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Quality of life after management of advanced osteoradionecrosis of the mandible
International Journal of Oral and Maxillofacial Surgery, 9, 42, pages 1121 - 1128
Osteoradionecrosis (ORN) of the mandible is a severe complication of radiation therapy for head and neck cancer. In this case series, the authors analyzed their treatment and quality of life outcomes over the past 6 years. A retrospective chart review of 42 patients treated surgically for advanced ORN was conducted. A telephone survey was conducted and quality of life (QOL) questionnaires were completed in a subset of patients. 30 patients responded to the telephone survey assessing QOL for speech, swallowing and overall functioning correlated with oral nutrition and performance status. Surgery for ORN can result in an improved QOL. Functional outcomes of oral intake, speech intelligibility, and eating in public correlated with patient rated QOL measures. A lack of improvement in QOL, despite the restoration of an intact mandible, relates to the persistent effects of chemoradiotherapy.
Keywords: osteoradionecrosis, quality of life, radiation therapy, functional outcomes, mandible reconstruction.
Radiation therapy plays an important role in the treatment of head and neck cancer. Osteoradionecrosis (ORN) is a late complication of radiation exposure, classically presenting as exposed bone through an opening in the overlying skin or mucosa, persisting as a non-healing wound for 3 months or more. 1 Patients who develop ORN usually experience the full spectrum of collateral damage from radiation therapy (i.e. xerostomia, chronic trismus, dysguesia, dysphagia, decreased tongue mobility).2, 3, 4, 5, 6, and 7 These problems, in addition to the neuropathic pain and chronic drainage from super-infection, can leave patients physically and emotionally disabled Although numerous studies have examined the effects of surgical and/or chemoradiotherapy on quality of life (QOL), only one study to date has examined QOL after surgical treatment for ORN in a standardized fashion. 8
The classic treatment algorithm by Marx often involves multiple debridements and hyperbaric oxygen (HBO) therapy. In this algorithm, advanced (Stage III) ORN patients are treated with a staged resection and reconstruction which can leave patients further disabled during the interim period. In recent years, microvascular surgical techniques have improved tremendously. Success rates of free tissue transfer have been quoted as high as 98% in the literature.9 and 10 Additionally, imaging studies have also improved tremendously with the advent of high resolution computed tomography (CT) scanning. In this study, the authors review a case series of 47 patients over 6 years at Beth Israel Medical Centre. They discuss their management algorithm for patients with advanced ORN and the patient's perceived functional outcomes after treatment, including normalcy of diet, eating in public, speech intelligibility, resolution of trismus, presence of pain and QOL.
Materials and methods
A cross sectional review of 42 patients with advanced ORN managed over the past 6 years at Beth Israel Medical Centre was conducted to identify potential patients for a telephone survey. This study was approved by the Institutional Review Board and all patients who were able to be reached provided consent to participate. All patients had Marx Stage III ORN. All patients were treated with a segmental mandibulectomy and free flap reconstruction. Charts were reviewed to determine location of disease utilizing the mandibular defect classification system described by Urken et al. 11 ( Fig. 1 ), prior HBO therapy, extent of resection, type of flap used for reconstruction, complications (i.e. flap failure, exposed hardware), dental rehabilitation (extractions, implants, tissue borne or implant borne prosthesis), and length of follow-up. The telephone survey included administration of the Performance Status Scale (PSS).12 and 13 All domains of the PSS, including normalcy of diet, eating in public and understandability of speech, were obtained by one clinician (CL) questioning the patient. Survey information also included patient-reported approximate percentage oral nutrition, subjective pain level on a 1–10 scale, 14 and the presence of trismus. The Karnofsky Performance Status (KPS) Scale Index was completed by CL, based on the telephone interview information, to classify the functional impairment. 15 All patients who underwent the telephone survey were mailed paper QOL questionnaires including the Speech Handicap Index (SHI),16 and 17 European Organization for Research and Treatment of Cancer Quality of life Questionnaire-H&N 35 (EORTC H&N35), 18 and the Eating Assessment Tool (EAT-10). 19 For further clarification, the speech-language pathologist (SLP) evaluation of performance status using the PSS and KPS scale was completed via a telephone survey (n = 30, i.e. 71% response rate) whereas the patient-rated QOL assessment was done using results of a postal survey (n = 18, i.e. 60% response rate).
