Abstract
Objective
Surgical treatment of venous malformations (VMs) of the hand is challenging. The hand’s small functional units, dense innervation, and terminal vasculature can be easily compromised during invasive interventions like surgery or sclerotherapy, leading to an increased risk of functional impairment, cosmetic consequences, and negative psychological effects.
Methods
We have conducted a retrospective review of all surgically treated patients diagnosed with VMs of the hand between 2000 and 2019 and evaluated their symptoms, diagnostic investigations, complications, and recurrences.
Results
Twenty-nine patients (females, n = 15) with a median age of 9.9 years (range, 0.6-18 years) were included. Eleven patients presented with VMs involving at least one of the fingers. In 16 patients, the palm and/or dorsum of the hand was affected. Two children presented with multifocal lesions. All patients presented with swelling. Preoperative imaging was done in 26 patients and consisted of magnetic resonance imaging in nine patients, ultrasound in eight patients, and both modalities in nine patients. Three patients underwent surgical resection of the lesions without any imaging. Indications for surgery were pain and restriction of function (n = 16), and when lesions were preoperatively evaluated as completely resectable (n = 11). In 17 patients, a complete surgical resection of the VMs was performed, whereas in 12 children, an incomplete resection of VM was deemed due to nerve sheath infiltration. At a median follow-up of 135 months (interquartile range, 136.5 months; range, 36-253 months), recurrence occurred in 11 patients (37.9%) after a median time of 22 months (range, 2-36 months). Eight patients (27.6%) were reoperated because of pain, whereas three patients were treated conservatively. The rate of recurrences did not significantly differ between patients presenting with (n = 7 of 12) or without (n = 4 of 17) local nerve infiltration (P = .119). All surgically treated patients who were diagnosed without preoperative imaging developed a relapse.
Conclusions
VMs in the region of the hand are difficult to treat, and surgery is associated with a high recurrence rate. Accurate diagnostic imaging and meticulous surgery may contribute to improve the outcome of the patients.
Keywords: Vascular anomalies, Venous malformations, Surgical resection
Article Highlights.
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Type of Research: Single-center retrospective cohort study
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Key Findings: Eleven of 29 pediatric patients surgically treated for hand venous malformations developed a recurrence.
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Take Home Message: Presurgical accurate diagnostic imaging and meticulous surgery may improve the outcome.
Venous malformations (VMs) are congenital developmental anomalies of the peripheral vascular system occurring with an incidence of 1 to 2 in 10,000 and represent the most frequent form of vascular malformations.1,2 Their clinical presentation can range from mild forms that do not impact daily activities to major extensions affecting organ functioning and quality of life, depending on the location and extent of the malformation.
Hands play a pivotal role in everyday life due to their capacity to perform fine and precise movements. Although functionality remains beyond doubt fundamental and the primary outcome of importance in hand surgery, it is also recognized that hand aesthetics is an essential factor in determining the effectiveness of surgical intervention in the eyes of the patient, as human hands are an indispensable part of the body that contribute in everyday interactions, communication, and social integration.3
Vascular anomalies of the hand require special attention as they can impair both function and aesthetics of the hand and commonly pose a significant physical and psychological burden on the patient. The therapeutic options available for VMs of the hand include compression bandages, sclerotherapy, and surgical excision.4,5 However, the optimal treatment option has not been clearly defined yet. The treatment of hand VMs is specifically challenging due to the anatomical complexity of the region, the lack of clear indicators that can predict the evolution of the malformation, and the need for a long-term follow-up to evaluate the success of therapy.6
The present study aims to present our experience with the surgical treatment of children and adolescents with VMs of the hand in a cohort of patients treated between 2000 and 2019.
Patients and methods
Following approval by the local ethics committee (EK 32-236 ex 19/20), we retrospectively analyzed the data of all patients aged 0 to 18 years treated for histologically confirmed VMs located on the hand between January 2000 to December 2019. Patients’ medical records were scanned to collect detailed information concerning the onset of symptoms, diagnostic investigations, treatment modalities, complications, and recurrences per each confirmed case.
Patients diagnosed with syndromic VMs and those with malformations extending proximally to the forearm were excluded from our study.
