Skip to main content
Download PDF

The association between dietary inflammatory index and dietary total antioxidant capacity and Hashimoto’s thyroiditis: a case-control study

BMC Endocrine Disorders volume 24, Article number: 177 (2024) Cite this article

Abstract

Background

Hashimoto’s thyroiditis (HT) is an inflammatory disease characterized by increased reactive oxygen species. Diets rich in anti-inflammatory and antioxidant properties may be linked to a reduced risk of developing HT. The aim of this study was to investigate the association between the dietary inflammatory index (DII) and dietary total antioxidant capacity (DTAC) with HT in Iranian adults.

Methods

The study was a hospital-based case-control study conducted on 230 participants (115 cases and 115 controls). Dietary intake was assessed using a food frequency questionnaire (FFQ). The FFQ data were used to calculate DII and DTAC scores. Anthropometric measurements, thyroid function, and antibody tests were evaluated using standard methods. Multivariable logistic regression analysis was performed in both raw and adjusted models to determine the association between DII and DTAC scores with HT.

Results

The average age of the participants was 39.76 ± 9.52 years. The mean body mass index in the case and control groups was 28.03 ± 6.32 and 26.43 ± 5.13 (kg/m2), respectively (P = 0.036). In the HT group, the DII level was higher (P < 0.001) and the DTAC level was lower than those in the healthy group (P = 0.047). In the multivariable logistic regression model, after adjusting for confounding factors, subjects in the last tertile of DII had a nonsignificantly higher HT risk than those in the first tertile (OR = 1.75; 95% CI = 0.83–3.65; P = 0.130). Regarding DTAC, the subjects in the last tertile of DTAC had a significantly decreased risk of HT (OR = 0.47; 95% CI = 0.23–0.98; P = 0.043) compared to those in the first tertile. The DII had a positive correlation with anti-thyroid peroxidase antibody (anti-TPO), thyroglobulin antibodies (TG-Ab) and thyroid-stimulating hormone, while DTAC had a negative correlation with anti-TPO and TG-Ab (P < 0.050).

Conclusion

The increase in DII is not associated with an increase in the risk of HT, while DTAC can significantly reduce its risk. Having an anti-inflammatory and antioxidative diet can be effective in improving thyroid function. These conclusions should be confirmed in additional prospective studies.

Peer Review reports

Introduction

Hashimoto’s thyroiditis (HT) is the most common autoimmune disorder of the thyroid gland, causing dysfunction, particularly hypothyroidism, through increased inflammatory infiltration over time [1,2,3]. Many environmental and genetic factors, such as ethnicity, age, and sex, contribute to the development of HT [1,2,3,4]. Data shows that up to 79% of predisposition to the disease is due to genetic factors, with the remaining 21% attributed to environmental and sex hormone influences [5].

The global prevalence of HT in adults is estimated to be 7.5%, with a prevalence of 17.5% in women and 6.0% in men. The prevalence of HT varies by geographic region. In a systematic review and meta-analysis study, Africa had the highest prevalence (14.2%), while Asia had the lowest prevalence (5.8%) [6]. It’s incidence is estimated to be 0.8 per 1000 per year in men and 3.5 per 1000 per year in women. The disease affecting women 7–10 times more often than men [5, 7].

According to the findings, when cellular immune tolerance is lost, the production of thyroid autoantibodies increases. These autoantibodies cause the destruction of the thyroid and inflammation, leading to the potential destruction of thyroid cells. This process is triggered by an excessive increase in oxidative stress, beyond what is necessary for producing thyroid hormones. This imbalance prevents the complete neutralization of oxygen free radicals, resulting in mitochondrial dysfunction and ultimately increasing chronic inflammation in the body [8, 9].

Inflammation and oxidative stress are potential causes or aggravating factors of autoimmune thyroid diseases. Antioxidants play a crucial role in reducing oxidative stress and, consequently, inflammation. Therefore, a deficiency or excess of antioxidants may lead to thyroid dysfunction or worsen autoimmune diseases [10]. Research has indicated a negative correlation between two antibodies, thyroglobulin antibodies (Tg-Ab) and anti-thyroid peroxidase antibody (anti-TPO), and the total antioxidant status and oxidative stress index [11]. A meta-analysis revealed lower serum levels of certain antioxidants, such as selenium and zinc, in individuals with hypothyroidism compared to healthy individuals [12]. Another study found that vitamin A, which has antioxidant properties, can directly neutralize free radicals and eliminate lipid peroxides and singlet oxygen, thereby regulating thyroid hormone metabolism and inhibiting thyroid-stimulating hormone (TSH) secretion [13].

In addition to the effects of antioxidants on thyroid function, research has also shown the impact of an anti-inflammatory diet on thyroid diseases. A cross-sectional study demonstrated that decreasing the intake of inflammatory foods, such as animal products, can help reduce oxidative disorders associated with thyroid diseases [14]. Furthermore, a case report study highlighted the benefits of following an anti-inflammatory Paleo diet [15, 16] as a potential solution to alleviate the complications of HT [17].

Due to interaction or synergism, evaluating the consumption of one or more specific antioxidant nutrients alone cannot accurately reflect the antioxidant power of a diet. Additionally, not all dietary antioxidants or their inflammatory effects have been comprehensively investigated in HT disease. Therefore, using tools that can measure the overall impact of all antioxidants and nutrients involved in inflammation may be useful to track the effect of diet on HT. To achieve this concept, it may be possible to use the dietary total antioxidant capacity (DTAC) as a suitable tool to assess the effects of dietary antioxidants and the dietary inflammatory index (DII) to assess the level of dietary inflammation.

