Metastasis of clear cell renal cell carcinoma to the organs of the head and neck – an ongoing problem

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Metastasis of clear cell renal cell carcinoma to

the organs of the head and neck – an ongoing

problem

Przerzut raka jasnokomórkowego nerki do narządów głowy

i szyi – problem wciąż aktualny

Patrycja Torchalla, Małgorzata Czesak, Ewa Osuch-Wójcikiewicz

Chair and Department of Otorhinolaryngology, Head and Neck Surgery of the Medical University of Warsaw, Poland;

Department Head: Prof. Kazimierz Niemczyk MD PhD

Article history: Received: 18.01.2020 Accepted: 15.02.2021 Published: 16.02.2021

ABSTRACT: Introduction: Renal cell carcinoma accounts for about 2–3% of all malignancies. It is characterized by a high frequency of metastases, which are most often observed in the lungs, bones, liver, brain and regional lymph nodes. Literature highlights the rare occurrence of renal cancer metastases to the head and neck, even though it is the third most common cancer that metastasizes to the head and neck.

Case report: Below we present a case report of metastases of clear cell carcinoma from a kidney to the organs of the head and neck. The analysis was carried out retrospectively based on medical records of a patient hospitalized at the Department of Otorhinolaryngology, Head and Neck Surgery of the Medical University of Warsaw in the years 2009–2019. We describe an 81-year-old man after left-sided nephrectomy due to clear cell carcinoma, with numerous distant metastases, who was diagnosed with metastases to the left submandibular salivary gland 8 years after primary surgery, followed by a diagnosis of metastasis to the right submandibular salivary gland 3 years later. The patient underwent 2 radical procedures to remove the submandibular salivary glands. Due to the presence of lung metastases, treatment with a tyrosine kinase inhibitor was also implemented.

KEYWORDS: clear cell renal cancer, metastases, renal cell carcinoma, submandibular salivary gland

STRESZCZENIE: Wstęp: Rak nerkowokomórkowy stanowi ok. 2–3% wszystkich nowotworów złośliwych. Charakterystyczna dla niego jest wysoka częstotliwość przerzutów, które najczęściej obserwuje się w: płucach, kościach, wątrobie, mózgu oraz regionalnych węzłach chłonnych. W piśmiennictwie podkreślane jest rzadkie występowanie ognisk przerzutowych raka nerki w obrębie głowy i szyi, jednakże stanowi on trzeci co do częstości występowania nowotwów złośliwy przerzutujący do głowy i szyi.

Opis przypadku: Poniżej prezentujemy opis przypadku przerzutów raka jasnokomórkowego nerki do narządów głowy i szyi. Analizy dokonano retrospektywnie na podstawie dokumentacji pacjenta hospitalizowanego w Klinice Otorynolaryn- gologii, Chirurgii Głowy i Szyi Warszawskiego Uniwersytetu Medycznego w latach 2009–2019. Opisujemy przypadek 81-let- niego mężczyzny po nefrektomii lewostronnej z powodu raka jasnokomórkowego nerki, z licznymi przerzutami odległymi, u którego 8 lat po zabiegu operacyjnym wykryto przerzut do ślinianki podżuchwowej lewej, a następnie po 3 latach przerzut do ślinianki podżuchwowej prawej. Pacjenta poddano 2-krotnie radykalnemu zabiegowi chirurgicznemu usunięcia ślinianek podżuchwowych. Ze względu na obecność przerzutów w płucach, wdrożono także leczenie inhibitorem kinazy tyrozynowej.

SŁOWA KLUCZOWE: przerzuty, rak jasnokomórkowy nerki, rak nerkowokomórkowy, ślinianka podżuchwowa

INTRODUCTION

Malignant tumors of the urinary system include tumors of the kidneys, renal pelvis, ureter and bladder. Bladder and kidney tumors

ABBREVIATIONS

RCC – renal cell carcinoma WHO – World Health Organization

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are most common among this group. According to the data from 2018 published by the National Cancer Registry, in Polish popula- tion malignant tumors of the bladder account for 6.7% of all tumors in men and 1.4% in women, while renal tumors account for 3.8% in men and 2.1% in women [1].

