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Multiple Onychopapillomas and BAP1 Tumor Predisposition Syndrome | Genetics and Genomics | JAMA Dermatology

Multiple Onychopapillomas and BAP1 Tumor Predisposition Syndrome | Genetics and Genomics | JAMA Dermatology

 



Key Points

Question 
What are the prevalence and histology of nail abnormalities in patients with (BRCA1-associated protein) BAP1 tumor predisposition syndrome (TPDS)?

Findings 
In this cohort study of 47 patients with BAP1 TPDS, a high number of patients had nail changes consistent with onychopapilloma, and among individuals aged 30 years or older, the prevalence of onychopapilloma was even higher. Polydactylous involvement with onychopapillomas was detected in nearly all patients who had nail involvement.

Meaning 
These findings suggest that multiple onychopapillomas may be a novel cutaneous diagnostic sign in adults with BAP1 TPDS.

Importance 
BRCA1-associated protein (BAP1) tumor predisposition syndrome (TPDS) is a cancer genodermatosis associated with high risk of uveal and cutaneous melanoma, basal cell carcinoma, and multiple internal malignant neoplasms, including mesothelioma and renal cell carcinoma. Early detection of the syndrome is important for cancer surveillance and genetic counseling of family members who are at risk.

Objective 
To determine the prevalence of nail abnormalities in individuals with pathogenic germline variants in BAP1.

Design, Setting, and Participants 
In this prospective cohort study, individuals who were known carriers of pathogenic BAP1 germline variants were consecutively enrolled between October 10, 2023, and March 15, 2024. Dermatologic evaluation for nail abnormalities was performed, including a history of nail abnormalities and associated symptoms, physical examination, medical photography, and nail biopsy for histopathology. This was a single-center study conducted at the National Institutes of Health Clinical Center.

Main Outcomes and Measures 
Primary outcomes were the prevalence and spectrum of nail changes and histopathologic characterization.

Results 
Among 47 participants (30 female [63.8%]; mean [SD] age, 46.4 [15.1] years) ranging in age from 13 to 72 years from 35 families, nail abnormalities were detected in 41 patients (87.2%) and included leukonychia, splinter hemorrhage, onychoschizia, and distal nail hyperkeratosis. Clinical findings consistent with onychopapilloma were detected in 39 patients (83.0%), including 35 of 40 individuals aged 30 years or older (87.5%). Nail bed biopsy was performed in 5 patients and was consistent with onychopapilloma. Polydactylous involvement with onychopapillomas was detected in nearly all patients who had nail involvement (38 of 39 patients [97.4%]).

Conclusions and Relevance 
This study found that BAP1 TPDS was associated with a high rate of nail abnormalities consistent with onychopapillomas in adult carriers of the disease. Findings suggest that this novel cutaneous sign may facilitate detection of the syndrome in family members who are at risk and patients with cancers associated with BAP1 given that multiple onychopapillomas are uncommon in the general population and may be a distinct clue to the presence of a pathogenic germline variant in the BAP1 gene.

BRCA1-associated protein (BAP1) tumor predisposition syndrome (TPDS) (OMIM 614327) is an autosomal-dominant syndrome associated with cutaneous and internal malignant neoplasms. BAP1 was identified as a tumor suppressor gene in 2008, and the BAP1 protein acts as a deubiquitinating enzyme that exerts control over many integral cellular processes.1 Carriers of pathogenic variants of the gene are at particularly increased risk of cutaneous melanoma (17%-36%), uveal melanoma (24%), malignant mesothelioma (14%-24%), and kidney cell carcinoma (11%), although other cancers have also been described, including basal cell carcinoma, meningioma, breast cancer, bladder cancer, cholangiocarcinoma, and hepatocellular carcinoma.2,3