DTAC was developed as a quantitative tool to assess the number of dietary antioxidants based on tables obtained from serum samples. It can evaluate total dietary antioxidants without the need for blood samples [18, 19]. The DII, another quantitative tool, has been identified to assess the impact of diet on health outcomes, from blood concentrations of inflammatory cytokines to chronic diseases. It can classify a person’s diet from the highest level of inflammation (high DII score) to the lowest level (low DII score) [20]. The DII has been established to evaluate the inflammatory potential of a diet based on inflammatory and anti-inflammatory food compounds that interact with six biological factors, including interleukin-4 (IL-4), IL-1B, IL-6, IL-10, CRP, and tumor necrosis factor-α (TNF-α) [20].

Considering the difference between the dietary patterns of Middle Eastern countries and Western countries, and the limited number of studies on the effect of DII and DTAC on autoimmune thyroid diseases, especially HT, the present study was conducted to investigate the relationship between DII and DTAC with HT in an Iranian adult population. The hypothesis of the study was that DII can increase the risk of HT, while DTAC can decrease it. The specific research aims of the study were to determine DTAC and DII scores in individuals with HT and healthy participants. The study also aimed to evaluate the relationship between DTAC and DII scores and serum levels of thyroid functional indices, including Anti-TPO, Tg-Ab, TSH, and free T4 (FT4).

Materials and methods

Study design and population

The study was a case-control study conducted between September and December 2022 on patients referred to the two reference endocrinology clinics in Tehran, Iran. The sample size was determined based on a previous study [21] and by G power software [22].

A total of 840 subjects were assessed for the study. The age range of the participants was 20–65 years. The age range of 20–65 years was selected because previous studies have indicated that autoimmune thyroid disorders are age-related [2]. The study subjects (cases and controls) were selected by an endocrinologist after a physical examination and necessary tests (TSH, FT4, TG-Ab, and anti-TPO) to diagnose HT or rule out thyroid diseases. The inclusion criteria were as follows: not having infectious diseases, not using drugs or supplements that change the oxidant and antioxidant status of the body, not taking a higher dose of nonsteroidal anti-inflammatory drugs (> 300 mg/day), and not having any other autoimmune diseases. Healthy subjects were selected from individuals referred to the clinics for thyroid examination. All inclusion criteria were as confounding factors in the study variables. Because of age-related feature of the HT, the subjects in the two groups were matched based on their age.

Before the start of the study and after fully justifying the objectives and methods of the study, written informed consent was obtained from all participants. The study protocol was approved by the Medical Ethics Committee at Tabriz University of Medical Sciences (Registration No: IR.TBZMED.REC.1401.583). All stages of the research were conducted in accordance with the Helsinki Declaration.

Anthropometric measurements

Weight measurements were taken with minimal clothing and without shoes, using a calibrated Seca scale with an accuracy of 0.1 kg. The subject’s height was measured in a standing position, looking forward, without shoes, and with heels against the wall, using a Seca stadiometer with an accuracy of 0.1 cm. Body mass index (BMI) was calculated by dividing weight (kg) by the square of height (m2). Waist circumference was measured with a body measuring tape with an accuracy of 0.1 cm without imposing any pressure on the body at the narrowest point between the last rib and iliac crest at the end of natural exhalation. Hip circumference was measured using a body measuring tape with an accuracy of 0.1 cm in a condition where the person was in a standing position, without additional covering, and measured parallel to the ground at the head of the femur, which is equivalent to the largest circumference of the hips. The waist to hip ratio (WHR) was then calculated by dividing the waist circumference (cm) by the hip circumference (cm). All anthropometric measurements were conducted by a trained and skilled individual.

Assessment of food intake and calculation of DII and DTAC

To determine the DII and the amount of antioxidants consumed in the diet, the individual’s food intake over the past year was assessed using a semiquantitative food frequency questionnaire (FFQ). The FFQ consists of 168 food items that were designed according to the Willett method and were adapted to include Iranian foods. The validity and reliability of this questionnaire have been tested and confirmed [23]. The average size of each food item in the FFQ was explained to every participant in the study. They were then asked to indicate how often they consumed each food item. After noting the frequency of consumption (per day, week, month, or year) for each item in the questionnaire, all the scales were converted to grams using a household scale guide. The energy, macronutrient, and micronutrient content of each food item were analysed using nutritionist IV software.

To calculate the DII, the average global food intake was subtracted from the average daily intake and divided by the global standard deviation. The resulting Z scores were converted into percentiles. The obtained number was multiplied by the inflammatory effect score, and then all the values were added together [20]. Based on scoring, a higher score indicates an inflammatory state, a lower score suggests an anti-inflammatory state, and a zero score indicates a neutral state.

In this study, 33 out of the 45 food parameters listed in the DII table were calculated. These parameters included various vitamins such as A, D, E, B1, B2, B3, B6, B12, C, beta-carotene, caffeine, carbohydrates, total fat, trans fat, saturated fat, protein, cholesterol, polyunsaturated fatty acids (PUFAs), monounsaturated fatty acids (MUFAs), omega 3, omega 6, fiber, energy, magnesium, iron, zinc, selenium, and foods like garlic, onion, tea, pepper, and spices.