Bladder cancer affects mainly men (about 80% of cases) and is the fifth most common malignancy in men. In more than 80% of cases it occurs over the age of 60. The main symptoms include massive hematuria with clots, frequent urination, vesical tenesmus. The most common forms of bladder cancer are transitional cell carcinoma (which accounts for the highest proportion of urinary tract malignancies in developing countries) [2], occurring in about 90%

of cases, followed by adenocarcinoma and squamous cell carcinoma. Bladder cancer usually gives metastases to regional lymph nodes of the pelvis, lungs, liver, bones, and brain. Metastases to distant lymph nodes, especially cervical, are extremely rare and are associated with an adverse prognosis and short survival. Lit- erature describes casuistic cases of metastasis of bladder cancer to the head and neck organs, i.e. cervical lymph nodes [3] or temporal bone [4].

Renal cell carcinoma (RCC) accounts for approximately 2–3% of all malignancies [5–7], making it the most common cancer of the urinary tract in adults [8]. It is twice as common in men than compared to women [9, 10]. The highest morbidity is observed in the 6^th–7^th decades of life [11, 12]. Risk factors for its development include exposure to tobacco smoke, obesity or excess weight, alcohol abuse, and long-term occupational exposure to toxic agents, i.e. arsenic, cadmium, gasoline, petroleum or asbestos. Initially it may remain asymptomatic due to its small size. The classic triad of symptoms, which includes hematuria, palpable abdominal tumor and lumbar pain [9], currently occurs in only 5–10% of patients and reflects an advanced stage of the disease [6]. Contrast computed tomography of the abdomen and pelvis is the method of choice for evaluation of staging tumor. The final diagnosis is determined based on histopathological examination. Tumor staging is assessed based on TNM classification. According to the 2016 World Health Organiza- tion (WHO) classification there are several dozen histological types of RCC, the common including: clear cell carcinoma (65–70%), papillary carcinoma (15–20%), chromophobe carcinoma (5–7%) [13].

The clinical course of RCC is usually unpredictable. Primary tumors differ with regard to the rate of growth and the occurrence of distant metastases. Lang et al. also mention cases of spontaneous regression of primary foci [14].

It is the third most common malignant tumor below the clavicle that metastases to the head and neck following cancers of the breast and lung [14, 15].

Radical nephrectomy (recommended in stages I, II, III) provides approximately 96% of 5-year survival for stage I patients, while only 23% of stage IV patients reach 5-year survival. Targeted therapy us- ing tyrosine kinase inhibitors or mTOR kinase inhibitors is implemented at an advanced stage of the disease. Other methods used in the treatment include immunotherapy with interferon alpha or radiotherapy. Chemotherapy has little therapeutic value [5].

In this publication, we present a case of a patient after left-sided nephrectomy due to clear cell renal cell carcinoma, diagnosed with metastases to the head and neck. In 2013, a case of a patient being treated at the Department due to metastasis of clear cell carcinoma of the kidney to the tongue was reported on [16].

CASE REPORT

In August 2015, an 81-year-old man was admitted to the Depart- ment of Otorhinolaryngology, Head and Neck Surgery of the Warsaw Medical University for surgical treatment of right submandibular salivary gland tumor. Patient’s medical history included hyperten- sion, glaucoma and osteoarthritis, as well as surgery for right testic- ular hydrops. In December 2007, the patient underwent left-sided nephrectomy due to renal cancer (G2, pT1b). Because of the presence of metastases to the lungs, subcutaneous tissue, peritoneum and right adrenal gland in 2012, the patient was treated with pazopanib at the Institute of Oncology.

An ultrasound of the neck performed in June 2015 showed abun- dantly vascularized, solid mass, 24 x 21 x 26 mm in diameter, within left submandibular salivary gland. Aspiration biopsy of the tumor was subsequently performed, revealing protein-rich fluid containing granulocytes, lymphocytes and a few macrophages.

Based on the clinical picture, the patient was qualified for radical excision of the left submandibular salivary gland under general anesthesia. Surgery and postoperative period were uncomplicated. After 3 days, the patient was discharged home in good general condition with recommendations for further follow-up in otolaryngological and oncology outpatient clinics.

