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Iodine-125 brachytherapy in the management of squamous cell carcinoma of the oral cavity and oropharynx Clare Stannard1,*, Gerrie Maree2, Susan Tovey2, Alistair Hunter1, Julie Wetter1 1

Department of Radiation Oncology, Groote Schuur Hospital, University of Cape Town, Cape Town, South Africa 2 Department of Medical Physics, Groote Schuur Hospital, University of Cape Town, Cape Town, South Africa

ABSTRACT

PURPOSE: Brachytherapy is an acknowledged modality for treating head and neck cancers and has moved from low-dose-rate (LDR) to high-dose-rate remote afterloading to reduce staff exposure. Iodine-125 (125I) is a low-energy source and can be used for LDR brachytherapy with minimal staff exposure. The results of treating with this isotope at Groote Schuur Hospital, Cape Town, are reported here. METHODS AND MATERIALS: 125I brachytherapy was used to treat 114 tumors from 1994 to 2010. Brachytherapy alone was used for 72 tumors, 39 postsurgery and 33 de novo. A brachytherapy boost together with external beam radiotherapy was used for 42 tumors, eight postsurgery and 34 de novo. Tumors were in the tongue, floor of mouth, soft palate, and tonsil, and mainly T1 or T2 classification. Brachytherapy was administered via an applicator or in plastic tubes implanted into the soft tissues or through the submandibular region. RESULTS: Local control rates of 80.7% at 5 years and 80% at 10 years were comparable to LDR, pulsed-dose-rate, and high-dose-rate results with iridium-192, likewise the 5- and 10-year diseasespecific survival rate of 74.3%. Complications of soft tissue ulceration occurred in 21 patients (18.4%) and healed spontaneously in 20 patients. There was no mandibular necrosis. CONCLUSIONS: 125I can be used as the sole treatment or as a boost to external beam radiotherapy, with or without surgery for early mouth cancer. It combines the radiobiological advantages of LDR brachytherapy with minimum staff exposure. It is a flexible system. Local control is excellent with acceptable morbidity, and the treatment time is short. Ó 2014 American Brachytherapy Society. Published by Elsevier Inc. All rights reserved.

Keywords:

Brachytherapy; Iodine-125; Head and neck cancer; Tongue cancer; Oropharyngeal cancer

Introduction Brachytherapy is acknowledged as a valuable modality in the treatment of head and neck cancer. Its ability to restrict the radiation to a confined area reduces the dose Received 18 September 2013; received in revised form 13 February 2014; accepted 19 February 2014. Informed consent: All cases were discussed at a multidisciplinary meeting, the consensus recommendation for brachytherapy was explained to the patient, and informed consent was obtained. Conflicts of interest: The authors have no proprietary interest in any part of the study. Ethical considerations: Approval for the retrospective study has been granted by The Human Research Ethics Committee, Faculty of Health Sciences, University of Cape Town, Cape Town, Africa. * Corresponding author. Division of Radiation Oncology, Department of Radiation Medicine, Groote Schuur Hospital, Observatory 7925, Cape Town, South Africa. Tel.: þ27-21-4044271; fax: þ27-21-4045259. E-mail address: [email protected] (C. Stannard).

to normal surrounding tissues. It can be given as the sole treatment or as a boost to external beam radiotherapy (EBRT) with or without previous surgery. The most experience in the head and neck region is with low-dose-rate (LDR) iridium-192 (192Ir) (1e7), but subsequently highdose-rate (HDR) and pulsed-dose-rate (PDR) afterloaders have been developed. These reduce staff exposure to radiation and allow optimization of the dose distribution (8e11). Iodine-125 (125I) has been used since 1974 to treat tumors in and around the eye (12, 13). The great advantage is the low energy of the sources (27e35 kV), which allows effective screening of surrounding sensitive structures. Apart from the use of 125I seeds on and around the eye and orbit (14), they have been used for various other tumors, mainly as permanent prostate implants. The William Beaumont Hospital changed from LDR 192Ir to 125I in 1986 because of the increasing number of breast implants being performed and the concern for staff exposure (15, 16). They also treated

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base of tongue tumors with an I boost to EBRT (17). Others have used 125I seeds as a permanent implant alone for advanced recurrent tumors of the head and neck or as a boost to EBRT in surgical patients with positive resection margins (18e22). The individual seeds are expensive, but as they have a half-life of 60 days, they can be reused several times for temporary implants, thus making them cost effective. The Departments of Radiation Oncology, Medical Physics, and Ophthalmology at Groote Schuur Hospital and the University of Cape Town have been using 125I to treat eye tumors since 1974 and changed from using 192Ir to 125I for tumors of the oral cavity and oropharynx as the seeds were readily available. We report here on the results of using this isotope in the oral cavity and oropharynx.

