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	Cover Letter
Vitamin D Levels and their Relationship to Thyroid Malignancy
Matthew Marino, MD1; Drew Hinson, MS1; Eric R. Siegel, MS2; Jonathon Rutledge, MD1; Donald L. Bodenner, MD, PhD3, 4; Brendan C. Stack, Jr, MD, FACS, FACE1, 4 
Significance of present submission: Vitamin D deficiency, endemic in the USA, has been observed in many cancer patients and thought to be a potential risk factor. We performed a retrospective chart review of 255 patients receiving total (n=197) or completion (n=58) thyroidectomy for both benign (n=190) and malignant disease (n=65) at the University of Arkansas for Medical Sciences  between October 2005 and July 2013. Postoperative 25-hydroxyvitamin D levels were universally collected and reported when available (n=197). Vitamin D levels had a median (quartiles) of 25 (21-37) ng/mL among those with malignant pathology (n=49) versus 27 (19.5-35) ng/mL among those with benign (n=148) pathology; the difference was not statistically significant (P=0.72). There is no correlation between perioperative 25-hydroxyvitamin D status and pathological findings in patients undergoing completion and total thyroidectomy.
Conflicts of Interest/Agreement of: The authors have NO confilict(s) of interest and are in agreement with publication guideliines as determined by the JOR. 
Number of Tables: 3


*Author Information: 1. Department of Otolaryngology-Head and Neck Surgery, University of Arkansas for Medical Sciences (UAMS), Little Rock, AR; 2. Department of Biostatistics, UAMS; 3. Depatment of Geriatrics, UAMS; 4. UAMS Thyroid Center

*Corresponding Author: Corresponding Author: Brendan C. Stack, Jr., MD, FACS, FACE, 4301 W. Markham St. #543, Little Rock, AR 722135 (501) 686-5140; (501) 686-8029 (fax);  HYPERLINK "mailto:bsstack@uams.edu" bsstack@uams.eduVitamin D Levels and their Relationship to Thyroid Malignancy
M Marino, D Hinson, ER Siegel, J Rutledge, DL Bodenner, BC Stack Jr.

Abstract

Vitamin D deficiency, endemic in the USA, has been observed in many cancer patients and thought to be a potential risk factor. We performed a retrospective chart review of 255 patients receiving total (n=197) or completion (n=58) thyroidectomy for both benign (n=148) and malignant disease (n=49) at the University of Arkansas for Medical Sciences  between October 2005 and July 2013. Postoperative 25-hydroxyvitamin D levels were universally collected and reported when available (n=197). Vitamin D levels had a median (quartiles) of 25 (21-37) ng/mL among those with malignant pathology versus 27 (19.5-35) ng/mL among those with benign pathology; the difference was not statistically significant (P=0.72). There is no correlation between perioperative 25-hydroxyvitamin D status and pathological findings in patients undergoing completion and total thyroidectomy.
Key words