Microscopically, histopathological examination of the postoperative material showed metastasis of clear cell renal cell carcinoma; immunohistochemistically: EMA (+), vimentin (+), CD10 (+).

In January 2018, a tumor of the right submandibular region was observed during oncological follow-up. An ultrasound examination of the neck was performed, showing a 14-mm hypoechogenic lesion with central blood flow in the right submandibular salivary gland.

The patient was re-referred for surgical treatment. On admission to the Department physical examination revealed a painless, soft, movable tumor, approx. 2 x 2 cm in diameter in the right submandibular salivary gland.

During hospitalization, radical excision of the right submandibular salivary gland was performed. The perioperative and postoperative period was uncomplicated. Histopathological examination of a 4 x 3.5 x 2.5-cm tissue fragment showed salivary gland with metastatic clear cell renal cell carcinoma. Immunohistochemistically:

CD10+, PAX8+, vimentin+, CKAE1/E3+, mucus-, PAS+.

Patient was discharged home on day 2 post-op in good general condition with recommendations for further follow-up at the Otolar- yngology Clinic and Oncology Clinic.

Patient himself ceased the follow-up visits at the ENT Clinic.

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Tab. I. The time of occurrence of metastases of malignant tumors of the urinary system to the organs of the head and neck (selected Polish literature).

AUTHORS GENDER AND

AGE OF THE PATIENT AT THE TIME OF DETECTION OF METASTASIS

PRIMARY CANCER AND DATE OF ITS DETECTION

LOCATION OF

METASTASIS TIME FROM NEPHROCTOMY TO MANIFESTATION OF METASTASIS

SYMPTOMS OF

METASTASIS SIZE OF

METASTASIS TREATMENT

Wróbel

et al. 1992 [11] M 42 Clear cell carcinoma of

the left and right kidney Laryngopharynx 3 months after left- -sided nephrectomy and enucleation of the tumor from the right kidney

Dysphagia, sensation of a foreign body in the throat, sensory disturbances (tingling, numbness) of the tongue base

No data Surgery and chemotherapy

Pietniczka

the right kidney Maxillo-ethmoid

ridge on the left Metastasis was the first manifestation of renal cancer

Epistaxis No data Surgical

Szlenk

et al. 1994 [25] K 55 K 71 K72

K 72

Clear cell carcinoma of the left kidney

Clear cell carcinoma of the right kidney Clear cell carcinoma of the left kidney

Clear cell renal cell carcinoma – left side

Left nasal cavity and nasal sinuses on the left Left nasal cavity + left maxillary sinus

Maxillary sinuses on the left

Larynx and laryngopharynx with cervical lymph nodes on the right

Metastasis was the first manifestation of renal cancer Metastasis was the first manifestation of renal cancer Metastasis was the first manifestation of kidney cancer 5 years from left- -sided nephrectomy

Epistaxis

Painful tumor in the left frontal region, causing left-sided ptosis

Hoarseness, difficulty swallowing, tumor on the neck on the right

No data

Diameter approx. 3 cm No data

Radiation therapy and surgery Surgical Surgical + palliative

Surgical

Swierz

et al. 1994 [36] K 64 Clear cell carcinoma of the left kidney, no exact date of diagnosis

Right eyeball 3 months after left-

-sided nephrectomy Visual disturbances, right-sided exophthalmos

No data Radiotherapy

Darewicz

et al. 1996 [37] M 62 K 76

Clear cell renal cell carcinoma

Clear cell carcinoma of the right kidney

Cranial vault

Mandible

Metastasis was the first manifestation of renal cancer Metastasis was the first manifestation of renal cancer

No data

Surgical

No data

Lipiński et al.

