J Stomatol Oral Maxillofac Surg 124 (2023) 101330

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Review

Metastasis of malignant tumors to the oral cavity: Systematic review of

case reports and case series
~o Carame
Ana Margarida Lopesa,*, Filipe Freitasb, Miguel Vilaresc, Joa ^ sb
a
Faculdade de Medicina Dentaria da Universidade de Lisboa, Lisbon, Portugal
b
Department of Oral Surgery and Oral Medicine, Faculdade de Medicina Denta ria da Universidade de Lisboa, Lisbon, Portugal
c
Department of Head and Neck Surgery, Instituto Portugu^es de Oncologia de Lisboa, Lisbon, Portugal

A R T I C L E I N F O A B S T R A C T

Article History: Objective: To summarize published information regarding malignant tumors with metastasis to the oral
Received 27 September 2022 cavity.
Accepted 7 November 2022 Materials and methods: This was a systematic review with meta-analysis. An electronic search of Pubmed, Sco-
Available online 9 November 2022
pus, and Google Scholar databases from inceptions to February 2022 were performed. Only case reports or case
series with histopathological results demonstrating metastasis to the oral cavity were included. The main out-
Keywords:
comes included demographics, primary site, metastatic site, clinical manifestations, and patient survival. The
Oral metastasis
quality of primary articles was assessed using the Joanna Briggs Institute - University of Adelaide scorecards for
Oral cancer
Metastatic tumor
case reports and case series. Descriptive analysis and a Kaplan-Meier survival curve were performed.
Oral metastization Results: 273 articles were selected (50 case series and 223 case reports), for a total of 950 cases. The mean age
Oral neoplasm was 57.11 years. Males were more affected (57.5%). The most common primary sites in women and men was
breast (29.8%), and lung (24.8%), respectively. In »1/3 of the cases, oral metastasis preceded tumor dissemi-
nation. Jawbones were more affected (56.7%) than soft tissues (37.9%), with the mandible being the most
affected site (45.5%), followed by the gingiva (19.9%). The most common clinical manifestation was a mass or
nodule. Most radiographic evidence was radiolucency of the jaw (60.6%). 3-year and 5-year survival rates
were 14.2 and 10.7%. In the majority of cases, the primary tumor was the first to be diagnosed, while in
30.4%, metastasis was the first sign of the disseminated disease. This can be implied that the oral metastasis
should be included in the differential diagnosis list of the oral diseases.
Conclusion: Clinicians should be aware of the possibility of, albeit uncommon, oral metastases. Because the
extracted data in this review was relatively generalized, the investigators cannot develop the diagnostic clues
of oral metastasis, which require further investigations.
© 2022 The Author(s). Published by Elsevier Masson SAS. This is an open access article under the CC BY-NC-
ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)

1. Introduction
Although tumors of other organs can metastatize to the oral cav-
ity, the reported incidences are quite low, accounting from 1 to 8% of
all oral tumors [1]. The oral metastasis may involve osseous or soft
tissue, or both [1−3]. To the best of our knowledge, no systematic
review with meta-analysis regarding this issue has existed hitherto,
even though oral/oral-maxillofacial surgeons and other health care
providers in related specialties should include metastastatic tumors
to the oral cavity in the differential diagnosis list.
This systematic review was aimed to summarize published informa-
tion concerning malignant tumors with metastases to the oral cavity. The
investigators hypothesized that there would be novel information on
this matter available for inclusion in this systematic review. The specific
aims of this study were to (1) apply the principle of evidence-based med-
icine to clinical research practice, 2) perform a systematic review, and if
possible, with meta-analysis, (3) provide information extracted from the
primary papers, and 4) propose the diagnostic clues relative to the oral
metastasis of malignancy from other organs.
2. Methods and case selection
A systematic review of case reports and case series on metastasis
of malignant tumors to the oral cavity was performed, according to
PRISMA (the PRISMA 2020 statement) recommendations [4].
2.1. Search strategy

