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. 2017 Sep 5;12(4):534–541. doi: 10.1007/s12105-017-0850-x

Metastases to the Parathyroid Glands: A Comprehensive Literature Review of 127 Reported Cases

Justin L Bauer 2, Sherwin Toluie 3, Lester D R Thompson 1,✉
PMCID: PMC6232203  PMID: 28875280

Abstract

Metastases to the head and neck organs are uncommon, potentially representing the initial presentation of an occult malignancy. Single case reports and small series report metastases to the parathyroid gland, but there is no large review of the literature on secondary tumors involving the parathyroid glands. A review of the English literature between 1950 and 2017 was performed of all metastases or secondary involvement of the parathyroid glands. One hundred and twenty-seven cases of metastatic tumors were reported, although potentially significantly unrepresented in autopsy series (parathyroid glands are not routinely examined) and due to reporting bias. Women were affected more commonly than men (5.8:1; 99 vs. 17, respectively), with a mean age at presentation of 58.5 years, when reported. The most common primary sites of malignancies that metastasized to the parathyroid glands were breast carcinomas (66.9%, n = 85), melanoma (11.8%, n = 15), and lung carcinoma (5.5%, n = 7), with carcinomas representing 86.6% of metastases. Metastases were nearly always identified as part of widely metastatic disease, with only five (3.2%) cases reported as isolated metastases. Tumor-to-tumor metastases comprised 5.5% of all metastases to the parathyroid glands (metastases to parathyroid adenoma). A significant clinical finding of metastases to the parathyroid glands was the development of deranged calcium homeostasis, well beyond the 9 (7.2%) cases with primary parathyroid gland disease present. Although concurrent conditions (renal disease; bone metastases) may partially affect calcium metabolism, the onset of calcium derangement seemed to coincide with parathyroid gland metastases and not systemic disease. In summary, metastases to the parathyroid glands are uncommon, potentially under-recognized in patients who have otherwise widely metastatic tumors. Women are affected more often than men, with breast carcinomas (66.9%) and melanoma (11.8%) the most common primary tumors. Calcium homeostasis is affected, probably as a result of parathyroid gland parenchymal destruction.

Keywords: Parathyroid glands, Parathyroid neoplasms, Parathyroid hormone (PTH), Comorbidity, Calcium, Metastatic tumors, Secondary neoplasms, Breast neoplasms, Lung neoplasms, Melanoma

Introduction

Many tumors metastasize to the head and neck region. However, if lymph node metastases are excluded, organ metastases are uncommon. Specifically, metastases to the parathyroid glands are seldom reported, with only isolated single case reports, small series or autopsy reports that include parathyroid gland involvement in generalized disease. Parathyroid gland tissue is seldom systematically evaluated during a typical autopsy [1, 2]. Great care is taken to preserve parathyroid gland function during thyroid gland surgery [3]. Symptoms, if present at all, are likely to be nonspecific in nature, and thus antemortem manifestations are rare. As a result, the actual incidence and prevalence of cancers metastatic to the parathyroid glands is unknown. One of the few studies to highlight metastases to the parathyroid glands was a prospective study of 160 consecutive cancer death autopsies, identifying parathyroid gland involvement by metastatic tumor in 11.9% of patients [4]. In other series, parathyroid gland involvement was identified in the context of widely metastatic disease, just one of many organs affected [5], while isolated metastases to the parathyroid gland in surgical pathology material as the only metastatic site is exceptional [3, 6–8]. The most comprehensive literature review on the topic thus far was by Shifrin et al. [5], with this report expanding the review of 15 articles to 28 articles in an attempt to more thoroughly elucidate the nature of the metastatic phenomenon.

Methods

A review of English publications between 1950 and 2017 was performed to identify all reported cases of metastases to the parathyroid glands [1–28]. The review was conducted via searches of PubMed and Google Scholar databases using various combinations of search terms “parathyroid gland”, “parathyroid”, “metastasis”, “metastases”, “cancer”, “malignancy”, “endocrine organ”, “autopsy”, “post-mortem”, “neoplasm”, “surgical pathology,” “melanoma”, “sarcoma” and “tumor-to-tumor”. Individual case reports, case series, surgical pathology studies, and autopsy studies were all included. Particular attention was applied to series from the same institution or by the same authors to reduce duplication. All leukemias and lymphomas and direct extension/invasion into the parathyroid gland from adjacent malignancies were excluded, as they are not regarded as true metastases.