1998 [33] M 38 Clear cell carcinoma of the right kidney, no exact date of diagnosis

Skin of the left

cheek Metastasis was the

first manifestation of renal cancer

Buccal tumor No data BAC of buccal tumor

Kupajski I. et al. 1999 [34] M 52

M 54

Clear cell renal cell

carcinoma, 1996 Left eyeball

Occipital bone

Metastasis was the first manifestation of renal cancer (1996) 2 years after right- -sided nephrectomy

Loss of vision, pain in the left eye

Occipital pain

No data

Surgical:

enucleation of the left eye

Teleradiotherapy to the occipital area and treatment with interferon alpha Kołacińska

et al. 2001 [35] M 74 Clear cell carcinoma of the right kidney, 2000, Nephrectomy not performed due to contraindications to surgery

Tongue 5 months after being

diagnosed with clear cell renal cell carcinoma

Tongue tumor Diameter

approx. 2 cm Hormonal treatment

Cieszyńska

the right kidney, 1993 Left brain hemisphere, nasal cavity, all paranasal sinuses on the left side, left orbit

7 years after right-

-sided nephrectomy Epistaxis on the left

side No data Palliative

radiotherapy

Jordan

et al. 2004 [32] M 87 K 64

Renal cancer

Clear cell carcinoma of the right kidney

Retroauricular lymph nodes – right side Level II cervical lymph nodes – right side

Metastasis was the first manifestation of renal cancer 9 years after right- -sided nephrectomy

No data No data

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AUTHORS GENDER AND AGE OF THE PATIENT AT THE TIME OF DETECTION OF METASTASIS

PRIMARY CANCER AND DATE OF ITS DETECTION

LOCATION OF

METASTASIS TIME FROM NEPHROCTOMY TO MANIFESTATION OF METASTASIS

SYMPTOMS OF

METASTASIS SIZE OF

METASTASIS TREATMENT

Stodulski

et al. 2006 [27] K 67 K 71 M 69

K 55

Clear cell carcinoma of the left kidney

Clear cell carcinoma of the left kidney Papillary renal cancer – left

Left – sided clear cell renal cell carcinoma

Nasopharynx and right nasal cavity Right parotid gland

Level III/IV cervical lymph nodes on the left side

Right occipital lobe, epiglottis

One month after left- sided nephrectomy

10 years after left- -sided nephrectomy One year after left- -sided nephrectomy

Metastasis was the first manifestation of renal cancer

Nasal obstruction, recurrent bleeding and purulent nasal discharge Tumor in the area of the right mandibular angle

Cervical tumor on the left

Tumor of the right occipital lobe, bleeding from the pharynx

3.5 x 4 x 3 cm

Diameter approx. 3 cm No data

No data

Surgery + palliative chemotherapy Surgical

Surgical: Crile operation Palliative

Stańczyk

the left kidney Mid-pharynx: left

lateral wall 11 months after left-

-sided nephrectomy Recurrent pharyngeal bleeding, sensation of throat obstruction, swallowing problems, shortness of breath

3 x 2 cm Surgical

Kaliszewski

et al. 2007 [8] K 74 Clear cell carcinoma – left side, no exact date of diagnosis

Thyroid gland 20 years after left-

-sided nephrectomy Tachypnea, shortness of breath, chronic dry cough, stridor and hoarseness.

5.2 x 2.6 cm Surgical

Kamiński

et al. 2008 [23] M 69 Clear cell renal cell

cancer – right side, 1995 Nasal cavity and

upper lip 10 years from right-

-sided nephrectomy Epistaxis 1.5 x 1.5 cm Surgical Lewandowski

et al. 2009 [20] K 54 Clear cell carcinoma of the right kidney, no exact date of diagnosis

Mandible 10 years of right-sided

nephrectomy Fetox ex ore, bleeding from the tumor, speech disorders, dysphagia

3 x 3 cm Partial resection

Lewandowski

et al. 2009 [20] M 80 Right-sided clear cell renal cell carcinoma, 2007

Upper gum, alveolar process, hard palate, upper lip mucosa

Unknown time from right-sided nephrectomy

Dysphagia No data Palliative

chemotherapy

Łukawska

the left kidney, 1999 Tongue 13 years from left-

-sided nephrectomy Tumor of the root of the tongue on the right side

1.7 x 2.45 cm Palliative radiotherapy

Milner et al.

