Open Access

Polymorphous low-grade adenocarcinoma: an analysis of epidemiological studies and hints for pathologists

  • Vera Cavalcanti de Araujo1Email author,
  • Fabricio Passador-Santos1,
  • Cecilia Turssi1,
  • Andresa Borges Soares1 and
  • Ney Soares de Araujo1
Diagnostic Pathology20138:6

DOI: 10.1186/1746-1596-8-6

Received: 5 December 2012

Accepted: 9 January 2013

Published: 15 January 2013

Abstract

Background

This study is an analysis of the prevalence of polymorphous low grade adenocarcinoma (PLGA) in epidemiological surveys of salivary tumors published in the English language from 1992 to 2012.

Methods

These surveys included studies from different researchers, countries and continents. The 57 surveys for which it was possible to calculate the percentage of PLGAs among all malignant minor salivary gland tumors (MMSGT) were included in this review.

Results

The statistical analyses show significant differences in the PLGA percentage by time period, country and continent in the studies included in this review. The percentage of PLGAs among MMSGTs varied among the studies, ranging from 0.0% to 46.8%. PLGA rates have varied over the period studied and have most recently increased. The frequency of reported PLGA cases also varied from 0.0% to 24.8% by the country in which the MMSGT studies were performed. The PLGA percentages also varied significantly by continent, with frequencies ranging from 3.9% in Asia to 20.0% in Oceania

Conclusion

Based on these results, we concluded that although the accuracy of PLGA diagnoses has improved, they remain a challenge for pathologists. To facilitate PLGA diagnoses, we have therefore made some suggestions for pathologists regarding tumors composed of single-layer strands of cells that form all of the histological patterns present in the tumor, consistency of the cytological appearance and uniformly positive CK7, vimentin and S100 immunohistochemistry, which indicate a single PLGA phenotype.

Virtual slide

The virtual slide(s) for this article can be found here:http://​www.​diagnosticpathol​ogy.​diagnomx.​eu/​vs/​1059098656858324​

Keywords

Polymorphous low-grade adenocarcinoma Epidemiological review Diagnosis hints

Introduction

Polymorphous low-grade adenocarcinoma (PLGA) is a malignant epithelial tumor characterized by cytological uniformity, morphological diversity, an infiltrative growth pattern and low metastatic potential[1]. This tumor was recognized as a distinct entity in 1983 by Freedman and Lumerman and Batsakis et al., and it was named polymorphous low-grade adenocarcinoma by Evans and Batsakis in 1984[24].

Clinically PLGA presents as an indolent asymptomatic swelling but occasionally can be painful and even ulcerate. The most common location of PLGA is the palate, although other locations have been described. It occurs more frequently in women affecting mainly the sixth and seventh decade of life. For more details on clinical presentation, prognosis and treatment, we recommend the reviews by Pogodzinski et al., and Paleri, Robinson and Bradley[5, 6]. In general these authors indicate a low grade malignancy and good prognosis of this tumor They also recommend a very careful and systematic follow- up,since recurrences and rare metastases can occur many years after the surgery.

The tumor is characterized by single-layer strands of cells that can form lobular, tubular, cribriform, trabecular, papillary-cystic and cystic histological patterns, which can be illustrated by the presence of extracellular matrix between the strands of cells identified in lobular or solid patterns[7].

Most PLGA cells are cytologically uniform and range from small to medium in size, with vesicular oval nuclei and inconspicuous nucleoli. Their cytoplasm is ample and exhibits a variable appearance, including eosinophilic, basophilic and clear aspects. The cells have indistinct outlines that lend a syncytial pattern to the active cellular mass. Groups of cells with a coarsely eosinophilic granular cytoplasm, mimicking oncocytes, are occasionally observed, as are mucous cells[1, 8].

The cells show a unique electron microscopy and immunohistochemical phenotype. All cells have microvilli apically and are attached to the basal lamina. The cells are positive for vimentin, CK 7 and S100, a pattern only shared by the mammary analogue secretory carcinoma, as recently described by Skalova et al. and rarely by focal plasmacytoid cells in pleomorphic adenoma[810]. A regular distribution of positive staining for β1, β2 and β3 integrins and striking bipolar staining in all of the neoplastic cells reinforces this unique phenotype[11].

Single cells, usually infiltrating surrounding structures, and clear cells in nests are also observed in the lobular PLGA subtype. The stroma appears either strongly eosinophilic and hyalinized, or muco-hyalinized with a bluish tint. Foci of residual salivary gland acini surrounded by neoplastic cells are occasionally found. Peri-neural invasion by groups of tumor cells is a frequent finding, and psammoma-like structures are occasionally observed. This tumor frequently presents with prominent vascularity[8].

Despite greater understanding of this tumor, PLGA remains a diagnostic challenge for pathologists. This conclusion is based on the variability of the epidemiological results obtained by several groups who have studied this tumor.

We have reviewed the epidemiological studies in an attempt to analyse the proportion of PLGAs in salivary gland tumors.

Materials and methods

This analysis included 57 epidemiological studies of salivary gland tumors published in the English language from 1992 to 2012. The year 1992 marked the inclusion of PLGA in the World Health Organization (WHO) classification of salivary gland tumors[12]. Studies were included in the analysis if they contained the data needed to calculate the fraction of PLGAs in the malignant minor salivary gland tumor (MMSGT) total.

The studies addressing only major salivary gland tumors were excluded because the few cases published on that topic do not significantly contribute to the understanding of PLGA; similarly, studies that included only children and adolescents were excluded from this analysis.

When data were available, we extracted the following information: total number of salivary gland tumors; number of minor salivary gland tumors and their fraction of the total number of tumors; number of MMSGTs and their fraction of the total number of minor salivary gland tumors; number of PLGAs and their fraction of the total number of MMSGTs; and the total number of minor salivary gland tumors.