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Table 1 Tumor characteristics Characteristics

Total no.

Full dose

Boost þ EBRT

Patients Tumors Site Tongue Soft palate FOM Tonsil TNM classification T1 T2 T3 N0 N1 N2

112 114

72

42

54 29 21 10

37 15 17 3

17 14 4 7

46 56 12 101 9 4

43 24 5

3 32 7

EBRT 5 external beam radiotherapy; FOM 5 floor of mouth.

Methods and materials This is a retrospective case series of patients treated from 1994 to 2010, with followup to 2012 and a median followup of 39 months. All patients were assessed in the Combined Head and Neck Clinic by head and neck surgeons and radiation oncologists before treatment. Since 1994, 152 tumors that were suitable for treatment with brachytherapy in the oral cavity or oropharynx, as the whole or part of the management, were treated with 125I seeds. This report is confined to those patients with squamous cell carcinoma of the tongue, floor of mouth (FOM), soft palate, and tonsil. Those with carcinoma in situ (7), salivary gland tumors (13), reported previously (23), and sarcomas (2) were excluded as were other sites, for example, lip, tracheal stoma (11), and those with no followup (5). There were 112 patients, 82 males and 30 females, with a median age of 60 years (range, 4e92 years). Two patients had two tumors treated; therefore, there were 114 tumors (Table 1). Tumors were classified according to the American Joint Committee on Cancer Staging Manual, Seventh Edition, for this analysis (24). Most of the tumors were T1 or T2 and node negative (Table 1). There were 12 recurrent tumors. Brachytherapy can be given in a variety of ways depending on the site and volume to be treated. An 125I applicator alone was used in 5 patients, combined with 125I seeds in plastic tubes implanted interstitially into adjacent tissues in a further 4 patients; a single plane or volume implant was used in 50 patients; circles of seeds in 44 patients; and submandibular hoops in 11 patients (Figs. 1 and 2; Table 2). Before surgery, the implant is designed according to the tumor volume, required dose, dose rate, and availability of seeds. The volume to be treated is the gross tumor volume with a 5e10-mm margin. Usually the trains of seeds are placed 1 cm apart. The applicator usually covers the tumor by 5e10 mm, and the dose is prescribed to 4e5 mm from

its surface. The model of the volume is planned on the computer. The Brachy component of the Theraplan Plus Treatment Planning System (Theratronics International Limited, Kanata, Ontario, Canada) is used to plan the implant and the dose to be delivered from the applicator, together if required. Dose calculations at a point consist of the sum of doses at that specific point for each of the implanted sources (considered as point sources). Dose rates are calculated at each grid point of a cube lattice that contains the model. Thus, isodose curves may be generated in any arbitrary plane. The seed positions and activities are adjusted on the computer until optimum homogeneity is established. With an applicator, the surface dose is about three times the prescription dose. The applicator or plastic tubes are then loaded with the designated seeds according to the computer-generated plan. The applicator consists of two layers of plastic made from a dental impression enclosing the 125I seeds glued to one surface in their predetermined position and a layer of ash metal, a lead alloy, to protect adjacent structures (23). The plastic tubing is prepared with 30 cm of filler inside the tube, and the end is sealed. The 125I seeds are then inserted up to the filler according to the plan, with or without nylon spacers in between them. A further 30 cm of the filler is inserted up to the seeds to secure them, and the end is sealed. A curved needle is crimped on to the end of each tube for intraoral implants. Markings can be put on the filler material to assist positioning of the implant. Circles of seeds are ideal for tongue tumors that are small or previously excised. Using curved needles, the tubes are placed at regular intervals (usually 1 cm) through the lateral tongue to encompass the tumor or scar with at least a 5-mm margin, and the two ends of each tube are crossed over and sutured together just beyond the seeds to form a circle. An active length of 3 cm will form a 1 cm diameter circle and 4 cm a 1.3 cm circle (Fig. 1). The surplus tubing is fastened to each cheek with transparent adhesive dressing.

