Quality of Life and Surgical Outcomes After Soft-Tissue Reconstruction of Complex Oncologic Defects of the Spine and Sacrum

Dolan, Roisin T. MD, MRCSI1,a; Butler, Joseph S. PhD, FRCS(Tr&Orth)2; Wilson-MacDonald, James FRCS(Tr&Orth)2; Reynolds, Jeremy FRCS(Tr&Orth)2; Cogswell, Lucy FRCS(Plast)1; Critchley, Paul FRCS(Plast)1; Giele, Henk FRCS(Plast)1

Journal of Bone & Joint Surgery - American Volume:
doi: 10.2106/JBJS.N.01353
Scientific Articles
Abstract

Background: Tumor-related spinal surgery has been revolutionized by recent advances in spinal stabilization, modern neuroimaging, and perioperative intensive medicine. This study examines clinical outcomes and factors associated with complications following reconstruction of complex oncologic defects of the spine and sacrum, in an attempt to increase preoperative recognition of high-risk patients with diminished wound-healing capacity and to optimize clinical outcomes in this cohort.

Methods: We performed a retrospective analysis of fifty-five consecutive patients who underwent soft-tissue reconstruction with or without osseous stabilization of defects following spinal or sacral tumor resection at a quaternary referral center over a twelve-year period. Surgical outcomes included the prevalence of postoperative complications and success of wound closure at the latest follow-up. Health-related quality-of-life outcomes were assessed using the EORTC QLQ-C30 (European Organization for Research and Treatment of Cancer 30-Item Core Quality of Life Questionnaire) and SF-36 (Short Form-36) questionnaires.

Results: The mean age of the cohort was 46.7 years (range, eighteen to seventy-one years), with a male preponderance (3:1). Soft-tissue reconstructions (n = 70 flaps) were performed in the fifty-five patients. Overall, 36.3% of patients had wound complications. There was a twofold higher wound complication rate after delayed (60%) compared with immediate (29%) reconstruction (p = 0.03). Patients undergoing delayed reconstruction reported significantly lower SF-36 and EORTC QLQ-C30 scores.

Conclusions: Orthoplastic management of spinal tumors should involve a strategy for preoperative recognition of patients at risk of compromised wound-healing. Prophylactic soft-tissue reconstruction can achieve stable definitive wound closure and potentially avoid the need for secondary procedures in appropriately selected patients.

Level of Evidence: Prognostic Level IV. See Instructions for Authors for a complete description of levels of evidence.

Author Information

1Department of Plastic & Reconstructive Surgery, Nuffield Orthopaedic Hospital, Oxford University Hospitals, Oxford, United Kingdom

2Department of Trauma & Orthopaedic Surgery, Nuffield Orthopaedic Hospital, Oxford University Hospitals, Oxford, United Kingdom

E-mail address for R.T. Dolan: roshdolan@hotmail.com

Article Outline

Innovations in spinal stabilization, advances in perioperative medicine, and modern neuroimaging have facilitated radical resection of advanced tumors of the spine and sacrum. However, such complex defects present a substantial reconstructive challenge1-7. Creation of a large dead space in addition to use of extensive instrumentation and allograft material in a population of patients with compromised wound-healing capacity have led to postoperative wound complication rates ranging from 12% to 38%7-10.

Delayed reconstruction (i.e., revision of primarily closed surgical incisions resulting in reconstructive needs that had been unforeseen at the time of the primary procedure) has been associated with a higher rate of spinal wound morbidity, with potentially devastating sequelae, compared with primary reconstruction. Consequently, there has been a shift in the surgical management of complex spinal tumors toward a combined orthoplastic (orthopaedic and plastic surgery) management strategy to facilitate timely, definitive prophylactic soft-tissue reconstruction at the time of tumor resection for select patients. This transition has been tailored to streamline preoperative recognition of high-risk patients with diminished wound-healing capacity and to prevent wound complications by providing stable, well-vascularized soft-tissue coverage and tension-free wound closure at the time of initial spinal surgery for at-risk patients1,8.

There is growing recognition that evaluation of the success of surgical interventions should ideally incorporate patient’s self-assessment of functional outcome11-17. Although functional outcomes in similar patient cohorts have been previously examined, health-related quality of life (HRQoL) as an outcome following treatment of complex spinal tumors remains largely under-evaluated7,8,15-17.