These patients were further matched by age and time of follow up with other head and neck cancer patients not participating in this study but seen in this clinic and for whom QOL information had been previously obtained and recorded in the database (with informed consent obtained from all patients). This was done to assess the impact of ORN on performance status and QOL in terms of speech and swallowing as compared to treated head and neck cancer patients who did not experience ORN. The authors also compared the EORTC H&N35 data to published data examining QOL with HBO therapy only for management of ORN.
Means and central tendency were obtained for variables including normalcy of diet, ability to eat in public, understandability of speech, percent oral intake, subjective pain level, and presence of trismus. A matched pair analysis using non parametric tests (i.e. Mann–Whitney test, 2 tailed) was conducted to compare differences in mean across variables in surgically treated patients treated with/without ORN surgery. A Kruskal–Wallis test was performed to assess differences in performance status and QOL based on flap type. Pearson correlation coefficients were calculated using IBM SPSS 19.0 to examine relationships between QOL based on paper surveys with pain, presence of trismus, normalcy of diet, eating in public, understandability of speech, percent oral intake, and subjective pain level.
42 patients underwent ORN surgery (31 males, 11 females, mean age 64 years). In these 42 patients, treated tumour sites included base of tongue (BOT), buccal, floor of mouth, retromolar trigone, lip, mandible, nasopharynx, parotid, tongue ( Table 1 ). Sites of mandibular defects from ORN can be found in Table 2 . The majority of ORN sites included the body and body-symphysis-body. Surgical outcomes for each patient can be seen in Table 3 . Acute complications were seen in only one patient who developed acute respiratory distress syndrome (ARDS) and pneumonia during her hospitalization. Hardware complications occurred in 6 patients (14%), with exposed hardware (1 patient), wound infection (1 patient), wound dehiscence (2 patients), with one requiring an ALT flap and the other requiring a pectoralis flap, skin necrosis (1 patient) requiring a pectoralis flap, and loosened screws (1 patient). Three patients had ORN progression (7%) and one patient developed new ORN on the opposite body of the mandible, due to new dental extractions without HBO therapy, requiring a second fibular free flap.
|Base of tongue||10||23.8|
|Floor of mouth||3||7.1|
|Left Retromolar trigone||1||2.4|
B: body; RB: ramus-body; BSB: body-symphysis-body; CRB: condyle-ramus-body; S: symphysis; CC: condyle-condyle; CRBSBRC: condyle-ramus-body-symphysis-body-ramus-condyle.
|Pt no.||Tumour site||Flap type||ORN site||Acute complications||Hardware complications||ORN progression||New ORN|
|12||Mandible||Scapular||S||ARDS + PNA||Yes|
|35||Tonsil||Fibular||B||Wound, DH, VC|
FOM: floor of mouth: RMT: retromolar trigone; BOT: base of tongue; CRBSBRC: condyle to condyle; B: body; BSB: body-symphysis-body; RB: ramus-body; CRB: condyle-ramus-body; S: symphysis; ARDS: acute respiratory distress syndrome; PNA: pneumonia; DH: dehiscence; VC: venous congestion.