The volume of the malformations was estimated on ultrasound or magnetic resonance imaging (MRI) images using the formula calculating the volume of an ovoid structure (0.524 × length × width × height).7
The indications for surgical intervention were: (1) pain exacerbated during increased use of the hand (eg, writing at school); (2) poor response to or continuous need of painkillers; (3) the presence of a well-defined malformation in which a complete excision could be performed; and (4) the presence of an unclear lesion in which surgery was required for histopathological analysis to clarify the dignity of the lesion.
Surgery was performed by pediatric and plastic surgeons with extensive experience in the field of VMs and hand surgery using tourniquet occlusion of the forearm, magnifying glasses, and microsurgical instruments. The goal of the procedure was the complete excision of the lesion without compromising surrounding tissue such as tendons or nerves.
Clinical success was defined as the absence of clinically significant recurrence after the first surgical procedure. Relapse was defined as the reappearance of pain and/or swelling at the excision site, in which subsequent imaging demonstrated the recurrence of the VM.
Statistical analysis
Statistical analysis was performed using IBM SPSS Statistics, version 22 (IBM Corp, Armonk, NY). Metric data are presented as medians, interquartile range (IQR), and ranges or means and standard deviations depending on normal distribution. Group comparisons were performed with the Mann-Whitney U test. Categorical data are presented as numbers, and percentages and comparisons were made applying the Fisher exact test. P-values of < .05 were considered to be statistically significant.
Results
During the 20-year study period, 29 pediatric patients were treated for an isolated VM of the hand and/or wrist. Fifteen patients (51.7%) were female, and 14 (48.3%) were male. The median age at the first presentation was 9.9 years (IQR, 6.1 years; range, 0.6-18 years). Seventeen children (58.6%) presented at a prepubertal age (n = 9 female; n = 8 male), and the remaining 12 (41.4%) presented after puberty (n = 6 female; n = 6 male).
Localization
Thirteen malformations (44.8%) were located on the right hand, and 16 (55.2%) were reported on the left. In 11 patients (37.9%), the malformation involved at least one of the fingers (n = 1 thumb; n = 4 index; n = 2 middle; n = 1 ring; n = 3 little finger). The dorsal or palmar side of the hand was involved in 16 patients (55.2%). In two patients (6.9%), the VM extended to both the hand and fingers. Further detailed characteristics of all cases are shown in the Table.
Table.
Characteristics of 29 pediatric patients treated for venous malformations (VMs) of the hand
| ID | Age, years | Gender | Side | Area | Aspect | Localization | Diagnostics | Surgical indication | Nerval infiltration | Relapse, months | Treatment of relapse |
|---|---|---|---|---|---|---|---|---|---|---|---|
| 1 | 8.7 | M | Right | Hand | Dorsal | Between MC I and II | MRI | Pa | Yes | ‒ | ‒ |
| 2 | 8.3 | F | Right | Finger | Palmar | Proximal phalanx V | US | Pa | No | ‒ | ‒ |
| 3 | 13.4 | M | Left | Hand | Palmar | Between MC II and IV | US + MRI | Pa | Yes | ‒ | ‒ |
| 4 | 7.8 | F | Right | Hand/finger | Dorsal | Between MC IV and V, finger V | MRI | Pa | Yes | 36 | Sc |
| 5 | 17.1 | F | Left | Hand | Dorsal | Between MC IV and V | MRI | Pa | Yes | 22 | Su |
| 6 | 12.3 | F | Right | Finger | Palmar | Proximal phalanx V | US + MRI | CL | No | ‒ | ‒ |
| 7 | 14.2 | M | Left | Hand | Palmar | Finger II, between FDS and FDP | US + MRI | Pa | Yes | 11 | Co |