Characteristic benign melanocytic tumors were the first physical findings associated with the BAP1 hereditary syndrome discovered in families.4 These melanocytic proliferations are termed BAP1-inactivated melanocytoma (BIM) in the most recent World Health Organization classification of skin tumors, and have been previously referred to as BAPoma, Wiesner nevus, nevoid melanoma–like proliferation, atypical Spitz tumor, melanocytic BAP1-mutated atypical intradermal tumors, and BAP1-inactivated spitzoid tumor.5,6 BIMs are most frequently detected on the head and neck (41%), trunk (33%), or upper limbs (25%) and present as dome-shaped, pink papules resembling common intradermal nevi, although pigmented lesions are also common.7 Histologically, BIMs typically demonstrate a distinct intradermal pattern of epithelioid dermal melanocytes resembling Spitz nevi with loss of BAP1 expression. A second population of smaller nevoid cells is often present.6 BIMs are important markers to identify carriers of germline BAP1 variants but may not be biopsied due to their banal clinical appearance.8 To our knowledge, no other benign cutaneous manifestations have been associated with BAP1 TPDS.

Onychopapilloma is a benign tumor of the nail that presents with longitudinal leukonychia, erythronychia, or splinter hemorrhage, along with nail plate abnormalities, including longitudinal ridging, onycholysis, or V-shaped distal nicking. This nail condition was first described as “localized, distal subungual keratosis with multinucleate cells” by Baran and Perin in 19959 and renamed onychopapilloma by the same authors in 2000.10 The nail abnormality typically extends linearly from the proximal nail matrix to the end of the nail, with a characteristic focal subungual keratotic papule at the hyponychium. There may be 2 bands present on the same digit, but to our knowledge, polydactylous onychopapilloma has not been previously reported in the literature.11 According to a 2022 review,12 approximately 250 patients with onychopapilloma have been described in the literature, primarily from 4 series consisting of 41 to 68 patients and smaller case reports and case series.1315 In this study, we investigated the prevalence of nail findings consistent with polydactylous onychopapillomas in adult patients with BAP1 TPDS.

This cohort study was approved by the National Institutes of Health (NIH) institutional review board. All patients provided informed consent to participate in the trial and for use of clinical images of their nails.

Patients with mesothelioma and their family members with germline pathogenic variants in BAP1 were enrolled at the NIH on a long-term follow-up study to comprehensively characterize the natural and clinical history of malignant neoplasms associated with BAP1 TPDS (ClinicalTrials.gov Identifier: NCT03830229). As part of the study, dermatology screening was performed at baseline and annually for participants aged 2 years and older. After nail changes were detected in several participants, the protocol was amended to prospectively evaluate all subsequent patients for nail changes in a systematic manner, including nail biopsy and medical photography of nail abnormalities.

Patients were evaluated by the Dermatology Consultation Service at the NIH for the presence of fingernail or toenail abnormalities, including longitudinal leukonychia and erythronychia, splinter hemorrhages, nail ridging, subungual hyperkeratosis, nail plate abnormality, or other nail dystrophy. Patients were asked to report any pain or other discomfort associated with their nails and nail fragility or splitting. Clinical photography was performed. For patients who underwent nail unit excision, a wing block technique was used to anesthetize the distal digit. Longitudinal fusiform excision of all (or in the case of broader lesions, a representative portion) of the affected nail plate, nail bed, and distal nail matrix was performed.16 Defects were closed with 4-0 polypropylene sutures or left to granulate. Race and ethnicity were self-reported on a written questionnaire with the following questions: “Mother’s ethnic background/ancestry; Father’s ethnic background/ancestry,” with confirmation and clarification as needed in person at the time of genetic counseling. Race and ethnicity data were reported because nail findings, including nail color changes, may appear differently in different populations.

A total of 47 individuals with BAP1 TPDS (30 female [63.8%] and 17 male [36.2%]; mean [SD] age, 46.4 [15.1] years; median [IQR] age, 47 [33.5-60.0] years; 45 White [95.7%]) from 35 families were prospectively evaluated for nail abnormalities between October 10, 2023, and March 15, 2024. Participant ages ranged from 13 to 72 years. There was 1 pediatric (teenage) patient enrolled (Table).


