A Literature Review in Renal Carcinoma Metastasis to the Oral Mucosa and a New Report of an Epulis-Like Metastasis

653

MAKOS AND PSOMADERIS

J Oral Maxillofac Surg 67:653-660, 2009

A Literature Review in Renal Carcinoma Metastasis to the Oral Mucosa and a New Report of an Epulis-Like Metastasis Christos P. Makos, DDS,* and Konstantinos Psomaderis, MD, DDS† Metastatic tumors represent 1% of the oral malignancies1,2 most often originating from the breast, lungs, and kidneys.3-5 Concerning the oral cavity, metastases are usually located in the posterior region of the mandible. Metastatic lesions to the oral soft tissues and gingiva have also been reported.6 Metastatic tumors to the gingiva are extremely rare. Tsianos et al7 reviewed 14 well-documented cases of gingival metastasis without involvement of the underlying jaw bone and presented another case of frank malignant metastasis to the gingiva. Of these cases, 13 were carcinomas and 2 were sarcomas. The maxillary gingiva was involved in 5 cases, the mandibular gingiva in 7, and both of them in 3. The first case of hypernephroma metastasized to the gingiva was reported in 1928 by Branch and Norton.8 Hypernephroma (Grawitz tumor, renal cell carcinoma, renal clear cell carcinoma [RCCC]) accounts for more than 90% of kidney malignancies.9 It is considered to be one of the most unpredictable tumors, showing an explosive growth and spread, associated with either a silent regional growth with no metastases or a metastasis as first evidence in distal organs.10 In 1883 Grawitz introduced the term hypernephroma, speculating that this tumor originates from the adrenal crest migrating into the renal paren-

*Maxillofacial Surgeon and Associate Director, Department of Oral and Maxillofacial Surgery, General Hospital of Kilkis, Kilkis, Greece. †Maxillofacial Surgeon, Staff Grade, Department of Oral and Maxillofacial Surgery, Red Cross General Hospital of Athens, Athens, Greece. Address correspondence and reprint requests to Dr Psomaderis: Department of Oral and Maxillofacial Surgery, Red Cross General Hospital of Athens, 1, Athanasaki St, 11526 Athens, Greece; e-mail: [email protected] © 2009 American Association of Oral and Maxillofacial Surgeons

0278-2391/09/6703-0030$36.00/0 doi:10.1016/j.joms.2008.10.006

chyma. Later on, it was proved that this tumor originates from the epithelium of the renal tubuli, having clear cells as the main cellular component. Previous terms such as Grawitz tumor and renal cell carcinoma are no longer used. About 50% of kidney malignancies metastasize, and 15% of these cases show manifestations at the extracranial head and neck region.11,12 We present a rare case of RCCC metastasized to the maxillary gingiva mimicking an epulis. We also present a detailed review of the accessible international literature related to oral metastases of this carcinoma.

Report of a Case In 2001, a 63-year-old man was referred for a maxillary and rather rapidly growing epulis-like mass extending from the right central maxillary incisor to the first right maxillary premolar, which had been present for 3 months (Fig 1). The mass was painless and semihard, with normal covering mucous membrane and a wide base. The dental radiograph and orthopantomogram did not disclose any pathology related to the underlying maxillary bone or to the dental roots. The mass was easily excised with the patient under local anesthesia. The medical history of the patient included a right nephrectomy 2 years before because of an RCCC (Fig 2) and a pathologic fracture of the right femur 10 months before because of metastasis of the primary renal malignancy (Fig 3). The technetium Tc 99 scintigram disclosed multiple lesions in the vertebra, ribs, sternum, and pelvis but none at the facial skeleton. Histologic examination of the excised specimen showed a clear cell carcinoma of the gingiva (Fig 4) with positive histologic correlation to the primary renal cell carcinoma (Fig 5). The diagnosis of a metastatic RCCC to the maxillary gingiva was made. No further therapy was applied to the oral disease. The patient died from renal failure 5 months later.