In this study, we analyzed the fraction of PLGAs in the total number of MMSGTs. It was not possible to obtain the absolute or relative frequencies of malignant salivary tumors, either among minor salivary tumors alone or among major and minor tumors, from studies that reported only MMSGTs.

Statistical analysis

Data were tabulated and descriptive statistics were calculated using frequency tables. G tests were used to ascertain whether the PLGA fraction of all MMSGTs varied by the year, country and continent in which the studies were performed. We would like to emphasize that at no point was it presumed that these studies reflect the prevalence of this tumor with respect to the aforementioned variables (year, country and continent). The significance level was set at 5%. The statistical calculations were performed using the SPSS 20 software package (IBM corporation, Armonk, NY, USA).

Results

Fifty-seven surveys of salivary gland tumors were included in this review (Table 1)[1368]. From 26,960 cases of salivary gland tumors, 431 (1,6%) were accepted by the authors as been PLGAs.
Table 1

The distribution of salivary gland tumors, minor salivary gland tumors and polymorphous low-grade adenocarcinoma in the studies included in this review

Author

Year

Country

SGTs

MSGTs

MMSGTs

PLGAs

   

n

n

% in relation to SGTs

n

% in relation to Minor SGTs

n

% in relation to MMSGTs

Onyango et al.

1992

Kenya

417

189

45.3

58

30.7

0

Rippin e Potts

1992

England

194

194

88

45.4

0

Loyola et al.

1995

Brazil

164

164

65

39.6

4

6.2

Neely et al.

1996

USA

106

106

47

44.3

22

46.8

Rivera-Bastidas et al.

1996

Venezuela

62

62

28

45.2

0

Rushing et al.

1996

USA

277

27

9.7

16

59.3

0

Kusama et al.

1997

Japan

129

129

49

38.0

 

Nagler et al.

1997

Israel

245

67

27.3

33

49.3

3

9.1

Jones et al.

1998

England

145

145

103

71.0

 

Lopes et al.

1999

Brazil

196

196

129

65.8

3

2.3

Maaita et al.

1999

Jordan

221

42

19.0

20

47.6

0

Pacheco-Ojeda et al.

2000

Ecuador

308

28

9.1

14

50.0

0

Koivunen et al.

2002

Finland

40

4

10.0

4

0

Vargas et al.

2002

Brazil

124

6

4.8

4

66.7

0

Masanja et al.

2003

Tanzania

153

66

43.1

37

56.1

0

Hyan et al.

2004

Australia

30

30

30

6

20.0%

Kokemueller et al.

2004

German

155

90

58.1

90

7

7.8

Poomsawat et al.

2004

Thailand

60

54

90.0

37

68.5

1

2.7

Strick

2004

England

21

21

21

5

23.8

Toida et al.

2004

Japan

82

82

27

32.9

0

Vuhahula

2004

Uganda

268

88

32.8

47

53.4

7

14.9

Lima et al.

2005

Brazil

245

46

18.8

22

47.8

0

Ito et al.

2005

Brazil

496

113

22.8

53

46.9

9

17.0

Luukkaa et al.

2005

Finland

46

46

46

8

17.4

Otho et al.

2005

Niger

79

33

41.8

14

42.4

0

Yih et al.

2005

USA

213

213

94

44.1

18

19.1

Ascani et al.

2006

Italy

454

30

6.6

7

23.3

0

Ansari et al.

2007

Iran

130

18

13.8

16

88.9

0

Buchner et al.

2007

USA

380

380

156

41.1

27

17.3

Jones et al.

2007

England

741

455

61.4

172

37.8

28

16.3

Ladeinde et al.

2007

Niger

120

76

63.3

52

68.4

5

9.6

Pires et al.

2007

USA

546

546

241

44.1

28

11.6

Wang et al.

2007

China

737

737

397

34

8.6

Copeli et al.

2008

Italy

43

43

43

1

2.3

Li et al.

2008

China

3,461

914

26.4

539

59.0

1

0.2

Rahman et al.

2008

Paquistan

70

70

70

2

2.9

Subhashraj et al.

2008

India

684

150

21.9

59

39.3

0

Chijiwa et al.

2009

Japan

22

22

22

0

Dhanuthai

2009

Thailand

311

311

164

52.7

2

1.2

Gao et al.

2009

China

1,062

519

48.9

519

19

3.7

Mucke et al.

2009

German

95

95

95

14

14.7

Ochicha et al.

2009

Niger

78

19

24.4

7

36.8

2

28.6

Oliveira et al.

2009

Brazil

599

87

14.5

50

57.5

0

Targa-Stramandinoli et al.

2009

Brazil

14

14

7

50.0

1

14.3

Tilakaratne et al.

2009

Sri Lanka

713

486

68.2

276

56.8

27

9.8

Carrillo et al.

2010

Mexico

77

77

77

0

Erovic et al.

2010

Austria

32

32

32

0

Kakarala & Bhattacharyya

2010

USA

639

639

639

0

Kruse et al.

2010

Switzerland

27

27

27

0

Tian et al.

2010

China

6,982

1,977

28.3

1228

62.1

29

2.4

Bjorndal et al.

2011

Denmark

952

266

27.9

266

66

24.8

Morais et al.

2011

Brazil

303

37

12.2

26

70.3

3

11.5

Schwarz et al.

2011

German

41

41

41

8

19.5

Venkata et al.

2011

India

185

185

138

74.6

18

13.0

Bello et al.

2012

Finland

1,888

177

9.4

68

38.4

11

16.2

Bello et al.

2012

Israel

330

111

33.6

71

64.0

8

11.3

Luksic et al.