The first purpose of this study was to assess surgical outcomes following immediate and delayed reconstruction of complex oncologic defects of the spine and sacrum. Secondly, we attempted to identify patient, disease, and treatment-related factors associated with postoperative complications specific to this cohort. Finally, we sought to compare patient-reported HRQoL outcomes following immediate and delayed reconstruction at the time of the latest follow-up.

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Materials and Methods

Study Design and Sample

We studied a retrospective case series of all consecutive patients who underwent soft-tissue reconstruction with or without osseous stabilization of defects following spinal and sacral tumor resection at the John Radcliffe Hospital and Nuffield Orthopaedic Hospital (Oxford University Hospitals, NHS Trust) quaternary referral centers between May 2001 and May 2013. Tumor ablative surgery with or without osseous stabilization was performed by orthopaedic spinal surgeons (J.W.-M. and J.R.), and soft-tissue reconstruction was performed by plastic surgeons (L.C., P.C., and H.G.).

Immediate reconstructions were performed at the time of the initial ablative spinal surgery by the plastic surgery team either to provide primary wound closure or as a preventative measure in patients deemed at high risk for wound-healing complications. Delayed reconstructions were performed as part of the treatment to manage a wound complication following a spinal surgery in which the wound was initially closed primarily by the reconstruction team.

We reviewed medical records in combination with data from a prospectively maintained database to collate and analyze information pertaining to patient demographics, histopathology, radiographic imaging, surgical interventions, reconstructive strategies, and patient outcomes (postoperative complications, disease recurrence, and patient survival).

All data were systematically reviewed to identify patient, disease, and treatment-related variables potentially associated with patient outcomes. Patient-related variables included age, history of smoking, body mass index, medical comorbidities (diabetes mellitus, ischemic heart disease, and peripheral vascular disease), preoperative nutritional status (hypoalbuminemia and anemia), and history of immunosuppressive medications or disorders. Disease-related variables included tumor subtype and defect location (cervical, thoracic, or lumbosacral). Treatment-related variables included previous chemotherapy and radiation therapy, previous spinal surgery, number of spinal levels resected, use of instrumentation for osseous stabilization, timing of reconstructive surgery (immediate or delayed), and type of soft-tissue reconstruction (local, pedicled, or free flap reconstruction).

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Surgical Outcomes Assessment

Surgical outcomes were evaluated on the basis of the prevalence of postoperative complications and the success of wound closure at the latest follow-up. Complications assessed included flap-related complications (partial and total flap loss, repeat exploration of microvascular anastomoses, venous congestion, hematoma, seroma, fat necrosis, wound dehiscence, and wound infection) and those related to the spinal surgery (transient neurological dysfunction, cerebrospinal fluid leak, exposure of instrumentation or periprosthetic infection, and paraspinal herniation). A body mass index of ≥25 kg/m2, history of smoking, ischemic heart disease, peripheral vascular disease, diabetes mellitus, hypercoagulation disorders, and preoperative hypoalbuminemia (albumin, <3.5 g/dL) and anemia (hemoglobin, <7 g/dL in females or <8 g/dL in males) were considered potential risk factors for flap-related complications. Previous spinal surgery, use of instrumentation for osseous stabilization, and multiple-level spinal surgery (two or more levels) were considered potential risk factors for spine-related or neurological complications. We defined major complications as those necessitating a return to the operating theater for further management.

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Quality-of-Life Outcomes Assessment

We sought to assess postoperative patient-reported health-related HRQoL outcomes, specifically comparing immediate versus delayed reconstructive outcomes, using the SF-36 (Short Form-36 Health Survey) and EORTC QLQ-C30 (European Organization for Research and Treatment of Cancer 30-Item Core Quality of Life) questionnaires18-20. Data were collated prospectively, and patients were invited to complete both questionnaires by mail at two time points: three months postoperatively and when their follow-up was complete and they were discharged from the service.

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SF-36

The acute version of the SF-36 assesses eight aspects or domains of HRQoL during the past week19. Physical and mental component summary scores (PCS and MCS, respectively) were also created using standard norm-based scoring methods21. The scales were scored numerically from 0 (the lowest level of functioning) to 100 (the highest level of functioning). The Norwegian SF-36 acute version 1.0 was used in this study.

