A, En bloc wide excision deep to the periosteum. B, The excisional defect produced is covered by a full-thickness skin graft.
A, Clinical aspect of a subungual squamous cell carcinoma (SCC) localized on the right hallux in one patient. B, Clinical result of the wide surgical excision after 1 year. C, Initial aspect of primary carcinoma in one patient. D, Clinical appearance of the recurrence 8 months after the wide surgical excision.
Each circle represents a patient (n = 55); the left thumb was the most commonly involved digit, followed by the right thumb and the right hallux.
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Topin-Ruiz S, Surinach C, Dalle S, Duru G, Balme B, Thomas L. Surgical Treatment of Subungual Squamous Cell Carcinoma by Wide Excision of the Nail Unit and Skin Graft Reconstruction: An Evaluation of Treatment Efficiency and Outcomes. JAMA Dermatol. 2017;153(5):442–448. doi:10.1001/jamadermatol.2017.0014
What is the outcome of subungual squamous cell carcinoma treated with wide surgical excision of the nail unit?
In this cohort study of 55 patients with subungual squamous cell carcinoma treated with wide surgical excision of the nail unit followed by full-thickness skin graft reconstruction with 5 years of follow-up, the rate of recurrence is low (4%) and patient satisfaction is very high, with a low number of important early and delayed complications.
Total nail unit excision followed by a full-thickness skin graft is a safe, functionally efficient, and cosmetically acceptable treatment for subungual squamous cell carcinoma.
The best surgical treatment modalities for subungual squamous cell carcinoma (SUSCC) without bone invasion need to be determined. The limited available data on Mohs micrographic surgery do not demonstrate its use as a standard procedure. A previous study in a limited series of patients has shown that wide surgical excision of the nail unit was associated with a low rate of recurrence.
To confirm the efficiency of wide surgical excision of the nail unit with full-thickness skin graft reconstruction on a series of patients with SUSCC with an extended follow-up and to evaluate short- and long-term postoperative morbidity and patient satisfaction.
Design, Setting, and Participants
A consecutive series of 55 patients with biopsy-proven SUSCC without bone invasion treated by wide surgical excision of the nail unit followed by full-thickness skin graft reconstruction from January 1, 2000, to August 31, 2012 were included. After a minimum follow-up of 5 years, the recurrences were collected from the referring physicians. Statistical analysis was conducted from January 1 to June 30, 2016.
Main Outcomes and Measures
Demographic data, pathologic characteristics of tumors, postoperative follow-up, and recurrences were collected from medical records. Patients’ satisfaction with surgery, quality of life, and delayed postoperative morbidity (functional outcome and sensory disorders) were assessed from a questionnaire mailed to patients and physicians.
Among the 55 patients (23 women and 32 men; mean age, 64 years), the mean follow-up was 6.6 years (range, 5.0-11.2 years), with a minimum follow-up of 5 years. Fifty-two questionnaires (95%) were returned. Two recurrences were observed. Minor early postoperative complications, such as graft infection and delayed wound healing, were seen in 6 patients; 8 patients experienced severe pain. Late postoperative complications included hypersensitivity to mechanical shocks (39 of 51 patients [76%]), mildly increased sensitivity to cold (38 of 51 patients [75%]), loss of fine touch sensation (17 of 35 patients [49%]), and epidermal inclusion cysts (9 of 51 patients [18%]). Most patients were very satisfied with cosmetic and global outcomes of the surgery.
Conclusions and Relevance
Total excision of the nail unit followed by a full-thickness skin graft is a safe and efficient treatment for SUSCC without bone involvement, with satisfying cosmetic and functional outcomes.
Subungual squamous cell carcinoma (SUSCC) is the most common cancer of the nail unit. Oncogenic human papilloma virus1-3 and exposure to iradiation4,5 or chemicals6 may play a role in the development of this condition. A history of trauma to the nail is common in patients with SUSCC, yet it may not be associated with the cancer.
