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The Role of the Human Papillomavirus in the Pathogenesis of Schneiderian Inverted Papillomas: An Analytic Overview of the Evidence

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Abstract

Background Evidence of an etiological role for human papillomavirus (HPV) in Schneiderian inverted papillomas IP arose in the late 1980’s; yet almost three decades later, the association between HPV and IP has yet to be universally accepted. This is probably due to the disparate HPV detection rates in IP reported in the literature. We analyzed the weight of published data in order to address the following questions: why do the HPV detection rates in IP vary so greatly? What is the relationship between low-risk (LR) and high-risk (HR) HPV types and HPV detection rates in IP? Is there a relationship between the presence and type of HPV in IP and recurrence and malignant progression? Materials and methods A search using the Pubmed search engine was performed to identify studies published in English from 01/87 through 12/06 using the MeSH terms ‘‘HPV’’ and ‘‘Inverted”, “Exophytic”, “Oncocytic Schneiderian” or “Fungiform papilloma’’. Data was abstracted from publications including histology, HPV target, HPV type, method of detection, etc. HPV results were stratified by histology and other variables. Tests for heterogeneity (between-study variability) were conducted, and weighted prevalence (WP) estimates and 95% confidence intervals (CI) were calculated using a random-effects inverse-variance model stratified on study. The association between HPV IP recurrence was estimated by random-effects inverse-variance weighted odds ratio (OR). Results Weighted estimates revealed similar detection rates across detection methods, 26.8% (95%CI 16.4–37.2%) by ISH, 25.2% (95%CI 14.7–35.6%) by consensus PCR, and 23.6% (95%CI 12.2–35.0%) by type-specific PCR. A preponderance of HPV 6/11 is found in IP as compared to HPV 16/18; the overall unadjusted ratio of LR to high-risk HR HPV types is 2.8:1 The HPV detection rates significantly increase (Wald t-test P < 0.02) in IPs with high-grade dysplasia (WP 55.8%, 95%CI 30.5-81.0%) and carcinoma (WP 55.1%, 95%CI 37.0–73.2%) as compared to IPs with no dysplasia or mild dysplasia (WP 22.3%, 95%CI 15.9–28.6%). Furthermore, the preponderance of LR HPV in benign IP (ratio LR/HR = 4.8:1) shifts in dysplastic and malignant IP. The LR/HR ratio is 1.1:1 for IPs with high-grade dysplasias, this ratio is inverted to favor HR HPV (1:2.4) for malignant IP. Recurrences developed in 44 of 236 patients; HPV was detected in 27 of 44 IPs (WP 57.9%, 95%CI 31.6–84.2%) that developed recurrences and in 24 of 192 IPs (WP 9.7%, 95%CI 4.4–15.0%) that did not develop recurrence. The presence of HPV was significantly associated with the likelihood of developing recurrence (weighted OR of 10.2, 95%CI 3.2–32.8). Conclusions We hypothesize that LR HPV may induce IP formation, and then are lost as infected cells are shed, as a “hit and run” phenomenon. HPV detection rates increase in dysplastic IP and SCC-ex-IP with increasing ratio of HR to LR HPV types, compared to nondysplastic IP. We believe that one explanation for the variation in HPV detection rates between different studies may be the actual histologic composition of the cohort. That is, if one series contains a higher frequency of dysplastic and malignant IP, it may have a higher detection rate than another series which contains only nondysplastic IP. We hypothesize that the higher rates of HPV detection in dysplastic and malignant IP may be related to HPV integration. The implication of this is that HPV sub-type testing may identify patients at risk for recurrence, or progression to dysplasia and malignancy, and thus may impact surveillance protocols.