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Fig. 1. Tongue implant with four circles of iodine-125 seeds in plastic tubes. (a) Diagram of implant. (b) Implant being inserted. (c) Lateral X-ray. (d) Isodose rate distribution of implant.

Implants of the soft palate are done intraorally with adequate exposure. The technique has been described previously with 192Ir (25), except that the tubes are preloaded with 125I seeds (Fig. 2). Large tumors that cannot be implanted intraorally can be approached via the submandibular region. Trocars and cannulas are inserted in pairs at regular intervals from the

submandibular region into the tongue or FOM as required. They may have to be inserted more than once to achieve the correct position in the tongue. The tube containing the 125I seeds is fed through the straight cannula, looped over the tongue or FOM, and passed out through the adjacent cannula usually 1 cm away. Several hoops are inserted at regular intervals to cover the tumor. Plastic buttons and crimps

Fig. 2. Soft palate implant with three tubes of seeds. (a) Diagram of implant. (b) Anteroposterior X-ray. (c) Lateral X-ray. (d) Isodose rate distribution of implant.

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Table 2 Treatment details Brachytherapy

No. of tumors

Applicator Applicator þ tubes of seeds Single plane/volume

5 4 50

Circles Submandibular hoops

44 11

Treatment

Total no.

No surgery

67

Surgery

47

Full-dose brachytherapy

72

Boost þ EBRT

42

Neck dissections

Site FOM FOM, soft palate Soft palate, FOM, tonsil; 2e7 tubes of seeds Tongue; 3e9 tubes of seeds Tongue, FOM; 1e7 tubes of seeds

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applicator and an implant, they can be removed at different times to achieve the optimum dose. Implants are usually removed with analgesia only. The neck was treated either with a neck dissection and/ or with radiation in 48 patients: four N2, six N1, and 38 N0 disease as well as five T1, 36 T2, and seven T3. The primary site was in the tongue (22), soft palate (11), tonsil (eight), and FOM (seven). Statistical analysis

Subtotal Full-dose brachytherapy Boost þ EBRT Full-dose brachytherapy Boost þ EBRT Postsurgery No surgery Postsurgery No surgery

No.

Clinically

16

N positive

10

N negative

6

KaplaneMeier survival curves were plotted, and the logrank test applied for comparisons. A p-value of !0.05 was considered to be significant.

33 34 39 8 39 33 8 34

Results

Pathologically N N N N

positive negative positive negative

6 4 1 5

FOM 5 floor of mouth; EBRT 5 external beam radiotherapy.

are placed on the tubes externally next to the skin to secure them in the correct position for the duration of the implant. All implants are inserted under general anesthetic and done to comply as closely as possible to the preplanned position. The part of the tube containing the seeds is covered with a protective ash metal shield during the procedure until all the tubes are in place and ready to be pulled into the correct position. Steroids may be given during the procedure to reduce swelling. Analgesics are given routinely but not antibiotics. A feeding nasogastric tube is usually inserted for the duration of the treatment. Protective dentures of ash metal enclosed in plastic are worn during the treatment of tumors of the oral cavity. A three-dimensional reconstruction of the implant is obtained after implantation using two orthogonal radiographs taken approximately in the center of the implant. Corresponding seeds are marked on the two films and imported into the computer with a digitizer. The activity of each seed, calculated in the preplan, is added, and isodose rate curves generated as explained previously. The dose required is prescribed to the isodose that most nearly encompasses the tumor. Thus, the actual implant time can be calculated. The hot spot is taken as the area encompassed by the isodose that covers at least two seeds, which is 10e15% of the area of the tumor. This isodose rate should not be more than 1.5e2 times the prescription dose to the tumor. If an applicator is used in addition to interstitial tubes, the distributions are combined. Although the optimum dose rate is aimed for, the dose rate and thus the prescribed time are the variables in each implant. If there is a difference in dose rates between an