2012

Croatia

768

297

38.7

210

70.7

4

1.9

Total

26,960

11,079

41.1

6,891

62.2

431

6.3

SGTs: salivary gland tumors; MSGTs minor salivary gland tumors; MMSGTs: malignant minor salivary gland tumors; PLGA: polymorphous low-grade adenocarcinoma.

There has been a significant increase (p < 0.0001 for the G test) in the fraction of PLGA cases reported in the literature since 2007, as shown in Table 2. Epidemiological studies from 1992 to 1994 and 2001 to 2003 included no reports of PLGAs, whilst 1.8% of the MMSGTs reported from 1998 to 2000 were PLGAs. Higher percentages were noted from 1995 to 1997 and 2007 to 2012. The highest PLGA percentages were reported in the studies published from 2004 to 2006 (Table 2).
Table 2

The numbers and percentages of polymorphous low-grade adenocarcinomas in malignant minor salivary gland tumors by publication year as described in the studies included in this review

  Year

MMSGTs

PLGA

PLGA/MMSGTs

 

n

%

n

%

%

1992-1994

146

2.1

0

0.0

0.0

1995-1997

341

4.9

29

6.7

8.5

1998-2000

163

2.4

3

0.7

1.8

2001-2003

45

0.7

0

0.0

0.0

2004-2006

488

7.1

61

14.2

12.5

2007-2009

2,885

41.9

191

44.3

6.6

2010-2012

2,823

41.0

147

34.1

5.2

  Total

6,891

100.0

431

100.0

6.3

MMSGTs: malignant minor salivary gland tumors; PLGA: polymorphous low-grade adenocarcinoma.

The frequency of PLGA also varied significantly (p < 0.0001 for the G test) by country, as shown in Table 3. Of the 431 PLGA cases included in this review (Table 1), 95 (22.0%) were from studies performed in the USA, 83 (19.3%) were from Chinese studies and 66 (15.3%) were from Danish studies. The percentage of PLGAs among MMSGTs varied among the studies, ranging from 0.0% to 24.8% (Table 3).
Table 3

The numbers and percentages of polymorphous low-grade adenocarcinomas in malignant minor salivary gland tumors by country as described in the studies included in this review

Country

MMSGTs

PLGA

PLGA/MMSGTs

 

n

%

n

%

%

Australia

30

0.4

6

1.4

20.0

Austria

32

0.5

0

0.0

0.0

Brazil

356

5.2

20

4.6

5.6

China

2,683

38.9

83

19.3

3.1

Croatia

210

3.0

4

0.9

1.9

Denmark

266

3.9

66

15.3

24.8

Ecuador

14

0.2

0

0.0

0.0

England

384

5.6

33

7.7

8.6

Finland

118

1.7

19

4.4

16.1

German

226

3.3

29

6.7

12.8

India

197

2.9

18

4.2

9.1

Iran

16

0.2

0

0.0

0.0

Israel

104

1.5

11

2.6

10.6

Italy

50

0.7

1

0.2

2.0

Japan

98

1.4

0

0.0

0.0

Jordan

20

0.3

0

0.0

0.0

Kenya

58

0.8

0

0.0

0.0

Mexico

77

1.1

0

0.0

0.0

Niger

73

1.1

7

1.6

9.6

Paquistan

70

1.0

2

0.5

2.9

Sri Lanka

276

4.0

27

6.3

9.8

Switzerland

27

0.4

0

0.0

0.0

Tanzania

37

0.5

0

0.0

0.0

Thailand

201

2.9

3

0.7

1.5

Uganda

47

0.7

7

1.6

14.9

USA

1,193

17.3

95

22.0

8.0

Venezuela

28

0.4

0

0.0

0.0

Total

6,891

100.0

431

100.0

6.3

MMSGTs: malignant minor salivary gland tumors; PLGA: polymorphous low-grade adenocarcinoma.

The frequency of reported PLGA cases also varied significantly (p < 0.0001) by the continent in which the MMSGT studies were performed. The continent with the highest reported frequency of PLGAs was Asia, with 3,702 of the 6,891 reported cases (53.7%), followed by America (24.2%) and Europe (19.1%), as shown in Table 4. The PLGA percentages also varied significantly by continent, with frequencies ranging from 3.9% in Asia to 20.0% in Oceania.
Table 4

The numbers and percentages of polymorphous low-grade adenocarcinomas in malignant minor salivary gland tumors by continent as described in the studies included in this review as described in the studies included in this review

Continent

MMSGTs

PLGA

PLGA/MMSGTs

 

n

%

n

%

%

 Africa

178

2.6%

14

3.2%

7.9%

America

1,668

24.2%

115

26.7%

6.9%

 Asia

3,702

53.7%

144

33.4%

3.9%

Europe

1,313

19.1%

152

35.3%

11.6%

Oceania

30

0.4%

6

1.4%

20.0%

 Total

6,891

100.0

431

100.0

6.3

MMSGTs: malignant minor salivary gland tumors; PLGA: polymorphous low-grade adenocarcinoma.

Discussion

Analysis of the data from 57 epidemiological studies reflects a variety of methodologies, some examined all (major and minor) salivary gland tumors, while others examined only tumors of the minor glands but included benign and malignant tumors or even MMSGTs alone. This variability most likely reflects differences between the institutions from where most of the data were collected, such as hospitals and medical or dental schools. In other words, it does not reflect the real epidemiology of this tumor in these countries or continents, since they are a few isolated reports.

Nevertheless, it was possible to discern the PLGA percentages among the MMSGT cases, which was the aim of this study. We observed that PLGA rates have varied over the period studied and have most recently increased, most likely due to improved PLGA diagnostic accuracy. Over the last two study periods, the PLGA fraction has stabilized at a value that probably reflects a more accurate percentage of PLGAs among MMSGTs.