| 8 | 14.8 | F | Right | Finger | Palmar | Finger II | MRI | CL | No | ‒ | ‒ |
| 9 | 8.7 | F | Left | Hand | Palmar | Medial palmar area | US + MRI | CL | No | ‒ | ‒ |
| 10 | 13.6 | F | Left | Hand | Palmar | Medial palmar area | MRI | CL | No | ‒ | ‒ |
| 11 | 15.3 | M | Left | Hand | Palmar | Distal wrist | US + MRI | CL | No | ‒ | ‒ |
| 12 | 12.5 | F | Left | Finger | Palmar | Middle phalanx III | US + MRI | CL | No | ‒ | ‒ |
| 13 | 16.9 | M | Left | Finger | Dorsal | Extensor apparatus III | US | Pa | Yes | ‒ | ‒ |
| 14 | 16.4 | M | Right | Hand | Palmar | Between MC III and IV | US + MRI | Pa | No | ‒ | ‒ |
| 15 | 9.3 | F | Left | Hand | Palmar | Flexor tendons IV and V | - | Pa | Yes | 13 | Su |
| 16 | 10.0 | M | Left | Finger | Dorsal | Middle phalanx IV | US | Pa | No | ‒ | ‒ |
| 17 | 11.6 | M | Right | Hand | Palmar | Finger III and IV | MRI | Pa | Yes | 33 | Su |
| 18 | 1.3 | M | Left | Finger | Palmar | Proximal phalanx II | - | Pa | No | 6 | 3x Su |
| 19 | 0.6 | F | Right | Finger | Dorsal | Proximal phalanx II | - | CL | No | 35 | Sc |
| 20 | 6.4 | F | Left | Hand | Palmar | Between MC IV and V | MRI | CL | Yes | 22 | Su |
| 21 | 9.9 | F | Left | Finger | Palmar | Finger II | US + MRI | UM | Yes | ‒ | ‒ |
| 22 | 7.8 | F | Right | Hand | Palmar | Distal wrist | US + MRI | Pa | Yes | 33 | Co |
| 23 | 9.9 | M | Right | Hand | Palmar | Thenar eminence | US | UM | No | 2 | Su |
| 24 | 1.8 | M | Right | Hand | Dorsal | Between MC II and IV | MRI | CL | No | ‒ | ‒ |
| 25 | 13.1 | M | Left | Hand | Palmar | Thenar eminence | US | CL | No | ‒ | ‒ |
| 26 | 5.8 | M | Right | Hand | Dorsal | Between MC I and II | US | Pa | No | ‒ | ‒ |
| 27 | 18.0 | F | Left | Finger | Palmar | Proximal phalanx I | MRI | Pa | Yes | ‒ | ‒ |
| 28 | 9.5 | F | Left | Hand/finger | Palmar | Distal wrist and finger III | US | Pa | No | ‒ | ‒ |
| 29 | 4.2 | M | Right | Finger | Dorsal | Finger V | US | CL | No | 36 | Su |
CL, Circumscribed lesion; Co, conservative; F, female; M, male; MC, metacarpal; MRI, magnetic resonance imaging; Pa, pain; Sc, sclerotherapy; Su, surgery; US, ultrasound; UM, unclear mass.
Presentation
All 29 patients presented with local swelling, accompanied by bluish discoloration of the skin in only 17 of them (58.6%). In 16 cases (55.2%), the onset of pain was reported to occur before the first consultation. The triad of swelling, discoloration, and pain was present from the beginning in 11 patients (37.9%). None of the patients had deficits concerning the range of motion and cutaneous sensation at the time of the first presentation.
Diagnostics
Preoperative imaging consisted of MR angiography with T1- and T2-weighted sequences in nine (31%), ultrasound in eight (27.6%), and both in further nine (31%) patients. In five patients (17.2%), an X ray investigation was performed to rule out osseous abnormalities, which had shown phleboliths in two cases, suggesting a VM. Three children (10.3%) underwent no preoperative imaging, because the sole clinical investigation was judged enough for surgery; all three patients had localized lesions, which enlarged suddenly, and two of them had a strong pain.
In all malformations investigated by sonography (n = 17), it was possible to estimate the volume of the lesion (median, 0.89 mL; IQR, 1.61 mL; range, 0.20-2.95 mL). In 13 of the 18 patients undergoing MRI, the median lesions’ volume was 2.27 mL (IQR, 6.55 mL; range, 0.1-82.8 mL). In two cases, MRI revealed intraosseous infiltration, and both patients had a recurrence. The results of the ultrasound in eight patients, who received an ultrasound examination only, revealed a well circumscribed mass with no benefit expected from an additional MRI study.