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Authors and Affiliations

  1. Department of Otolaryngology, Mount Sinai School of Medicine, New York, NY, 10021, USA

    William Lawson

  2. Departments of Epidemiology & Population Health and Medicine, Montefiore Medical Center, Albert Einstein College of Medicine, Bronx, NY, 10461, USA

    Nicolas F. Schlecht

  3. Departments of Pathology and Otolaryngology, Montefiore Medical Center, Albert Einstein College of Medicine, 111 East 210th Street, Bronx, NY, USA

    Margaret Brandwein-Gensler

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Appendix

Appendix

 

Detection Methodology for HPV in Inverted Papillomas

Author

Year

Target

Method*

HPV types

Positive cases/Subjects (%)*

Median Age

M:F

Comments

Respler

1987

DNA

SB

11

+1/2 (50%)

12.5

1:1

 

Syrjanen

1987

DNA

ISH

6/11/16/18

5/14 HPV 11 (36%)

58

2:1

4 coinfections

1/14 HPV 16 (7%)

1 recurrence

4/14 HPV 11 and 16 (29%)

 

Brandsma

1987

DNA

SB, ISH

2, 6/11, 16/18

+2/9 HPV 11 (22% by SB)

NA

+1 HPV 6 (ISH) probably exophytic papilloma

+1/6 HPV 6 ( 17% by ISH)

 

Weber

1988

DNA

ISH

6b, 11

+16/21 (76%)

45

2.5:1

+1 case: with SCC, +3 cases with “atypia”

Brandwein

1989

RNA

ISH

6/11, 16/18

+3/7 (43%) HPV 6/11

60

6:1

+3 cases with dysplasia +1 case:with SCC

+2/7 (29%) HPV 16/18

Siivonen

1989

DNA

ISH

6/11, 16

+8/21 (38%) HPV11

56

3.2:1

+3 cases: with SCC

+8/21 (38%) HPV 16

3 cases with coinfection

Ishibashi

1990

DNA

SB

6/11, 16/18

+1/7 (14%) HPV 6

61

1.3:1

 

Bryan

1990

DNA

PCR

6/11

+10/13 (77%) HPV 6/11

   

Judd

1991

DNA

ISH, PCR

6/11, 16/18, 33

0/9 HPV+

67

1:1.3

 

Furuta

1991

DNA

ISH, PCR, DB

6/11, 16/18

+3/26 (12%) HPV 11 (DB & ISH)

NA

+1 case by DB & ISH with SCC. 1 additional IP with

+1/26 (4%) HPV 16 (DB & ISH)

 

SCC + HPV 16 by PCR

Sarkar

1992

DNA

ISH, PCR

6b/11, 16/18

0/24 HPV+

 

McLachlin

1992

DNA

ISH, PCR

6/11, 16/18, 31/33/35

+3/17 (18%) HPV 6/11

57

14:1

+1 case with dysplasia +1 HPV 16 case with SCC

+1/17 (6%) HPV 16

Kashima

1992

DNA

PCR

6/11, 16/18

+7/29 (24%) HPV 6/11

NA

Wu

1993

RNA

ISH, PCR, SB

57b

+12/15 (80%) HPV 57b

NA

+1 case with dysplasia +2 cases with SCC

Tang

1994

DNA

ISH

6/11, 16/18, 31/33/35

0/26

NA

Buchwald

1995

DNA

ISH, PCR

6/11, 16/18, 31/33/35, 45, 51, 52 consensus L 1 (MY09/MY11)

+4/57 HPV 6/11 (7%)

NA

+2 cases with SCC

+1/57 HPV 18 (2%)

 

Beck

1995

DNA

PCR

6/11, 16/18, 31/33, 35, 57 consensus L1, MY09/MY11, E6 (WD72, WD76, WD66, WD67, WD154)

+18/39 (46%) HPV 6/11

59 mean

2.6:1

+5 with dysplasia +10 with SCC

+5/39 (13%) HPV 16/18

MacDonald

1995

DNA

PCR

6/11, 16/18

+8/20 (40%) HPV 6/11

NA

+1 case with SCC

+1/20 (5%) HPV 16

 