We also noted that the percentage varied by the continent where the studies were performed and by individual authors. Based on these results, we suggest that geographical differences alone cannot account for the varying incidence rates, such as occurs with Warthin tumor, which has a lower incidence in Africa, and with the lymphoepithelial carcinoma that has an evident predilection for Inuits (Eskimo), Chinese and Japanese[33, 37, 69, 70]. Also based on these differences it is impossible to extracting other important data as the differences in ACC survival rates between Chinese and occidental data as recently demonstrated by Zhou et al.[71].

Despite our improved understanding of this entity over time, worldwide differences found amongst the studies indicate that diagnosing PLGA remains challenging, probably because histological and cytological criteria are not uniformly applied. Interestingly, this diagnosis does not appear in some of the series, which used the designation “adenocarcinoma” with no further definition, which raises the question of whether a tumor is actually an adenocarcinoma NOS, a PLGA or another entity.

Since the 1990s, many studies have attempted to develop a useful marker for PLGA or to differentiate it from other histologically similar tumors[7275]. To date there has been no reliable molecular marker to distinguish PLGA from other MMSGTs[76]. The major research focus is currently on finding immunohistochemical differences between PLGA and adenoid cystic carcinoma (ACC), mainly in the cribriform histology, common to both tumors, which has been tirelessly attempted[7787].

Controversy on this subject persists in the literature. Some authors believe that immunohistochemistry does not have any proven diagnostic value for identifying PLGA[6, 78, 88, 89]. However, we do not share this opinion as we have successfully used immunohistochemistry in difficult cases or to confirm a histological diagnosis.

For diagnostic purposes, it is essential to characterize the morphology of the cell, the diversity of the histological tumor patterns and to recall that the PLGA cellular population exhibits a constant cytological appearance, despite a variety of growth patterns.

In our experience it is important to note that tumor cytology and histology are usually sufficient for a final diagnosis. However, immunohistochemistry is valuable in unclear PLGA cases, however. Uniformly positive vimentin and CK 7 staining, except for the rare two-layer ducts, is sufficient for a final PLGA diagnosis (Figure 1). S100 is also positive in almost all of the cells, but this characteristic is only diagnostically supportive. When examining cytoskeleton filaments in salivary gland tumors, it is also important to observe which cells are positive for each protein, rather than simply indicating the percentage of tumors in a series that are positive for each marker. Using this information, the immunohistochemistry of the cytoskeleton filament contributes greatly to the diagnosis of salivary gland tumors, especially PLGAs.
https://static-content.springer.com/image/art%3A10.1186%2F1746-1596-8-6/MediaObjects/13000_2012_Article_691_Fig1_HTML.jpg
Figure 1

The morphological and immunohistochemical aspects of PLGA. 1A: H&E staining shows a tumor histology composed of uniform single-cell strands. Diffuse and strong CK7 (1B) and vimentin (1C) immunohistochemical positivity are shown.

Declarations

Authors’ Affiliations

(1)
Department of Oral Pathology, Sao Leopoldo Mandic Institute and Research Center