Thyroid cancer, vitamin D deficiency, 25-hydroxyvitamin D

Introduction
Thyroid cancer is the most common endocrine-related malignancy, accounting for roughly 1% of all malignant disease. It is more common in females and is the seventh leading cause of new cancer diagnoses in women (SEER) [1]. Approximately 94% of these are differentiated thyroid carcinoma, which derive from follicular epithelial cells and include papillary and follicular carcinomas. To date risk factors  identified for thyroid cancer include iodine deficiency, exposure to ionizing radiation, genetic mutations and genetically inherited familial syndromes such as MEN IIA and IIB, familial adenomatous polyposis, Cowden�s disease, and Gardner�s syndrome.  However, most thyroid malignancies are sporadic with no readily identifiable cause or associated risk factor(s) [2].
Recent data from the National Health and Nutrition Examination Surveys (NHANES) suggest that about one-third of the US population is at risk for vitamin D inadequacy or deficiency [3]. This encompasses individuals with vitamin D levels less than 40 nmol/lit or 16 ng/ml as defined by the Institute of Medicine (IOM) report on dietary reference intakes (DRI) [4]. Deficiencies in Vitamin D have been linked to increased risk of colon, breast, and prostate cancer based on both ecological and population-based cohort studies [5-7]. Additionally, animal studies have demonstrated increased risk of cancer in models that lack the vitamin D receptor gene, which mediates the effect of vitamin D on multiple genes that exert anti-proliferative and anti-metastatic effects on cells [8-9].
 Vitamin D refers to a group of fat-soluble vitamins as well as their metabolites and analogues. D3 or cholecaciferol is produced in skin exposed to sunlight (UV-B).  It then undergoes hydroxylation in the liver to 25-hydroxyvitamin D [25(OH)D] and then again in the kidney to form the physiologically more active metabolite 1,25-dihydroxyvitamin D [1,25(OH)� D].  Plasma 25(OH)D is generally considered the best indicator of overall vitamin D status, since it is determined by the amount of skin exposure to ultraviolet light, the quantity of vitamin D consumed through foods and supplements, and the body's ability to produce D3 in the skin and then to hydroxylate it in the liver [10]. Plasma levels of 25(OH)D usually range between 10 and 50 ng/ml,  In contrast, 1, 25(OH)� D acts as a hormone to increase calcium absorption, and plasma levels are tightly regulated at 30 pg/ml to ensure calcium homeostasis [11].
With the relatively high prevalence of low Vitamin D �as  measured by 25(OH)D�in the US population and its suspected contribution to the development of multiple malignancies, we sought to investigate 25(OH)D and its potential relationship to thyroid cancer.  Limited data exists regarding the relationship between vitamin D levels and the risk of thyroid malignancy.  This study aimed to examine a cohort of patients undergoing either completion or total thyroidectomy and to compare the 25(OH)D levels between those whose surgical pathology was either benign or malignant.
Materials and methods
A retrospective chart review was performed after approval from the IRB at the University of Arkansas for Medical Sciences.  Data were retrospectively collected on consecutive patients who underwent completion and total thyroidectomy at the University of Arkansas for Medical Sciences between October 2005 and August 2013.  Postoperative 25(OH)D levels were collected routinely and reported when available. Values reported were in ng/ml.  Pathology reports were also reviewed and dichotomized as benign or malignant. Additionally, demographic data, which included age, sex, and race, were collected.  
Data were summarized by pathology group (benign vs. malignant) using proportions for categorical data, and using medians and quartiles for continuous data. Pathology groups were compared for differences in proportions via Fisher�s exact test, and for differences in means via Kruskal-Wallis test.� Multivariate logistic regression was used to assess the effect of vitamin D on malignancy while adjusting for potential confounders.  All comparisons employed an alpha=0.05 significance level, and all analyses utilized SAS v9.3 software (The SAS Institute, Cary, NC).
Results 
During the study period, 255 total and completion thyroidectomies were performed.  Total (n=197) was more common than completion (n=58) surgery.  Benign pathology (n=190) was more common than malignant pathology (n=65).  The most common benign pathology was multinodular goiter (69%), followed by Hashimoto�s thyroiditis (7%) and Grave�s disease (14%) (Table 1).  The most frequent malignant diagnosis was papillary carcinoma, which accounted for 77% of malignant diagnoses (Table 1). One hundred and ninety seven patients had complete data sets and 58 did not.   Patients excluded from further analysis for incomplete data had no differences with the study group in terms of proportions of benign and malignant thyroid pathology.
	The median age of those undergoing thyroidectomy was 50 years for those with benign disease compared to 53 years for those with malignant disease (p=0.12). Females more commonly underwent completion and total thyroidectomy than males for both malignant and benign pathology.  In terms of race, whites constituted 83% and blacks constituted 15% of patients undergoing thyroidectomy independent of pathology (Table 2).  Gender was significant for both dichotomized and continuous data.  Females were less likely to have malignant pathology (odds ratio 0.358 (0.158-0.811)).    
	25-hydroxyvitamin D levels were analyzed as both a categorical and continuous variables.  When analyzing vitamin D as a continuous variable, the overall vitamin D level in the cohort had a median (quartiles) of 26 (20�36) ng/ml.  When comparing vitamin D levels as a continuous variable between benign and malignant disease, the medians (quartiles) were 27 (19.5�35) ng/mL in the benign group versus 25 (21�37) ng/mL in the malignant group, and were not statistically different (Kruskal-Wallis P=0.72).  Subjects were also categorized as having vitamin D insufficiency if their serum levels were less than 30 ng/mL, following Endocrine Society Guidelines [12]. Using this definition, rates of vitamin D insufficiency were found to be 59% in the malignant group and 57% in the benign group, and were not significantly different (Fisher�s exact P=0.87) (Table 3).