Gaffey

1996

DNA, RNA

ISH

6/11, 16/18, 31/33, 35, 42–45, 51, 52, 56

+1/20 (5%) HPV 16

NA

+1 HPV 11 case with SCC

+1/20 (5%) HPV 11

 

Shen

1996

DNA

PCR

6/11, 16/18 consensus L1, MY09/MY11

+17/46 (37%) HPV 6/11

NA

Includes +1/6 with SCC (HPV 16)

+1/46 (2%) HPV 16

 

Ogura

1996

DNA

PCR

2a, 5b, 6b, 11, 16/18, 57, 58

+2/9 (22%) HPV 16

51

1.4:1

 

+1/9 (11%) HPV 57

Caruana

1997

DNA

PCR

6b, 11, 16/18, 31/33 consensus L1, MY09/MY11

+2/19 (11%) HPV 6b/11

64

1.6:1

+4/8 cases with dysplasia +2/4 cases with SCC

+7/19 (37%) HPV 16

Bernauer

1997

DNA

PCR

6/11, 16/18 consensus L1, MY09/MY11

+7/22 (33%) consensus primers

53

2.5:1

+2/2 cases with SCC, one of which was HPV 18

+1/22 (5%) HPV 18

Hwang

1998

DNA

PCR

6/11, 16/18, 33

+3/42 (7%) HPV 6/11 + 2/42 (5%) HPV 16

NA

+1 case with dysplasia +2 cases with SCC

Mirza

1998

DNA

ISH

6/11, 16/18

+5/28 (18%) HPV 6/11

NA

+1 case with dysplasia

+2/28 (7%) HPV 16/18

 

+1 case with SCC

  

+1 case with low-risk/high-risk coinfection

Kassim

1998

DNA

PCR

16

4/10 (40%) HPV 16

49

All male

 

Saegusa

1999

DNA

PCR

16/18

+6/28 (36%) HPV 16/18

NA

Weiner

1999

DNA

PCR

6b/11, 16/18 consensus L1, MY09/MY11, GP5+/GP6+

+3/83 (4%) HPV 11

NA

includes +1/7 with SCC. 6 SCC arose in IP, 1 arose in an oncocytic papilloma, derivation of one positive case not specified

+2/83 (3%) HPV 16

 

+1/83 (1%) HPV 18

 

Kraft

2001

DNA

ISH, PCR

6/11, 16/18, 31/33/51 consensus L1, MY09/MY11

+1/29 (3%) HPV 11

NA

Fischer

2005

DNA

PCR

consensus L1, CP66F, CP69F

+4/6 (67%) HPV+

NA

Sequencing in +3 cases: homology with HPV 21/34/56/60/66/80

McKay

2005

DNA

PCR

6/11, 16/18, 31/33, 35, 45, 52, consensus L1, MY09/MY11

+1/14 (7%) HPV 11 + 2/14 (14%) HPV 18

NA

HPV integration present in 4 cases with severe dysplasia or SCC

Katori

2006

DNA

ISH

 

+12/29 (41%) HPV 6/11

52 mean

1.9:1

+5 cases with severe dysplasia and +4 cases with SCC. No mention of coinfection, we assume there was none

+9/29 (31%) HPV 16/18

Hoffman

2006

DNA

PCR

6/11, 16, consensus L1/L2, MY09/MY11

+3/26 (12%) HPV 6/11

61

1.9:1

 

+2/26 (8%) other IP with consensus primers

  1. * ISH––in situ hybridization; PCR––polymerase chain reaction; SB––southern blot; SCC––squamous cell carcinoma

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Lawson, W., Schlecht, N.F. & Brandwein-Gensler, M. The Role of the Human Papillomavirus in the Pathogenesis of Schneiderian Inverted Papillomas: An Analytic Overview of the Evidence. Head and Neck Pathol 2, 49–59 (2008). https://doi.org/10.1007/s12105-008-0048-3

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