The Ferric Reducing Ability of Plasma (FRAP) method was used to calculate DTAC. FRAP values for each food item, were determined using tables from previous studies. The frequency of consumption for each food item per person was converted to grams, then multiplied by the corresponding antioxidant capacity values, and expressed as mmol per 100 g of food (mmol/100 g). The total values were then summed to calculate the dietary total antioxidant capacity for each participant. For Iranian foods which come in various types, such as bread, the overall average consumption was taken into account [24].

Biochemical assessments

Information related to biochemical indices such as TSH, FT4, anti-TPO, and Tg-Ab was collected through tests requested by an endocrinologist or from the last recorded tests in the individuals’ medical files. TSH was measured using a sandwich Enzyme-Linked Immunosorbent Assay (ELISA). Anti-TPO and Tg-Ab were assessed using a sequential ELISA. FT4 levels were determined using an Enzyme Immunoassay (EIA). All tests were performed in a laboratory using laboratory kits from the Monokit brand of Saman Tajhiz Noor, Iran.

Physical activity

To assess the physical activity of participants, the subjects were divided into two groups: those engaging in appropriate physical activity, performing 150–300 min of aerobic activity with moderate intensity, along with muscle strengthening activities of moderate intensity or higher, at least twice a week; and sedentary subjects engaging in physical activity less than the defined amount [25].

Statistical analysis

Means and standard deviations were used for continuous variables, while frequencies and percentages were used for categorical variables. The Kolmogorov‒Smirnov test was employed to assess the normality of the data. Multivariate logistic regression was conducted to examine the association between HT risk among tertiles of DII and DTAC in the crude model and two adjusted models. Model 1 was adjusted for age (years), sex (male/female), and energy, while model 2 further adjusted for BMI, physical activity, and waist circumference.

To calculate the P trend for the odds ratio among DII and DTAC tertiles, the index was considered as a rank variable. Statistical analysis of the data was conducted using IBM SPSS Statistics for Windows, Version 26.0 (IBM Corporation, Armonk, NY, USA), with a P value of < 0.050 considered significant.

Results

The flow chart of the study is presented in Fig. 1. A total of 230 subjects aged between 20 and 65 took part in the study, and their data were analyzed (115 controls and 115 HTs). The mean age and BMI of the participants were 39.76 ± 9.52 years and 27.23 ± 5.8 kg/m2, respectively. In Table 1, the baseline characteristics of the study participants are shown. There were no significant differences between the two groups in terms of mean age, weight, smoking status, WHR, or FT4. However, differences in gender, height, BMI, physical activity, waist and hip circumferences, as well as anti-TPO, TSH, Tg-Ab levels, DII and DTAC were found to be significant. The number of subjects engaging in appropriate physical activity was significantly higher in the healthy group compared to the HT group (P < 0.001). The mean of DII was higher and DTAC was lower in the case group than in the control group (P < 0.001 and P = 0.047, respectively).

Fig. 1
figure 1

Flow chart of the study

Full size image
Table 1 General and biochemical indices of the study population.a
Full size table

In Table 2, dietary intakes in the two groups are shown. The total energy intake in the case group was significantly higher than that in the control group (P < 0.040). The two groups did not have significant differences in protein, carbohydrate, and fat intake. The intake of fiber, vitamin A, vitamin E, vitamin C, vitamin B1, vitamin B3, vitamin B6, vitamin B9, iron, and magnesium in the control group was significantly higher than that in the HT group. In comparison, the intake of omega 6, vitamin B12, and vitamin D in the group with HT was significantly higher than that in the control group. The consumption of fruits, vegetables, legumes, and refined grains in the control group was significantly higher than that in the HT group. The group with HT had a higher consumption of fish and chichen compared to the control group.

Table 2 Selected dietary and nutrients intake among case and control groups.a
Full size table

In Table 3, dietary intakes across tertiles of DII and DTAC in the two groups are displayed. As the tertile of DII increased, there was a significant increase in the intake of carbohydrates, fiber, vitamin B1, vitamin B3, vitamin B9, iron, magnesium, and selenium, while energy intake decreased. For DTAC, the intake of 7 parameters, including carbohydrate, vitamin B3, vitamin B9, magnesium, zinc, nuts, and red meat was significantly higher in the third tertile of DTAC compared to the first tertile.

Table 3 Selected ditary and nutrients intake among tertiles of the dietary inflammatory index and dietary total antioxidant capacity.a
Full size table

The odds ratios of HT in the DII and DTAC tertiles are shown in Table 4. In both the crude and adjusted models, no significant relationship was found between DII and the risk of HT. Similarly, in both the crude and adjusted model 1, no significant association between DTAC and HT risk was found. However, after further adjusting for BMI, waist circumference, and physical activity, the odds of developing HT in the highest DTAC tertile decreased by 53% compared to the lowest tertile (OR = 0.47; 95% CI = 0.23–0.98; P < 0.043).

Table 4 Risk of Hashimoto’s thyroiditis in dietary inflammatory index and dietary total antioxidant capacity tertiles
Full size table

A positive correlation was observed between DII and anti-TPO, Tg-Ab, and TSH. In contrast, a negative correlation was observed between DTAC and anti-TPO and Tg-Ab (Table 5).

Table 5 The correlation between dietary inflammatory index and dietary total antioxidant capacity with laboratory findings
Full size table

Discussion

The results of the current study showed that the mean DTAC was lower in individuals with HT, and that a decrease in DTAC was associated with an increased risk of HT. While the mean DII was higher in HT subjects compared to the control group, there was no statistically significant relationship between DII and HT after adjusting for various confounding variables (Tables 1 and 4).