Two articles included in this study, namely the Bumpers et al. and Cifuentes et al. articles presented cases from the same institution over the years 1959–1974 [14] and 1971–1990 [22]. Given a 4-year overlap, there may potentially be a small number of repeated cases. Further, the Viadana et al. article includes only breast carcinoma metastatic to endocrine organs, but does not separate out parathyroid glands specifically, but no doubt also has potential overlap [29]. Similar to the Viadana et al. paper, the Patel et al. article contained cases of metastases to the parathyroid gland amongst a larger analysis of autopsy or surgical pathology specimens, but did not provide details as to how many parathyroid metastasis cases were included, and thus were excluded from this analysis [29, 30].

Results

Table 1 includes a listing of all 127 cases of metastasis to the parathyroid glands reported and incorporated into this literature review [1–28]. The vast majority of the cases developed in female patients (n = 99), no doubt accounted for by the high number of breast carcinoma cases (n = 85), with the overall average age when reported, of 58.5 years. Women outnumbered men by 5.8:1 (85.3 vs. 14.7%, respectively). Carcinomas were the most common tumor type (86.6%, n = 110), followed by melanoma (11.8%, n = 15), and sarcoma (1.6%; n = 2). Within the carcinoma category, breast carcinoma (66.9%, n = 85) were most common (Fig. 1) [4, 6, 8, 9, 12, 14, 17–20, 22, 23, 29], with the majority ductal carcinoma, followed by lobular carcinoma, although in many cases the exact tumor type was unspecified (Table 2). Some suggest that lobular carcinomas are more likely to metastasize, but this finding was not identified by others. Similarly, lung and thymic carcinoma were often not further broken down, although neuroendocrine carcinomas (n = 3) were noted. Melanomas were identified from primarily skin primaries (n = 12), although anal and palate (mucosal) sites were also documented, along with an ocular tumor [1, 4, 16]. A soft tissue sarcoma and a rhabdomyosarcoma each metastasized to the parathyroid glands [4]. Thyroid neoplasms most commonly showed direct extension [31], but hematogenous metastases were noted in three cases (Fig. 2). Nearly all of the cases (n = 122) were part of widely disseminated disease at the time of the identification of the parathyroid gland involvement, with only 5 (3.2%) cases reported as isolated metastases [3, 6–8, 28].

Table 1.

Literature review of 127 reported metastases to parathyroid glands (listed in chronological publication order) [1–28]