2014 [30] M 67 Clear cell carcinoma of

the right kidneys Hard palate Metastasis was the first manifestation of renal cancer

Pain in the palate No data Surgical

Lazar- -Poniatowska et al. 2015 [26]

K 61 Clear cell carcinoma of the left kidney, no exact date of diagnosis

Thyroid gland 19 years from left-

-sided nephrectomy No data No data Surgical

Kędzierska et al. 2018 [24] M 52

M 59

Clear cell carcinoma of

the right kidney, 2010 Right maxillary sinus Right maxillary sinus

2 months after right- -sided nephrectomy 6 years from right- -sided nephrectomy

No data No data

No data 2.1 × 2.1 × 2.4 cm

Surgical

Pazopanib Presented case M 81

M 84

Clear cell carcinoma of

the left kidney, 2007 Left submandibular salivary gland Right submandibular salivary gland

8 years from left- -sided nephrectomy 12 years from left- -sided nephrectomy

Asymptomatic cervical tumor on the left side, Cervical tumor on the right side, asymptomatic

2.5 x 2 x 2.3 cm 4 x 3.5 x 2.5 cm

Surgical Surgical

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DISCUSSION

In the discussed clinical case, the primary focus was clear cell carcinoma of the kidney. Due to its rich vascularity, it carries high risk of metastasis [17], which is 2 times higher than that of other histological subtypes of RCC [18].

Approximately 25% of patients are diagnosed with distant metastases [19] at the time of cancer diagnosis, while 50% of metastases are diagnosed over many years of follow-up [18, 19]. Metastases are most often located in the lungs (50–60%), regional lymph nodes (60%), bones (30–40%), liver (30–40%), brain (5%) and in the skin [17]. Such metastases are observed in 8–14% of patients with RCC [9, 17], isolated metastases to the head and neck are found in only 1% of patients [5, 20]. The most common metastatic locations in this area include the thyroid gland [21] and parotid glands [9, 17].

Metastases to other organs, including the tongue and other salivary glands, are extremely rare [16, 17]. However, they should be taken into account in differential diagnosis, especially in patients with a history of clear cell carcinoma.

Polish literature includes several casuistic case reports of clear cell renal cell carcinoma metastases to the nasal cavities and paranasal sinuses [12, 22–25], thyroid gland [8, 26], salivary glands [21, 16, 28], larynx [25, 27, 29], hard palate [30], laryngopharynx [11, 25], oropharynx [31], nasopharynx [27] and cervical lymph nodes [25, 27, 32] (Tab. I.).

Symptoms of clear cell carcinoma metastasis to the head and neck are non-specific. They do not have any characteristics that could distinguish them from primary tumors of this region. Symptoms depend on the location of the tumor and its size.

RCC metastases to the thyroid gland

Metastatic tumors account for approximately 4% of all thyroid tumors [8], of which approximately 1% comes from renal cell carcinoma [2].

RCC metastases to nasal cavities and paranasal sinuses

Among the paranasal sinuses, maxillary sinuses are the most common site of metastatic foci from clear cell renal cell carcinoma. They are followed by: ethmoid sinuses, frontal, cavernous, while RCC metastases to the nasal septum are extremely rare.

Rich vascularity of the tumor is usually the cause of profuse nasal hemorrhages. Skodulski et al. [28] emphasize that unilateral, recurrent and very abundant nosebleeds are the most important symptom of RCC metastasis to the nose and paranasal sinuses.

Other symptoms suggestive of cancer include nasal obstruction, swelling and pain.

RCC metastases to salivary glands and tongue

Approximately 0.1% of metastatic tumors in salivary cells are derived from RCC. Symptoms of metastases to the salivary glands

or to the tongue are similar to those of primary tumors, including ulcers, swelling and polyps.

There are several theories describing the dissemination of RCC metastases. Metastases can spread through arterial, venous, and lymphatic vessels [6] as well as through direct infiltration. Cieszynska et al. [22] underscore that clear cell renal cell carcinoma often extends into the lumen of the renal vein and through venous plexuses metastasizes to the head and neck, bypassing the lungs due to increased intraabdominal and intrathoracic pressures causing retrograde blood flow. The same authors add that the tumor can also spread through the lymphatic vessels to the lymph nodes along the renal hilum and large abdominal vessels.