30 patients (24 men and 6 women, mean age 67 years) responded by phone and were interviewed. Of these 30 patients, 18 (60%) completed mailed QOL questionnaires. Mean length of time from ORN surgery until telephone survey was 23.4 months (range 1–51 months). All but one of the patients underwent HBO treatment prior to ORN surgery. 8 patients (26%) underwent dental rehabilitation, with placement of implants and one with an implant borne prosthesis. With respect to pain since ORN surgery, 60% denied pain, 30% reported mild pain, and 10% moderate pain. No patient reported severe pain. Of those reporting pain, 89% (7 patients) were at the ORN operative site and 11% (1 patient) reported chronic pain at the donor site. 73% reported trismus and numbness following ORN surgery. Of those reporting numbness, all but one reported numbness of the face, cheek and lip associated with sacrifice of V3. One patient reported numbness at the donor site (i.e. shoulder/scapular region). With respect to diet following ORN surgery, (30%) of patients tolerated regular diets, 30% soft diets, 7% pureed diets and 7% liquid diets with the remaining 17% being dependent on a gastric tube. Regarding eating in public, 58% of patients do not restrict location, 8% eat in selected environments and 35% avoid eating in public. 27% of patients had gained weight since their ORN surgery, 4% lost weight and 69% reported stable weight.
QOL paper survey responses were each subdivided into 2 groups. Specifically, the EAT-10 scores were divided into ≤3 (normal) 19 ratings and >3 (abnormal) ratings; responses on the SHI were subdivided into: ≤6 (no speech problems) 16 and >6 (speech problems). Subjects were divided in two groups by age, including those 65 years and over (77%) and those under 65 years (23%), as 65 years was the mean age.
Outcomes compared to other surgically treated head and neck cancer patients without ORN
Since no studies to date have examined the performance status and combined QOL measures the authors used with the ORN population, they completed a pair wise matching of each patient who underwent ORN surgery with other head and neck cancer patients in the database based on age (±5 years). The results were categorized based on duration of follow up (less than 1 year, 1–3 years, and more than 3 years). Their performance status scores as well as QOL measures (EAT-10 and SHI) (Table 4 and Table 5) were compared. As can be seen in Table 4 , patients with ORN faired more poorly as compared to other head and neck cancer patients on the eating in public domain at all time points, with ratings of eating in public (score of 75 or greater) in the no-ORN group versus eating only in the presence of selected persons in selected places (score of 50–74) in the ORN group. Normalcy of diet was also lower in the ORN group, though not significantly. Scores at each time point in the ORN group varied from pureed to soft foods as compared to including firm foods such as raw carrots and meats in the no-ORN group. When comparing QOL for the ORN/no ORN groups ( Table 5 ), scores on the EAT-10 were significantly higher (i.e. poorer QOL) for the ORN group at <1 year and 1–3 year follow-up time points. QOL in the >3 year follow-up improved for the EAT-10. QOL scores for the SHI were worse for the ORN group as compared to the non-ORN group, though not significantly so.
|Follow up < 1 year|
|Normalcy of diet||Yes||9||59||40||0.297|
|Eating in public||Yes||9||64||44||0.605|
|Understandability of speech||Yes||9||97||8||0.730|
|Follow up 1–3 years|
|Normalcy of diet||Yes||11||46||40||0.016|
|Eating in public||Yes||11||55||38||0.005|
|Understandability of speech||Yes||11||91||13||0.300|
|Follow up >3 years|
|Normalcy of diet||Yes||11||49||37||0.116|
|Eating in public||Yes||11||55||42||0.088|
|Understandability of speech||Yes||11||90||18||0.705|
|Follow up < 1 year|
|Follow up 1–3 years|
|Follow up > 3 years|
Relationship between QOL and other outcome variables
When examining the relationship between flap type and performance across the three domains of the PSS using the Kruskal–Wallis test, it was found that understandability of speech statistically significantly differed (p = 0.024) among all the flap types. Using the Mann–Whitney test, it was found that the understandability of speech differed significantly (p = 0.006) between patients reconstructed with fibular free flaps (i.e. more understandable) compared with those reconstructed with iliac crest flaps (96 vs 75, respectively) ( Table 6 ). A possible explanation for poorer speech understandability in the iliac crest flap group may be that 50% of these patients had palate cancers, which likely resulted in hypernasality and reduced intelligibility. Normalcy of diet and eating in public were also marginally significantly different (p = 0.074 and 0.080, respectively) between patients reconstructed with various flaps (Kruskal–Wallis test).