References

  1. Luna MA, Wenig BM: Polymorhpous low grade adenocarcinoma. World health organization classification of tumours. Pathology and genetics of head and neck tumors. Edited by: Barnes L, Eveson JW, Reichart P, Sidransky D. 2005, Lyon: IARC Press, 223-224. 1
  2. Evans HL, Batsakis JG: Polymorphous low-grade adenocarcinoma of minor salivary glands. A study of 14 cases of a distinctive neoplasm. Cancer. 1984, 53 (4): 935-942. 10.1002/1097-0142(19840215)53:4<935::AID-CNCR2820530420>3.0.CO;2-V.View ArticlePubMed
  3. Freedman PD, Lumerman H: Lobular carcinoma of intraoral minor salivary gland origin. Report of twelve cases. Oral surgery, oral medicine, and oral pathology. 1983, 56 (2): 157-166. 10.1016/0030-4220(83)90282-7.View ArticlePubMed
  4. Batsakis JG, Pinkston GR, Luna MA, Byers RM, Sciubba JJ, Tillery GW: Adenocarcinomas of the oral cavity: a clinicopathologic study of terminal duct carcinomas. J Laryngol Otol. 1983, 97 (9): 825-835. 10.1017/S0022215100095062.View ArticlePubMed
  5. Pogodzinski MS, Sabri AN, Lewis JE, Olsen KD: Retrospective study and review of polymorphous low-grade adenocarcinoma. Laryngoscope. 2006, 116 (12): 2145-2149. 10.1097/01.mlg.0000243200.35033.2b.View ArticlePubMed
  6. Paleri V, Robinson M, Bradley P: Polymorphous low-grade adenocarcinoma of the head and neck. Curr Opin Otolaryngol Head Neck Surg. 2008, 16 (2): 163-169. 10.1097/MOO.0b013e3282f70441.View ArticlePubMed
  7. Raitz R, Martins MD, Araujo VC: A study of the extracellular matrix in salivary gland tumors. J Oral Pathol Med. 2003, 32 (5): 290-296. 10.1034/j.1600-0714.2003.00019.x.View ArticlePubMed
  8. Araujo V, Sousa S, Jaeger M, et al.: Characterization of the cellular component of polymorphous low-grade adenocarcinoma by immunohistochemistry and electron microscopy. Oral oncol. 1999, 35 (2): 164-172. 10.1016/S1368-8375(98)00102-X.View ArticlePubMed
  9. Gonzalez-Garcia R, Rodriguez-Campo FJ, Munoz-Guerra MF, et al.: Polymorphous lowgrade adenocarcinoma of the palate: report of cases. Auris Nasus Larynx. 2005, 32 (3): 275-280. 10.1016/j.anl.2005.03.019.View ArticlePubMed
  10. Skalova A, Vanecek T, Sima R, et al.: Mammary analogue secretory carcinoma of salivary glands, containing the ETV6-NTRK3 fusion gene: a hitherto undescribed salivary gland tumor entity. Am J Surg Pathol. 2010, 34 (5): 599-608.PubMed
  11. Araujo VC, Loducca SV, Sousa SO, Williams DM, Araujo NS: The cribriform features of adenoid cystic carcinoma and polymorphous low-grade adenocarcinoma: cytokeratin and integrin expression. Ann Diag Pathol. 2001, 5 (6): 330-334. 10.1053/adpa.2001.29339.View Article
  12. Seifert G, Sobin LH: World health classification of tumors. Histological typing of salivary gland tumours. 1991, Berlin: Springer, 2View Article
  13. Onyango JF, Awange DO, Muthamia JM, Muga BI: Salivary gland tumours in Kenya. East Afr Med J. 1992, 69 (9): 525-530.PubMed
  14. Rippin JW, Potts AJ: Intra-oral salivary gland tumours in the west midlands. Br Dent J. 1992, 173 (1): 17-19. 10.1038/sj.bdj.4807925.View ArticlePubMed
  15. Loyola AM, de Araujo VC, de Sousa SO, de Araujo NS: Minor salivary gland tumours. A retrospective study of 164 cases in a Brazilian population. Eur J Cancer B Oral Oncol. 1995, 31B (3): 197-201.View ArticlePubMed
  16. Neely MM, Rohrer MD, Young SK: Tumors of minor salivary glands and the analysis of 106 cases. J Okla Dent Assoc. 1996, 86 (4): 50-52.PubMed
  17. Rivera-Bastidas H, Ocanto RA, Acevedo AM: Intraoral minor salivary gland tumors: a retrospective study of 62 cases in a Venezuelan population. J Oral Pathol Med. 1996, 25 (1): 1-4. 10.1111/j.1600-0714.1996.tb01214.x.View ArticlePubMed
  18. Rushing T, Strohm SS, Christie DW, Krolls SO: Salivary gland tumors in Mississippi. Miss Dent Assoc J. 1996, 52 (3): 33-35.PubMed
  19. Jones AV, Craig GT, Speight PM, Franklin CD: The range and demographics of salivary gland tumours diagnosed in a UK population. Oral oncol. 2008, 44 (4): 407-417. 10.1016/j.oraloncology.2007.05.010.View ArticlePubMed
  20. Kusama K, Iwanari S, Aisaki K, et al.: Intraoral minor salivary gland tumors: a retrospective study of 129 cases. J Nihon Univ Sch Dent. 1997, 39 (3): 128-132. 10.2334/josnusd1959.39.128.View ArticlePubMed
  21. Nagler RM, Laufer D: Tumors of the major and minor salivary glands: review of 25 years of experience. Anticancer Res. 1997, 17 (1B): 701-707.PubMed
  22. Lopes MA, Kowalski LP, da Cunha Santos G, Paes de Almeida O: A clinicopathologic study of 196 intraoral minor salivary gland tumours. J Oral Pathol Med. 1999, 28 (6): 264-267.View ArticlePubMed
  23. Maaita JK, Nabih A, Al-Tamimi S, Wraikat A: Salivary gland tumors in Jordan: a retrospective study of 221 patients. Croat Med J. 1999, 40 (3): 539-542.
  24. Pacheco-Ojeda L, Domeisen H, Narvaez M, Tixi R, Vivar N: Malignant salivary gland tumors in quito, ecuador. ORL J Otorhinolaryngol Relat Spec. 2000, 62 (6): 296-302. 10.1159/000027772.View ArticlePubMed
  25. Koivunen P, Suutala L, Schorsch I, Jokinen K, Alho O-P: Malignant epithelial salivary gland tumors in northern Finland: incidence and clinical characteristics. Eur Arch Otorhinolaryngol. 2002, 259 (3): 146-149. 10.1007/s00405-001-0435-9.View ArticlePubMed
