CASE REPORT

Jonathan Irish, MD, Section Editor

Collision tumors of the thyroid: A case report and review of the literature Neil Ryan, MRCS(Eng),1* Graham Walkden, MBChB,2 Darko Lazic, MRCPath,3 Paul Tierney, FRCS,1 1

United Bristol Healthcare NHS Trust, ENT Bristol, United Kingdom, 2North Bristol NHS Trust, Surgery Bristol, United Kingdom, 3Great Western Hospital, Histopathology Swindon, United Kingdom.

Accepted 5 December 2014 Published online 30 June 2015 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/hed.23936

ABSTRACT: Background. Collision tumors of the thyroid are a rare pathology that present a diagnostic and treatment challenge. In this report, we present an interesting case and a review of the current literature as to inform management. Methods and Results. An 88-year-old woman presented with acute airway compromise and vocal cord paralysis. CT identified a thyroid mass and widespread metastasis. Histopathology identified the lesion as a collision tumor consisting of a squamous cell carcinoma (SCC) and papillary thyroid carcinoma. The patient was managed with surgery and palliative radiotherapy. However, she died from complications of a lower respira-

tory tract infection. We also present a review of the literature with 33 cases reviewed. Conclusion. Management of collision tumors is complex because of the duality of the pathology. They should be managed in a multidisciplinary team setting and treatment should be patient specific. Generally, the most aggressive neoplasm should guide treatment. We recommend C 2015 Wiley Periodicals, surgical management with adjunct therapy. V Inc. Head Neck 37: E125–E129, 2015

KEY WORDS: thyroid, collision tumor, surgery, cancer, review

INTRODUCTION

Histopathology

Collision tumors are defined as geographically coexistent but histologically distinct and morphologically independent neoplasms.1 In this report, we present the rare case of a collision tumor consisting of a native papillary thyroid malignancy abutting a squamous cell carcinoma (SCC). To our knowledge, this is the second such case reported in the literature.2,3 We also review the literature and present known collision and mixed tumors of the thyroid, outlining their constituents and natural history.

Macroscopically, there was irregular soft tissue measuring 50 3 30 3 25 mm. There was a tumor evident on gross examination of a diameter of at least 30 mm. On microscopic examination, the thyroid was infiltrated with invasive neoplasm. This showed a mixture of papillary and follicular architecture with some of the cells showing enlarged and clear nuclei with inclusions and grooving. The “classical” papillary carcinoma, however, merged imperceptibly with a high-grade neoplastic component that showed a striking contrast in morphological appearance. This component was comprised of sheets of cells that demonstrated epithelioid morphology and squamous appearance, with a high mitotic activity and areas of necrosis.

CASE REPORT An 88-year-old woman of Cantonese descent was transferred to a tertiary head and neck center after developing inspiratory stridor and airway distress. She was noted to have a pronounced goiter. Flexible nasoendoscopy revealed a bilateral vocal cord palsy. The patient proceeded to an emergency surgical tracheostomy and partial thyroidectomy. She had undergone radioiodine therapy for hyperthyroidism 20 years prior. After histopathological diagnosis and discussion at a multidisciplinary team meeting, the patient underwent staging CT, which revealed a lesion in the left apex of the thyroid gland and further metastases.

Immunochemistry The papillary tumor was reactive for CK7, CK19, TTF1, and thyroglobulin. The tumor was negative for CK5/6, P63, and CK20. This immune profile was in keeping with a papillary thyroid carcinoma. Analysis of the epithelioid tumor showed a strong reaction with CK5/6 and p63 and was TTF1 and thyroglobulin negative. This confirmed an SCC.

DISCUSSION Literature review

*Corresponding author: N. Ryan, United Bristol Healthcare NHS Trust, ENT Bristol, Marlborough Street, Bristol BS1 3NU, United Kingdom. E-mail: [email protected]

We undertook a literature search of the Embase, PubMed (including Medline), and Web of Science databases using the search strategy “thyroid AND (collision OR mixed OR composite) AND (tumor$ OR neoplas* OR cancer OR