There are few studies on the relationship between DII and thyroid diseases. Two case-control studies conducted on patients with thyroid cancer showed a positive and significant relationship between thyroid cancer and DII [26, 27]. In the present study, although no correlation was found between DII and the risk of HT disease, a significant and positive correlation was observed between serum thyroid indices (anti-TPO and Tg-Ab, TSH) and DII. This suggests that DII is significantly related to thyroid function and that following an anti-inflammatory diet can help regulate thyroid function in individuals with HT.

These results were similar to those of a cross-sectional study that demonstrated a significant positive relationship between the DII and total T4, T3, FT4, and TSH in a group with iodine deficiency [21]. Chen et al. in a cross-sectional study using data from the National Health and Nutrition Examination Survey (NHANES: 2007 to 2012) database, showed that DII was positively correlated with thyroid function tests such as total T4, and TSH [28].

The association between different dietary patterns and thyroid function has been assessed in many studies. Alkhatib et al. in a study using data from three cycles of the NHANES (2007–2012), showed that dietary patterns such as fat–processed grains–sugars–meats, and oils–nuts–potatoes–low-fat meats are related to hypothyroidism in the U.S. adult population [29]. Additionally, Matana et al., in a study of 1887 participants with and without elevated plasma TPO-Ab and/or Tg-Ab, found that frequent consumption of animal fats and butter-as pro-inflammatory foods- was associated with positive plasma TPO-Ab and/or Tg-Ab. Conversely, frequent consumption of vegetables, dried fruit, nuts, and muesli-as anti-inflammatory foods- was linked to negative findings of TPO-Ab and/or Tg-Ab [30]. In our study, the consumption of fruits, vegetables, legumes, and refined grains in the control group was significantly higher than that in the HT group. Conversely, the HT group consumed more fish and chicken (Table 2). Similar to our findings, Ruggeri et al. showed that HT subjects consumed more meat, fish, and dairy products than the control group, while the control group had a higher intake of legumes, fruits, vegetables, and nuts than the HT group [14]. In contrast to our results on food intake in the HT and control groups, Kalicanin et al. [31] reported that the consumption of red meat and whole grains was higher in healthy individuals than in HT patients. Their study found that HT patients consumed more processed meat than the control group [31].

Building on the current study and past research, the precise influence of specific dietary patterns on thyroid function has yet to be fully established. However, the role of dietary elements such as vitamins and micronutrients in inflammation and thyroid function is well understood. According to the results of the studies, some foods, such as dried fruits, reduce the expression of the IL-6 gene and inhibit the differentiation of T helper-17 (Th17) cells that intervene in the pathogenesis of autoimmune thyroid disease. On the other hand, foods rich in saturated fatty acids (SFA) and carbohydrates lead to an excessive release of inflammatory cytokines (such as IL-6, IL-17, TNF-α), while decreasing anti-inflammatory cytokines such as IL-10 and IL-4. This disrupts the immune balance and increases oxidative stress by CD4+ helper T cells acting against regulatory T cells. Immune system imbalance and oxidative stress ultimately lead to increased inflammation and, consequently, thyroid disorders [32,33,34,35]. Fruits and vegetables, as part of a healthy diet, are rich in fiber, carotene, folate, phytochemicals, various polyphenols, and vitamins B, C, and E. Their antioxidant properties are crucial for reducing inflammation and regulating the immune system in the body [36, 37].

The lack of correlation between DII and HT disease in our study and discrepancies in the results of the effect of dietary patterns on thyroid function could be due to the multifactorial nature of HT. It is important to note that diet is just one of many factors that affect inflammatory processes and thyroid function. Other factors, such as race, climate, age, food composition, and cooking methods, can also impact how different types of food affect thyroid function and thyroid diseases. Additionally, the interplay between environmental factors, and genetic factors can also play a significant role in the development of autoimmune diseases.

Based on the results of the studies, oxidative stress in patients with HT is significantly higher than in healthy individuals, which contributes to increasing inflammation and the oxidative vicious cycle [38, 39]. Reactive oxygen species (ROS) are necessary for the initial stages of thyroid hormone production through iodide oxidation [40, 41]. In other words, ROS play a crucial role in maintaining normal thyroid function. To prevent excessive ROS production, thyroid cells release oxidases that catalyze ROS production. Additionally, the repair system activated by ROS-induced damage helps in the processes of autophagy and apoptosis to eliminate damaged cells. However, research indicates that elevated levels of oxidative stress may be a key factor in the development or worsening of autoimmune thyroid symptoms [8, 42].

The mechanisms of increased oxidative stress in HT and other autoimmune thyroid diseases are not well understood. Several studies suggest that excessive production of free radicals and reactive oxygen species, as well as apoptosis and necrosis, are the main causes of thyroid diseases. Over time, these factors can lead to the failure and malfunction of the thyroid gland [43]. The accumulation of ROS may cause oxidative changes in DNA, proteins, and lipids, acting as an oxidant and predisposing a person genetically to disrupt the oxidative balance and create autoimmune processes with destructive effects on the patient’s body [44]. Furthermore, inflammation can increase oxidative stress through the peroxidation of thyroid epithelial cells and activation of the NOX enzyme (nicotinamide adenine dinucleotide phosphate (NADPH) oxidase). This creates a vicious cycle, where inflammation disrupts the redox balance, and vice versa [45, 46].