Laboratory examinations of coagulation were performed in 18 patients (62.1%) and were evaluated as normal in all cases.
Treatment
Pain was the leading cause for surgery in more than one-half of the patients (n = 16; 55.2%). In view of their progressive behavior, the removal of circumscribed lesion was indicated in 11 patients. In the remaining two children, surgical removal was performed due to the uncertain nature of the mass. Both of these children had undergone preoperative imaging (ultrasound in one and ultrasound and MRI in the other patient). The median time between the initial presentation and surgical intervention was 3 months (IQR, 4.5 months; range, 0-21 months).
In 17 patients, the surgical reports describe that the VMs could be completely removed macroscopically (Fig 1). However, in 12 cases, an infiltration of the nerve sheath by anomalous venous tissue was reported, and even though the VMs were removed from the nerve sheath, complete resection could not be performed.
Fig 1.
Surgical resection of a localized venous malformation (VM) of the right hand in a 16-year-old boy (Patient 14). Image of the surgical approach to the VM (A) and of the operative field after excision of the VM (B), showing the sixth and seventh finger nerves without infiltration. (C) Clinical image at 1 month after surgery.
Postoperative complications included partial functional impairment due to scarring in three patients, and one limited abduction of the second and third finger following complete removal of the proximal metacarpal muscles due to their massive infiltration by the VM (Fig 2).
Fig 2.
Surgical resection of a localized venous malformation (VM) of the left hand in a 13-year-old boy (Patient 3). (A) Clinical image of the swelling in the left palmar region between the second and fourth metacarpal bones. (B) T2-weighted magnetic resonance imaging (MRI) image of the VM of the left hand. (C) Image of the surgical approach to the VM. (D) Image after complete surgical resection of the VM, showing dissected tendons and neurovascular structures. (E) Clinical image at 6-month follow-up after surgery; no relapse was noted.
Recurrences
At a median follow-up time of 135 months (IQR, 136.5 months; range, 36-253 months) clinical success was achieved in 18 children (62.1%). Recurrence of the malformation, however, occurred in 11 patients (37.9%) after a median time of 22 months (IQR, 24 months; range, 2-36 months). Recurrence in these cases was confirmed by MRI in eight patients and by ultrasound in three others. The mean age of the patients with recurrences did not significantly differ from the patients without recurrences (mean age, 8.2 ± 5.1 years vs 11.5 ± 4.2 years; P = .055).
Two patients with recurrences were asymptomatic 11 and 33 months after the first surgical intervention (Fig 3). Therefore, no further invasive treatment was considered necessary. These two patients did not develop any symptoms for the next 3 and 6 years, respectively.
Fig 3.
Surgical resection of a localized venous malformation (VM) of the left hand in a 14-year-old boy (Patient 7). (A) Clinical image of the swelling in the left palm. (B) Preoperative T2-weighted magnetic resonance imaging (MRI) images of the VM. (C) Clinical image at 3 months after surgery. (D) Surgical image showing the infiltration of the second and third finger nerves by the VM. (E) T2-weighted MRI images showing a relapse of the VM 11 months after surgery.
One patient presented with a relapse 3 years after the initial intervention. In this case, the VM extended into the fourth metacarpal space and was treated by sclerotherapy with polidocanol. Unfortunately, the same patient presented with a second painless lesion 4 years after the procedure. Therefore, the patient was proposed to undergo sclerotherapy again, but the patient’s definitive decision has not been received yet.
Seven patients underwent a re-excision of the malformation due to the pain not responding to conservative treatment, which consisted of individualized compression bandages and painkillers. Sclerotherapy was considered only when surgery was deemed non-radical. The procedure led to remission of symptoms with an uneventful median follow-up time of 159.2 months (IQR, 72 months; range, 116.2-211 months) in six patients. One patient required three subsequent excisions 1, 2, and 4 years following the initial intervention.