Author Date Sex Primary Tumor type Tumor-to-tumor metastasisa
Woolner et al. [9] 1958 F Breast Lobular carcinoma Yes
Drickman et al. [10] 1961 M Rectum Adenocarcinoma
F Rectum Adenocarcinoma
King et al. [11] 1964 F Breast Lobular carcinoma
Margolis et al. [12] 1969 F Breast Lobular carcinoma Yes
Horwitz et al. [4] 1972 M Lung nr
M Stomach nr
F Breast nr
F Breast nr
F Breast nr
F Breast nr
F Breast nr
F Breast nr
F Skin Melanoma
F Breast nr
F Thymus Thymoma
F Breast nr
F Skin Melanoma
M Thigh Spindle cell sarcoma
F Skin Melanoma
F Salivary gland Mucoepidermoid carcinoma
M Lung nr
F Breast nr
F Breast nr
F Tongue nr
M Skin Melanoma
F Breast nr
M Skin Melanoma
F Breast nr
F Breast nr
F Breast nr
F Breast nr
F Breast nr
F Breast Lobular carcinoma
F Skin Melanoma
F Breast nr
F Breast nr
M nr (Testis) Carcinoma (? Seminoma)
F Skin Melanoma
M Lung nr
M Prostate nr
F Breast nr
F Anus Melanoma
F Thigh Rhabdomyosarcoma
F Breast nr
F Breast nr
M Kidney Clear cell renal cell carcinoma
F Breast nr
F Breast nr
Borden et al. [13] 1976 M Skin Melanoma
Cifuentes et al. [14] 1979 F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
Schwartz et al. [15] 1982 F Kidney Clear cell renal carcinoma Yes
de la Monte et al. [16] 1983 nr nr Melanoma
nr nr Melanoma
nr nr Melanoma
nr nr Melanoma
nr nr Melanoma
Watanabe et al. [17] F Breast Ductal adenocarcinoma
de la Monte et al. [18] 1984 F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Lobular carcinoma
Inoshita et al. [1] 1985 M Hard palate Melanoma Yes
Gattuso et al. [2] 1988 nr Lung Small cell carcinoma
nr Lung Large cell carcinoma
Hermus et al. [19] F Breast Mammary carcinoma
Goddard et al. [20] 1990 F Breast Lobular carcinoma
Benisovich et al. [21] 1991 F Lung Adenocarcinoma Yes
Bumpers et al. [22] 1993 F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Ductal adenocarcinoma
F Breast Lobular carcinoma
F Breast Lobular carcinoma
F Breast Lobular carcinoma
F Breast Lobular carcinoma
F Breast Lobular carcinoma
F Breast Lobular carcinoma
F Breast Lobular carcinoma
F Breast Lobular carcinoma
Mariette et al. [23] F Breast nr
Tang et al. [24] 2002 nr Thyroid Papillary thyroid carcinoma
nr Thyroid Papillary thyroid carcinoma
Pazaitou-Panayiotou et al. [25] 2005 n/r Thyroid Differentiated thyroid carcinoma
Venkatraman et al. [26] 2006 F Lung Adenocarcinoma PH
Fulciniti et al. [6] 2010 F Breast Ductal adenocarcinoma Yes
Lee, HE et al. [7] 2011 M Liver Hepatocellular carcinoma Yes
Chrisoulidou et al. [3] 2012 nr Thyroid Follicular thyroid carcinoma
Lee et al. [8] 2013 F Breast Ductal adenocarcinoma PH
Shifrin et al. [5] M Thymus Well differentiated neuroendocrine carcinoma PH
Ofo et al. [27] 2014 M Kidney Clear cell renal cell carcinoma
Torregrossa et al. [28] 2016 M Kidney Clear cell renal cell carcinoma (intrathyroidal parathyroid gland)
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aPH parathyroid gland hyperplasia, nr not reported

Fig. 1.

Fig. 1

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Pleomorphic ductal cells are arranged in a glandular formation, representing metastatic breast ductal adenocarcinoma to the parathyroid gland parenchyma

Table 2.

Primary sites of 127 reported malignancies metastatic to the parathyroid glands

Primary site Number of cases
Breast (adenocarcinoma) 85
Skin melanoma 13
Lung (adenocarcinoma and neuroendocrine carcinomas) 7
Unknown 6
Thyroid carcinoma (differentiated) 4
Kidney clear cell renal cell carcinoma 4
Thymic tumors 2
Soft tissue sarcoma (thigh) 2
Rectum adenocarcinoma 2
Liver hepatocellular carcinoma 1
Hard palate melanoma 1
Stomach adenocarcinoma 1
Salivary gland (mucoepidermoid carcinoma) 1
Tongue 1
Prostate adenocarcinoma 1
Anus melanoma 1
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Fig. 2.

Fig. 2

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Tumor deposits of an oncocytic follicular thyroid carcinoma identified within parathyroid gland tissue

Tumor-to-tumor metastasis is uncommon, defined as one tumor metastasizing to another tumor. In this review, 5.5% of the total reported cases of metastases to the parathyroid glands were shown to represent metastases to parathyroid gland adenomas (n = 7; Table 3). An additional three cases had underlying parathyroid hyperplasia affected by metastases [5, 8, 26].

Table 3.