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malignan* OR nodule$).” This identified 566 articles, which were hand-searched for pertinent articles. Their reference lists were also searched for additional cases. Bilroth first established the criteria for multiple primary tumors in 1879. These were later simplified by Warren and Gates4 to comprise 3 conditions that must be met: (1) each tumor must demonstrate a definite picture of malignancy, (2) each tumor must be distinct, and (3) the possibility that one was a metastatic lesion from the other must be excluded. In total, 33 cases of collision tumors were identified in 27 different publications. They are presented in Table 1. There was predominance toward women (21 cases). Ages ranged from 27 to 84 years, with a mean average of 53.4 years. The main presentation was that of an anterior cervical mass. Three articles reported that their patients were symptomatic at presentation. Metastases were present in the majority of patients at presentation (23 cases) and these were often mixed with a combination of the 2 collision tumors (13 cases). In just 1 case, the fine-needle aspiration cytology detected the collision of 2 distinct tumors. It did, however, successfully identify a malignant pathology in 20 cases, illustrating the importance of this investigation. Treatment was consistently multimodal. Survival data was sporadic at best, allowing no firm conclusions to be drawn. However, long-term survival (>5 years) was reported in 3 cases. Of note, these were all medullary-papillary combinations, which is in line with survival rates for singleton papillary or medullary tumors. Furthermore, of collision tumors involving SCC, 2 patients survived for over 8 months. Clarity of definition aids further discussion. Collision tumors are defined as coexistent geographically but histologically distinct and morphologically independent neoplasms.1 They are a separate entity from mixed tumors, whereby there is a common cell of origin for both tumors. Furthermore, they are distinguished from composite tumors, which have 2 discrete cellular populations.3 Tumors of the thyroid are responsible for approximately 2% of all malignancies in the United States.5 The most common thyroid malignancy is papillary carcinoma, accounting for 80% of cases. Its incidence is increasing.6 Follicular cancers account for around 10% of thyroid cancers, medullary for around 4%, Hurthle cell tumors for around 3%, and anaplastic carcinomas for around 2%.7 Sarcomas or rare types account for a minute proportion of cases. SCCs have been reported to arise de novo within the thyroid but are a highly uncommon primary neoplasm.8 The origin of squamous cells within the thyroid could result from a branchial cyst or a persistent thyroglossal duct. Collision tumors of the thyroid gland are an increasingly common pathology, although they remain rare. A population-based study has placed the incidence of differentiated thyroid cancer and medullary cancer coexistence at 12.3% of all medullary cancers.9 This coincidence was found to be increasing. Metastasis to the thyroid is thought to be rare. Incidence varies depending on source, ranging from 1.25% to 24.2% of autopsy studies.3,10,11 However, clinically relevant incidence lies between 0.05% and 3.1%, which is surprisingly infrequent given the vascularity of thyroid tissue.12–14 The E126

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most common primaries include the kidneys, breasts and lungs.14 Several authors have published hypotheses on the formation of collision tumors. First, Lax et al15 proposed that they arise from a single pluripotent precursor cell. In the reported case, both tumors were found to be carcinomas, lending support to this theory. In the case of medullary and papillary collision tumors in particular, the ultimobranchial body may represent an embryological nest for such a stem cell.16 However, no equivalent has been proposed for SCC. The failing of this “pluripotent precursor cell” theory is that collision tumors involving cell types of distinct embryological origin have been recorded within the thyroid.17 The second theory is of “neoplastic coercion”: a single neoplasm arises and by its very presence alters the microenvironment to promote and facilitate the development of a new second neighboring tumor. Its growth may be further propagated by the shared environmental experience of the tissue; that being a common oncogenic process, such as ionizing radiation, for example. This theory of pathogenesis fails to explain the rarity of these tumors, or define the conditions that need to exist for one tumor to promote the growth of the neighboring tumor. The final theory postulates the “chance meeting” of 2 primary tumors, either by de novo local genesis or a chance deposition of a metastasis next to an unrelated primary tumor.3,18 The thyroid would be an “at-risk” tissue because of its high vascularity. We also note that there remains the possibility of a combination of these theories. For example, consider a chance meeting of 2 tumors, 1 of metastatic origin that is aided in seeding by neoplastic coercion. Specific case reports have alluded to risk factors for the development of collision tumors of the thyroid. Darwish et al19 suggests that lymphocytic infiltration, present in some forms of thyroiditis, may predispose a patient to the condition. Furthermore, in the case of medullary and papillary collision, the risk is thought to be increased by multiple endocrine neoplastic syndromes.20 Ultimately, there is simply not enough data, evidence, or understanding to support or exclude any one hypothesis. Our literature review suggests that, accounting for 20 of 33 cases, the most common collision tumor of the thyroid is that of medullary and papillary carcinomas. These are also the most common singleton tumors of the thyroid. Metastatic deposits were common at presentation (12 cases) within this subgroup, which is consistent with the corresponding rates reported for singleton tumors.21 The next most common combination was SCC and papillary carcinomas, all of which had metastasized at presentation. Again, this is in keeping with metastasis rates among singleton SCC. The treatment of collision tumors poses a unique challenge. As practiced across all oncology, treatment should be developed in a multidisciplinary framework with a patient-centered approach. Intrinsically, the most aggressive singleton tumor identified should inform treatment. In the vast majority of cases found in the literature, the authors adopted multimodal treatment with surgery and adjunct therapy (30 cases). In a noteworthy number of patients, 3 or more modalities were utilized (11 cases).