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QLQ-C30

The EORTC QLQ-C30 is a questionnaire specifically developed to assess the quality of life of cancer patients. It is a thirty-item questionnaire incorporating nine multiple-item scales and six single items. The multiple-item scales consist of a global health scale, three symptom scales, and five functional domains. All questions are answered using a 4-point Likert scale except for those in the global health section, which uses a 7-point Likert scale. EORTC QLQ-C30 Version 3.0 was used in this study.

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Statistical Analysis

Descriptive statistics demonstrating patient characteristics are presented as the mean and standard deviation (SD) or as the number and percentage. Differences in means between groups were assessed using an independent-samples t test. A p value of <0.05 was considered significant. All statistical analyses were performed using SPSS software (version 20.0; IBM).

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Source of Funding

No external funding was received for this study.

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Results

Patient Demographics

Fifty-five consecutive patients underwent tumor resection with or without osseous stabilization from May 2001 to May 2013, and all of these patients underwent soft-tissue reconstruction of spinal and sacral defects (Table I). The mean age of the fifty-five patients was 46.7 years (range, eighteen to seventy-one years), with a male preponderance (male-to-female ratio, 3:1). The mean follow-up duration was 55.5 months (range, thirteen to 128 months). At the most recent follow-up, 14.5% (eight) of the patients had tumor recurrences and 5% (three) had died.

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Osseous Stabilization and Soft-Tissue Reconstruction

The majority of patients in the cohort (forty-nine, 89%) had a primary (spinal or sacral) tumor, with the most frequent histological subtype (in twenty-two, 40%) being chondrosarcoma. The thoracic spine was most the most common level of disease involvement (in thirty-eight, 69%) (Table I). The number of levels resected averaged 2.5, ranging from one to seven levels in select cases (Table II). Instrumentation for osseous stabilization of the spine was used in 73% (forty) of the patients, with anterior fusion being the most commonly employed technique (in twenty, 36% of the cohort). Fifteen patients (27%) had had prior spinal surgery at the same or a distant site.

The soft-tissue and osseous reconstructive strategies are summarized in Table II. The fifty-five patients underwent seventy flap procedures. A pedicled latissimus dorsi myocutaneous flap was the most commonly employed flap to reconstruct spinal defects (Fig. 1). Thirteen patients (24%) underwent reconstruction with two or more flaps. A free fibula osteoseptocutaneous flap was the flap of choice for reconstruction of osseous defects following spinal instrumentation. Immediate reconstruction was performed in 64% (thirty-five) of the patients. As shown in Figure 2, there was a 4.8-fold increase in the number of immediate reconstructions performed during the second half of the study period (2007 to 2013) compared with the first half (2001 to 2006) (p = 0.003).

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Surgical Outcomes: Complications and Identified Trends

Twenty patients (36%) had had at least one postoperative complication at the time of the latest follow-up. The fifty-one procedure-specific complications in this cohort included wound-related complications (n = 37) and sequelae from spinal surgery (n = 14) (Fig. 3). Wound-related complications included total or partial flap necrosis (six of fifty-five patients, 11%), infection (ten, 18%), dehiscence (eight, 14.5%), seroma (eight, 14.5%), and hematoma (five, 9%). Sequelae pertaining to spinal surgery were cerebrospinal fluid leakage (four, 7%), transient motor and/or sensory deficits (five, 9%), and exposed or infected instrumentation (five, 9%). When analyzed according to the timing of reconstruction, there was a preponderance of complications in the delayed reconstruction group (thirty-one of the fifty-one complications, 61%) compared with the immediate reconstruction group (twenty, 39%) (p < 0.04). The rates of the most frequently occurring postoperative complications were compared according to the timing of reconstruction. The rate of complete flap loss was 9% (three) in the immediate reconstruction groups compared with 0% in the delayed reconstruction group, and the rate of revision surgery was 17% (six) compared with 10% (two), respectively (Fig. 4).

Eight (14.5%) of the patients required revision surgery for major complications. Specifically, three patients (5%) required debridement of failed pedicled vertical rectus abdominis myocutaneous (VRAM) flaps covering sacral defects. All three underwent delayed reconstruction. At exploration, all three flaps were found to be hypoperfused as a result of tension on the relatively short pedicle as it spanned the pelvis to provide myocutaneous cover of sacral hardware and dead space. Following debridement of devitalized tissue, these defects were then reconstructed with free latissimus dorsi flaps, without complication, as a second procedure. One patient (2%) required debridement of bilateral grade-IV ischial pressure ulcers secondary to pressure necrosis partly related to instrumentation. These defects required reconstruction with bilateral anterolateral thigh fasciocutaneous flaps as a second procedure. Four patients (7%) developed deep cavity abscesses with associated sinus formation in the overlying skin, which required irrigation and debridement of devitalized tissue, with removal of instrumentation in two of the four patients. Exposure of instrumentation of the cervical spine occurred in one patient (2%), requiring bilateral trapezius myocutaneous advancement flaps to cover the exposed hardware and achieve tension-free wound closure. At the time of the latest follow-up, all patients had closed wounds.