* Corresponding author. An electronic search was carried out from April 2021 to February
E-mail address: lopesana2@campus.ul.pt (A.M. Lopes). 2022. The terms “metasta*” AND “oral” were used, restricting their

https://doi.org/10.1016/j.jormas.2022.11.006
2468-7855/© 2022 The Author(s). Published by Elsevier Masson SAS. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/)
A.M. Lopes, F. Freitas, M. Vilares et al.
presence to the title of the article, in the Pubmed, Scopus, and Google
Scholar databases. The search was limited to human studies and writ-
ten in English. There was no date limit. A manual search was also con-
ducted through the references of the included articles.
2.2. Selection criteria
In this systematic review, only case reports or case series were
included in which a biopsy and anatomopathological examination of
the lesion was performed with confirmation of metastasis. All articles
refer to the location in the oral cavity occupied by the metastasis.
Letters to the editor, systematic or literature reviews, cases in
which the biopsy did not confirm the lesion as a metastasis, cases in
which the primary tumor was in the oral cavity, cases in which the
metastases were outside the limits of the oral cavity, articles pub-
lished in languages other than English, and animal studies were
excluded.
2.3. Data extraction
After introducing the keywords in the aforementioned databases,
6975 results were obtained. First, the titles of the articles were read,
and 618 articles were selected for reading the abstract. Of these, 300
articles were chosen for full-text reading. Duplicate articles (149)
were removed, and 130 articles obtained from manual searches were
included. After reading the 281 articles, 8 were removed (5 because
the lesion was not confirmed as metastasis in an anatomopathologi-
cal examination, 1 because the metastasis was outside the limits of
the oral cavity, 1 because the primary tumor was located in the oral
cavity, and 1 because it did not allow the use of the information nec-
essary for this review). Thus, 273 articles (50 case series and 223 case
reports) were chosen for inclusion in the present systematic review.
The reading, selection, and analysis of the articles included in this
systematic review were performed by one operator.
(Appendix A)
Fig. 1 presents the flowchart with the schematic systematization
of the selection process.
Fig. 1. Flowchart with the schematic systematization of the selection process.
2
Journal of Stomatology oral and Maxillofacial Surgery 124 (2023) 101330
2.4. Data collected
Information was collected on age, sex, year of publication, place
where the study was carried out, histology of the metastasis, location
in the oral cavity, site of origin of the tumor, first diagnosis (primary
or metastasis), time of evolution of the lesion, clinical manifestations,
radiological images, time between diagnosis of the primary tumor
and oral metastasis, the time between diagnosis of metastasis and
death, time of clinical follow-up, treatment of metastasis and confir-
mation of metastases in other locations outside the oral cavity. This
data was entered into the Microsoft Office ExcelÒ 2016 version 2202
program (Microsoft, Redmond, USA).
2.5. Analysis of the quality of scientific literature
The quality of articles was assessed using the Joanna Briggs Insti-
tute − University of Adelaide scorecards for case reports and case
series [5].
2.6. Data analysis
Statistical analysis was performed using SPSSÒ version 28.0 (IBM,
Armonk, NY, USA). A descriptive analysis of all previously described
data was performed. Two Kaplan-Meier curves were also performed
to analyze the probability of survival.
3. Results
This systematic review involved 950 cases of primary tumor
metastases in the oral cavity, published between 1928 and 2021.
Table 1 shows information regarding demographics, oral location,
clinical and imagiological features, first diagnosis, the time of evolu-
tion, the time between diagnosis, time between diagnosis of the oral
metastasis and death, and follow-up.
A.M. Lopes, F. Freitas, M. Vilares et al. Journal of Stomatology oral and Maxillofacial Surgery 124 (2023) 101330

Table 1 3.2. Sex

Demographics, location, clinical and imagiological features of the metastatic lesions.