Prevalence of Nail Abnormalities

Among all patients with BAP1 TPDS, 41 individuals (87.2%) demonstrated 1 or more nail abnormalities of the fingernails or toenails. Nail changes included leukonychia, erythronychia, splinter hemorrhage, distal onycholysis, nail splitting, and onychoschizia. The most characteristic finding was the presence of focal hyperkeratotic spicule at the nail hyponychium underlying a band of longitudinal leukonychia consistent with onychopapilloma. We detected onychopapillomas in 39 participants (83.0%), and it was slightly more common in males (15 males [88.2%]) compared with females (24 females [80.0%]) and in older adults, occurring in 35 of 40 individuals aged 30 years or older (87.5%). Polydactylous nail changes were detected in nearly all patients diagnosed with onychopapilloma (38 of 39 patients [97.4%]) (Figure 1, Figure 2, and Figure 3; eFigures 1-6 in Supplement 1). Nail involvement ranged from a thin band of leukonychia or splinter hemorrhage with very small area of hyponychial hyperkeratosis (eFigures 3 and 6 in Supplement 1) to broad areas involving the entire nail with extensive nail dystrophy (Figure 3B and C). Thumbnails were the most commonly affected digits, with involvement in 36 individuals who had onychopapillomas (92.3%) and 36 participants overall (76.6%). In 1 patient, there was complete destruction of all fingernails, which she attributed to nail damage and paronychia from artificial nails, and this individual was not considered to have onychopapillomas (16 females and 1 male reported a history of use of acrylic, gel, or dip nails) (eFigure 7 in Supplement 1).

There were 5 patients who underwent nail unit biopsy. Optimal histologic results were achieved with longitudinal embedding and examination of the nail plate with attached nail bed epithelium. Histologic findings included epithelial acanthosis and papillomatosis with overlying subungual hyperkeratosis and parakeratosis consistent with onychopapilloma. There were also metaplastic changes in the epithelium, including cellular enlargement with abundant eosinophilic cytoplasm and occasional multinucleated cells. No cytologic atypia was observed (Figure 4). BAP1 immunohistochemistry was performed to evaluate for loss of protein expression in affected skin tissue but failed to show a consistent loss of nuclear staining (as is typically seen in BIM).

In this cohort study, we found a high prevalence of nail abnormalities consistent with onychopapilloma in adult carriers of germline BAP1 pathogenic variants. Early detection of BAP1 TPDS is critical, particularly in individuals at increased risk (eg, first-degree relatives of patients with known BAP1 TPDS), given that carriers of germline BAP1 variants are at increased risk of multiple internal malignant neoplasms and require long-term surveillance.3 Furthermore, because skin cancers associated with BAP1 TPDS (melanoma and basal cell carcinoma) are relatively common in the general adult population, a diagnosis of either skin cancer may not immediately prompt further evaluation for an underlying cancer syndrome. A histologic diagnosis of BIM may facilitate a diagnosis of BAP1 TPDS, but BIMs clinically resemble banal intradermal nevi and may not be biopsied in the absence of suspicion of BAP1 TPDS. By contrast, onychopapillomas are uncommon in the general population and distinct in clinical appearance, particularly when a column of keratotic material is detected at the distal hyponychium. Furthermore, based on the existing literature, we believe the sporadic occurrence of polydactylous nail onychopapilloma to be exceedingly rare.11 Therefore, we believe that when polydactylous onychopapillomas are present, it may be a distinct cutaneous sign of a germline BAP1 variant.

In our study, the detection of longitudinal nail changes (leukonychia, erythronychia, or splinter hemorrhage) and distal nail hyperkeratosis rendered a straightforward clinical diagnosis of onychopapilloma for most patients. However, many patients had subtle abnormalities of 1 or more additional nails (eg, longitudinal leukonychia) that could easily be overlooked without careful examination of the hyponychium for a column of distal hyperkeratosis. Whereas longitudinal erythronychia has been reported more commonly than leukonychia in other series of onychopapilloma in the literature,12,13 we found longitudinal leukonychia to be the predominate feature of onychopapilloma in patients with BAP1 TPDS. Distal nail hyperkeratosis was also very common, but it should be noted that patients frequently removed distal hyponychial hyperkeratosis by filing, clipping, or onychophagia. Therefore, extremely careful nail examination may be required to confirm polydactylous onychopapilloma involvement.