There are two mechanisms to combat oxidative stress in our body: enzymatic and nonenzymatic mechanisms. Both mechanisms are related to the food macro- and micro nutrients. Enzymatic systems involve antioxidants such as superoxide dismutase, catalase, glutathione peroxidase, and thioredoxin. Non-enzymatic mechanisms include the action of molecules with strong antioxidant and anti-inflammatory properties, such as catechin, curcumin, ascorbic acid, retinol, carotenoids, tocopherol and other antioxidants [47, 48].

Dietary components play a significant role in the oxidant/antioxidant and inflammatory/anti-inflammatory status of the body [14, 47]. In autoimmune thyroiditis, the total antioxidant capacity of serum is reduced [49], so dietary antioxidants can help the body fight against this condition. In a study on euthyroid women with HT, Ginnakou et al. showed that fruit and vegetable consumption reduces oxidative stress [50].

To date, the overall impact of antioxidants on oxidative stress caused by HT disease is not well defined. It is evident that the body’s antioxidant defense systems against the harmful effects of ROS operate at different levels [47, 51]. Antioxidants can neutralize free radicals by accepting or donating electron(s) to eliminate the free radicals. They have various pathways to target ROS and inhibit oxidative stress. They can scaveng reactive oxygen species, prevent and repair DNA damage, prevent lipid peroxidation, influence and modulate immunue system functions, and modulate signal transduction pathways and gene expression [52,53,54].

Strengths and limitations

Our study had several strengths. One of them was the use of regression models adjusted for potential confounders and the collection of dietary data with a validated FFQ questionnaire. Another strength was the use of the FRAP method to measure the DTAC. The advantage of this method was the inclusion of a wide variety of food items (approximately 3100 items), such as vegetables, spices, drinks, and medicinal plants, compared to other methods [24]. However, it measures antioxidant capacity in vitro, which might not accurately reflect in vivo conditions like as absorption, metabolism, and distribution in tissues, possibly resulting in over or underestimation. Additionally, we did not have FRAP values specifically for Iranian foods. Therefore, we used an international data base, which may not accurately reflect the antioxidant content of Iranian foods due to differences in geographical location and growing conditions. Due to the case-control design of the study, cause-and-effect relationships cannot be defined.

Conclusion

The risk of HT is not related to DII in HT patients, but there is a positive and significant correlation between serum thyroid function indices and DII. DTAC significantly reduces the risk of HT. Consuming an anti-inflammatory and antioxidative diet can be effective in managing autoimmune thyroid diseases like HT. These conclusions should be confirmed in additional clinical and prospective studies with larger sample sizes.

Data availability

No datasets were generated or analysed during the current study.

Abbreviations

Anti-TPO:

Anti-thyroid peroxidase antibody

BMI:

Body mass index

DTAC:

Dietary total antioxidant capacity

DII:

Dietary inflammatory index

FFQ:

Food frequency questionnaire

FRAP:

Ferric reducing ability of plasma

FT4:

Free thyroxin

HT:

Hashimoto’s thyroiditis

ROS:

Reactive oxygen species

TG-Ab:

Thyroglobulin antibodies

TSH:

Thyroid-stimulating hormone

WHR:

Waist-to-hip ratio

References

  1. Ralli M, Angeletti D, Fiore M, D’Aguanno V, Lambiase A, Artico M, et al. Hashimoto’s thyroiditis: an update on pathogenic mechanisms, diagnostic protocols, therapeutic strategies, and potential malignant transformation. Autoimmun Rev. 2020;19(10):102649. https://doi.org/10.1016/j.autrev.2020.102649.

    Article  CAS  PubMed  Google Scholar 

  2. Ragusa F, Fallahi P, Elia G, Gonnella D, Paparo SR, Giusti C, et al. Hashimotos’ thyroiditis: epidemiology, pathogenesis, clinic and therapy. Best Pract Res Clin Endocrinol Metab. 2019;33(6):101367. https://doi.org/10.1016/j.beem.2019.101367.

    Article  PubMed  Google Scholar 

  3. Mikulska AA, Karaźniewicz-Łada M, Filipowicz D, Ruchała M, Główka FK. Metabolic characteristics of Hashimoto’s Thyroiditis patients and the role of microelements and diet in the disease management- an overview. Int J Mol Sci. 2022;23(12). https://doi.org/10.3390/ijms23126580.

  4. Wrońska K, Hałasa M, Szczuko M. The role of the immune system in the course of Hashimoto’s Thyroiditis: the current state of knowledge. Int J Mol Sci. 2024;25(13):6883. https://doi.org/10.3390/ijms25136883.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Mincer DL, Jialal I, Hashimoto Thyroiditis. [Updated 2023 Jul 29]. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2024. https://www.ncbi.nlm.nih.gov/books/NBK459262/