Continent (n = 950) n/% As for the sex of patients, information was available for 884 cases.
Males were the most affected, with 57.5% of cases (n = 508). Females
Asia 378/39.8
represent 42.5% of cases (n = 376), which makes a ratio of 1.35:1.
Europe 284/29.8
North America 188/19.8 Appendix C summarizes the relation between sex and mean age,
South America 63/6.6 primary tumor site, oral site, and mean evolution time.
Africa 33/3.5
Oceania 4/0.4
3.3. Age
Sex (n = 884) n/%
Female 376/42.5
Male 508/57.5 Information about age was present in 680 cases. The mean age at
Mean Age (n = 680) 57,11 y (SD§ 17.61) diagnosis was 57.11 years (standard deviation § 17.61), ranging from
Range: 4 mo - 92 y 4 months to 92 years.
Age Groups (n = 680) n/%
It was possible to relate sex and age in 679 cases. In females, the
0−18 y 33/4.9
19−30 y 31/4.6 mean was 53.82 years, with a standard deviation § 18.38 (n = 285),
31−40 y 30/4.4 while in males it was 59.48 years with a standard deviation §16.67
41−50 y 87/12.8 (n = 394).
51−60 y 163/24.0 The age group with the highest number of cases was 61 to
61−70 y 193/28.4
71−80 y 110/16.2
70 years, with 193 cases (28.4%). The age group with the fewest cases
>=81 y 33/4.9 was from 31 to 40 years old, with 30 cases (4.4%). Up to the age of 40,
Oral site (n = 950) n/% there were only 94 cases, representing 13.9% of the total.
Jawbones 538/56.7
Mandible 432/45.5
3.4. Primary tumor site
Maxilla 106/11.2
Soft tissues 361/37.9
Gingiva 189/19.9 Regarding the location of the primary tumor, information was
Tongue 60/6.3 present in 921 cases. The most common origin of metastases was the
Buccal mucosa 45/4.7 lung, representing 17.3% of the cases (n = 159), followed by the breast
Parotid gland 13/1.4
Floor of mouth 9/0.9
with 12.6% (n = 116), the kidney with 12.5% (n = 115), and the liver
Lip 8/0.8 with 8.9% (n = 82). In 75 cases (8.1%), the origin of the primary tumor
Tonsil 8/0.8 was unknown. Table 2 presents the frequencies regarding primary
Submandibular gland 6/0.6 tumor sites and describes the relationship between the primary
Submandibular area 5/0.5
tumor and oral site.
Soft palate 5/0.5
TMJ 5/0.5 It was possible to relate sex with the location of the primary
Vestibule 5/0.5 tumor in 805 cases. In females, the most common origin was the
Hard palate 2/0.2 breast, representing 29.8% of oral metastases, followed by thyroid at
Oropharynx 1/0.1 11.1%, lung at 8.8%, and kidney at 8.5%. In males, the most common
Multiple 51/5,4
First diagnosis (n = 592) n/%
origin was the lung, representing 24.8% of cases, followed by the kid-
Metastatic lesion 180/30.4 ney at 16.8%, the liver with 11.2%, and the prostate at 9.1%.
Primary tumor 400/67.7 It was possible to associate the location of the primary tumor with
Simultaneous 12/2.0 the location of the metastasis in the oral cavity in 757 cases. Of the
Radiographic images (n = 345) n/%
most common tumors, 100% of the cases originated from the adrenal
Radiolucent 209/60.6
Radiopaque 16/4.6 glands, 75% from the thyroid, 73% from the prostate, and 67,7% from
Mixed 13/3.8 the breast metastasized to the jawbones. In turn, 51.1% of the metas-
No image 107/31.0 tases from the lung, 53.1% from the kidney, 65.2% from the stomach,
Mean evolution time (n = 149) 3.19 mo (SD§5.98) and 70.4% from the skin metastasized to the soft tissues.
Range: 2 d−60 mo
Mean time between primary and metastasis diagnosis 31.23 mo (SD§42.62)
As for the histological characteristics of the metastasis, informa-
(n = 268) tion was available in 838 cases. The tumors that most frequently
Range:0−316 mo metastasized were hepatocellular carcinoma (n = 75/8.9%), lung ade-
Mean time between metastasis diagnosis and death 9.81 mo (SD§15.97) nocarcinoma (n = 70/8.4%), renal cell carcinoma (n = 60/7.2%), breast
(n = 297)
adenocarcinoma (n = 48/5.7%) and renal clear cell carcinoma (n = 39/
Range: 3 d−142 mo
Mean time of follow-up (n = 70) 31.89 mo (SD§40.23) 4.7%).
Range: 1−233 mo
3.5. Oral site