The differential diagnosis for polydactylous leukonychia includes Hailey-Hailey disease and tuberous sclerosis complex. In the former condition, pain associated with intertriginous skin involvement characteristic of Hailey-Hailey disease is typically present.17 Leukonychia, erythronychia, and splinter hemorrhages may also be detected in patients with tuberous sclerosis complex.18 Ungual tumors associated with tuberous sclerosis complex may occur at the subungual distal nail and should be differentiated from focal hyperkeratosis of the hyponychium characteristic of onychopapilloma. Lichen planus commonly affects the nails and may present with polydactylous nail involvement with longitudinal erythronychia and nail dystrophy. In a single-center study of 65 patients with erythronychia who underwent biopsy, 41 individuals (63%) had onychopapilloma, followed by lichenoid inflammation (5 individuals [8%]), glomus tumor (4 individuals [6%]), wart (3 individuals [5%]), and squamous cell carcinoma (SCC) in situ (2 individuals [3%]).14 Importantly, only 4 patients in this study had involvement of multiple nails, 3 of whom were diagnosed with lichen planus and 1 with median canaliform dystrophy of the nail. Evaluation for other sites of common involvement by lichen planus (oral, genital, and skin) and careful inspection of the subungual surface of the free edge of the nail plate for the presence of a focal keratotic mass characteristic of onychopapilloma will facilitate differentiation of lichen planus from onychopapilloma. Detection of small onychopapillomas may be further aided by use of dermatoscopy.13

In 2021, the first case to our knowledge of subungual SCC in the setting of BAP1 TPDS was described.19 In this report, a patient presented with a 5-year history of slowly growing subungual tumor of the left thumb. The other nails were described as normal. The first case of malignant onychopapilloma was also reported in a male aged 58 years described as healthy with no relevant personal or family history.20 This patient presented with typical nail features of onychopapilloma, including longitudinal erythronychia, distal splitting of the nail plate, and subungual hyperkeratosis of the hyponychium. The former report raises the possibility that subungual SCC may occur in the BAP1 TPDS setting, whereas the latter suggests that a nail lesion with typical appearance of onychopapilloma does not obviate all risk of SCC. Importantly, both patients in these cases reported nail pain that led to nail biopsy. In our cohort, nail fragility was a common complaint, but significant pain was not reported by any patients. However, in a published series of 68 patients with isolated onychopapilloma, pain was reported in 41%; 62 patients in this series underwent biopsy, and no SCCs were detected.15 This discrepancy in pain symptoms may be due to patients in the latter study seeking evaluation specifically for a symptomatic nail issue compared with the cross-sectional evaluation of all patients with BAP1 TPDS in our cohort. Alternatively, the biological behavior of onychopapilloma may differ in the BAP1 TPDS setting. Regardless, given that the risk of subungual SCC in the BAP1 TPDS setting is unclear, new or worsening nail pain symptoms or a rapid change in the appearance of the nail should prompt consideration of nail biopsy, even in the presence of long-standing polydactylous nail changes. It should be noted that nail clipping demonstrating subungual hyperkeratosis and papillomatosis has been proposed as an alternative method to diagnose onychopapilloma; however, this diagnostic method does not exclude the possibility of subungual malignant neoplasm.12