Seven cases of tumor-to-tumor metastasis involving the parathyroid gland [1, 6, 7, 9, 12, 15, 21]

Article Primary malignancy Primary tumor site Secondary tumor
Woolner et al. [9] Carcinoma Breast Parathyroid adenoma
Margolis et al. [12] Poorly differentiated adenocarcinoma Breast Parathyroid adenoma
Schwartz et al. [15] Clear cell carcinoma Kidney Parathyroid adenoma
Inoshita et al. [1] Melanoma Hard palate Parathyroid adenoma
Benisovich et al. [21] Adenocarcinoma Lung Parathyroid adenoma
Fulciniti et al. [6] Infiltrating ductal carcinoma Breast Parathyroid adenoma
Lee et al. [7] Hepatocellular carcinoma Liver Parathyroid adenoma
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Serum calcium levels were reported in only 58 patients. Of these patients, 23 (39.7%) experienced hypercalcemia while 17 patients (29.3%) experienced hypocalcemia, and the remaining patients were eucalcemic. Serum parathyroid hormone levels were reported in 12 patients, with 9 patients (75%) experiencing elevated levels, and only 1 patient (8.3%) reported with a reduced level. Reporting of numbers of parathyroid glands evaluated, number of glands affected and the percent of gland replaced by tumor was inconsistent. However, all eight patients reported to have nearly complete replacement of the parathyroid gland tissue by the metastatic deposit, had hypocalcemia [4, 11, 17, 19, 20, 23]. Four of these eight patients had parathyroid hormone (PTH) values measured, three had elevated PTH levels and one had a low PTH value. Thus, in the patients with elevated PTH levels, it would seem that the remaining parathyroid gland tissue was responding appropriately to the hypocalcemia from a different cause, and resulting in elevated PTH levels.

Discussion

This English literature review from 1950 to 2017 selected 127 reported cases of metastatic disease, which secondarily affected the parathyroid gland tissue. It is likely that clinically significant disease identified during life is uncommon, but that when there is widely disseminated disease, parathyroid gland involvement by metastatic tumors is probably significantly underreported. Horwitz et al. [4] reported a prospective study of 160 cancer patient autopsies, with 11.9% of patients having at least one parathyroid gland with metastatic involvement. de la Monte et al. [16] identified parathyroid gland metastases in 28% of patients with melanoma. In another study, de la Monte et al. [18] reported 6% of 187 patients with breast cancer showed parathyroid gland metastases, while Bumpers et al. [22] reported 24% of patients who died of breast cancer had parathyroid gland involvement. Further, Cifuentes et al. [14] reported that when a parathyroid gland was affected by metastatic breast cancer, an average of 18 other sites throughout the body also contained metastases. Horwitz et al. [4] also reported that parathyroid gland involvement was part of widespread metastases (bone, liver, lymph nodes, lungs, spleen, kidney, heart, gastrointestinal tract, genital system, brain and skin) in addition to other endocrine organs affected (adrenal glands, pituitary gland, thyroid gland and pancreas). Bumpers et al. [22] reported 35% of patients who died of breast cancer had multiple endocrine organs involved with metastatic breast cancer. Thus, it can be extrapolated, in the vast majority of cases, parathyroid gland metastases present as part of widely disseminated disease. Thus, the identification of only 127 cases reported in the literature is probably due to a selection and publication bias, with parathyroid gland involvement in metastatic disease much more common than suggested.

If one considers the incidence of new cancers diagnosed each year, with breast, lung, prostate, colorectal and melanoma listed in descending order of frequency (Cancer Facts & Figures 2017, American Cancer Society, Atlanta, Georgia, accessed 07/10/2017), it is perhaps not surprising that breast (66.9%), melanoma (11.8%) and lung (5.5%) account for the most common tumors that metastasize to the parathyroid glands. However, disease burden, lymphovascular supply, and perhaps embryologic considerations must also be taken into consideration, with reporting bias of tumor types that cause the most disease-related death also contributing. Metastatic pathways may be related, with thyroid, parathyroid, thymus and anterior pituitary derived from branchial arches, via the foregut ultimately. Thus, metastases to these organs are also documented in other foregut derived organs like stomach and pancreas [16]. Functional relationships as suggested by calcium regulation, which include bone, kidney, thyroid and parathyroid glands, may also account for patterns of organ involvement, while several endocrine organs are also commonly simultaneously affected (adrenal, pituitary, parathyroid, thyroid and pancreas) [4, 14, 16, 18, 22]. Thus, the single case reports of isolated metastatic disease to the parathyroid glands alone, as the only metastatic finding in living patients are exceptional [3, 6–8], with widespread disease the more likely scenario. It is of note that metastatic renal cell carcinoma (clear cell carcinoma specifically) to parathyroid glands is very infrequently reported [4, 15, 27, 28], even though late and widespread metastases from renal cell carcinoma are well known [32]. Importantly, the differential diagnostic consideration of a metastatic clear cell carcinoma within the clear cell parathyroid gland parenchyma may prove challenging since both tumors could be PAX8 and RCC immunoreactive. However, a positive reaction with CAIX and CD10 and a negative reaction with chromogranin and parathyroid hormone studies would help confirm a renal cell carcinoma.