The median number of seeds used was 20 (range, 9e75), the median activity was 51.6 mCi (range, 16.4e192.6 mCi), and the median dose rate was 0.5 Gy/h. Although the range was 0.2e1.35 Gy/h, 82% of implants were treated with a dose rate between 0.3 and 0.7 Gy/h. Implants were usually designed to give the full dose over 5 days or a boost over 2e3 days, so that the weekly operating schedule could be maintained. Sixty-seven tumors were treated with radiotherapy (RT) alone, 33 had full-dose brachytherapy, and 34 had a brachytherapy boost with EBRT in 31 of them. Forty-seven tumors had surgery with the addition of RT for margins that were close, dysplastic, or involved; 39 of these had full-dose brachytherapy and eight had a brachytherapy boost with EBRT (Table 2). The interval from surgery to RT was a median of 7 weeks, range 0e17 weeks, being more than 8 weeks in 10 patients (21%). Chemotherapy, methotrexate in most cases, was given to 23 patients as a holding measure while awaiting RT or surgery. Thus, full-dose brachytherapy was given to 72 tumors; 39 postsurgery and 33 as the sole treatment (Table 2). They received a median dose of 59.2 Gy (range, 26.8e64.4 Gy). Three patients received less than 50 Gy; one was a 4-yearold boy and 2 implants had to be removed early because of medical problems. Forty-two tumors were treated with brachytherapy as a boost; and in 8 patients this was after surgery. Only 39 received EBRT as 2 patients died postimplant of a cerebrovascular accident and pulmonary embolus, respectively, and 1 patient refused further treatment. The median boost dose was 22.7 Gy (range, 9.9e30.2 Gy). Six patients received less than 15 Gy, usually for a suboptimal implant. The EBRT dose was increased accordingly in three of them. In 7 patients, brachytherapy was given 1e3.5 weeks (median, 2 weeks) after EBRT. Eleven patients had the brachytherapy during EBRT, usually within the first 2 weeks, and in 22 patients EBRT was given immediately after brachytherapy (medians, 0 weeks; range, 0e5 weeks). The median total dose of EBRT was 50 Gy (range, 42.4e70 Gy).

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Lymph node metastases appeared 0e46 months after treatment in 24 patients, 7 of whom had a primary recurrence also. Initially, 20 had been N0 and 4 were N1/N2. Subsequent neck dissections performed on 11 of these 24 patients revealed ECS in 10 of them. Ten of the 11 patients also had RT to the neck, and 7 were salvaged. Complications

Fig. 3. KaplaneMeier graph of local control of 114 tumors and diseasespecific survival of 112 patients.

Local control (LC), locoregional control, diseasespecific survival (DSS), and overall survival were 80.7%, 61.4%, 74.3%, and 57.2% at 5 years and 80%, 58.9%, 74.3%, and 39.2% at 10 years, respectively (Fig. 3). There was no significant difference according to site, T classification, whether surgery was performed, or whether full-dose brachytherapy or a brachytherapy boost to EBRT was given (Fig. 4). There were no recurrences among the 10 patients who had a delay of more than 8 weeks after surgery, with a median followup of 43 months (range, 10e136 months) and no recurrences in the patients who received a suboptimal dose of brachytherapy. There was no extracapsular spread (ECS) in the seven neck dissections performed for positive nodes. The neck remained clear in 5 of these patients and in 1 of the 3 patients treated with RT alone.

Mucositis developed after about 7e10 days and persisted up to 4 weeks if the full dose was given with brachytherapy. A mucosal ulcer of a few millimeters developed in 21 patients (18.4%) 1e25 months (median, 6 months), postimplant, and took 1e7 months (median, 3 months) to heal. The ulcer occurred in 10 patients (13.9%) after the implant alone and in 11 (26.2%) after the implant and EBRT. Fifteen (71.4%) occurred in T2 tumors, but site and previous surgery had no effect. The median full dose of those developing an ulcer was 59.5 Gy, boost 24.6 Gy, and median EBRT dose 50 Gy. The median dose rate was 0.5 Gy/h; only 2 patients had a dose rate of more than 0.7 Gy/h. One patient with a recurrent tumor had received 60 Gy EBRT previously. Smoking appears to contribute to the ulcer, and cessation improved healing. One patient required surgery to a FOM ulcer, and the others healed spontaneously. There was no mandibular necrosis. One elderly patient became disorientated, fell of bed, and swallowed the protective shield. Although the shield was removed, he developed pneumonia and died. Forty-one patients (36.6%) had one or more primary cancers in the aerodigestive tract before or after those currently reported.

Fig. 4. KaplaneMeier graphs of local control for (a) site, (b) T classification, (c) with or without surgery, and (d) full-dose brachytherapy or brachytherapy boost þ external beam radiotherapy (EBRT).

