Commentary Open Access
Volume 2 | Issue 2 | DOI: https://doi.org/10.33696/cancerimmunol.2.014

Verrucous Carcinoma of the Esophagus: Its Unique Etiology and Association with Human Papilloma Virus

  • 1Department of Digestive and Transplantation Surgery, Tokyo Medical University Hachioji Medical Center, Hachioji, Tokyo, 193-0998, Japan
  • 2Department of Gastroenterological Surgery, Tokai University School of Medicine, Isehara, Kanagawa, 259-1193, Japan
+ Affiliations - Affiliations

*Corresponding Author

Kazuo Koyanagi, kkoyanagi@tsc.u-tokai.ac.jp

Received Date: May 02, 2020

Accepted Date: May 14, 2020


Verrucous carcinoma of the esophagus (VCE) is a rare variant of esophageal squamous cell carcinoma. Most cases of VCE presents as an exophytic, slow-growing mass with a superficial growth pattern. Even when VCE exhibits a characteristic pattern during an endoscopic examination, it is very difficult to make a definitive diagnosis of VCE preoperatively, because biopsy specimens are only characterized by nonspecific acanthosis and hyperkeratosis or parakeratosis associated with inflammation. As well as the characteristics of VCE, the etiology of the disease is even unique. VCE is typically associated with chronic mucosal irritation such as reflux esophagitis, achalasia, and lye ingestion that has resulted in esophageal inflammation or a long-term local disease process in addition to the classic risk factors of nicotine and alcohol consumption. Recent studies had indicated that human papilloma virus (HPV) infection might be associated with VCE. While HPV may be related to VCE initiation, involvement of HPV in the etiology of VCE requires further investigation. VCE’s etiology and therapeutic strategy, including the vaccination against HPV, should be established.


Verrucous carcinoma, Esophagus, Human papilloma virus


Verrucous carcinoma is an extremely rare disease, and it is unique in terms of its appearance, growth pattern, and etiology. In 1948, Ackerman first described verrucous squamous cell carcinoma (VSC) as a variant of oral squamous cell carcinoma [1], and he collected 31 cases of oral neoplasms under the name, “Verrucous Carcinoma of the Oral Cavity.” VSC was described as having the following characteristics: slow growing, well-differentiated, irregular surface appearance with a propensity to spread locally, and VSC has subsequently been reported in the mouth, nasal cavity, larynx, glans penis, scrotum, vulva, vagina, cervix, endometrium, urinary bladder, and anorectal region. Verrucous carcinoma of the esophagus (VCE) is a rare variant of esophageal squamous cell carcinoma. In 1967, Minielly et al. described VCE for the first time in a series of five cases [2]. Interestingly, there are reports suggesting an association between VCE and human papilloma virus (HPV) infection, stating that HPV may be involved in the carcinogenesis of VCE. Although VCE exhibits the same typical appearance and growth patterns as VSC in other organs, because of the paucity of cases neither its etiology nor therapeutic strategies have not been well assessed. In this commentary we reviewed previous reports and discussed VCE, in particular association between its etiology and HPV infection.

Review of the Literature Concerning VCE

We used the keywords “esophagus” and “verrucous carcinoma” to search the literature in the PubMed database during the period from 1983 to 2018 (Table 1). Only 48 cases of VCE (including our case) have been described since Minielly’s first report of VCE [2]. Males have predominated, but the proportion of women with VCE (28 males, 18 females, 2 gender unknown) has been higher among esophageal squamous cell carcinoma patients. The male-female ratio is about 3:2, and VCE patients’ ages (median, 64 years; range, 36-79 years) have been similar to those of esophageal squamous cell carcinoma patients. The most common chief complaint was dysphagia (in 39 (85%) of the 46 cases). The tumors have predominantly been located in the lower third of the esophagus (30 cases, 64%), and their frequent location in the lower-third of the esophagus may be associated with chronic esophageal mucosal inflammation. Almost all patients had a medical history that resulted in esophageal injury or inflammation before the diagnosis of VCE: 90% of the patients have had an associated chronic disease or condition (e.g., achalasia, reflux esophagitis, candida esophagitis, and heavy consumption of nicotine and alcohol).