Subungual squamous cell carcinoma is found predominantly in men aged 50 to 69 years7,8 and affects mainly the thumb and index fingers. It may present with minimal changes to the nail such as erythronychia, or mimic benign yet monodactylic nail conditions such as onychomycosis,9,10 chronic paronychia,11,12 or viral wart.13,14 Diagnosis is often delayed in patients with SUSCC. However, patients with SUSCC have an excellent prognosis after tumor excision when bone is not involved. Untreated SUSCC shows slow and locally invasive growth. Bone invasion is observed in about 20% of cases of SUSCC.4,7 Metastasic spread and death are extremely rare.3,7,15 Little is known about the prognosis factors of SUSCC at early stages, but depth of invasion7 and histopathologic signs of human papilloma virus infection3 might indicate an unfavorable prognosis.
There is currently no standard therapeutic approach for SUSCC. Radiographic evidence of bone infiltration requires partial amputation of the digit. In other cases, conservative surgical treatment should be performed to optimize quality of life. Mohs micrographic surgery (MMS) has been advocated in short series16-19 as the best therapeutic option for SUSCC, because it has a high rate of cure and spares tissue. However, performing MMS on the the nail unit is time consuming and is a challenging location for this procedure, requiring trained surgeons and pathologists.20,21 Moreover, a tissue-sparing procedure such as MMS does not always offer the same functional and aesthetical advantage on the nail unit. Wide surgical excision (WSE) of the nail unit followed with full-thickness skin graft is an interesting alternative to MMS in patients with SUSCC. However, to our knowledge, the literature does not have information about the efficiency and tolerance of the postoperative results. In a previous study performed at Université Claude Bernard Lyon 1 and Centre Hospitalier Lyon Sud, Dalle et al7 compared 2 different standard surgical procedures in a small series of 29 patients and showed that WSE of the nail unit had a lower rate of recurrence (1 recurrence of 20 patients [5%]), whereas partial surgical excision of the nail unit led to a significantly higher number of recurrences (5 recurrences of 9 patients [56%]). These results led us to treat all subsequent patients with WSE of the nail unit.
The aim of our study was to confirm the efficiency of WSE of the nail unit with full-thickness skin graft reconstruction in a series of patients with SUSCC with extended follow-up and to document immediate and delayed postoperative morbidity as well as patients’ satisfaction about cosmetic and functional results.
All cases of biopsy-proven SUSCC treated by WSE of the nail unit followed with full-thickness skin graft from January 1, 2000, to August 31, 2012, at Université Claude Bernard Lyon 1 and Centre Hospitalier Lyon Sud were included. None of these patients presented with radiographic evidence of bone involvement on results of radiograph, computed tomographic scan, or magnetic resonance imaging. Medical records were reviewed for demographic data, clinical and pathologic information, immediate and delayed postoperative events, and outcome. Information about recurrence, immediate postoperative morbidity (delayed healing, infection, major bleeding, or intense pain [visual analog scale score >7] that required consultation or an increase in analgesia), delayed postoperative morbidity (hypersensitivity to cold or trauma, complications requiring a reintervention, functional disability [stiffness, need for physiotherapy, balance or walking disorder after toe surgery, or difficulty in precision grip or in wearing shoes]), aesthetic discomfort, and overall satisfaction after surgery were also evaluated using questionnaires that were mailed to patients, their dermatologist, and general physician. The questionnaire sent to patients focused on the functional complications and the assessment of quality of life, whereas the questionnaire sent to practitioners was centered on the postoperative complications and the recurrences. A reminder letter was sent to patients who did not respond after 1 month. Remaining nonrespondents (n = 2) were contacted by telephone.
This strictly observational retrospective study with no expected or potential individual benefit for patients and investigators was not under the scope of relevant French law (Huriet-Serusclat; No. 88-1138) and therefore did not require ethical committee approval. All patients provided verbal informed consent for the surgical procedure and written informed consent for the research use of their medical records.