Italy

Italy

Rossi39 (2005)

Rossi39 (2005)

R&L thyroid

Indian

Israel

India

USA

Jordan

Plauche22 (2012)

Warman2 (2011)

Walveka3 (2006)

Brandwein-Gensier1 (2004) Younes24 (2005)

Japan

Czech Rep

Austria

Shimizu26 (2000)

Ryska27 (2003)

Lax15 (1994)

Austria Korea

Switzerland

Lax15 (1994) Eom28 (2008)

Rausch29 (2009)

Italy

Saudi Arabia

USA

Mattioli (2008)

Meshikh31 (2004)

Papi32 (2003)

30

Austria

Lax (1994)

15

Italy

Fellegara (2007)

25

L thyroid

Iran

Alavi22 (2011)

R thyroid

R&L thyroid

R thyroid

L thyroid

R&L thyroid R thyroid

R&L thyroid

L thyroid

R&L thyroid

L thyroid

L thyroid

R thyroid

R thyroid

L thyroid

R thyroid

Italy

R thyroid

R thyroid

R thyroid

L thyroid

Location

Rossi (2005)

39

USA

Country

Nabili (2007)

40

Authors

F

M

F

F

M F

F

F

M

F

F

F

F

F

F

F

M

M

M

F

F

Gender

TABLE 1. Summary of published thyroid collision tumour cases.

72

39

50

83

28 43

49

49

52

44

30

55

86

65

84

62

32

34

27

61

63

Age

Thyroid mass

Thyroid mass

Enlarged node

Enlarged node Thyroid mass, dysphonia Thryoid mass

Thyroid mass

Thyroid mass

Thyroid mass

Thyroid mass

Thyroid mass

Thryoid mass dysphagia Thyroid mass

Thyroid mass, respiratory distress Thyroid mass

Thyroid mass

Thyroid mass

Thyroid mass

Thyroid mass

Thyroid mass

Thyroid mass

Presentation

MTC

PTC

MTC Atypical follicular cells Atypical squamous cells No cells

Oncocytic tumour & CCT Follicular neoplasm NK

Adenomatous

NK

NK

Foamy macrophages & inflamatory cells Follicular variant of PTC NK

Follicular neoplasm

PTC

NK

PTC

MTC

Carcinoma

FNA

Yes: node (PTC & MTC)

Yes: node (PTC & MTC)

Yes: node (SCC)

Yes: node (PTC & SCC)

Yes: node (MTC & PTC) No

Yes: lung (unknown histology) Yes: nodes (MTC & limited PTC)

Yes: kidney (CCT)

Yes: node (MTCfollicular & MTC)

NK

Yes: node (PTC)

Yes: lung (liposarcoma)

Yes: scalp (SCC)

Yes: local invasion of l ayrnx (SCC)

No

Yes: node (PTC & MTC)

No

No

Yes: lung (adenocarcinoma) Yes: node (PTC)

Spread

MTC: CT, CGA

MTC: CEA, CT MTC-follicular: TG, CEA, CGA PTC: TG Oncocytic: TG CCT: EMA PTC: TG MTC: CEA, CT, CGA, NSE PTC: CT, CGA MTC: NSE, CEA, Phe5, ACTH NK PTC: CK7, TG SCC: p63 SCC: CK5, CK6 PTC: TG, TTF PTC: TTF-1, TG SCC: p63 NK

PTC: CEA, CT MTC:TG NK

PTC: TTF-1 SCC: CK NK

PTC: TTF-1 SCC: CK5

PTC: TG, CK19 MTC: CT, CEA PTC: TG, CK19 MTC: CT, CEA PTC: TG, CK19 MTC: CT, CGA NK

TFF-1 (both), TG (papillary), CEA (lung) CK19, TG, CK34

IHC

NK (i) PTC (ii)SCC (i) PTC (ii) SCC (i) PTC (ii) SCC (i) MTC (ii) PTC (i) MTC

(iii) MTC (i) oncocytic tumour (ii) CCT (i) MTC (ii) PTC (i) MTC (ii) PTC

(i) PTC-follicular (ii) SCC (i) PTC-follicular (ii) liposarcoma (i) MTC (ii) PTC (i) PTC (ii) Hurthie cell carcinoma (i) PTC (ii) MTC-follicular

(i) adenocarcinoma (ii) PTC (i) MTC (ii) PTC (i) MTC (ii) PTC (i) MTC (ii) PTC (i) MTC (ii) PTC (i) follicular carcinoma (ii) PTC (i) PTC (ii) SCC