  26. Vargas PA, Gerhard R, Araujo Filho VJF, de Castro IV: Salivary gland tumors in a Brazilian population: a retrospective study of 124 cases. Rev Hosp Clin Fac Med Sao Paulo. 2002, 57 (6): 271-276.View ArticlePubMed
  27. Masanja MI, Kalyanyama BM, Simon ENM: Salivary gland tumours in Tanzania. East Afr Med J. 2003, 80 (8): 429-434.PubMed
  28. Hyam DM, Veness MJ, Morgan GJ: Minor salivary gland carcinoma involving the oral cavity or oropharynx. Aust Dent J. 2004, 49 (1): 16-19. 10.1111/j.1834-7819.2004.tb00044.x.View ArticlePubMed
  29. Kokemueller H, Swennen G, Brueggemann N, Brachvogel P, Eckardt A, Hausamem JE: Epithelial malignancies of the salivary glands: clinical experience of a single institution-a review. I Int J Oral Maxillofac Surg. 2004, 33 (5): 423-432. 10.1016/j.ijom.2004.02.007.View ArticlePubMed
  30. Poomsawat S, Punyasingh J, Weerapradist W: A retrospective study of 60 cases of salivary gland tumors in a Thai population. Quintessence Int Berlin, Germany. 1985, 35 (7): 577-581.
  31. Strick MJ, Kelly C, Soames JV, McLean NR: Malignant tumours of the minor salivary glands–a 20 year review. Br J Plastic Surg. 2004, 57 (7): 624-631. 10.1016/j.bjps.2004.04.017.View Article
  32. Toida M, Shimokawa K, Makita H, et al.: Intraoral minor salivary gland tumors: a clinicopathological study of 82 cases. Int J Oral Maxillofac Surg. 2005, 34 (5): 528-532. 10.1016/j.ijom.2004.10.010.View ArticlePubMed
  33. Vuhahula EAM: Salivary gland tumors in Uganda: clinical pathological study. Afr Health Sci. 2004, 4 (1): 15-23.PubMed CentralPubMed
  34. Lima SS, Soares AF, de Amorim RFB, Freitas RDA: Epidemiologic profile of salivary gland neoplasms: analysis of 245 cases. Braz J Otorhinolaryngol. 2005, 71 (3): 335-340.View ArticlePubMed
  35. Ito F, Ito K, Vargas P, de Almeida OP, Lopes M: Salivary gland tumors in a Brazilian population: a retrospective study of 496 cases. Int J Oral Maxillofac Surg. 2005, 34 (5): 533-536. 10.1016/j.ijom.2005.02.005.View ArticlePubMed
  36. Luukkaa H, Klemi P, Leivo I, et al.: Salivary gland cancer in Finland 1991–96: an evaluation of 237 cases. Acta Oto Laryngol. 2005, 125 (2): 207-214. 10.1080/00016480510003174.View Article
  37. Otoh EC, Johnson NW, Olasoji H, Danfillo IS, Adeleke OA: Salivary gland neoplasms in Maiduguri, north-eastern Nigeria. Oral Dis. 2005, 11 (6): 386-391. 10.1111/j.1601-0825.2005.01137.x.View ArticlePubMed
  38. Yih W-Y, Kratochvil FJ, Stewart JCB: Intraoral minor salivary gland neoplasms: review of 213 cases. Journal of oral and maxillofacial surgery. 2005, 63 (6): 805-810. 10.1016/j.joms.2005.02.021.View ArticlePubMed
  39. Ascani G, Pieramici T, Messi M, Lupi E, Rubini C, Balercia P: Salivary glands tumours: a retrospective study of 454 patients. Minerva Stomatol. 2006, 55 (4): 209-214.PubMed
  40. Ansari MH: Salivary gland tumors in an Iranian population: a retrospective study of 130 cases. J Oral Maxillofac Surg. 2007, 65 (11): 2187-2194. 10.1016/j.joms.2006.11.025.View ArticlePubMed
  41. Buchner A, Merrell PW, Carpenter WM: Relative frequency of intra-oral minor salivary gland tumors: a study of 380 cases from northern California and comparison to reports from other parts of the world. J Oral Pathol Med. 2007, 36 (4): 207-214. 10.1111/j.1600-0714.2007.00522.x.View ArticlePubMed
  42. Jones AS, Beasley NJ, Houghton DJ, Helliwell TR, Husband DJ: Tumours of the minor salivary glands. Clin Otolaryngol Allied Sci. 1998, 23 (1): 27-33. 10.1046/j.1365-2273.1998.00088.x.View ArticlePubMed
  43. Ladeinde AL, Adeyemo WL, Ogunlewe MO, Ajayi OF, Omitola OG: Salivary gland tumours: a 15-year review at the dental centre Lagos university teaching hospital. Afr J Med Med Sci. 2007, 36 (4): 299-304.PubMed
  44. Pires FR, Pringle GA, de Almeida OP, Chen S-Y: Intra-oral minor salivary gland tumors: a clinicopathological study of 546 cases. Oral oncol. 2007, 43 (5): 463-470. 10.1016/j.oraloncology.2006.04.008.View ArticlePubMed
  45. Wang D, Li Y, He H, et al.: Intraoral minor salivary gland tumors in a Chinese population: a retrospective study on 737 cases. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2007, 104 (1): 94-100. 10.1016/j.tripleo.2006.07.012.View ArticlePubMed
  46. Copelli C, Bianchi B, Ferrari S, Ferri A, Sesenna E: Malignant tumors of intraoral minor salivary glands. Oral oncol. 2008, 44 (7): 658-663. 10.1016/j.oraloncology.2007.08.018.View ArticlePubMed
  47. Li L-J, Li Y, Wen Y-M, Liu H, Zhao H-W: Clinical analysis of salivary gland tumor cases in west china in past 50 years. Oral oncol. 2008, 44 (2): 187-192. 10.1016/j.oraloncology.2007.01.016.View ArticlePubMed
  48. Rahman B, Mamoon N, Jamal S, et al.: Malignant tumors of the minor salivary glands in northern Pakistan: a clinicopathological study. Hematol Oncol Stem Cell Ther. 2008, 1 (2): 90-93.View ArticlePubMed
  49. Subhashraj K: Salivary gland tumors: a single institution experience in India. Br J Oral Maxillofac Surg. 2008, 46 (8): 635-638. 10.1016/j.bjoms.2008.03.020.View ArticlePubMed