  6. Hu X, Chen Y, Shen Y, Tian R, Sheng Y, Que H. Global prevalence and epidemiological trends of Hashimoto’s thyroiditis in adults: a systematic review and meta-analysis. Front Public Health. 2022;10:1020709. https://doi.org/10.3389/fpubh.2022.1020709.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Klubo-Gwiezdzinska J, Wartofsky L. Hashimoto thyroiditis: an evidence-based guide to etiology, diagnosis and treatment. Pol Arch Intern Med. 2022;132:16222. https://doi.org/10.20452/pamw.16222.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Kochman J, Jakubczyk K, Bargiel P, Janda-Milczarek K. The influence of oxidative stress on thyroid diseases. Antioxidants. 2021;10(9):1442. https://doi.org/10.3390/antiox10091442.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Cheserek MJ, Wu GR, Ntazinda A, Shi YH, Shen LY, Le GW. Association between thyroid hormones, lipids and oxidative stress markers in subclinical hypothyroidism. J Med Biochem. 2015;34(3):323–31. https://doi.org/10.2478/jomb-2014-0044.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Mancini A, Di Segni C, Raimondo S, Olivieri G, Silvestrini A, Meucci E, et al. Thyroid hormones, oxidative stress, and inflammation. Mediators Inflamm. 2016;2016:6757154. https://doi.org/10.1155/2016/6757154.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Tian X, Li N, Su R, Dai C, Zhang R. Selenium Supplementation May decrease thyroid peroxidase antibody titer via reducing oxidative stress in Euthyroid patients with Autoimmune Thyroiditis. Int J Endocrinol. 2020;2020:9210572. https://doi.org/10.1155/2020/9210572.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Talebi S, Ghaedi E, Sadeghi E, Mohammadi H, Hadi A, Clark CCT, et al. Trace element status and hypothyroidism: a systematic review and meta-analysis. Biol Trace Elem Res. 2020;197:1–14. https://doi.org/10.1007/s12011-019-01963-5.

    Article  CAS  PubMed  Google Scholar 

  13. Farhangi MA, Keshavarz SA, Eshraghian M, Ostadrahimi A, Saboor-Yaraghi AA. The effect of vitamin A supplementation on thyroid function in premenopausal women. J Am Coll Nutr. 2012;31(4):268–74. https://doi.org/10.1080/07315724.2012.10720431.

    Article  CAS  PubMed  Google Scholar 

  14. Ruggeri RM, Giovinazzo S, Barbalace MC, Cristani M, Alibrandi A, Vicchio TM, et al. Influence of dietary habits on oxidative stress markers in Hashimoto’s thyroiditis. Thyroid. 2021;31(1):96–105. https://doi.org/10.1089/thy.2020.0299.

    Article  CAS  PubMed  Google Scholar 

  15. Hollywood J, Hutchinson D, Feehery-Alpuerto N, Whitfield M, Davis K, Johnson L. The effects of the Paleo Diet on autoimmune thyroid disease: a mixed methods review. J Am Nutr Assoc. 2023;42(8):727–36. https://doi.org/10.1080/27697061.2022.2159570.

    Article  CAS  PubMed  Google Scholar 

  16. Whalen KA, McCullough ML, Flanders WD, Hartman TJ, Judd S, Bostick RM. Paleolithic and Mediterranean diet pattern scores are inversely associated with biomarkers of inflammation and oxidative balance in adults. J Nutr. 2016;146(6):1217–26. https://doi.org/10.3945/jn.115.224048.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Abbott RD, Sadowski A, Alt AG. Efficacy of the autoimmune protocol diet as part of a multi-disciplinary, supported lifestyle intervention for Hashimoto’s thyroiditis. Cureus. 2019;11(4):e4556. https://doi.org/10.7759/cureus.4556.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Wang Y, Yang M, Lee SG, Davis CG, Koo SI, Chun OK. Dietary total antioxidant capacity is associated with diet and plasma antioxidant status in healthy young adults. J Acad Nutr Diet. 2012;112(10):1626–35. https://doi.org/10.1016/j.jand.2012.06.007.

    Article  CAS  PubMed  Google Scholar 

  19. Puchau B, Zulet MA, de Echávarri AG, Hermsdorff HHM, Martínez JA. Dietary total antioxidant capacity: a novel indicator of diet quality in healthy young adults. J Am Coll Nutr. 2009;28(6):648–56. https://doi.org/10.1080/07315724.2009.10719797.

    Article  PubMed  Google Scholar 

  20. Shivappa N, Steck SE, Hurley TG, Hussey JR, Hébert JR. Designing and developing a literature-derived, population-based dietary inflammatory index. Public Health Nutr. 2014;17(8):1689–96. https://doi.org/10.1017/S1368980013002115.

    Article  PubMed  Google Scholar 

  21. Liu N, Ma F, Feng Y, Ma X. The association between the dietary inflammatory index and thyroid function in US adult males. Nutrients. 2021;13(10):3330. https://doi.org/10.3390/nu13103330.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Faul F, Erdfelder E, Lang A-G, Buchner A. G* power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods. 2007;39(2):175–91. https://doi.org/10.3758/bf03193146.

    Article  PubMed  Google Scholar 

  23. Mirmiran P, Esfahani FH, Mehrabi Y, Hedayati M, Azizi F. Reliability and relative validity of an FFQ for nutrients in the Tehran lipid and glucose study. Public Health Nutr. 2010;13(5):654–62. https://doi.org/10.1017/S1368980009991698.

    Article  PubMed  Google Scholar 

  24. Carlsen MH, Halvorsen BL, Holte K, Bøhn SK, Dragland S, Sampson L, et al. The total antioxidant content of more than 3100 foods, beverages, spices, herbs and supplements used worldwide. Nutr J. 2010;9(3):1–11. https://doi.org/10.1186/1475-2891-9-3.

    Article  Google Scholar 

  25. WHO Guidelines on Physical Activity and Sedentary Behaviour. Geneva: World Health Organization; 2020. PMID: 33369898.

  26. Paquet M, Shivappa N, Hébert JR, Baron-Dubourdieu D, Boutron-Ruault M-C, Guénel P, et al. Dietary inflammatory index and differentiated thyroid carcinoma risk: a population-based case-control study in New Caledonia. Am J Epidemiol. 2020;189(2):95–107. https://doi.org/10.1093/aje/kwz192.