Tumour

TT, IND, RI, EBR

TT, IND, RI

TT, IND, RI

IT, IND

TT, IND, RI TT, RI, EBR

TT, IND

TT, RI

TT, RI

PT, IND

TT

TT, BLND

STT, EBR

TT, BLND, EBR, RI

PT, EBR, TRAC

TT, EBR

TT, IND

TT, IND

TT, IND

TT, BLND

NK

Therapy

Alive at 6 mo

Alive at 4 y

Alive at 12 mo

NK

Alive at 19 mo Alive at 8 mo

Dead at 3 y

Alive at 3 y

NK

Alive at 20 y

NK

NK

Dead at 21 mo

Alive at 3 mo

Dead by 3 mo

NK

Alive at 12 mo

NK

NK

NK

NK

Survival

Japan

Japan

Italy

Japan

Germany

USA

Seki33 (2004)

Seki33 (2004)

Pastolero16 (1996)

Ishida34 (1985)

Behrend35 (2002)

Gero36 (1988)

Italy

Italy

Turkey

Diongi37(2007)

Giacomelli20 (2007)

Yilmaz38 (2012)

Bahrain

Darwish19 (1995)

R&L thyroid

R&L thyroid

R thyroid

R thyroid

R&L thyroid

R thyroid

R thyroid

R&L thyroid

R thyroid

R&L thyroid

R thyroid

R thyroid

Location

F

M

F

F

F

M

M

M

F

M

F

M

Gender

55

67

69

50

31

65

69

61

31

41

78

36

Age

Thyroid mass

Thyroid mass

Thyroid mass

Thyroid mass

Enlarged node

Thyroid mass

Incidental on ultrasound Thyroid mass

Thyroid mass

Thyroid mass

Thyroid mass

Thyroid mass

Presentation

MTC

NK

PTC

NK

NK

Giant cells

PTC

NK

NK

Follicular cells

MTC

MTC

FNA

No

Yes: node (PTC & MTC)

No

No

Yes: node (MTC)

Yes: node (MTC)

No

No

Yes: node (PTC & MTC)

Yes: node (PTC & MTC)

Yes: node (PTC & MTC)

Yes: node (PTC & MTC)

Spread

(ii) PTC (i) MTC (ii) PTC (i) MTC (ii) PTC (i) MTC (ii) PTC (iii) follicular (i) MTC (ii) PTC (i) MTC (ii) PTC (i) MTC (ii) PTC (i) MTC (ii) PTC (i) MTC (ii) PTC (i) MTC (ii) PTC (i) MTC (ii) PTC (i) MTC (ii) PTC (i) MTC (ii) PTC

PTC: CK19, TG MTC: CEA PTC: TG MTC: CEA PTC: TG MTC: CT, CEA, CGA PTC: NK Follicular: NK MTC: CT, CEA, CGA PTC: TG MTC: CT, CEA PTC: TG MTC: CT PTC: TG MTC: CT PTC: TG NK

MTC: CT, CEA, CGA PTC: TG NK

MTC: CT, CEA, CGA, NSE PTC: NK NK

Tumour

IHC

TT

TT, BLND,

TT, IND, RI

TT, IND, RI

TT, IND, EBR

TT, IND, RI

TT

TT, IND RI,

TT, IND

TT, IND, EBR

PT, IND

TT, IND

Therapy

NK

NK

Alive at 6 mo

Alive at 24 mo

Alive at 16 y

Alive at 6 mo

NK

Alive at 15 mo

NK

NK

Alive at 6 mo

NK

Survival

ACTH: adrenocorticotropic hormone; BLND: bilateral neck dissection; CEA: carcinoembryonic antigen; CGA: chromogranin A; CK: cytokeratin; CT: calcitonin; EBR: external bream radiotherapy; EMA: epithelial membrane antigen; IND: ipsilateral neck dissection; IT; ipsilateral thyroid lobectomy; MTC: medullary thyroid carcinoma; NSE: anti-neuron-specific enolase; PT: partial thyroidectomy; PTC: papillary thyroid carcinoma; RI: radio-iodine; SCC: squamous cell carcinoma; STT: subtotal thyroidectomy; TG: thyroglobulin; TRAC: tracheostomy; TTF: thyroid transcription factor; TT: total thyroidectomy.

USA

Nicolas (2005)

41

Italy

Diongi (2007)

37

Country

Authors

TABLE 1. Continued

COLLISION

Kim et al18 suggests that collision tumors behave more aggressively than singleton tumors. However, looking at the body of information, we find that metastatic and survival rates are consistent with matched singleton pathology.21 The authors of this article would recommend surgical management with an appropriate adjunct therapy, guided by histology, patient state, and preference. To conclude, collision tumors of the thyroid are incredibly rare. They present both a diagnostic and treatment challenge. There has been limited research into their etiology and how clinicians should best manage patients with the condition. Here, we present another case and review the available literature in order to provide a framework for treating this rare and complex pathology.

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TUMORS OF THE THYROID

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Collision tumors of the thyroid: A case report and review of the literature.

Collision tumors of the thyroid are a rare pathology that present a diagnostic and treatment challenge. In this report, we present an interesting case...
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