|Fibular flap||Scapular flap||Iliac crest||p value|
|Normalcy of diet||61 (SD = 36) a||50 (SD = 35)||13 (SD = 25) 1||0.074|
|Eating in public||69 (SD = 37)||45 (SD = 37)||25 (SD = 35)||0.080|
|Understandability of Speech||96 (SD = 9) b||90 (SD = 14)||75 (SD = 20) 2||0.024|
a p = 0.050.
b p = 0.006.
The authors examined the effects of pain at the operative site across the various domains of the PSS scale using a pain intensity numeric rating scale. 19 patients had no pain, 8 patients complained of mild pain (1–3) and 3 patients complained of moderate pain (4–6). Patients who complained of any pain also had a worsened normalcy of diet (44 no pain vs 58 pain), eating in public (55 no pain vs 62 pain) and understandability of speech (89 no pain vs 95 pain) scores. The authors also compared PSS evaluations across two pain categories (mild vs moderate) and found that a marginally statistically significant difference (p = 0.064) existed in their normalcy of diet scores using a 2 tailed Mann–Whitney test (60 mild vs 13 moderate) ( Table 7 ). Patients with trismus performed worse on the normalcy of diet and eating in public domains of the PSS but their difference in means was not statistically significant (Mann–Whitney test). A Karnofsky performance scale was also used to assess these patients and the mean score for all the patients was 80 (min 50; max 90). This score represents ‘Normal activity with effort; some signs or symptoms of disease’. 15
|Normalcy of diet||Eating in public||Understandability of speech|
|No pain||56 (SD = 37)||60 (SD = 38)||94 (SD = 11)|
|Mild pain||60 (SD = 35) *||69 (SD = 34)||94 (SD = 9)|
|Moderate pain||13 (SD = 23) *||25 (SD = 43)||75 (SD = 25)|
* p = 0.064.
PSS domains were correlated with patient-perceived QOL to determine whether objective performance status was predictive of patient-related QOL. All three domains of the PSS statistically significantly correlated in a negative direction with all patient perceived QOL surveys ( Table 8 and Fig. 2 ). Higher scores on the PSS indicate better functioning for all three domains, whereas higher scores on the QOL scales indicate poorer functioning. 11% of the patients had a normal EAT-10 score (i.e. <3) whereas 89% had abnormal scores. Similarly, 12% of the patients also had normal SHI scores (i.e. <6) whereas 88% had abnormal scores. Scores 3 or greater on EAT-10 are considered abnormal and can be used to document initial dysphagia severity. 19 Scores above 6 on the SHI are used as a cut-off to identify patients with speech deficits that affect daily life, with 95% sensitivity and 90% specificity. 16 When examining the relationship between flap type and performance across the QOL forms (EAT-10 and SHI) using the Kruskal–Wallis test, it was found that SHI differed marginally significantly (p = 0.066) across flap types. On further analysis, using the Mann–Whitney test of significance, the difference was found to be between patients reconstructed with fibular free flaps (SHI 24) and those reconstructed with iliac crest flaps (SHI 64) ( Table 9 ). This finding agreed with the speech pathologist's findings for the PSS understandability of speech subscale, as patients with iliac crest flaps demonstrated poorer speech understandability than patients with fibular flaps, for the reason noted above. Swallowing as determined by EAT-10 was slightly better (not statistically significant) in the patients reconstructed using a fibular flap as compared to scapular and iliac crest flaps (20 vs 23 vs 28, respectively). A similar result reporting better swallowing in patients reconstructed with a fibular free flap compared to other flap types was reported by Chang et al. 8 using the University of Washington QOL (UW-QOL-R).
