that was conducted in Poznan, Poland, there were high TPO among long-standing T1D. 53% of females had high TPO. The HgA1c and TSH show insignificant relation to gender. [28] In the present study, the TPO levels were not measured.

In a study conducted in Sao Paulo, Brazil, the serum T3 and free T3 levels were lower in patients with diabetes (p < 0.001) and for free T4, there was an insignificant relationship with T1D [29]. This study was contradictory to the results of the current research, which shows a nonsignificant relationship between the levels of Hg A1C and T3 and T4 levels. However, the present work showed that 11.3% of patients had abnormal TSH level, 69.5% had unusual T3 level, and 12.1% had abnormal T4 level. The observed difference between the present study and other studies could be due to the usage of different instrument and reference ranges in measuring the standards of the laboratory variables. It could also be attributed to being a high altitude city (Taif city), different area and country, a matter that needs more studies to explain that difference.

Also, in a study conducted in Bucharest, Romania, the thyroid autoimmunity is present among T1DM. Among the participants, 18% were positive for thyroid antibody (anti-TPO) [30]. Because of the lack of TPO test in our study, we do not know if there is a relation. But, the high percentage of patients with an abnormal level of T3 in the present study (69.5%) may indicate the presence of sub-clinical thyroid disorder.

A limitation of the present work was the small sample size and conducting the study on diabetic patients from a hospital setting.


Conclusion

The present study showed that 11.3% of the patients had abnormal TSH level, 69.5% had abnormal T3 level, and 12.1% had abnormal T4 level. Also, nearly all the patients had poor compliance with HgA1c. No significant relation in HgA1c, TSH, and T4 to the age, sex, and MDI or pump users. This study called for the assessment of thyroid profile in all type 1 diabetic patients in their routine evaluation to allow early detection and management of any thyroid dysfunction among those patients. Also, an assessment of the TPO level was done to detect autoimmunity.


List of Abbreviations

DM Diabetes mellitus
GAD Glutamic acid decarboxylase
HLA Human leucocytic antigen
MDI multiple daily injections

Conflicts of interest

The authors declare that there is no conflict of interest regarding the publication of this article.


Funding

None.


Consent for publication

Informed consent was obtained from all the participants.


Ethical approval

The research Ethics center at the Research Center at King Abdulaziz Specialist Hospital KAASH approved the study. There was no contact with patients because we are using Electronic files only. IRB Registration Number With KACST, KSA: HAP-02-T-067, Approval number: 168, Date 30 /12 /2018.


Author details

Hosam Talal Mashrah1, Raed Saeed Alghamedi1, Abdulaziz Amin Faydh1, Nawaf Eidhah Althobaiti1, Faisal Sultan Alosaimi1, Mona Modhef Algurashi2, Hameed Khashiban Alswat3, Gamal Mohamed Elnemr4

  1. Medical Student, Medical College, Taif University, Saudi Arabia
  2. Nurse, Diabetic and Endocrinology center, King Abdulaziz Specialist Hospital, Saudi Arabia
  3. Diabetic and Endocrinology center, King Abdulaziz Specialist Hospital, Saudi Arabia
  4. Department of Internal Medicine, College of Medicine, Taif University, Saudi Arabia

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How to Cite this Article
Pubmed Style

Mashrah HT, Alghamdi RS, Faydh AA, Althobati NE, Alosimi FS, Alqurashi MM, Alswat HK, Elnemr GM. Prevalence of Thyroid disorders among patients with Type One Diabetes Mellitus. IJMDC. 2019; 3(11): 926-932. doi:10.24911/IJMDC.51-1566748654


Web Style

Mashrah HT, Alghamdi RS, Faydh AA, Althobati NE, Alosimi FS, Alqurashi MM, Alswat HK, Elnemr GM. Prevalence of Thyroid disorders among patients with Type One Diabetes Mellitus. https://www.ijmdc.com/?mno=62683 [Access: October 15, 2021]. doi:10.24911/IJMDC.51-1566748654


AMA (American Medical Association) Style

Mashrah HT, Alghamdi RS, Faydh AA, Althobati NE, Alosimi FS, Alqurashi MM, Alswat HK, Elnemr GM. Prevalence of Thyroid disorders among patients with Type One Diabetes Mellitus. IJMDC. 2019; 3(11): 926-932. doi:10.24911/IJMDC.51-1566748654



Vancouver/ICMJE Style

Mashrah HT, Alghamdi RS, Faydh AA, Althobati NE, Alosimi FS, Alqurashi MM, Alswat HK, Elnemr GM. Prevalence of Thyroid disorders among patients with Type One Diabetes Mellitus. IJMDC. (2019), [cited October 15, 2021]; 3(11): 926-932. doi:10.24911/IJMDC.51-1566748654



Harvard Style

Mashrah, H. T., Alghamdi, . R. S., Faydh, . A. A., Althobati, . N. E., Alosimi, . F. S., Alqurashi, . M. M., Alswat, . H. K. & Elnemr, . G. M. (2019) Prevalence of Thyroid disorders among patients with Type One Diabetes Mellitus. IJMDC, 3 (11), 926-932. doi:10.24911/IJMDC.51-1566748654



Turabian Style

Mashrah, Hosam Talal, Raed Saeed Alghamdi, Abdulaziz Amin Faydh, Nawaf Eidhah Althobati, Faisal Sultan Alosimi, Mona Modhef Alqurashi, Hameed Khashiban Alswat, and Gamal Mohamed Elnemr. 2019. Prevalence of Thyroid disorders among patients with Type One Diabetes Mellitus. International Journal of Medicine in Developing Countries, 3 (11), 926-932. doi:10.24911/IJMDC.51-1566748654



Chicago Style

Mashrah, Hosam Talal, Raed Saeed Alghamdi, Abdulaziz Amin Faydh, Nawaf Eidhah Althobati, Faisal Sultan Alosimi, Mona Modhef Alqurashi, Hameed Khashiban Alswat, and Gamal Mohamed Elnemr. "Prevalence of Thyroid disorders among patients with Type One Diabetes Mellitus." International Journal of Medicine in Developing Countries 3 (2019), 926-932. doi:10.24911/IJMDC.51-1566748654



MLA (The Modern Language Association) Style

Mashrah, Hosam Talal, Raed Saeed Alghamdi, Abdulaziz Amin Faydh, Nawaf Eidhah Althobati, Faisal Sultan Alosimi, Mona Modhef Alqurashi, Hameed Khashiban Alswat, and Gamal Mohamed Elnemr. "Prevalence of Thyroid disorders among patients with Type One Diabetes Mellitus." International Journal of Medicine in Developing Countries 3.11 (2019), 926-932. Print. doi:10.24911/IJMDC.51-1566748654



APA (American Psychological Association) Style

Mashrah, H. T., Alghamdi, . R. S., Faydh, . A. A., Althobati, . N. E., Alosimi, . F. S., Alqurashi, . M. M., Alswat, . H. K. & Elnemr, . G. M. (2019) Prevalence of Thyroid disorders among patients with Type One Diabetes Mellitus. International Journal of Medicine in Developing Countries, 3 (11), 926-932. doi:10.24911/IJMDC.51-1566748654