  50. Chijiwa H, Sakamoto K, Umeno H, Nakashima T, Suzuki G, Hayafuchi N: Minor salivary gland carcinomas of oral cavity and oropharynx. J Laryngol Otol Suppl. 2009, 123 Suppl: 52-57.View Article
  51. Dhanuthai K, Boonadulyarat M, Jaengjongdee T, Jiruedee K: A clinico-pathologic study of 311 intra-oral salivary gland tumors in Thais. J Oral Pathol Med. 2009, 38 (6): 495-500. 10.1111/j.1600-0714.2009.00791.x.View ArticlePubMed
  52. Gao N, Li Y, Li L-J, Wen Y-M: Clinical analysis of head and neck cancer cases in southwest china 1953–2002. J Int Med Res. 2009, 37 (1): 189-197.View ArticlePubMed
  53. Mucke T, Robitzky LK, Kesting MR, et al.: Advanced malignant minor salivary glands tumors of the oral cavity. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2009, 108 (1): 81-89. 10.1016/j.tripleo.2009.01.013.View ArticlePubMed
  54. Ochicha O, Malami S, Mohammed A, Atanda A: A histopathologic study of salivary gland tumors in Kano, northern Nigeria. Indian J Pathol Microbiol. 2009, 52 (4): 473-476. 10.4103/0377-4929.56121.View ArticlePubMed
  55. de Oliveira F, Duarte E, Taveira C: Salivary gland tumor: a review of 599 cases in a Brazilian population. Head Neck. 2009, 3 (4): 271-275. 10.1007/s12105-009-0139-9.View Article
  56. Targa-Stramandinoli R, Torres-Pereira C, Piazzetta CM, Giovanini AF, Amenabar JM: Minor salivary gland tumours: a 10-year study. Acta Otorrinolaringol Esp. 2009, 60 (3): 199-201. 10.1016/S0001-6519(09)71231-2.View ArticlePubMed
  57. Tilakaratne WM, Jayasooriya PR, Tennakoon TMPB, Saku T: Epithelial salivary tumors in Sri Lanka: a retrospective study of 713 cases. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2009, 108 (1): 90-98. 10.1016/j.tripleo.2009.01.026.View ArticlePubMed
  58. Erovic BM, Schopper C, Pammer J, et al.: Multimodal treatment of patients with minor salivary gland cancer in the case of recurrent disease. Head Neck. 2010, 32 (9): 1167-1172. 10.1002/hed.21312.View ArticlePubMed
  59. Carrillo JF, Maldonado F, Carrillo LC, et al.: Prognostic factors in patients with minor salivary gland carcinoma of the oral cavity and oropharynx. Head Neck. 2011, 33 (10): 1406-1412. 10.1002/hed.21641.View ArticlePubMed
  60. Kakarala K, Bhattacharyya N: Survival in oral cavity minor salivary gland carcinoma. Otolaryngol Head Neck Surg. 2010, 143 (1): 122-126.View ArticlePubMed
  61. Kruse ALD, Gratz KW, Obwegeser JA, Lubbers H-T: Malignant minor salivary gland tumors: a retrospective study of 27 cases. Oral Maxillofac Surg. 2010, 14 (4): 203-209. 10.1007/s10006-010-0217-x.View ArticlePubMed
  62. Tian Z, Li L, Wang L, Hu Y, Li J: Salivary gland neoplasms in oral and maxillofacial regions: a 23-year retrospective study of 6982 cases in an eastern Chinese population. Int J Oral Maxillofac Surg. 2010, 39 (3): 235-242. 10.1016/j.ijom.2009.10.016.View ArticlePubMed
  63. Bjorndal K, Krogdahl A, Therkildsen MH, et al.: Salivary gland carcinoma in Denmark 1990–2005: a national study of incidence, site and histology. Results of the Danish head and neck cancer group (DAHANCA). Oral oncol. 2011, 47 (7): 677-682. 10.1016/j.oraloncology.2011.04.020.View ArticlePubMed
  64. Morais M, Azevedo P, Carvalho C, Medeiros L, Lajus T, Costa ALL: Clinicopathological study of salivary gland tumors: an assessment of 303 patients. Cad Saude Publica. 2011, 27 (5): 1035-1040. 10.1590/S0102-311X2011000500020.View Article
  65. Schwarz S, Muller M, Ettl T, Stockmann P, Zenk J, Agaimy A: Morphological heterogeneity of oral salivary gland carcinomas: a clinicopathologic study of 41 cases with long term follow-up emphasizing the overlapping spectrum of adenoid cystic carcinoma and polymorphous lowgrade adenocarcinoma. Int J Clin Exp Pathol. 2011, 4 (4): 336-348.PubMed CentralPubMed
  66. Venkata V, Irulandy P: The frequency and distribution pattern of minor salivary gland tumors in a government dental teaching hospital, Chennai, India. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2011, 111 (1): e32-e39. 10.1016/j.tripleo.2010.08.019.View ArticlePubMed
  67. Bello IO, Salo T, Dayan D, et al.: Epithelial salivary gland tumors in Two distant geographical locations, Finland (Helsinki and Oulu) and Israel (Tel Aviv): a 10-year retrospective comparative study of 2,218 cases. Head Neck Pathol. 2012, 6 (2): 224-231. 10.1007/s12105-011-0316-5.PubMed CentralView ArticlePubMed
  68. Lukšić I, Virag M, Manojlović S, Macan D: Salivary gland tumours: 25 years of experience from a single institution in Croatia. J Craniomaxillofac Surg. 2012, 40 (3): e75-81. 10.1016/j.jcms.2011.05.002.View ArticlePubMed
  69. Tsang WYW, Kuo TT, Chan JKC: Lymphoepithelial carcinoma. World health organization classification of tumours. Pathology and genetics of head and neck tumors. Edited by: Barnes LE, Eveson JW, Reichart P, Sidransky D. 2005, Lyon: IARC Press, 251-152. 1
  70. Simpson RHW, Eveson JW: Wharthin tumour. World health organization classification of tumours. Pathology and genetics of head and neck tumors. Edited by: Barnes LE, Evenson JW, Reichart P, Sidransky D. 2005, Lyon: IARC Press, 263-265. 1