The heterogeneity of the cohort with regard to patient, disease, and treatment-related factors (Tables I and II) prevents a sound statistical analysis; however, trends regarding the association of certain factors with higher complication rates were identified (Table III). Twenty-two (40%) of the patients reported a history of smoking, and the complication rate was 68% for the smokers compared with 21% for the nonsmokers. Thirty-three (60%) of the patients underwent reconstruction of surgical defects that had previously been irradiated, and the complication rate was 57% in these patients compared with 10% in those who had required no radiation therapy. The mean body-mass index (BMI) of the cohort was 26.7 kg/m2, with thirty-eight (69%) of the patients reported as clinically obese (BMI, ≥25 kg/m2), and the complication rate was 53% in those patients compared with 12% in those of normal BMI.

Over one-quarter of the cohort (fifteen, 27%) had had prior spinal surgery and forty (73%) had instrumentation for osseous stabilization, and the latter patients had a complication rate of 50% compared with 13% for those who did not have spinal instrumentation. Twenty-five (45.5%) of the patients had spinal surgery involving at least two levels, and the complication rates in those patients was 60% compared with 23% in those who did not have multiple-level spinal surgery.

Twenty-five (45.5%) of the patients had received prior chemotherapy. Seventeen (31%) of the patients had diabetes mellitus, and twelve (22%) had a history of either peripheral vascular or ischemic heart disease. With respect to preoperative nutritional status, few patients in this cohort were identified with hypoalbuminemia (eight, 14.5%) or anemia (nine, 16%).

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HRQoL Outcomes

The response rate among the fifty-two living patients invited to complete the SF-36 and EORTC QLQ-C30 questionnaires was 19% (ten) for the first postoperative time point. Given this low response rate and the resulting risk of respondent bias, we did not further analyze these results.

The response rate for the second time point was 62% (thirty-two), with a mean postoperative follow-up time of 40.1 months (range, thirteen to 111 months). The mean scores for each SF-36 domain were obtained, and patients were dichotomized into immediate and delayed reconstruction groups. Of the thirty-two respondents, nineteen (59%) had undergone immediate, prophylactic reconstruction of defects and thirteen (41%) had undergone delayed reconstruction. The patients who had undergone delayed reconstruction had lower mean raw SF-36 scores (indicating poorer functioning) in the physical functioning (p = 0.02), role limitations (p = 0.01), and general health (p = 0.03) domains and the PCS (p = 0.04) compared with the patients who had undergone immediate reconstruction of defects (Table IV).

Similarly, on the EORTC QLQ-C30 functional domains, the patients who had undergone delayed reconstruction had lower mean raw scores (indicating poorer functioning) in the physical functioning (p = 0.04) and role functioning (p = 0.01) domains compared with the patients who had undergone immediate reconstruction (Table V). For the symptom and single-item QLQ-C30 scales, the patients who had undergone delayed reconstruction had higher mean raw scores (indicating poorer functioning) in the fatigue (p = 0.04), insomnia (p = 0.02), and appetite loss (p = 0.01) scales compared with the patients who had undergone immediate reconstruction (Table V).

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Discussion

Tumor-related spinal surgery has been revolutionized by recent advances in spinal instrumentation, novel allograft constructs, neuroimaging, and perioperative intensive medicine1,7. Despite advancements in modern spinal surgery, complex defects of the spine and sacrum remain a substantial reconstructive challenge1-7. In this series of tumors of the spine and sacrum, we evaluated surgical and HRQoL outcomes of patients following radical resection and soft-tissue reconstruction, with or without osseous reconstruction, in the immediate and delayed settings, and we identified factors predictive of wound complications.