Regarding the site in the oral cavity occupied by the metastasis,

3.1. Country and continent of each case
The information about the country where the cases were analyzed
was present in all 950 cases. The countries with the most reported
cases were, in descending order: the USA (176 cases), South Korea
(110 cases), Germany (66 cases), Israel (62 cases), and Brazil (61
cases). (Appendix B)
Regarding the continent of origin of each case, 378 cases came
from Asia, 284 from Europe, 188 from North America, 63 from
South America, 33 from Africa, and 4 from Oceania (for a total of
950).
3
information was available in all cases (n = 950). Bone structures were
more affected (56.7%/n = 538) than soft tissues (37.9%/n = 361). In
5.4% of the cases, the metastasis occupied multiple sites (n = 51).
The most affected location was the mandible, representing 45.5%
of the cases (n = 432), followed by the gingiva in 19.9% of the cases
(n = 189), and the maxilla in 11.2% (n = 106) and by tongue in 6.3%
(n = 60).
As it was possible to associate sex with an oral location in 711
cases, it was feasible to verify that, in hard tissues, the distribution is
similar between sexes (1.2:1, with a predominance of males). In soft
tissues, metastases are more frequent in males (1.73:1).
A.M. Lopes, F. Freitas, M. Vilares et al. Journal of Stomatology oral and Maxillofacial Surgery 124 (2023) 101330

Table 2 radiographic translation, metastases from all sources produced more

Frequencies regarding primary tumor sites and relation between primary tumor site radiolucent images than radiopaque or mixed ones (except for
and oral site.
metastases from the stomach, where there was one case correspond-
Primary tumor site (n/%) Oral site (n/% primary tumor site) ing to each image, and from the testis, where there was one case
n = 757 with radiolucent translation and one case with radiopaque transla-
Jawbones Soft tissues Multiple tion).
Appendix D summarizes the relationship between the primary
Lung 159/17.3 54/41.2 67/51.1 10/7.6
tumor site and imagiological features.
Breast 116/12.6 67/67.7 24/24.4 8/8.1
Kidney 115/12.5 41/42.7 51/53.1 4/4.2
Liver 82/8.9 37/58.7 20/31.7 6/9.5 3.7. First diagnosis
Unknown primary 75/8.1 52/83.9 10/16.1 0/0.0
Thyroid 45/4.9 27/75.0 8/22.2 1/2.8
Information regarding prior knowledge of tumor presence was
Prostate 43/4.7 27/73.0 7/18.9 3/8.1
Skin 40/4.3 3/11.1 19/70.4 5/18.5
available in 592 cases. In 67.6% of cases (n = 400), the primary tumor
Colon 27/2.9 18/69.2 8/30.8 0/0.0 was the first to be diagnosed, while metastasis was the first sign of
Stomach 24/2.6 7/30.4 15/65.2 1/4.3 disseminated tumor disease in 30.4% (n = 180). In 2% of cases, metas-
Soft tissues 23/2.5 9/52.9 7/41.2 1/5.9 tasis and primary tumor were diagnosed simultaneously (n = 12).
Bone and cartilage 18/2.0 8/50.0 8/50.0 0/0.0
Colon-rectum 18/2.0 5/83.3 1/16.7 0/0.0
Uterus 17/1.8 10/66.7 5/33.3 0/0.0 3.8. Evolution before diagnosis
Rectum 17/1.8 7/41.2 8/47.1 2/11.8
Esophagus 13/1.4 10/83.3 2/16.7 0/0.0 Information on the time of evolution of the lesion before diagnosis
Adrenal glands 10/1.1 10/100.0 0/0.0 0/0.0
was given in 149 cases. The mean time of evolution of the lesion was
Urinary bladder 10/1.1 2/25.0 4/50.0 2/25.0
Pleura 8/0.9 3/37.5 5/62.5 0/0.0
3.19 months, with a standard deviation of §5.98, ranging from 2 days
Stomach-oesophagus 8/0.9 0/0.0 1/100.0 0/0.0 to 60 months.
Cervix 7/0.8 3/42.9 3/42.9 1/14.3 In females, information was present for 47 cases, and the mean
Hematopoietic tissue 6/0.7 4/80.0 1/20.0 0/0.0 time of evolution before diagnosis was 4.68 months. In males, infor-
Testis 5/0.5 3/60.0 2/40.0 0/0.0
mation was available in 101 cases, and the mean was 2.53 months.
Retina 5/0.5 3/60.0 0/0.0 2/ 40.0
Pancreas 4/0.4 1/33.3 2/66.7 0/0.0
Ovary 4/0.4 2/100.0 0/0.0 0/0.0 3.9. Interval between diagnosis of the primary tumor and oral
Ureter 3/0.3 3/100.0 0/0.0 0/0.0 metastasis
Pancreaticobiliary 3/0.3 2/100.0 0/0.0 0/0.0
Neuroendocrine tissue 3/0.3 3/100.0 0/0.0 0/0.0
Mediastine 2/0.2 2/100.0 0/0.0 0/0.0
Regarding the interval between the diagnosis of the primary
Brain 2/0.2 2/100.0 0/0.0 0/0.0 tumor and the oral metastasis, information was available in 268
Cerebelum 2/0.2 2/100.0 0/0.0 0/0.0 cases. The mean value of this interval was 31.23 months with a stan-
Nasopharynx 2/0.2 1/100.0 0/0.0 0/0.0 dard deviation of §42.62, ranging from 0 months (in cases where the
Lymphoid tissue 2/0.2 0/0.0 1/50.0 1/50.0
diagnosis was made simultaneously) to 316 months.
Retroperitoneum 2/0.2 1/100.0 0/0.0 0/0.0
Bile duct 2/0.2 0/0.0 1/100.0 0/0.0 In the case of hard tissues, this mean was 32.82 months with a
Nasal 2/0.2 0/0.0 1/100.0 0/0.0 standard deviation §41.56 (information available in 122 cases), while
Total 921/100.0 428/56.5 282/37.3 47/6.2 in soft tissues it was 29.03 months with a standard deviation §43.02
(information taken from 127 cases).