No Author Year Age/Sex Chief complaint Past history Location 1st diagnosis Tumor size (cm) Treatment Prognosis T N M  
1 Minielly2) 1967 58/M dysphagia achalasia upper benign 9×8.5 OPE 1m, dead 3 0 0  
2   1967 70/F dysphagia diverticulum upper VC large tumor RT unknown N/A N/A N/A  
3   1967 70/F dysphagia achalasia upper VC large tumor RT 2m, dead 4 N/A N/A  
4   1967 36/M dysphagia diverticulum lower SCC 9×8 OPE 2m, dead 4 + N/A  
5   1967 57/M dysphagia none lower benign N/A BSC 5m, dead N/A N/A N/A  
6 Parkinson26) 1970 76/M melena obstruction middle SCC 7.5 BSC 1m, dead 1b 0 0  
7 Meyerowitz27) 1971 45/M hematemesis none lower benign 8×5.5 OPE, RT 9m, dead 2 N/A 0  
8 Sridher28) 1980 54/M dysphagia hiatal hernia lower benign 2 OPE unknown 1b 0 N/A  
9 Sakurai16) 1983 78/M dysphagia none upper VC 10×5 CT 6m, alive 4 N/A N/A  
10 Agha29) 1984 66/M dysphagia acid burn upper VC large tumor BSC 2m, dead 4 N/A N/A
11 Barbier30) 1987 50/F dysphagia hiatal hernia lower VC N/A OPE 10m, alive 1a 0 0
12 Koerfgen31) 1988 75/M dysphagia traumatic stenosis lower benign N/A OPE 36m, alive 2 0 0
13   1988 54/? dysphagia none lower benign 6.5×6.5 OPE 18m, alive 2 0 0
14 Jasim7) 1990 79/M dysphagia hiatal hernia lower benign 9×6 BSC dead N/A 0 0
15 Biemond13) 1991 76/F dysphagia, dyspnea RE middle benign 15 BSC 1m, dead 4 0 0
16 Roach32) 1993 67/M dysphagia achalasia upper benign 7 BSC 2m, dead 4 0 0
17 Garrard33) 1994 51/F dysphagia none middle VC 10 OPE 9m, alive 2 0 0
18 Kavin4) 1996 76/? odynophagia none lower benign N/A BSC 1m, dead N/A + N/A
19 Malik34) 1996 66/M dysphagia RE lower benign 5×2 OPE 36m, alive 2 0 0
20 Tajiri35) 2000 40/M none none lower VC 0.6×0.8 EMR 48m, alive 1a 0 0
21 Ereno36) 2001 65/F dysphagia none middle N/A 11 OPE N/A N/A N/A N/A
22 Osborn6) 2003 67/M dysphagia achalasia lower benign 8×8 OPE 9m, alive 2 0 0
23 Devlin8) 2004 56/F abdominal pain none lower benign 2.7 OPE 14m, alive 1b 0 0
24 Pfitzmann37) 2004 66/F N/A none lower N/A N/A OPE N/A N/A N/A N/A
25 Liberale21) 2005 41/M chest pain none lower VC N/A Antiviral Tx 6m, dead 4 N/A N/A
26 Na5) 2009 50/M dysphagia RE middle VC 7.5×4.8 OPE 6m, alive 2 0 0
27 Oh14) 2009 73/F dysphagia RE upper benign 3.5 BSC 23m, alive 1a 0 0
28 Garcia38) 2010 71/F dysphagia obstruction middle benign 3.9×2.5 OPE N/A 2 0 0
29 Tonna22) 2010 61/M dysphagia none extensive benign 10 OPE 12m, alive 1b 0 0
30 Munson39) 2010 63/F dysphagia none extensive VC 16 CRT N/A 3 + 0
31 Taniyama40) 2012 74/M nausea none middle benign 5 OPE 6m, alive 2 0 0
32 Vieira25) 2013 58/M dysphagia none N/A benign N/A OPE 1m dead 2 0 0
33 Sweetser3) 2014 61/M dysphagia N/A extensive N/A N/A OPE, CRT 72m, alive 2 0 0
34   2014 73/F dysphagia N/A lower N/A N/A CRT 36m, alive N/A N/A N/A
35   2014 66/M dysphagia N/A lower N/A N/A OPE 120m, alive 1 0 0
36   2014 70/F dysphagia N/A extensive N/A N/A OPE 6m, dead 1 0 0
37   2014 71/M dysphagia N/A middle N/A N/A N/A 36m, dead 2 0 0
38   2014 57/M N/A N/A lower N/A N/A N/A N/A 3 0 0
39   2014 75/F dysphagia N/A lower N/A N/A N/A N/A 1 0 0
40   2014 62/M dysphagia N/A extensive N/A N/A OPE 96m, alive 3 0 0
41   2014 63/F dysphagia N/A extensive N/A N/A CRT 12m, alive 3 0 0
42   2014 68/M dysphagia N/A extensive N/A N/A OPE, CRT 24m, alive 1 0 0
43   2014 62/F dysphagia N/A middle N/A N/A OPE 24m, alive 1 0 0
44 Abe41) 2016 68/M none N/A lower benign 1 ESD N/A 1a 0 0
45 Cox42) 2017 62/M dysphagia none middle SCC 9.5 OPE N/A 1b 0 0
46 Hoffmann43) 2018 61/M dysphagia systemic sclerosis lower VC N/A OPE 24m, alive 1b 0 0
47   2018 52/F dysphagia none lower VC 10 OPE 24m, alive 2 0 0
48 Tabuchi12) 2020 56/F dysphagia none lower benign 12 OPE 96m, alive 3 0 0