Tumor-to-tumor metastases are a well-documented, albeit uncommon, finding. Endocrine organs, kidney, lung, and liver all have a significant blood flow, expressly related to functional requirements of the organ. Blood flow is disrupted by the development of a neoplasm or in the setting of hyperplasia. Thus, the disrupted blood supply or change in blood flow results in entrapment of tumor emboli within the tumor, and tumor-to-tumor metastasis may be seen [1, 6, 7, 9, 12, 21, 32, 33]. All of the tumor-to-tumor metastases in the reported cases were to parathyroid gland adenoma (Table 3). However, several cases also developed in parathyroid gland hyperplasia, another potential source of abnormal architecture and blood flow.

The parathyroid glands function in calcium homeostasis, with PTH secretion integrally related to the interplay of calcium metabolism by bone, kidney, skin and gastrointestinal functions. As such, deranged calcium metabolism reflected through hyper- or hypocalcemia, would be an expected finding. While the calcium levels were not reported in many of the patients, when it was reported, 68.4% of patients experienced either hypercalcemia (38.6%) or hypocalcemia (29.8%) during evaluation. If the patients with parathyroid gland adenoma and hyperplasia are removed from further consideration (n = 9), a significant cohort of patients still manifested calcium abnormalities. Serum parathyroid hormone levels were elevated in 75% of patients tested, while reduced in only 8.3%. These findings may suggest that at least part of the serum calcium abnormalities may be accounted for by destruction or replacement of the parathyroid gland parenchyma by the neoplastic infiltrate, while other factors in cancer patients (low albumin due to cachexia; gut absorption; renal function; bone metastases releasing calcium; paraneoplastic syndromes related to parathyroid hormone related peptide or malignant hyperthermia) contribute to calcium and parathyroid hormone alterations [4, 5, 11, 13, 17, 19–21, 23]. The inability of the glands to produce parathyroid hormone could lead to clinical hypocalcemia, while destruction of the gland by a rapidly growing tumor could also lead to release of stored PTH, flooding PTH into the peripheral circulation and causing abnormal serum calcium levels [5].

In summary, metastatic malignancies to the parathyroid glands usually present in middle aged to older women, who have widely disseminated disease. Breast carcinomas represent the majority of tumors (66.9%), while melanomas are also identified quite commonly (11.8%). Tumor-to-tumor metastases are uncommon (5.5%). Calcium homeostasis is frequently affected, more disproportionately than disseminated disease would suggest, probably as a result of parathyroid gland parenchymal destruction. Thus, parathyroid gland involvement should be considered in patients who have metastatic disease and calcium alterations.

Acknowledgements

A special thanks to Ms. Hannah B. Herrera for her research assistance. The views expressed are those of the authors solely and do not represent endorsement from Southern California Permanente Medical Group.

Funding

No external funding was obtained for this study.

Compliance with Ethical Standards

Conflict of interest

All authors declare that he/she has not conflict of interest as it relates to this research project.

Ethical Approval

All procedures performed in this retrospective data analysis involving human participants were in accordance with the ethical standards of the institutional review board (IRB #5968), which did not require informed consent.

Contributor Information

Justin L. Bauer, Email: jlb@dartmouth.edu

Sherwin Toluie, Email: sherwintoluie@yahoo.com.

Lester D. R. Thompson, Phone: 818-719-2613, Email: Lester.D.Thompson@kp.org

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