Surgery was routinely performed by a single dermatologist at our institution (L.T.)22 and was performed under nerve block of the toe or finger, with a tourniquet on the digit or toe. The surgical treatment consisted of an en bloc wide excision of the nail unit including the 2 lateral nail folds, the proximal nail fold, and the hyponychium of the finger or toe (Figure 1 and Figure 2). A proximal transverse incision was made at the base of the distal phalanx, from 3 to 5 mm beyond the interphalangeal joint depending on the fingers or toes affected, superficial enough to prevent a distal extensor tendon injury. This incision was prolonged laterally and distally to the hyponychium at the tip, down to the bone, with an extra margin ranging from 2 to 5 mm beyond these structures. Distal to proximal sharp dissection of the nail bed was then performed, directly down to the periostium, to ensure an adequate depth of excision. The matricial horns were then completely destructed using monopolar electrocautery. A full-thickness skin graft was harvested from the internal aspect of the nondominant arm and inset over the wound with 4.0 nonabsorbable nylon sutures. After surgery, a petrolatum gauze bolster with mupirocin 2% ointment was applied and held in place with 3.0 nonabsorbable nylon sutures. The mean time for the total procedure was 45 minutes. Patients were seen once for removal of the gauze bolster after 7 days, then for suture removal after 3 weeks.
Statistical analysis was conducted from January 1 to June 30, 2016. All discrete variables were reported as numbers and percentages, and continuous variables were reported as medians and means. We did not use standard validated quality-of-life scales for this study because no scale was specific enough for surgery of a digit or toe and because we shortened the questionnaire with a goal of a high number of returned questionnaires. We considered visual analog scales a good alternative to validated quality-of-life scales.
Fifty-five consecutive patients (32 men [58%] and 23 women [42%]) were included (Table 1). The mean age at diagnosis was 64 years (range, 35-90 years). The left thumb was the most commonly involved digit (12 [22%]), followed by the right thumb (11 [20%]) and the right hallux (8 [15%]) (Figure 3). The mean diagnostic delay was 34 months (range, 2-182 months). Seven patients had received treatment before the surgical procedure: 1 patient (2%) had previously been treated with dynamic phototherapy and 6 (11%) had been treated with partial surgical excision of the nail unit.
Preoperative pathologic examination showed in situ SUSCC in 6 patients (11%) and invasive SUSCC in the other 49 (89%). The depth of invasion, as defined by the distance from the upper layer of the living epithelium to the deepest carcinoma cell, ranged from 0.35 to 4 mm (mean, 1.1 mm). Most cases of SUSCC involved both the nail bed and matrix (35 [64%]). Pathologic features of viral infection (ie, koilocytes and eosinophilic inclusions) were observed in 6 cases of SUSCC (11%). Results of pathologic examination showed negative margins in all 55 surgical resection specimens.
The median follow-up was 6.6 years, and all patients had a minimum 5-year follow-up. Two recurrences were observed (4%). These 2 local recurrences both occurred after short follow-up periods of 7 and 8 months, respectively, with time before diagnosis of 12 and 6 months, respectively. Both recurrent cases of SUSCC were invasive, measuring 0.6 and 1.5 mm, respectively, and well differentiated, with no features of human papilloma virus infection. Resection margins were described as negative at pathologic examination of primary carcinoma for both, yet shorter than 1 mm at the site of recurrence. Surgical excision of the recurrence was subsequently performed for both patients. The first patient showed no further recurrence at the end point date (June 30, 2016; 6.25 years of disease-free survival after recurrence). The second patient developed another local recurrence 5 months after the resection of the first recurrence, and the patient underwent distal amputation of the digit. No further relapse was observed (2.33 years of disease-free survival after the second recurrence).
No regional or distant metastases or disease-related death was reported for the 55 patients. Five patients, however, died of unrelated causes.
Immediate postoperative complications were defined as all events that occurred within a 3-month period following the procedure. Of the 55 patients, 6 showed immediate postoperative complications, including 1 with a graft infection and 5 with delayed wound healing (defined as a healing period longer than 1 month) (Table 2). Eight patients (15%) reported severe pain days after surgery with no predilection for any digit. No abnormal bleeding was recorded during the immediate postoperative period, and no complications were reported at the skin graft donor sites.
Information on delayed postoperative outcomes was obtained from medical records and from questionnaires returned by 52 patients and physicians (95%).
Epidermal inclusion cysts were observed in 9 patients (18%) and appeared as asymptomatic or painless swelling underneath or beside the skin graft. They occurred after a mean period of 17 months. Almost all inclusion cysts (8 [89%]) developed within a 3-year period after surgery. When considering distribution of inclusion cysts over time, no decreasing trend in the incidence of this complication could be observed, taking into account that approximately 1 WSE was performed per month.