Information about the presence of more metastases in addition to
the oral lesion was provided in 251 cases, and in 228 cases the pres-
ence of other metastases was confirmed.
3.6. Clinical and radiological manifestations
The most common clinical manifestation was the presence of a
mass or nodule, which occurred in 517 cases (426 masses, 70 ulcer-
ated masses, and 21 masses present in a socket after an extraction).
The presence of pain was reported in 190 cases (20.0%). In 95
cases, the absence of pain was stated. In 666 cases, no information
was provided.
In 91 cases, sensory alterations were reported (such as paresthe-
sia, hypoesthesia, or numb-chin syndrome), hemorrhage in 75 cases,
mobility and tooth loss in 43 cases, limitation of mandibular move-
ment, deviations, and TMD in 41, ulcer in 15, difficulty in eating or
chewing in 11, dysphagia or odynophagia in 7, discomfort when
using removable prosthesis in 6, halitosis in 6, fracture of the mandi-
ble in 5, difficulty in phonation in 4, fistula in 4 and infection in 3
cases. Fig. 2 summarizes the information about clinical manifesta-
tions and symptoms.
Regarding the radiological images, the information was present
for 345 cases. In 209 cases, a radiolucent lesion was reported (60.6%),
107 had no lesion (31.0%), 16 had a radiopaque lesion (4.6%), and 13
had a mixed lesion (3.8%).
It was possible to associate the radiological images with the loca-
tion of the primary tumor in 337 cases. In cases where there was a
4
3.10. Interval between diagnosis of metastasis and death
Information on the interval between diagnosis of metastasis and
death was available in 297 cases. Its mean value is 9.81 months with
a standard deviation of §15.97, ranging from 3 days to 142 months.
3.11. Follow-up
Information on clinical follow-up was available in 70 cases. The
mean value was 31.89 months with a standard deviation of § 40.23,
ranging from 1 month to 233 months.
3.12. Survival
Survival analysis was performed based on cases that provided
information on the interval between diagnosis of metastasis and
death or clinical follow-up, using a Kaplan-Meier survival curve. After
1 year, the probability of survival is 31.7%; after 3 years it is 14.2%,
and after 5 years it is 10.7%.
Comparing the probability of survival between sexes, it was possi-
ble to ascertain that in females, this probability is 38.2% after 1 year,
19.6% after 3 years, and 15.2% after 5 years. In males, the probabilities
of survival are, respectively, 27.3%, 10.6%, and 7.7%. There was, there-
fore, a statistically significant difference between females and males
(p=0.023), indicating a higher probability of survival for females
(Fig. 3).
A.M. Lopes, F. Freitas, M. Vilares et al. Journal of Stomatology oral and Maxillofacial Surgery 124 (2023) 101330

Fig. 2. Absolute frequency of clinical manifestations and symptoms.