We did not observe any statistical differences of the incidence of recurrence based on gender (P = .558) and the pubertal stage (P = .230) at the onset of the malformation, even considering only female patients (P = .455).
The rate of recurrences did not significantly differ between patients presenting with (n = 7 of 12) or without (n = 4 of 17) local nerve infiltration (P = .119). All three patients who underwent surgical excision without preoperative imaging developed a relapse (Table).
Discussion
Our study presents our experience managing children and adolescents affected by VMs of the hand. We demonstrate that surgery is an effective option for patients with VMs of the hand. However, recurrences occurred in more than one-third of our study patients. We also show that these patients require meticulous preoperative imaging because surgical intervention after a simple clinical examination led in our hands to a 100% recurrence rate.
VMs are congenital anomalies that are classified on the basis of the involved vascular type (capillary, venous, arteriovenous, lymphatic) and rheologic characteristics (high-flow, low-flow). VMs represent the most frequent isolated low-flow malformation, with a prevalence of 1% of the general population.8,9 In 92% of the cases, they occur sporadically, and their etiology still remains unclear. However, a somatic mutation of TIE-2, a tyrosine-kinase receptor playing a crucial role in angiogenesis and cardiovascular development, can be found in up to one-half of the affected patients.10,11 High-flow malformations may also be present in the hand, but they are extremely rare and have a peculiar clinical course. In the present study, we have chosen to analyze only VMs to have a sample as homogeneous as possible.12
VMs histologically consist of normal endothelial cells surrounded by a poor and disarranged mural smooth muscle layer covering enlarged and tortuous venous channels.13 They can be located in any part of the body and can potentially infiltrate neighboring structures and tissues.5,13 Historically, this type of VM were classified as ‘extratruncular forms’ in the Hamburg classification, originating from a developmental arrest in the reticular stage of the embryonic vascular development. As they consist of embryonic mesodermal remnants, they could potentially proliferate and manifest as infiltrating lesions.14 This rationale allows potential treatment with an mTor inhibitor like rapamycin, which can suppress vascular proliferation.15
VMs are already present at birth and grow proportionally to the patient. They usually remain asymptomatic until the first thrombotic episode, significant compression of neighboring structures, or pain triggered by bleeding.13 These events are favored by dilation of the malformed veins due to the exhaustion of the weak malformed vascular wall typically occurring around puberty, in addition to the phenomenon of localized intravascular coagulation that characterizes VMs.16,17 In our series, we did not observe any correlation between the onset of pain and pubertal development. Given the predictable evolution of these lesions in young patients, with progressive swelling and pain, and although there are no clear guidelines in the literature describing the optimal timing of treatment for asymptomatic VM, we decided to remove asymptomatic but circumscribed lesions.18 In addition to these general hallmarks, VMs of the hand need special consideration. They can involve the skin and subcutaneous tissue, infiltrate muscles, nerves, bones, and tendons and cause symptoms often exacerbated by continuous fine movements, sometimes inducing functional impairment. In our series, all except two patients who showed macroscopic nerve involvement at surgery presented with pain that could not be controlled with painkillers.
Once VMs become evident, imaging is required to characterize the type of vessels involved and plan the treatment carefully. Because of its accessibility, ultrasound is considered the first diagnostic tool. It usually shows a hypoechoic and compressible lesion and, if combined with doppler, provides information about vascularization and feeding vessels and helps distinguish VMs from high-flow malformations. The differentiation between venous and lymphatic vessels is more challenging.13 If the VM is not circumscribed and clearly of a localized character, further imaging by MRI is needed, allowing flow characterization by angiography sequences and precise definition of involved structures by T1 and T2 weighted sequences and fat saturation.19,20 The importance of preoperative MRI for planning of treatment in these patients is best illustrated by the three cases in our series who did not receive any preoperative imaging, and the indication for surgical intervention was based on sole clinical judgement, presuming a superficial lesion. They all experienced a recurrence. In our series, radiography was performed only in cases with unclear history and suspected trauma or to exclude osseous deformities. Its diagnostic potential if pathognomonic phleboliths are visualized13 was reported in two patients in our series.