|Patients’ perceived QOL||Normalcy of diet||Eating in public||Understandability of speech||% oral intake|
|EAT-10||−0.79 *||−0.72 *||−0.65 *||−0.76 *|
|(SHI)||−0.75 *||−0.65 *||−0.89 *||−0.62 *|
* Statistically significant (p < 0.05).
|Fibular||Scapular||Iliac crest||p value|
|EAT-10||20 (SD = 13)||23 (SD = 11)||28 (SD = 15)||0.284|
|SHI||24 (SD = 19) a||41 (SD = 17)||64 (SD = 35) a||0.066|
a p = 0.033.
On the EORTC H&N35 scale, domains of swallowing, speech and social contact were negatively and strongly correlated (p < 0.05) with percent nutritional intake and all PSS subscales (normalcy of diet, eating in public, understandability of speech). When comparing performance on various domains of the EORTC H&N35 scale, patients treated with HBO therapy were found to fare better than patients treated with ORN surgery 20 ( Table 10 ). Harding et al. did not provide details regarding how many patients underwent surgery prior to HBO therapy. 20 When domains of EORTC H&N were compared across the various flap types, patients reconstructed with fibular flaps reported better swallowing, speech and sense (taste and smell) compared to patients reconstructed using other flap types. This was similar to the results reported by Chang et al. 8 using the University of Washington QOL (UW-QOL-R) regarding better performance in their fibular flap group.
|EORTC QLQ-H&N35||After HBO therapy a||After ORN surgery (reconstructed with flaps)||p value|
|Pain||33.04 (n = 28)||32.14 (n = 14)||0.920|
|Swallowing a||19.94 (n = 28)||56.57 (n = 14)||0.002|
|Senses problems||25.93 (n = 27)||30.86 (n = 14)||0.516|
|Speech problems||22.22 (n = 27)||37.93 (n = 14)||0.100|
|Social eating problems a||39.81 (n = 27)||60.76 (n = 14)||0.031|
|Social contact problems||15.13 (n = 26)||29.50 (n = 14)||0.100|
|Less sexuality||51.33 (n = 25)||37.58 (n = 12)||0.192|
a Based on date from Harding et al. 20
42 patients underwent ORN surgery, with few acute complications and few hardware complications. Fewer acute and hardware complications were seen than that reported by Chang et al., who noted a 37% complication rate. 8 The majority of patients denied pain, though most reported continued trismus and numbness. Mucke et al. found a similar reduction in mouth opening in ORN patients following surgery and radiotherapy. 21 Patients in their study had not undergone treatment for ORN at the time of assessment. QOL as reported on the SHI, EAT-10, and EORTC H&N35 (swallowing, speech and social contact) correlated with functional outcomes of percent oral intake, normalcy of diet, eating in public and understandability of speech. Patient-rated QOL outcomes related to swallowing were similar to those found by Chang et al., 8 with restrictions on diet found in some of their patients. Clearly, inability to communicate, eat and join others socially for meals can result in significantly reduced QOL.3, 4, and 5
Stage III ORN is defined by full thickness devitalization of bone, resorption of the inferior border of the mandible, fistula, or a pathological fracture. In the authors’ institution, these patients are treated with an aggressive surgical extirpation of all diseased hard and soft tissue with immediate reconstruction with a vascularized free flap. The ability to transplant tissue allows the surgeon to resect all of the diseased hard and soft tissue more aggressively, rather than leaving residual areas of unhealthy tissue. Bony continuity is re-established immediately, allowing a foundation for future dental rehabilitation. Since the reconstruction is performed immediately, there is no need for an external fixator or maxillomandibular fixation. Patients in this study underwent prior HBO at outside tertiary care facilities. The authors’ clinical management includes definitive ORN surgery following prior HBO. Should patients demonstrate Stage IV ORN with no prior HBO treatment, the authors do not recommend HBO, but recommend surgery. Should patients demonstrate Stage I or Stage II ORN, HBO is recommended as a first course of treatment. Clearly, more studies are needed to compare outcomes of treatment with HBO vs surgery for ORN.