VC: Verrucous carcinoma; SCC: Squamous cell carcinoma; OPE: Operation; CRT: Chemoradiation; CT: Chemotherapy; RT: Irradiation; EMR: Endoscopic mucosal resection; ESD: Endoscopic submucosal dissection; Antiviral Tx: Antiviral treatment; BSC: Best supportive care; RE: Reflux esophagitis; N/A not assessed

Table 1: Reported cases of Verrucous carcinoma of esophagus.

VCE tumor sizes have been relatively large, but depth of invasion has generally been shallow. In 23 (48% of the 48 cases reported) of the 29 cases in which tumor size was recorded, the tumor measured 5 cm or more in diameter. Tumor invasion has been limited to the muscle layer (T1 and T2): in 68% of the patients in which depth of tumor invasion was recorded, but in seven cases (17%) the tumor was locally advanced (T4). This could be explained by the difficulty of making the diagnosis of VCE. In addition, very low incidence of lymph node metastasis (8%) and distant organ metastasis (0%) have been special characteristics of VCE.

The histopathologic features of VCE include good preservation of the epithelial basement membrane and highly differentiated histology, both of which are important in differentiating VCE from other esophageal carcinomas. However, in the majority of cases, mucosal biopsies were diagnosed as acanthosis, hyperkeratosis, and parakeratosis, and these nonspecific pathological findings make the correct diagnosis of VCE difficult and delay the start of treatment. Using EUS may provide information that is crucial to the diagnostic process [3]. The majority of VCE patients have impressive inflammatory changes that extend deep into the submucosal space and the muscularis propria, and EUS is ideally suited to detecting such changes. Since distorted architecture and local invasion are readily visible by EUS, EUS may make it possible to establish the appropriate diagnosis of VCE.

The histological picture of VCE resembles that of benign squamous cell papilloma. However, VCE tends to be deep-growing and invasive, whereas papilloma tends to grow superficially. Biemond et al. [4] proposed that the presence of infiltration is essential to differentiating VCE from squamous papilloma. It should be noted that some squamous papilloma shows evidence of dysplasia without infiltration. However, because of the limited low-grade nevus cell nest formation and the highly keratinized surface of the tumors, it is not easy to diagnose VCE on the basis of the findings in preoperative biopsy samples. In fact, only 12 (25%) of the 48 cases were diagnosed as esophageal VC based on the biopsy pathology findings. As Oh et al. have reported, endoscopic mucosal resection (EMR) might be a useful means of making an accurate diagnosis in suspected cases of VCE [5].

Treatment consisted of surgery in 28 cases, chemoradiation therapy in 5 cases, radiotherapy in 3 cases, chemotherapy in 1 case, and best supportive care in 8 cases. Before 1990, all patients had undergone esophageal resection and experienced significant postoperative complications. Surgical treatment after 1990 yielded favorable results because of improvements in surgical procedures and perioperative management in recent years as well as because of the low malignant potentials of VCE. The effectiveness of radiotherapy and chemotherapy, on the other hand, has been very limited [6]. Chemotherapeutic regimens that have been used to treat squamous cell carcinoma have not been effective against VCE. There has been only one report of partial treatment response with bleomycin [7], and new drugs or regimens need to be developed. If a locally advanced tumor stage is the initial diagnosis and surgery is technically possible, esophageal resection should be considered because of the rarity of lymph node metastases and the limited chemo- and radio-sensitivity of VCE.

Association between VCE and Esophageal Mucosal Inflammation

In addition to the classic risk factors of nicotine and alcohol consumption, VCE is typically associated with chronic esophageal mucosal inflammation. Kavin et al. [8] reported a case of VCE in a patient who had chronic esophagitis secondary to a caustic injury as a result of ingesting aerosolized lye and kerosene syrup. After 16 years of serial endoscopic surveillance, a verrucous mass was detected in the distal esophagus, and serial biopsies showed progression from esophagitis to leukoplakia, then to papillary hyperplasia and, finally, to dysplasia. Similar findings had been reported in laboratory rats in which VCE was experimentally induced by prolonged exposure of the esophagus to N-methyl-N-nitrosoaniline [9]. The lesions observed in the rats progressed in stages from acanthosis and hyperkeratosis, to leukoplakia, and then to papillary hypertrophy, and within 500 days the esophageal surface transformed from its normal smooth appearance to having a verrucous exophytic appearance. We also described that candida esophagitis was diagnosed during long-term follow-up period and might be related to the VCE [10]. Thus, esophageal injury or irritation is likely to be a prerequisite for the sequential development of dysplastic changes over time.