    Article  PubMed  Google Scholar 

  27. Lécuyer L, Laouali N, Hajji-Louati M, Paquet M, Souchard V, Karimi M, et al. Adapted dietary inflammatory index and differentiated thyroid carcinoma risk in two French population-based case–control studies. Eur J Nutr. 2022;61(2):1097–108. https://doi.org/10.1007/s00394-021-02721-x.

    Article  CAS  PubMed  Google Scholar 

  28. Chen SMM, Peng, Yan MM, Zhang, Hao MM, Zou, Yandun MD. Relationship between thyroid function and dietary inflammatory index in Hashimoto thyroiditis patients. Medicine. 2023;102(46):e35951. https://doi.org/10.1097/MD.0000000000035951.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Alkhatib D, Shi Z, Ganji V. Dietary patterns and hypothyroidism in U.S. adult population. Nutrients. 2024;16(3):382. https://doi.org/10.3390/nu16030382.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Matana A, Torlak V, Brdar D, Popović M, Lozić B, Barbalić M, et al. Dietary factors associated with plasma thyroid peroxidase and thyroglobulin antibodies. Nutrients. 2017;9(11):1186. https://doi.org/10.3390/nu9111186.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Kaličanin D, Brčić L, Ljubetić K, Barić A, Gračan S, Brekalo M, et al. Differences in food consumption between patients with Hashimoto’s thyroiditis and healthy individuals. Sci Rep. 2020;10(1):10670. https://doi.org/10.1038/s41598-020-67719-7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Christ A, Lauterbach M, Latz E. Western diet and the immune system: an inflammatory connection. Immunity. 2019;51(5):794–811. https://doi.org/10.1016/j.immuni.2019.09.020.

    Article  CAS  PubMed  Google Scholar 

  33. Procaccini C, Carbone F, Galgani M, La Rocca C, De Rosa V, Cassano S, Matarese G. Obesity and susceptibility to autoimmune diseases. Expert Rev Clin Immunol. 2011;7(3):287–94. https://doi.org/10.1586/eci.11.18.

    Article  CAS  PubMed  Google Scholar 

  34. Manzel A, Muller DN, Hafler DA, Erdman SE, Linker RA, Kleinewietfeld M. Role of Western diet in inflammatory autoimmune diseases. Curr Allergy Asthma Rep. 2014;14(1):404. https://doi.org/10.1007/s11882-013-0404-6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Ruggeri RM, Cristani MT, Crupi F, Molonia MS, Burduja N, Alibrandi A, Campennì A, Cannavò S. Evaluation of paraoxonase activity and association with serum advanced glycation end products as reliable markers of oxidative stress in Hashimoto’s thyroiditis. Minerva Endocrinol (Torino). 2022. https://doi.org/10.23736/S2724-6507.22.03931-8.

    Article  PubMed  Google Scholar 

  36. Kawicka A, Regulska-Ilow B, Regulska-Ilow B. Metabolic disorders and nutritional status in autoimmune thyroid diseases. Postepy Hig Med Dosw (Online). 2015;69:80–90. https://doi.org/10.5604/17322693.1136383.

    Article  PubMed  Google Scholar 

  37. Benvenga S, Ferrari SM, Elia G, Ragusa F, Patrizio A, Paparo SR, Camastra S, Bonofiglio D, Antonelli A, Fallahi P. Nutraceuticals in Thyroidology: a review of in Vitro, and in vivo animal studies. Nutrients. 2020;12(5):1337. https://doi.org/10.3390/nu12051337.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Baser H, Can U, Baser S, Yerlikaya FH, Aslan U, Hidayetoglu BT. Assesment of oxidative status and its association with thyroid autoantibodies in patients with euthyroid autoimmune thyroiditis. Endocrine. 2015;48:916–23. https://doi.org/10.1007/s12020-014-0399-3.

    Article  CAS  PubMed  Google Scholar 

  39. Korkmaz H, Tabur S, Ozkaya M, Oguz E, Elboga U, Aksoy N, et al. Paraoxonase and arylesterase levels in autoimmune thyroid diseases. Redox Rep. 2016;21(5):227–31. https://doi.org/10.1080/13510002.2015.1107310.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Schieber M, Chandel NS. ROS function in redox signaling and oxidative stress. Curr Biol. 2014;24(10):R453–62. https://doi.org/10.1016/j.cub.2014.03.034.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Ameziane-El-Hassani R, Schlumberger M, Dupuy C. NADPH oxidases: new actors in thyroid cancer? Nat Rev Endocrinol. 2016;12(8):485–94. https://doi.org/10.1038/nrendo.2016.64.

    Article  CAS  PubMed  Google Scholar 

  42. Yun HR, Jo YH, Kim J, Shin Y, Kim SS, Choi TG. Roles of autophagy in oxidative stress. Int J Mol Sci. 2020;21(9):3289. https://doi.org/10.3390/ijms21093289.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Rostami R, Aghasi M, Mohammadi A, Nourooz-Zadeh J. Enhanced oxidative stress in Hashimoto’s thyroiditis: inter-relationships to biomarkers of thyroid function. Clin Biochem. 2013;46(4–5):308–12. https://doi.org/10.1016/j.clinbiochem.2012.11.021.