  71. Quan Z, Hong C, Hongkai Z, Yiding H, Honggang L: Increased numbers of P63-positive/CD117-positive cells in advanced adenoid cystic carcinoma give a poorer prognosis. Diagn Pathol. 2012, 7: 119-10.1186/1746-1596-7-119.View Article
  72. Gnepp DR, el-Mofty S: Polymorphous low-grade adenocarcinoma: glial fibrillary acidic protein staining in the differential diagnosis with cellular mixed tumors. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 1997, 83 (6): 691-5. 10.1016/S1079-2104(97)90321-8.View ArticlePubMed
  73. Furuse C, Tucci R, Machado de Sousa SO, Rodarte Carvalho Y, Cavalcanti de Araujo V: Comparative immunoprofile of polymorphous low-grade adenocarcinoma and canalicular adenoma. Ann Diag Pathol. 2003, 7 (5): 278-80. 10.1016/S1092-9134(03)00084-4.View Article
  74. Westernoff TH, Jordan RCK, Regezi JA, Ramos DM, Schmidt BL: Beta-6 integrin, tenascin- C, and MMP-1 expression in salivary gland neoplasms. Oral oncol. 2005, 41 (2): 170-4. 10.1016/j.oraloncology.2004.08.002.View ArticlePubMed
  75. Taufik D, Hussein MR: Juvenile pleomorphic adenoma of the cheek: a case report and review of literature. Diagn Pathol. 2009, 4: 32-10.1186/1746-1596-4-32.View Article
  76. Persson F, Fehr A, Sundelin K, Schulte B, Löning T, Stenman G: Studies of genomic imbalances and the MYB-NFIB gene fusion in polymorphous low-grade adenocarcinoma of the head and neck. Int J Oncol. 2012, 40 (1): 80-4.PubMed
  77. Loducca SV, Raitz R, Araujo NS, Araujo VC: Polymorphous low-grade adenocarcinoma and adenoid cystic carcinoma: distinct architectural composition revealed by collagen IV, laminin and their integrin ligands (alpha2beta1 and alpha3beta1). Histopathology. 2000, 37 (2): 118-23. 10.1046/j.1365-2559.2000.00900.x.View ArticlePubMed
  78. Darling MR, Schneider JW, Phillips VM: Polymorphous low-grade adenocarcinoma and adenoid cystic carcinoma: a review and comparison of immunohistochemical markers. Oral oncol. 2002, 38 (7): 641-5. 10.1016/S1368-8375(02)00003-9.View ArticlePubMed
  79. Edwards PC, Bhuiya T, Kelsch RD: C-kit expression in the salivary gland neoplasms adenoid cystic carcinoma, polymorphous low-grade adenocarcinoma, and monomorphic adenoma. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2003, 95 (5): 586-93. 10.1067/moe.2003.31.View ArticlePubMed
  80. Epivatianos A, Iordanides S, Zaraboukas T, Antoniades D: Adenoid cystic carcinoma and polymorphous low-grade adenocarcinoma of minor salivary glands: a comparative immunohistochemical study using the epithelial membrane and carcinoembryonic antibodies. Oral Dis. 2005, 11 (3): 175-80. 10.1111/j.1601-0825.2005.01110.x.View ArticlePubMed
  81. Beltran D, Faquin WC, Gallagher G, August M: Selective immunohistochemical comparison of polymorphous low-grade adenocarcinoma and adenoid cystic carcinoma. J Oral Maxillofac Surg. 2006, 64 (3): 415-23. 10.1016/j.joms.2005.11.027.View ArticlePubMed
  82. Woo VL, Bhuiya T, Kelsch R: Assessment of CD43 expression in adenoid cystic carcinomas, polymorphous low-grade adenocarcinomas, and monomorphic adenomas. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2006, 102 (4): 495-500. 10.1016/j.tripleo.2005.08.038.View ArticlePubMed
  83. Epivatianos A, Poulopoulos A, Dimitrakopoulos I, et al.: Application of alpha-smooth muscle actin and c-kit in the differential diagnosis of adenoid cystic carcinoma from polymorphous low grade adenocarcinoma. Oral oncol. 2007, 43 (1): 67-76. 10.1016/j.oraloncology.2006.01.004.View ArticlePubMed
  84. Prasad ML, Barbacioru CC, Rawal YB, Husein O, Wen P: Hierarchical cluster analysis of myoepithelial/basal cell markers in adenoid cystic carcinoma and polymorphous low-grade adenocarcinoma. Mod Pathol. 2008, 21 (2): 105-14.PubMed
  85. Ferrazzo KL, Neto MM, dos Santos E, dos Santos PD, de Sousa SOM: Differential expression of galectin-3, beta-catenin, and cyclin D1 in adenoid cystic carcinoma and polymorphous low-grade adenocarcinoma of salivary glands. J Oral Pathol Med. 2009, 38 (9): 701-7. 10.1111/j.1600-0714.2009.00776.x.View ArticlePubMed
  86. Shaimaa Ghazy E, Iman Helmy M, Houry Baghdadi M: Maspin and MCM2 immuno profiling in salivary gland carcinomas. Diagn Pathol. 2011, 6: 89-10.1186/1746-1596-6-89.PubMed CentralView ArticlePubMed
  87. Saghravanian N, Mohtasham N, Jafarzadeh H: Comparison of immunohistochemical markers between adenoid cystic carcinoma and polymorphous low-grade adenocarcinoma. J Oral Sci. 2009, 51 (4): 509-14. 10.2334/josnusd.51.509.View ArticlePubMed
  88. Gupta R, Gupta K, Gupta R: Polymorphous low-grade adenocarcinoma of the tongue: a case report. J Med Case Rep. 2009, 3: 9313-10.1186/1752-1947-3-9313.PubMed CentralView ArticlePubMed
  89. Simpson RH, Clarke TJ, Sarsfield PT, Gluckman PG, Babajews AV: Polymorphous low grade adenocarcinoma of the salivary glands: a clinicopathological comparison with adenoid cystic carcinoma. Histopathology. 1991, 19 (2): 121-9. 10.1111/j.1365-2559.1991.tb00002.x.View ArticlePubMed

Copyright

© de Araujo et al.; licensee BioMed Central Ltd. 2013

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://​creativecommons.​org/​licenses/​by/​2.​0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Advertisement