Discussion RCCC is considered to be one of the most unpredictable tumors, showing an explosive growth and spread, associated with either a silent regional growth with no metastases or a metastasis as first evidence in

654

RENAL CARCINOMA METASTASIS TO ORAL MUCOSA

FIGURE 1. Clinical appearance of maxillary epulis-like mass from the right central maxillary incisor to the first right maxillary premolar. Makos and Psomaderis. Renal Carcinoma Metastasis to Oral Mucosa. J Oral Maxillofac Surg 2009.

distal organs.10 Because of its initial slow growth, there are no special signs. A metastatic lesion is usually present in cases in which the primary tumor is sized over 3 cm. Indeed, in many cases an oral metastasis may be the first evidence of the malignancy.10,13,14 RCCC frequently invades the renal parenchyma and vascular network, causing thrombi to the lumen of the renal veins and neoplastic emboli for hematogenous spread. The circulation of neoplastic cells to the

FIGURE 3. Pathologic fracture of right femur because of metastatic RCCC. Makos and Psomaderis. Renal Carcinoma Metastasis to Oral Mucosa. J Oral Maxillofac Surg 2009.

pulmonary venous system and then to the head and neck area via the valveless paravertebral Batson venous plexus could explain the presence of metastatic foci at the oral cavity from the initial renal site but the

FIGURE 2. Abdominal scintigram showing right nephrectomy.

FIGURE 4. Histologic picture of excised maxillary epulis-like mass showing abundant clear cells embedded in loose fibrous connective tissue (hematoxylin-eosin stain, original magnification ⫻50).

Makos and Psomaderis. Renal Carcinoma Metastasis to Oral Mucosa. J Oral Maxillofac Surg 2009.

Makos and Psomaderis. Renal Carcinoma Metastasis to Oral Mucosa. J Oral Maxillofac Surg 2009.

MAKOS AND PSOMADERIS

FIGURE 5. Histologic picture of excised right kidney showing abundant clear cells embedded in loose fibrous connective tissue identical to those in maxillary epulis-like mass (hematoxylin-eosin stain, original magnification ⫻100). Makos and Psomaderis. Renal Carcinoma Metastasis to Oral Mucosa. J Oral Maxillofac Surg 2009.

lungs being free of disease. Indeed, tumor emboli can enter the cranial vault via a combined anterograde and retrograde flow pattern in the intracranial vascular sinus, arriving at the internal jugular vein, where other unusual flow patterns permit seeding to the specific head and neck structures. Other metastatic mechanisms include a right-to-left heart shunt, a spontaneous repression of the lung disease, and an undiagnosed microscopic seeding of the lung parenchyma.12,15,16 Criteria for considering an oral malignant neoplasm as metastatic are as follows: 1) a primary tumor with histologic verification, 2) a second oral lesion histologically relevant to the primary tumor, 3) a histopathologic appearance of the oral lesion distinct from that of a typical oral malignancy, and 4) exclusion of a possible direct extension from the primary tumor.14,17 A review of the accessible international literature disclosed 90 cases related to metastatic renal cancer in the oral region.1-5,7,8,10-75 We report 1 more case (Table 1). The reports from Muller-Mattheis et al60 (No. 66) and Hagen et al61 (No. 67) in Table 1 involve the same case reported in 2 different publications. The total number of cases reviewed including ours is 91. The age of the patients was not reported in 16 cases. Of the remaining 75 cases, the mean age varied from 1 to 84 years (mean, 56.4 years). Among the 52 male patients, it varied from 1 to 84 years (mean, 56.3 years), and among the 23 female patients, it varied from 18 to 83 years (mean, 56.3 years). Gender was not reported in 16 cases. Of the remaining 75 cases, oral metastasis was more frequent in male patients (52 cases) than in female patients (23 cases), with a male-female ratio of 2.26:1.

655 The location of the oral metastases in the 91 mentioned cases was reported as follows: 15 cases (15.55%) were located at the gingiva (mandibular gingiva in 3; maxillary gingiva in 5; maxillary gingiva, tongue, and upper lip in 1; mandibular and maxillary gingiva in 2; gingiva and tongue in 1; and not specified in 3); 17 cases (18.88%) at the jaws and gingiva (mandible and gingiva in 11; maxilla and gingiva in 5; and maxilla, mandible, and gingiva in 1); 38 cases (42.22%) at the jaws (mandible in 27, mandible and soft palate in 1, mandible and adjacent tissues in 1, maxilla in 8, and maxilla and nasal cavity in 1); and 21 cases (23.33%) at other sites (buccal mucosa in 2, hard palate in 2, soft palate in 1, palate in 3, lower lip in 2, oral soft tissues in 1, nasal cavity in 1, and tongue in 9). Finally, 31 cases (34.44%) of oral metastases were not located at the gingiva but were located at other soft tissue structures of the oral cavity. The history of the disease was not reported in 11 cases. The oral metastasis was the first evidence of the disease in 39 (48%) of the remaining 80 cases. It presented as synchronous in 2 cases, whereas there was a known history of renal malignancy ranging from 3 weeks to 10 years in 40 cases (50%). A detailed histologic examination of any epulis is necessary because metastatic lesions to the gingiva have a clinical resemblance to benign gingival tumors or localized inflammatory hyperplasic lesions, such as pyogenic granuloma, giant cell granuloma, and fibrous epulis.3,10 Histologically, there are various patterns of RCCC such as acinar, tubular, papillary, or solid type. The typical neoplastic cells are the clear cells with a round or polygonal shape and abundant cytoplasm containing cholesterol, cholesterol esters, phospholipids, and glycogen. The final exact diagnosis for a primary or metastatic “clear cell” lesion in the oral region and the identification of the primary tumor are difficult because of the diversity of the tumors containing clear cells.11,16 The fact that the clear cells are the main cellular component in several neoplasms originating from the salivary glands, thyroid gland, testes, breast, and colon, as well as mucoepidermoid carcinoma and calcifying epithelial odontogenic tumor,3,5,19 in conjunction with the fact that in several cases the primary renal tumor is not known, confuses both pathologists and clinicians. Indeed, most RCCCs are positive— but not in an exclusive manner—for keratin 8, keratin 18, epithelial membrane antigen, and vimentin.19,20 Thus the histologic, histochemical, and immunohistochemical evidence must be in close relation to the clinical picture, radiographic evidence, and other laboratory examinations for a correct diagnosis. In cases with oral metastases of RCCC the prognosis is poor, and most patients die within the first year after diagnosis, indicating that oral metastases are