Association between VCE and Human Papilloma Virus Infection

HPV infection accounts for approximately more than 5% of the worldwide human cancers [11]. HPV can infect the stratified epithelia of the skin or mucous membranes of the upper gastrointestinal, respiratory, or anogenital tract, potentially leading to the outcomes such as genital warts and laryngeal papilloma, and sometimes certain cancers. Various types of HPV have been associated with developing cancers in several organs: “low risk” and “high risk” depending on the oncological potential. VSC is uniquely suspected of being related to HPV. HPV infection has been reported to be associated with several cancers, and involvement of HPV in head and neck cancers, particularly oropharyngeal cancer, has recently become clear and been attracting attention. HPV infection due to sexual activity is the cause, and the HPV-positive rate in head and neck cancer patients has been increasing every year [12]. Developing the cancerous lesion after HPV infection may be associated with the immune status of the patients. De Socio et al. has reported a case of HPVassociated lips verrucous carcinoma in HIV-infected male patient [13]. HIV-positive patients have a 2 to 3 times higher prevalence of oral HPV infection than HIVnegative patients. It has also become clearer that HPV infection is the cause of almost all cases of cervical cancer, and HPV vaccination has been introduced worldwide as a means of preventing cervical cancer [14]. HPV may be involved in carcinogenesis [15]. HPV infection causes high expression of oncogenes E6 and E7 in basal cells, promotes proteolysis of tumor suppressor genes p53 and Rb, and inactivates their functions.

There have also been a number of reports of HPV being related to primary laryngeal VC [16]. Also, many studies have addressed a possible association between HPV infection and esophageal dysplasia. Tornesello et al. reported 66 esophageal cancer patients and demonstrated the relatively higher prevalence of HPV infection in welldifferentiated squamous cell carcinoma, suggesting a tropism of HPV replication in keratinized tissues [17]. Several investigators have clearly demonstrated the positive association between HPV and VCE [18,19]. There are many HPV genotypes, and genotypes 16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59 are considered to be a high-risk group [20]. Yong et al. reported associations between HPV type 16 and 18 infection and esophageal squamous cell carcinoma [21], and Vieira et al. have demonstrated HPV type 11 infection in endoscopic biopsy specimens of VCE [22]. Tonna et al. detected HPV type 51 deoxyribonucleic acid (DNA) in endoscopic biopsy specimens of VCE by performing polymerase chain reactions, and they stated that the presence of HPV DNA in the endoscopic biopsies raised the possibility that HPV infection underlies the hyperkeratosis and malignant transformation [19]. Liberale et al. [18] reported a case of HPV-positive VCE with esophagobronchial fistula in a 41-year-old man, initially responded to antiviral treatment.

Cappellesso et al. [20], on the other hand, have reported that HPV infection may not be involved in VCE, but, unlike Vieira et al. and Tonna et al., they tested surgically resected specimens for HPV infection by performing chromogenic hybridization. These different findings might be explained by destruction of HPV DNA in the formalin fixed paraffin embedded (FFPE) tissues of resected specimens, or HPV may have played an initiating role and no longer have been involved once the lesion underwent malignant transformation.

Until recently, no data have been available on the efficacy of the HPV vaccines in preventing HPV infections and its related cancers. However, nowadays, it is well known that vaccination against HPV during childhood and prior to HPV exposure can prevent HPV-associated cervical cancers later in their adult lives. Accordingly, it could be proposed to administer HPV vaccine against VSC including VCE to prevent the acceleration of malignant progression. We should investigate the association between VCE and HPV infection further to understand and successfully treat this disease.


VCE is a rare, well differentiated carcinoma that is slow growing and invades locally. VCE is difficult to diagnose, because histologic examination of mucosal biopsy specimens usually shows only nonspecific inflammatory changes. If VCE is suspected based on the history and clinical findings, we strongly recommend esophagectomy, because distant and lymph node metastasis are relatively rare. HPV may be involved in VCE initiation, and the possible etiological involvement of HPV should be investigated.

Conflicts of Interest

The authors declare that they have no conflicts of interest.


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