This treatment approach for advanced ORN differs significantly from that advocated by Marx in the 1970s. In his approach, the reconstruction is staged and the patient is left with an external fixator in place to space the mandible segments. 10 weeks after the initial resection and 20 HBO dives later, a reconstruction is performed with autogenous cancellous bone packed into a freeze-dried allogenic bone carrier. Another 10 dives of HBO is given postoperatively and maxillomandibular fixation is maintained for 8 weeks.
Advances in surgical techniques have allowed more efficient management of advance ORN by combining the extirpation and reconstruction into a single procedure. The use of HBO has been limited to early and intermediate stage disease; this treatment no longer used for advanced stage disease. Patients are no longer subjected to fixation for 8 weeks or the use of an external fixator for 10 weeks between extirpation and reconstruction. It is debatable whether the patients’ QOL has improved and their pain has reduced.
A drawback of this study is its retrospective nature. These patients were not evaluated pre-ORN surgery. When questioned, patients were often unable to remember or report functioning prior to ORN surgery, including level of pain, trismus, and specific type of diet. When questioned about need for and length of time on antibiotics, several patients could not remember either piece of information. Medical chart review revealed that several of these patients took antibiotics for up to a year prior to definitive surgery. Prospective studies are currently being conducted at the authors’ institution that include a baseline assessment prior to ORN surgery. This evaluation includes the PSS, swallowing information (i.e. percentage oral intake and diet type), perceived pain level, presence and degree of trismus, need for and duration of antibiotics and reported speech, swallowing and overall H&N QOL via paper questionnaires. Preoperative/baseline instrumental assessment of swallowing is also being included to document swallow functioning, as many oral and oropharyngeal cancer patients treated with chemoradiotherapy as adjuvant post-surgical treatment as well as those treated primarily develop significant oropharyngeal swallowing impairment.22 and 23 It is likely that many of these patients did not have normal swallow functioning pre-ORN surgery, due to changes in swallow physiology after chemoradiotherapy. Therefore, these patients need to be counselled regarding potential improvement in ORN-related symptoms, such as pain after ORN surgery, but not necessarily resolution of their prior problems, such as dysphagia, xerostomia and impairment in taste. It is clear, however, that the patients’ QOL correlates quite well with objective functional outcomes.
In conclusion, management of advanced ORN of the mandible has evolved significantly over recent years. Improvements in microvascular surgical techniques have allowed the development of an efficient and effective single stage definitive resection and reconstruction of the diseased mandible. Unquestionably patients experience improvement in their chronic pain and resolution of their chronic infection, yet, clearly, some patients remain unhappy with their outcomes. Expectations must be set appropriately prior to surgery because many patients have high hopes that addressing the devitalized mandible will have the added benefit of improving other collateral damage that resulted from the radiation therapy (i.e. trismus, xerostomia, dysphagia, and loss of taste).
Yes, approval was granted by the Beth Israel Medical Centre's Institutional Review Board, IRB# 179-10.
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1 Department of Otolaryngology, Head and Neck Surgery, Beth Israel Medical Center, Albert Einstein College of Medicine, New York, NY, USA
2 Department of Surgery, Division of Plastic Surgery, Beth Israel Medical Center, Albert Einstein College of Medicine, New York, NY, USA
Address: Adam S. Jacobson, Beth Israel Medical Center, Department of Otolaryngology – Head and Neck Surgery, Albert Einstein College of Medicine, 10 Union Square East, Suite 5B, New York, NY 10003, USA. Tel: +1 212 844 8775; Fax: +1 212 844 6975.
© 2013 International Association of Oral and Maxillofacial Surgeons, Published by Elsevier B.V.