656

RENAL CARCINOMA METASTASIS TO ORAL MUCOSA

Table 1. DATA ON HISTOLOGIC TYPE, GENDER, AGE, LOCATION, EXTENSION, METASTASIS, AND HISTORY OF RCCC METASTASES IN THE ORAL REGION

Type Gender

Age (yr)

1 Kostenko, 1911 2 Coenen,19 1914 3 Branch and Norton,8 1928 4 Stein,20 1929

HN HN HN

— — F

— — 64

HN

M

65

5 McNattin and Dean,21 1931 6 Trinca and Willis,22 1936 7 Berg,23 1936 8 Vogt,24 1939 9 Salman and Darlington,25 1944 10 Schrag and Jordan,26 1945 11 Bernier and Tiecke,27 1951 12 Stewart and Bruce,28 1953 13 Salman and Langel,29 1954

HN

—

HN

No.

Author 18

Location

Extension

Metastasis

Time

— — —

— — —

—

FE

—

Tongue — Tongue — R mandibular gingiva Edentulous molar lingual aspect AL maxilla and Upper R central gingiva lateral incisors area Tongue —

—

FE

—

—

Tongue

—

—

HN HN HN

— M M

— 63 54

Soft palate L mandible Hard palate

— — —

H (1 yr) FE H (2 yr)

HN

M

61

Tongue

—

HN

M

47

Lower lip

—

HN

M

70

HN

F

62

14 Shimosato et al,30 1959 15 Nesbitt,31 1959

HN

—

—

NB

M

4

16 Mallett,32 1961

RCC

F

72

17 Persson and Wallenius,33 1961 18 Meyer and Shklar,17 1965 19 Meyer and Shklar,17 1965 20 Meyer and Shklar,17 1965 21 Meyer and Shklar,17 1965 22 Jacobs et al,4 1966

RC

F

60

HN

M

57

Lungs and scalp L mandible Body and molar area Lungs, bones, and dura R mandibular gingiva Molar area Lungs, skull, brain, and bones Mandible — Lungs and bones L mandible and soft Lower L premolars Lungs and palate area bones L mandible Distally to lower L — second molar and angle AL mandibular Lower L central and — gingiva lateral incisors Mandible and gingiva Ramus Bones

HN

M

48

Maxilla

—

HN

F

73

Mandible and gingiva

—

RRCS

M

43

Mandible

—

RCC

—

—

R mandible and gingiva

23 Cranin et al,34 1966 RCC

M

72

24 Godby et al,35 1967 HN

M

45

25 Del Carmen and Korbitz,36 1970 26 Maki et al,37 1970 27 Boles et al,15 1971 28 Boles et al,15 1971 29 Dehner,38 1973 30 Eda et al,39 1973

HN

M

77

RCC RCC RCC RCC RCC

— M M M M

— 53 66 1 76

31 Eda et al,39 1973

RCC

M

54

— — Body Total hard palate

Lower R canine to second premolar area R mandible, gingiva, Lower R lateral and periodontium incisor and canine area L mandible and Lower L second gingiva premolar and first molar area L tongue Posterior lateral base

Mandible L mandible Buccal mucosa Mandible R and L maxilla and gingiva R mandible and gingiva

— — — — R molar and L premolar area Premolar area

Lungs

H (4 mo) H (9 mo) FE H (1 yr) FE H (1 yr) FE H (1.5 yr) —

Lungs, bones, and parotid Bones FE —

—

FE

—

—

—

S

—

H (16 mo)

—

H (3 wk)

Adrenal gland — — — —

FE FE FE H (13 mo) FE

Bones

FE

657

MAKOS AND PSOMADERIS

Table 1. CONTINUED

No.