Analysis of surgical outcomes revealed an overall wound complication rate of 36%. Despite a paucity of similar spinal reconstruction series, our findings are comparable with those reported previously8. It is postulated that higher complication rates following reconstruction of spinal defects are attributed to the diminished wound-healing capacity of patients with spinal tumors (advanced age, multiple comorbidities, chemotherapy and/or radiation therapy, and use of spinal instrumentation and allograft material). We propose that the high comorbidity risk profile in our cohort (73% with spinal instrumentation, 64% with previous radiation therapy, 47% clinically obese, 40% with a smoking history, 36% who underwent delayed reconstruction, and 31% with diabetes mellitus) combined with the complexity of cases presenting for tertiary and quaternary-level management may be substantial predisposing factors for higher wound complication rates.

The timing of reconstruction has been identified as a key prognostic indicator of surgical outcomes following spinal defect reconstruction7,8, and this was confirmed in the present study by the higher rates of wound-related complications associated with delayed reconstruction. High rates of major wound complications associated with delayed reconstruction may have potentially devastating consequences because such complications may expose vital neural structures, spinal instrumentation, and allograft material8. Challenges are multifactorial in the delayed setting and include the creation of a large defect or dead space following wound debridement requiring multiple flaps from local or distant sites, with limited tissue mobilization and unreliable perfusion secondary to radiation-induced fibrosis. Furthermore, there is a higher risk of iatrogenic spinal injury and instability associated with removal of stabilization devices due to infection5,9,22-27.

Thus, there has been a shift in the management of complex tumors of the spine to provide definitive, prophylactic (immediate) soft-tissue reconstruction at the time of tumor resection, in an attempt to optimize surgical outcomes for at-risk patients. This streamlined orthoplastics management strategy has been implemented at our institution, with the present study revealing a fivefold increase in prophylactic soft-tissue coverage over the study period. In concordance with the threefold reduction in the major complication rate previously cited following implementation of prophylactic reconstruction8, we report a twofold higher wound complication rate for the delayed (60%) compared with the immediate (29%) spinal reconstruction group (p = 0.03). Specifically, higher rates of free flap failure and revision surgery were observed in the delayed reconstruction group. These data add further credence to the role of prophylactic soft-tissue reconstruction in achieving stable, definitive wound closure with minimal patient morbidity. However, it is impractical to have a plastic surgeon’s input for every spinal tumor case in which the patient has a potential wound-healing problem and to have ready availability of the plastic surgeon if primary closure proves impossible intraoperatively1.

There is a broad consensus that assessing surgical outcomes in terms of patients’ subjective reports and psychological functioning provides an additional component to achieving a meaningful understanding of the effects of treatment11-17,28-31. To our knowledge, this is the first study to report HRQoL outcomes following soft-tissue reconstruction of oncologic spinal defects. In the present study, the patients who underwent delayed reconstruction reported significantly lower mean SF-36 PCS scores and EORTC QLQ-C30 physical functioning scores (poorer functioning) and higher EORTC QLQ-C30 symptom scale scores (more symptomatic) compared with the patients who underwent immediate, prophylactic reconstruction. These findings may reflect a negative impact of the higher wound complication rates, prolonged treatment period, and additional treatment interventions associated with delayed reconstructions on patients’ perception of their physical functioning. The HRQoL data, while subjective, may add further support to the benefits of immediate, prophylactic reconstructions for this subgroup of patients.

This study has several limitations. First, there are the inherent limitations associated with a retrospective study design and a heterogeneous patient sample. A further limitation is the difficulty associated with assessing HRQoL and functional outcomes in the postoperative setting without an appropriate preoperative comparison. The present study does, however, provide strong preliminary data for a subsequent comprehensive longitudinal study evaluating the association of specific biomedical factors with HRQoL scores and functional outcome following soft-tissue reconstruction of oncologic defects of the spine and sacrum.

Investigation performed at the Departments of Plastic & Reconstructive Surgery and Trauma & Orthopaedic Surgery, Nuffield Orthopaedic Hospital, Oxford University Hospitals, Oxford, United Kingdom

Disclosure: None of the authors received payments or services, either directly or indirectly (i.e., via his or her institution), from a third party in support of any aspect of this work. None of the authors, or their institution(s), have had any financial relationship, in the thirty-six months prior to submission of this work, with any entity in the biomedical arena that could be perceived to influence or have the potential to influence what is written in this work. Also, no author has had any other relationships, or has engaged in any other activities, that could be perceived to influence or have the potential to influence what is written in this work. The complete Disclosures of Potential Conflicts of Interest submitted by authors are always provided with the online version of the article.

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