Nail spicules were observed in 7 patients (14%). Epidermal inclusion cysts and spicules were both treated with surgical excision, and patients were referred for pathologic examination to rule out local recurrence.
For fingernail surgery, most common disruptions in daily life activities 1 year after surgery were difficulty in gripping objects (17 of 35 patients [49%]) and loss of motion of the interphalangeal joint (10 of 51 patients [20%]). Difficulty in gripping objects was correlated with partial loss of fine touch sensation and was limited to sharp or small objects. This sensitivity disorder persisted for 6 months in 11 patients. For joint stiffness, 9 patients required physiotherapy; however, stiffness continued for 6 months in 5 patients.
Only 1 patient reported difficulty with handwriting and 2 reported minor balance or walking disorder after toenail surgery. Eleven of 16 patients (55%) described mild discomfort in wearing tight shoes.
Mild sensitivity to cold was reported by 38 patients (75%). It was felt as digit numbness and stiffness, with no pain, relieved within a few minutes. Wearing gloves when exposed to cold prevented the sensitivity and did not affect activities. Not even slight contact hypersesthesia was reported by the patients; however, 39 patients (76%) reported increased sensitivity to mechanical shocks.
Most patients were satisfied with the cosmetic outcome after surgery, and only 1 patient reported significant aesthetic discomfort. Almost all patients (50 [98%]) reported no effect or a mild effect of WSE on their quality of life. Forty-seven patients (92%) were very satisfied (visual analog scale score, ≥8 of 10) with the global outcomes of surgery. This level of satisfaction increased (50 [98%]) when patients were informed that distal amputation of digit could have been an alternative treatment.
Our findings, on a series of 55 patients with a minimum follow-up of 5 years and a median follow-up of 6.6 years, confirm that WSE of the nail unit for SUSCC provides a high rate of cure. Two local recurrences were observed, representing a recurrence rate of 4%. Patients also reported a good level of satisfaction and an absence of significant impairment of quality of life.
The two largest series of patients with SUSCC treated with MMS, published by Mikhail16 (n = 24) and Goldminz and Bennett17 (n = 25), both demonstrated a recurrence rate of 8%, evaluated after a 3-year minimum follow-up and a median 5-year follow-up, respectively. Two further reports on smaller series of 15 and 8 patients with SUSCC treated with MMS18,19 showed no recurrence during mean follow-up periods of 3 years and 3.1 years. In contrast, Young et al20 reported a high recurrence rate of 22% after MMS in 13 patients’ SUSCC after a mean follow-up period of 51.5 months (range, 2-125 months). Two of their recurrent cases showed positive margins, whereas the tumors had been considered as cleared during surgery. This study illustrates the difficult challenge of MMS on the nail unit. Moreover, the tissue-sparing effect of MMS cannot be considered as relevant functionally and cosmetically on the nail unit as on other skin locations. In the literature, tumors most commonly recur 3 years after surgery.7,16,17,20 However, they may be observed for a prolonged period of up to 10 years.17 In most patients, management of local recurrences simply includes limited resection of the lesion. In exceptional circumstances when widespread, rapidly growing, or repetitive tumor recurrences occur, as in one of our patients, amputation might be required.
To our knowledge, our series is the only one with minimum follow-up of 5 years. Only 1 MMS series has a median, but not minimum, follow-up of 5 years, and all others cannot be compared either for the duration of the follow-up or for the number of patients included. Moreover, our study is the only one assessing patients’ long-term tolerance of surgery. Compared with previously published series of MMS, our study confirms the equivalent efficiency of WSE in the treatment of SUSCC.
This report also confirms positive outcomes and patient satisfaction associated with WSE of the nail unit. Full-thickness skin grafting allows a short healing time (<1 month) and appears to be a safe method with few immediate postoperative complications.