Author 40

32 Mori et al,

1974

Type Gender RCC

—

33 Morii,41 1975 34 Calonius et al,42 1975 35 Milobsky et al,43 1975 36 Tani et al,44 1976 37 Friedlander and Singer,45 1978 38 Nagayama and Oka,46 1979 39 Nagayama and Oka,46 1979 40 Susan et al,47 1979

RCC RA

— F

RA

Age (yr)

Location

Extension

—

Gingiva

— 81

Buccal mucosa L mandible

— Premolar area

F

66

AR maxilla

TCC RA

— M

84

Periapical pathosis of Lungs R central incisor — — Tip Lungs

CCC

F

61

CCC

F

RCCC

41 Susan et al,47 1979 42 Stypulkowska et al,2 1979 43 Stypulkowska et al,2 1979 44 Reczuk and Siciarz,48 1980 45 Buchner and Begleiter,10 1980 46 Quinn et al,3 1981

—

Mandible Tongue

—

Metastasis

Time

Lungs, bones, FE and adrenal gland — H —

H (4 yr) H FE

Molars and angle

43

L mandible and gingiva Palate

Adrenal gland FE

M

53

Palate

RCCC

M

62

LM palate

RCC

—

—

Mandible

Junction of hard and Lungs, bones, FE soft palate and liver Junction of hard and — FE soft palate — Lungs FE

RCC

—

—

Mandible

—

KA

—

—

Maxilla

—

RCC

M

46

RCC

M

52

47 Fitzgerald et al,49 1982

RCC

M

63

48 Bucin et al,50 1982

RTCC

M

67

49 Bucin et al,50 1982

RC

M

65

50 Matsumoto and Yanagihara,13 1982 51 Matsumoto and Yanagihara,13 1982 52 Nishimura et al,51 1982 53 Nishimura et al,51 1982 54 Nishimura et al,51 1982 55 Nishimura et al,51 1982 56 Schaffner et al,52 1982

RCCC

M

73

RCCC

M

48

KA

F

61

Mandible

KA

M

72

KTCC

M

KA

57 Sidhu et al,53 1982

—

From upper R to L lateral incisor L mandible Lower L first and second molar area R maxillary gingiva, Upper R canine to tongue, and upper second premolar lip area R mandible Alveolar process lower R premolar R maxillary gingiva Alveolar soft tissue upper R central incisor to R canine R and L maxilla and R and L maxilla, nasal cavity antrum, and nasal cavity R nasal cavity R maxillary antrum and nasal cavity

—

Bones and liver —

M maxillary gingiva

—

H (1 yr)

FE — H (2 mo)

Lungs

FE

Brain

S —

H (3 yr)

Parotid gland H (4 yr) Bones

FE

—

FE

—

—

FE

Gingiva

—

—

FE

61

Mandible

—

—

H

F

36

Mandible

—

—

FE

CCA

M

64

RA

F

32

58 Fay and Weir,5 1983 RCC

F

18

59 Lutcavage et al,54 1984

M

55

R mandibular gingiva Lower R second — and L maxillary premolar and gingiva upper R lateral incisor area L mandible and Lower L molars area Liver gingiva R mandible and Lower R canine and Supraclavgingiva first premolar area icular area Hard palate Midline Lungs, scalp, and bones

RCC

—

H

FE H (14 yr) H (1 yr)

658

RENAL CARCINOMA METASTASIS TO ORAL MUCOSA

Table 1. CONTINUED

No.

Author

Type Gender

55

Age (yr)

Location

Extension

Metastasis

Time

60 Zohar et al, 1985 CCC 61 Pick et al,56 1986 RCCC

F M

54 71

62 Favia et al,57 1986 63 Mocchi et al,58 1987

— F

58

64 Tsianos et al,7 1987 RCC

M

78

65 Florine et al,59 1988 66 Muller-Mattheis et al,60 1989

KCCS

M

1.3

RCC

F

47

A mandible and gingiva

67 Hagen et al,61 1989 RCC

F

46

A mandible and gingiva

68 Zachariades et al,1 1989 69 Ord et al,62 1990

MKC

M

78

L mandible

RC

M

58

70 Ord et al,62 1990

RC

M

73

71 Jones et al,11 1990

CCRC

F

62

72 Jones et al,11 1990 73 Aniceto et al,63 1990 74 Martinez Conde et al,64 1990 75 Pastremoli,65 1991

CCRC RA

F M

52 54

L maxilla, gingiva, and palate R maxilla and gingiva R mandible and gingiva R mandible R mandible