Overall, surgical resection is considered a viable option if the malformation is small and circumscribed because severe complications are not expected.21 Nevertheless, a meticulous surgical planning, as described by Upton et al, is mandatory.22 Three of our patients did not have any presurgical imaging evaluation, and all developed a recurrence. In the subsequent diagnostic images, the malformation was more extensive than initially hypothesized, confirming that clinical judgment alone underestimates the actual extent of the malformation in 76% of the cases.23
Traditionally, compression bandages, percutaneous sclerotherapy, and surgery are cornerstones of the treatment of VMs. Wearing compression garments on affected extremities avoids structural failure of the venous wall, facilitates venous drainage, provides symptomatic relief, and prevents thrombophlebitis and ulceration.5 However, in children, their effectiveness is often limited by poor compliance. Moreover, growing children need adjustment of the garment at least twice per year.24
Sclerotherapy is usually considered for extensive lesions or as a preoperative tool to facilitate surgical excision.9 By definition, it cannot be curative, consisting only in damaging the walls of malformed veins with their subsequent collapse.25 Good efficacy in controlling symptoms and progression of the malformation has been reported with several sclerosing agents such as tetradecyl sulfate, ethanol, or bleomycin. Regardless of the substance, sclerosant agents injected near nerves or fine muscles can cause damage to these structures. Even in experienced hands, a complication rate of up to 12%, including skin necrosis, transient or permanent neurological damage, muscle or fascial fibrosis, and renal failure, is reported.9 Furthermore, the terminal circulation of fingers implies the risk of damaging the digital arterial supply by extravasation of the sclerosing agent causing necrosis. In our center, we treated a patient in the past requiring a partial finger amputation after sclerotherapy, and we do not routinely use sclerotherapy as the first option for VMs in the area of the fingers. However, we use primary sclerotherapy in patients with larger VMs also in the hand region. In the present study, sclerotherapy was used in two patients after recurrence of the VM, and repeated imaging showed no possibility for complete surgical resection.
VMs are defined as localized if they involve a single anatomical district and diffuse if they spread in more than one body tissue. However, this feature does not reflect the possibility of complete resection of the lesion. An important parameter that needs to be considered is the infiltration of neighboring structures. It may be possible, for example, to define a VM localized in a finger, but complete resection may still not be possible due to the infiltration of skin, bone, tendons, muscles, and nerves. In our cohort, up to 30% of patients presented with infiltration of neighboring nerve tissue. Although incomplete resection is reported as a predisposing factor to recurrence,16 no difference in recurrence was observed in our patients. In case of VM, preoperative determination of osseous infiltration influences the recurrence rate because complete resection is not possible unless destructive surgery is performed. Both of our patients with osseous infiltration had a recurrence.
Surgery needs to be performed with a tourniquet and magnification, which allows accurate dissection of vessels, isolation, preservation of noble structures, and precise hemostasis.25 The importance of assessing the preoperative coagulation profile to exclude an underlying coagulopathy is often underlined.26 About one-half of our patients were screened preoperatively. However, all cases were negative, and we did not record any intra- or postoperative bleeding-related complications.
In conclusion, surgery in the case of an isolated and well-defined VM of the hand is a good option if preceded by MR angiography as accurate diagnostic imaging, and meticulous surgical planning. However, due to the potential infiltrative nature of these lesions and the difficulty to assess nerval infiltration by imaging, surgery is still associated with a relatively high recurrence rate. To the best of our knowledge, this is the most extensive series of pediatric patients with hand VMs presented in the current literature.
Author Contributions
Conception and design: PG, EH, GS
Analysis and interpretation: PG, BB, HT
Data collection: CF, BS, SS, CA
Writing the article: PG, BB, EH, GS
Critical revision of the article: PG, CF, BB, BS, SS, CAH, HT, EH, GS
Final approval of the article: PG, CF, BB, BS, SS, CAH, HT, EH, GS
Statistical analysis: PG, GS
Obtained funding: Not applicable
Overall responsibility: EH
Footnotes
Author conflict of interest: none.
The editors and reviewers of this article have no relevant financial relationships to disclose per the Journal policy that requires reviewers to decline review of any manuscript for which they may have a conflict of interest.
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