In histopathological examination metastatic tumors from clear cell renal cell carcinoma are characterized by a connective tissue capsule and presence of well-demarcated cells containing abundant amount of bright cytoplasm with cholesterol, cholesterol esters, phospholip- ids and glycogen in microscopic picture [30]; cell nuclei are round or oval with evenly spaced chromatin. Microscopically, eosinophilic cells containing numerous mitochondria may be present in addition to cells with a bright cytoplasm.

Immunohistochemical examination plays an important role in the differential diagnosis of primary and metastatic tumors. They are the diagnostic gold standard. As much as 50% of RCCs are positive for vimentin. The majority show positive expression for keratin 8 and 18 as well as EMA (epithelial membrane antigen). Moreover, CD10 (+) in combination with clinical examination and medical history is use- ful in the differential diagnosis of metastatic tumors of clear cell renal cell carcinoma [19]. Reactions: PAS (+), diastase (-) and CEA (-) [18].

Treatment of metastases of clear cell renal carcinoma to the head and neck should be considered individually, taking into account the location, the extent of neoplastic disease, patient’s general condition, current symptoms and life expectancy. Therapy may include surgical resection, radiotherapy, chemotherapy or immunotherapy [19]

to relieve pain and control bleeding. Choosing the right treatment is especially important in rapidly growing tumors that can cause air- way obstruction.

According to the 2017 National Cancer Network clinical trial guide (second edition), nephrectomy and resection of metastases should be performed if the primary tumor is resectable and distant metastases are isolated. This also applies to distant metastases that occurred several years after nephrectomy [19, 27]. Such manage- ment, includes radical excision of isolated metastasis together with nephrectomy, should be the treatment of choice to prolong patient survival [25, 27].

During surgical treatment, one should bear in mind the rich vascularity of metastatic tumors derived from clear cell renal cell carcinoma.

However, the vascular nature of these metastases is not always clini- cally obvious, as was in the case presented here.

RCC is described in the literature as resistant to radiotherapy, but there are studies showing the effectiveness of radiotherapy in the treatment of metastases [10, 15, 19].

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SUMMARY

RCC is the third most common cause of distant metastases to the head and neck, following breast and lung cancers. In the differential diagnosis of head and neck tumors, especially fast-growing ones, a clinician should take into consideration metastatic tumors, especially if a patient has a history of clear cell renal cell carcinoma.

Metastases to the head and neck require individualization of treatment. Surgical resection, radiotherapy, immunotherapy or chemotherapy should be taken into account. Metastases of clear cell renal cell carcinoma to the head and neck organs pose an inter- disciplinary challenge for oncologists, urologists, nephrologists and ENT specialists.

Radiation therapy, targeted immunotherapy and chemotherapy are the treatments of choice for patients with contraindications to general anesthesia or non-resectable lesions. Chemotherapy is reserved for patients, in whom immunotherapy had not produced the expected results [19]. In the described case radical surgical resection was performed twice in a patient with metastases to the submandibular salivary passages. In cases of clear cell renal cell carcinoma metastases to the tongue the prognosis is poor. Average survival from the diagnosis to death is 5.8 months [5, 14]. Reported 5-year survival of patients with multiple metastatic foci is 0–7% [14].

Literature states that isolated metastases and long time between primary treatment and the occurrence of metastasis are associated with bet- ter prognosis than multiple metastases and a short time interval from treatment of the primary focus to detection of distant metastases [17].

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Word count: 2335 Tables: 1 Figures:- References: 37 Access the article online: DOI: 10.5604/01.3001.0014.7722 Table of content: https://otorhinolaryngologypl.com/issue/13697

Some right reserved: Polish Society of Otorhinolaryngologists Head and Neck Surgeons. Published by Index Copernicus Sp. z o.o.

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Corresponding author: Małgorzata Czesak MD; Chair and Department of Otorhinolaryngology, Head and Neck Surgery of the Medical University of Warsaw; Banacha street 1a, 02-097 Warsaw, Poland; Phone: +48 (22) 599 25 21; E-mail: mczesak@wum.edu.pll

Cite this article as: Torchalla P., Czesak M., Osuch-Wojcikiewicz E.: Metastasis of clear cell renal cell carcinoma to the organs of the head and neck – an ongoing problem; Pol Otorhino Rev 2021; 10 (1): 1-7