HN

—

CCCR

M

62

R and L maxilla and L mandible and gingiva

76 Fandella et al,66 1992 77 Guyot et al,67 1999 78 Corsi et al,68 1994 79 Lee et al,69 1998

CCC

M

62

L maxilla

RCC CCC RCC

F M M

83 42 76

Mandible R oral soft tissues Maxilla

80 Toranzo-Fernandez CCS et al,70 2000 81 Honig,71 2000 HN

M

8

M

46

A maxilla

82 Martin et al,72 2000 RCC 83 Shetty et al,16 2001 RCC

M M

8 62

Mandible L mandible

84 Fukuda et al,14 2002 85 Pritchyk et al,12 2002 86 Pritchyk et al,12 2002 87 Pritchyk et al,12 2002

RCC

M

78

R mandible

RCC

M

70

Lower lip

—

Abdomen

H (5 yr)

RCC

F

53

Maxilla

—

Abdomen

FE

RCC

M

60

Tongue and gingiva

—

NB RA

L maxillary gingiva L mandible and adjacent tissues

—

—

L tuberosity — Body, premolar, Bones molar, and ascending ramus Mandible — — L maxilla and gingiva Upper R central — incisor to R canine area AL maxillary and Upper and lower L Lungs and mandibular gingiva lateral incisor area brain R mandible Angle and ramus Bones

Gingiva

L mandible

FE FE — H (2 yr) H (4 mo) H (2 yr)

From lower L lateral incisor to R central incisor area From lower L lateral incisor to R central incisor area Body

—

—

H (2 yr)

Molar area

—

H (8 yr)

Tuberosity

—

FE

Lower R premolars area Ramus Angle and ramus —

H

H (duration?)

Bones

FE

Bones —

FE FE

—

—

Upper R and lower Lungs L molars and upper L canine area Middle nasal meatus —

FE

— — Cheek and upper lip — Tuberosity and Ureter and alveolar ridge abdomen Body, angle, and — ascending ramus Alveolar crest, upper Lungs R central incisor to L central incisor area — — Condyle, ramus, and — body Lower R canine area —

H H (4 yr) FE

—

FE

H (3 yr) H (6 mo)

H (3 yr) FE H

H (4 yr)

659

MAKOS AND PSOMADERIS

Table 1. CONTINUED

No.

Author 73

Type Gender

Age (yr)

Location

Extension

Metastasis

Time

88 Marioni et al, 2004

RCC

F

57

Tongue

—

89 Heinroth et al,74 2006 90 Torres-Carranza et al,75 2006 91 Makos and Psomaderis,2008

RCC

F

53

Maxilla

—

Lungs, liver, H (10 yr) pancreas, and thyroid Pelvic FE

RCC

F

49

Tongue

—

Lungs

H (6 mo)

RCCC

M

63

AR maxillary gingiva From upper R central incisor to R first premolar area

Bones

H (2 yr)

Abbreviations: R, right; L, left; AL, anterior left; M, mesial; A, anterior; CCA, clear cell adenocarcinoma; CCC, clear cell carcinoma; CCRC, clear cell renal carcinoma; CCS, clear cell sarcoma; HN, hypernephroma; KA, kidney adenocarcinoma; KCCS, kidney clear cell sarcoma; KTCC, kidney transitional cell carcinoma; MKC, metastatic kidney cancer; NB, nephroblastoma; RA, renal adenocarcinoma; RC, renal carcinoma; RCC, renal cell carcinoma; RRCS, renal reticulum cell sarcoma; RTCC, renal transitional cell carcinoma; TCC, transitional cell carcinoma; H, history; FE, first evidence; S, synchronous. Makos and Psomaderis. Renal Carcinoma Metastasis to Oral Mucosa. J Oral Maxillofac Surg 2009.

often related to multiple metastases reflecting widespread disease.6,12 It is well accepted that radical surgery is indicated for isolated oral metastasis to optimize the quality of life and to improve the survival rate before any further progression of the disease can occur. The excision of an isolated oral metastasis after nephrectomy results in a 2-year survival rate in 41% of cases and in a 5-year survival rate in 13% of cases independent of the interval time between nephrectomy and clinical diagnosis of the metastatic lesion.2,3,6,12,13,16

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