Fig. 3. Kaplan-Meier survival curve by sex: There is a statistically significant difference between females and males (p = 0.023), indicating a higher probability of survival for females.

5
A.M. Lopes, F. Freitas, M. Vilares et al.
4. Discussion
The main aim of this systematic review was to gather and analyze
published information regarding oral metastasis of malignant tumors
in other body regions. Our main results demonstrated that oral
metastasis was dominant in males, with a male-to-female ratio of
1.35:1. The mean age at diagnosis was 57.11 years, and the most
common primary tumor site was the lung, followed by the breast and
kidney. Among those, oral hard tissues were more affected than soft
tissues with a ratio of 1.49:1. The most affected location was the man-
dible, followed by the gingiva, maxilla, and tongue. These findings
were in accordance with previous publications [3,6−10].
In »1/3 of the cases, oral metastasis developed before the tumor
dissemination stage, requiring particular attention of health care pro-
viders involving in oncologic patient care. Most clinical manifesta-
tions were a mass or nodule newly developed in the oral cavity,
which may be confused with other benign oral lesions, such as a pyo-
genic granuloma, or peripheral giant cell granuloma. However, many
patients with oral metastasis presented with pain, while benigh
lesions are usually painless. In other words, oral tumor pain may
relate to extensive tumor distribution and subsequently poor progno-
sis [6−8,10−16]. Due to its rarity and the importance of early detec-
tion, the recognition of metastatic lesions and its primary site(s) can
be challenging, both for the clinician and for the pathologist [13].
Relying on clinical diagnosis only can delay the diagnosis of the pri-
mary tumor, and consequently compromise appropriate treatments
[1,3,6,12]. Because these findings are non-specific, histopathological
analysis of the biopsy specimen is mandatory to confirm the diagno-
sis [7]. If there is a known malignancy, the pathologist’s objective
should be to assess the similarity between the oral lesion and the
original primary tumor, both via histomorphology and immunohisto-
chemical examinations [15].
It is important to note that oral metastasis usually indicates the
disseminated stage of cancers. In this review, 228 cases were found
with many metastases in addition to those in the oral cavity. Similar
to usual cancer treatment, oral metastasis should be apt to resection
with/without radio/chemotherapy. However, in late- or end-stage
patients, only palliative care should be provided to promote the
patient’s quality of life end [15].
The limitations of this systematic review include the case report/
series nature of the primary articles, and heterogeneity of the
included input. Many other oral metastatic cases may be hided as the
grey literature that has not been published elsewhere. The language
restriction in this study may also limit the cohort size of included
papers. Moreover, only one investigator-author performed data col-
lection and analysis; hence, the risk of bias could not be overlooked.
5. Conclusion
Metastasis of malignant tumors to the oral cavity is a rare event
and is characterized by a poor prognosis. A complete medical history
should be taken to know if there is any known malignant pathology.
Males were the most affected, and the age group with the most
cases was from 61 to 70 years. The primary tumor site with the most
cases was the lung. In males, the most common primary tumor site
was the lung, while in females it was the breast. In about 30%, metas-
tasis was the sign that evidenced the presence of a primary lesion,
which demonstrates that metastatic disease must be present in the
differential diagnosis, since it may be the first manifestation of a
tumor in another location. Hard tissues were more affected. The man-
dible was the most frequent location. In soft tissues, the gingiva was
the most affected. The mass or nodule was the most common clinical
Journal of Stomatology oral and Maxillofacial Surgery 124 (2023) 101330
manifestation, while pain was the most prevalent symptom. In cases
where bone was affected by metastasis, a radiolucent image was the
most reported.
Any mass present in the oral cavity should be biopsied and ana-
lyzed carefully, as metastatic lesions may resemble clinically benign
lesions. The oral/oral-maxillofacial surgeon plays a fundamental role
in the early diagnosis of oral cancer, as well as in the identification of
metastatic lesions in the maxillofacial territory.
Funding
This research did not receive any specific grant from funding
agencies in the public, commercial, or not-for-profit sectors.
Declaration of Competing Interest
None to declare.
Supplementary materials
Supplementary material associated with this article can be found
in the online version at doi:10.1016/j.jormas.2022.11.006.
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