Delayed surgical complications, including epidermal inclusion cysts and nail spicule regrowth, occurred in 18% and 14% of patients, respectively, treated with WSE of the nail unit. Such events are not considered major complications. They should systematically be treated surgically to exclude recurrence. Incidences of epidermal inclusion cysts after WSE of the nail unit followed by full-thickness skin graft varies in the literature,23-25 from 0%23 to 38%.25 This is a common complication of skin surgery, particularly after skin grafts. It arises from implantation of epidermal cells into the dermis or foreign body reactions around debris. In our study, inclusion cysts mostly developed within the 3 first years. Whether it might be correlated with surgeon experience remains difficult to assess. The incidence of nail spicule regrowth is commonly low in the literature, ranging from 0%23,25 to 11%,24 as also observed in our study. This complication is mostly determined by surgeon’s experience and can be avoided by thorough destruction of matricial horns.
Hypersensitivity to cold was reported by 75% of our patients. It was not associated with pain and did not affect activities of daily living. This is a common adverse effect after digit surgery and fingertip injuries, occurring in up to 100% of patients.26,27 Its incidence has not been documented in studies of MMS for SUSCC. Hypersensitivity to cold has been shown to be associated with a reduction of blood flow to the extremity, but the underlying mechanism remains unclear. Some authors have suggested a neuronal malfunction,26 while others believe it is caused by a vascular disturbance (possible vasospasm).27 Whether hypersensitivity to cold decreases with time is controversial.27 In our study, this symptom did not seem to improve over time. Regarding functional hand impairment 1 year after WSE of the nail unit, the main issue was difficulty in gripping very small objects, correlated with loss of fine touch sensation. This symptom is very common after any type of digit surgery. Although the fingers that underwent WSE were more vulnerable to mechanical shocks owing to the missing protective nail plate, no hypersensitivity to slight touch was reported.
None of the complications previously mentioned had a significant effect on patients’ quality of life. Only 1 patient reported a severe decrease in quality of life. Regarding cosmetic outcomes, wide nail unit excision followed by full-thickness skin graft reconstruction provides excellent results.23-25 Overall patient satisfaction following surgery was excellent, especially when considering that the alternative treatment was amputation. The functional consequences of WSE are minimal compared with those of amputation of a finger or toe because the thumb-index clamp, the strength of grip, and/or toe-mediated balance is preserved.
The main limitation of our study is that data on satisfaction and long-term complications, including recurrences, are collected from questionnaires sent to patients and physicians. We chose a closed questionnaire to avoid getting too much data and insignificant data; however, we cannot exclude a misclassification bias since evaluation was made by the patient or his or her physician and not by an independent observer.
On the basis of our experience, we propose that WSE of the nail unit with a full-thickness skin graft reconstruction could be performed for SUSCC in the absence of bone involvement since it is associated with a high rate of cure, a low risk of major complications, and a high level of patient satisfaction as well as little impairment of function and quality of life. Careful pathologic examination of the surgical margins is mandatory. Follow-up modalities of patients after surgical treatment of SUSCC should be better defined. On the basis of our experience and literature review and since most recurrences occur during the first 3 years, we suggest follow-up twice a year during the first year, then yearly for the following 2 years.
Accepted for Publication: January 3, 2017.
Corresponding Author: Luc Thomas, MD, PhD, Department of Dermatology, Centre Hospitalier Lyon Sud, 69495 Pierre-Bénite CEDEX, France (email@example.com).
Published Online: April 5, 2017. doi:10.1001/jamadermatol.2017.0014
Author Contributions: Drs Topin-Ruiz and Thomas had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Drs Topin-Ruiz and Surinach contributed equally to this work.
Study concept and design: Topin-Ruiz, Surinach, Dalle, Duru, Thomas.
Acquisition, analysis, or interpretation of data: All authors.
Drafting of the manuscript: Topin-Ruiz, Surinach, Duru, Thomas.
Critical revision of the manuscript for important intellectual content: Topin-Ruiz, Dalle, Balme, Thomas.
Statistical analysis: Topin-Ruiz, Surinach, Duru.
Obtained funding: Thomas.
Administrative, technical, or material support: Topin-Ruiz, Surinach, Balme, Thomas.
Study supervision: Surinach, Thomas.
Conflict of Interest Disclosures: None reported.
Funding/Support: This study was supported in part by grants from Université Claude Bernard Lyon 1, the Hospices Civils de Lyon, and the Ligue contre le cancer du Rhône.
Role of the Funder/Sponsor: The funding sources had no role in the design and conduct of the study; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.
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