Although we did not see consistent loss of BAP1 expression in our nail bed biopsies, biopsy material was available for only 5 individuals, and BAP1 immunohistochemistry should be explored further in additional biopsies in future studies. Loss of BAP1 expression is a useful adjunct to histopathologic diagnosis in melanocytic and nonmelanocytic neoplasms in BAP1 TPDS. Loss of expression has been described in basal cell carcinoma in patients with BAP1 TPDS,21 as well as the subungual SCC in a patient with BAP1 TPDS described previously.19 Loss of BAP1 expression has also been described in a patient with BAP1 TPDS and metastatic SCC presumed to be of primary skin origin.22

There are several limitations to this study, primarily due to the cross-sectional approach. Although nail changes were detected in nearly all adult participants, a precise determination of age of onset of nail changes could not be determined retrospectively by patient recall due to the slowly progressive and typically asymptomatic nature of the nail changes. Indeed, subtle nail involvement may have gone undetected by some patients for several years. In addition, only 1 individual aged younger than 20 years was enrolled. Most patients in the cohort were White, which may be due in part to a common Germanic ancestral origin for BAP1 TPDS kindreds in the US.23 The prevalence and clinical appearance of onychopapilloma may vary in other skin types. Additionally, the natural history of onychopapilloma should be evaluated prospectively to determine if patients with BAP1 TPDS are at increased risk of subungual SCC.

In this cohort study, we discovered a novel, benign nail finding strongly associated with germline BAP1 variants. We found that BAP1-associated onychopapillomas, or onychoBAPillomas, were highly penetrant in adult carriers, suggesting that onychoBAPillomas may serve as a new cutaneous marker to identify individuals at increased risk of the syndrome. Referral for genetic counseling is recommended when this distinct nail finding involves multiple nails. Given the uncertain biologic potential of the nail lesions, clinical photography and periodic observation is prudent to monitor lesions, and patients should be advised to return for reevaluation if a significant change occurs in the nail or nail pain develops.

Accepted for Publication: April 26, 2024.

Published Online: May 17, 2024. doi:10.1001/jamadermatol.2024.1804

Corresponding Author: Edward W. Cowen, MD, MHSc, Dermatology Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, 10 Center Dr, MSC 1908, Bethesda, MD 20892 ([email protected]); Raffit Hassan, MD, Thoracic and Gastrointestinal Malignancies Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bldg 10, 10 Center Dr, Rm. 4E-5330, Bethesda, MD 20892 ([email protected]).

Author Contributions: Drs Cowen and Hassan had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Ms Lebensohn and Ghafoor were co-first authors. Drs Hassan and Cowen were co-senior authors.

Concept and design: Lebensohn, Ghafoor, Hassan.

Acquisition, analysis, or interpretation of data: Lebensohn, Bloomquist, Royer, Castelo-Soccio, Karacki, Hathaway, Maglo, Wagner, Agra, Blakely, Schrump, Hassan, Cowen.

Drafting of the manuscript: Lebensohn, Bloomquist, Maglo, Hassan, Cowen.

Critical review of the manuscript for important intellectual content: Lebensohn, Ghafoor, Royer, Castelo-Soccio, Karacki, Hathaway, Wagner, Agra, Blakely, Schrump, Hassan.

Statistical analysis: Lebensohn, Cowen.

Obtained funding: Hassan.

Administrative, technical, or material support: Bloomquist, Royer, Wagner, Agra, Schrump, Hassan.

Supervision: Ghafoor, Hassan.

Conflict of Interest Disclosures: None reported.

Funding/Support: This work was supported by grant ZIA-BC-010816 from the Intramural Program of the Center for Cancer Research and National Cancer Institute and by the National Institute of Arthritis and Musculoskeletal and Skin Diseases of the National Institutes of Health.

Role of the Funder/Sponsor: The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

Meeting Presentation: This study was presented at the 2024 Society for Investigative Dermatology Annual Meeting; May 17, 2024; Dallas, Texas.

Data Sharing Statement: See Supplement 2.

Additional Contributions: The authors would like to thank participants in the study, including the parent of the pediatric patient for granting permission to use potentially identifying age information, and the National Institutes of Health Medical Photography for providing assistance with clinical images. No compensation specific to or related to this research study was provided to this group for this work.

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