	Multivariate analysis of low vitamin D status, age, gender, and race only revealed female gender as being significant, odds ratio 0.395 (95% confidence limits, 0.168-0.929).  This odds ratio was for thyroid malignancy and represents risk for cancer for each 1 year increase in age.
Discussion 
Vitamin D deficiency has been linked to multiple malignancies including breast, prostate, and colon cancers.  However, few studies have examined the relationship between thyroid malignancy and vitamin D status, and the outcomes of these studies have demonstrated conflicting results.  As our clinical routine, we measure 25(OH)D in all of our total and completion thyroidectomy patients immediately post operatively.  This moiety of vitamin D is felt to represent total body vitamin D stores best.  We feel this data is important in the post-operative calcium management of these patients who are at risk for post-operative hypoparathyroidism.  Patients found to be vitamin D deficient are repleted by our clinics standard protocol.
One recent pilot study evaluated 25(OH)D status in three groups of patients: patients with benign thyroid nodules, those with active thyroid cancer, and those with treated thyroid cancer.   A total of 111 patients were included and no difference between rates of vitamin D deficiency were identified among the three groups.   In this study, cancer stage and type were also evaluated and no difference in vitamin D status and stage or pathological type of cancer were identified.  This was a pilot study and was therefore limited by small sample size [1]. 
In a study by Penna-Martinez et al, 172 patients with differentiated thyroid carcinoma (DTC) were compared to 321 healthy controls with respect to expression of vitamin D receptor polymorphisms and serum vitamin D levels as measured by 25(OH)D and 1,25(OH)� D.  In this study, patients with DTC had lower circulating levels of 1,25(OH)� D while there was no significant difference in levels of 25(OH)D. This study also demonstrated association of specific alleles and haplotypes of VDR polymorphisms with DTC [13]. A more recent study  by the same group, compared 303 healthy controls to 253 patients with DTC and found a higher risk for DTC conferred by haplotypes within the CYP24A1 gene as well as low levels of  to 1,25(OH)� D in DTC patients [14]. Stepien et al looked at 50 consecutive thyroid cancer patients and compared both 1, 25(OH) � D and 25(OH) D to 27 healthy controls.  There was no difference in 25(OH) D levels; however, there were differences in the 1, 25(OH) � D level in cancer patients compared to controls [15]. Another recent pilot study by Jonklaas et al also examined 25(OH) D levels in addition to thyrotropin and selenium levels.  They demonstrated no association between 25(OH) D levels and cancer diagnosis as well as no association with disease stage [16]. 
	However, at least one study has demonstrated an increased risk of thyroid malignancy in patients with deficient 25(OH) D.  Roskies et al examined the risk of thyroid malignancy in 212 patients based on Vitamin D status.  In this study, they found a relative risk of thyroid malignancy of 2.0 in those with vitamin D deficiency, which was defined as a 25(OH) D level below 37.5 nmol/L [17]. Alternatively, our study demonstrated no relationship between 25(OH) D status and thyroid malignancy.  This seems to support the majority of studies in the literature, although the dataset is limited and somewhat inconsistent.  
Despite this, there does still appear be a potential role for vitamin D metabolism in the development of well-differentiated thyroid carcinoma.    Associations with specific genetic polymorphisms involved in vitamin D metabolism, which may impact the circulating level of 1,25(OH)� D and thereby inhibit its anticancer effects, have been linked to DTC.  
	This study is limited by several factors, including its retrospective nature and lack of randomization.  Additionally, we monitored vitamin D status based on solely on 25(OH)D levels; 1,25(OH)� D levels were not measured.  Measurement of 25(OH)D levels is generally considered the best representation of overall vitamin D status.  However, as discussed above, the literature  suggests that low levels of circulating 1,25(OH)� D, which mediates many of the anti-tumor actions of the vitamin D pathway through the VDR, may be more predictive of thyroid cancer risk. The suggestion then is that patients with the same 25(OH)D level likely have variable cancer risk based on the unique expression of enzymes involved in creation of 1,25(OH)� D which is not necessarily reflected in their 25(OH)D status. Therefore, understanding the potential role of vitamin D in thyroid cancer will involve further investigation into the genetic and molecular aspects of the vitamin D pathway that extend beyond routine laboratory evaluation of 25(OH)D.
References
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h�@�U�jL	h�@�UU�j�h�@�U�j�h�@�U�j�h�@�U�j(h�@�Ujh�@�0JB*UphD��j_h�@�Uh�@�B*phD�jh�@�B*UphD�h�@�6ion, treatment, and prevention of vitamin D deficiency: an Endocrine Society clinical practice guideline. JCEM Jul; 96(7):1911-30.
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17. Roskies M, Dolev Y, Caglar D, et al. (2012) Vitamin D deficiency as a potentially modifiable risk factor for thyroid cancer. J Otolaryngol Head Neck Surg 41(3):160-163.    HYPERLINK "http://www.ncbi.nlm.nih.gov/pubmed/22762696" http://www.ncbi.nlm.nih.gov/pubmed/22762696Table 1 � Pathology of completion and total thyroidectomy patients
Malignant (N=65) n (% of N)Benign (N=190)n (% of N)Papillary50 (77%)Multinodular goiter132 (69%)Follicular6 (9%)Grave�s disease 26 (14%)Hurthle cell7 (11%)Hashimoto�s14 (7%)Medullary1 (2%)Follicular/papillary neoplasm 14 (7%)Other1 (2%)Other4 (2%)
Table 2�Demographics of completion and total thyroidectomy patients
Age in years:
       median (quartiles)
50 (41�61)
53 (41�67)
0.12Sex, n (%)
       Male
       Female
23 (12%)
167 (88%)
17 (26%)
48 (74%)
0.010Race, n (%)
       Black
       White
31 (17%)
155 (83%)
7 (11%)
54 (89%)
0.42
Table 3 � Vitamin D levels in those with benign and malignant thyroid pathology
25(OH)Vit D, ng/mL:
       Median (quartiles)
27 (19.5�35)
25 (21�37)
0.7225(OH)Vit D insufficiency(%)
 
       Yes, <30 ng/mL
       No, e"30 ng/mL

85 (57%)
63 (43%)

29 (59%)
20 (41%)

0.87


















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