    Article  CAS  PubMed  Google Scholar 

  44. Sharifi-Rad M, Anil Kumar NV, Zucca P, Varoni EM, Dini L, Panzarini E, et al. Lifestyle, oxidative stress, and antioxidants: Lifestyle, oxidative stress, and antioxidants: back and forth in the pathophysiology of Chronic diseases. Front Physiol. 2020;11:694. https://doi.org/10.3389/fphys.2020.00694.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Ruggeri RM, Vicchio TM, Cristani M, Certo R, Caccamo D, Alibrandi A, et al. Oxidative stress and advanced glycation end products in Hashimoto’s thyroiditis. Thyroid. 2016;26(4):504–11. https://doi.org/10.1089/thy.2015.0592.

    Article  CAS  PubMed  Google Scholar 

  46. Matsuo K, Tanahashi Y, Mukai T, Suzuki S, Tajima T, Azuma H, et al. High prevalence of DUOX2 mutations in Japanese patients with permanent congenital hypothyroidism or transient hypothyroidism. J Pediatr Endocrinol Metab. 2016;29(7):807–12. https://doi.org/10.1515/jpem-2015-0400.

    Article  CAS  PubMed  Google Scholar 

  47. Jena AB, Samal RR, Bhol NK, Duttaroy AK. Cellular Red-Ox system in health and disease: the latest update. Biomed Pharmacother. 2023;162:114606. https://doi.org/10.1016/j.biopha.2023.114606.

    Article  CAS  PubMed  Google Scholar 

  48. Sies H, Berndt C, Jones DP. Oxidative stress. Annu Rev Biochem. 2017;86:715–48. https://doi.org/10.1146/annurev-biochem-061516-045037.

    Article  CAS  PubMed  Google Scholar 

  49. Metwalley KA, Farghaly HS, Saad K, Othman HA. Oxidative status in children and adolescents with autoimmune thyroiditis. Clin Exp Med. 2016;16:571–5. https://doi.org/10.1007/s10238-015-0386-x.

    Article  CAS  PubMed  Google Scholar 

  50. Giannakou M, Saltiki K, Mantzou E, Loukari E, Philippou G, Terzidis K, et al. The effect of obesity and dietary habits on oxidative stress in Hashimoto’s thyroiditis. Endocr Connect. 2018;7(9):990–7. https://doi.org/10.1530/EC-18-0272.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Shekhova E. Mitochondrial reactive oxygen species as major effectors of antimicrobial immunity. PLoS Pathog. 2020;16(5):e1008470. https://doi.org/10.1371/journal.ppat.1008470.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Muchtaridi M, Az-Zahra F, Wongso H, Setyawati LU, Novitasari D, Ikram EHK. Molecular Mechanism of Natural Food Antioxidants to regulate ROS in Treating Cancer: a review. Antioxidants. 2024;13:207. https://doi.org/10.3390/antiox13020207.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Ruggeri RM, Barbalace MC, Croce L, Malaguti M, Campennì A, Rotondi M, Cannavò S, Hrelia S. Autoimmune thyroid disorders: the Mediterranean Diet as a protective choice. Nutrients. 2023;15:3953. https://doi.org/10.3390/nu15183953.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Macvanin MT, Gluvic Z, Zafirovic S, Gao X, Essack M, Isenovic ER. The protective role of nutritional antioxidants against oxidative stress in thyroid disorders. Front Endocrinol (Lausanne). 2023;13:1092837. https://doi.org/10.3389/fendo.2022.1092837.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to the study participants for their honest responses and the valuable information they provided.

Funding

The present study was based on the MSc thesis in Nutrition Sciences of S. Alijani and was supported by a grant from the Vice-Chancellor for Research at Tabriz University of Medical Sciences (grant number [Pazhoohan Code]: 70036), Tabriz, Iran. The funder did not have a specific role in the conceptualization, design, data collection, analysis, decision to publish, or preparation of the manuscript.

Author information

Authors and Affiliations

  1. Student Research Committee, Department of Biochemistry and Diet Therapy, Faculty of Nutrition and Food Sciences, Tabriz University of Medical Sciences, Tabriz, Iran

    Sepideh Alijani

  2. Shahid Sardar Soleimani Hospital, Endocrine Clinic, Iran University of Medical Sciences, Tehran, Iran

    Maliheh Ghadir

  3. Nutrition Research Center, Department of Biochemistry and Diet Therapy, Faculty of Nutrition and Food Sciences, Tabriz University of Medical Sciences, Tabriz, Tell, Iran

    Bahram Pourghassem Gargari

Authors
  1. Sepideh Alijani
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maliheh Ghadir
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bahram Pourghassem Gargari
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

B.P.G and S.A designed the research; S.A and M.G implemented the research; SA performed the statistical analyses; B.P.G wrote the article and was responsible for the administration and supervision of the research. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Bahram Pourghassem Gargari.

Ethics declarations

Ethics approval and consent to participate

All participants provided written informed consent before participating in the study. The study protocol was approved by the Medical Ethics Committee at Tabriz University of Medical Sciences (Registration No: IR. TBZMED. REC.1401.583). All research stages were conducted in accordance with the Helsinki Declaration.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alijani, S., Ghadir, M. & Gargari, B.P. The association between dietary inflammatory index and dietary total antioxidant capacity and Hashimoto’s thyroiditis: a case-control study. BMC Endocr Disord 24, 177 (2024). https://doi.org/10.1186/s12902-024-01708-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12902-024-01708-z

Keywords

BMC Endocrine Disorders

ISSN: 1472-6823

Contact us