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Death was due to local recurrence or nodal disease or metastases in 23 patients, other carcinomas in 14 patients, and other causes, mainly heart and lung diseases, in 14 patients. Discussion The results show that the 5-year LC of 80.7% is comparable to previous studies of 65e97% for LDR (6, 10, 11, 17, 26, 27), 88% for PDR, with or without EBRT, most of whom had surgery (28), and 79e87% for HDR 192Ir (10, 26, 27, 29). DSS was 74.3% at 5 and 10 years, which compares favorably with 62e76% LDR 192Ir (1, 4, 30), 83e93% for PDR (28), and 88% for HDR (26). The complication rate of 18.4% compares favorably with 5e46% for LDR (1, 2, 7, 10, 11, 17), 17% for PDR (28), and 12e32% for HDR (10, 26, 29). Brachytherapy is part of the armamentarium for treating cancers of the head and neck, and most of the experience is with LDR 192Ir (1e7). Although the radiobiology, LC, and complications are well understood and acceptable, the concern is the staff exposure with 192Ir, and thus remote afterloading with HDR 192 Ir sources was developed to reduce staff exposure. Although it allows for optimization of the implant, the therapeutic index between tumor and normal tissue is decreased with HDR, and this may result in an increased risk of late complications. Thus, PDR was introduced to combine the radiobiological advantages of LDR with the physical and logistical advantages of HDR (8). 125 I made its debut in 1974 with its low energy of 28 kV compared with 380 kV of 192Ir. It could be shielded, minimizing the dose to surrounding structures and to staff and was thus an ideal isotope to use around the eye. Since then it has been used to treat a variety of tumors, but its use in the head and neck area has been limited to advanced or recurrent tumors or for positive surgical margins, usually as a boost (18e22). Apart from the article by Horwitz et al. (17) in which 58% of tumors were T1 or T2, there are no articles indicating that 125I has been used regularly for early disease. It has only been used as the sole treatment for advanced recurrencesdwith or without surgery. 125 I does, however, have several advantages. It is a LDR isotope, the radiobiology is understood, it treats a limited volume of tissue, and adjacent tissues can be screened. In our center, the planning, insertion, and hospital stay are considerably cheaper than for a full course of EBRT. It is cost effective in a center that has a steady supply of 125I. Hospital admission and general anesthetic are required, but treatment time is short, particularly if it is the sole treatment, which is beneficial to the patient, and any standard private room can be used. There is a significant reduction in radiation exposure to staff, patient, and visitors. Nursing care is thus far less of a problem. The time spent by the radiation oncologist on each patient is no more than that spent on a patient having EBRT. It has been highly successful in the postoperative management of salivary gland

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tumors of the palate (23). It is especially useful for unique tissues such as the soft palate, thus preserving function and avoiding xerostomia, postoperatively if only the primary tumor requires treatment, when surgical lists are full, when the patient has had RT for a previous tumor, and if the patient is reluctant to have surgery. A tracheostomy is not required; a feeding nasogastric tube is usually inserted as a precaution. The disadvantages are hospital admission for a few days, general anesthetic for insertion and occasionally for removal, and only minimal optimization is possible. Brachytherapy was usually given before EBRT or within the first 2 weeks of EBRT. Thus, the overall treatment time was 5.5e6 weeks, without any delays or opportunities for repopulation. The only exception was the soft palate where implanting a T2/T3 tumor at the start of treatment was a problem in 2 patients and much easier after a complete response with EBRT; but then, the overall treatment time is extended to 7e8 weeks. Although there appeared to be a difference in LC and DSS between those tongue tumors treated with brachytherapy alone vs. those that had a boost to EBRT, this was not significant, p 5 0.056 and p 5 0.067, respectively, unlike previous reports, which showed a marked decrease in LC for T2 tongue tumors treated with EBRT in addition to brachytherapy (31, 32). This was attributed to the higher dose that those treated exclusively with brachytherapy would have received, but it is also possible that the prolonged treatment time could have contributed to repopulation. Although not statistically significant, the T3 tumors appeared to do worse than earlier stages. It could be regarded as inappropriate to treat these with brachytherapy when other modalities, for example, chemoradiation, are available. Two of the patients with tongue tumors who were treated postoperatively had been irradiated previously and therefore did not have that option. Three other patients treated postoperatively were clear 24e46 months later. However, of those treated de novo with brachytherapy, with or without EBRT, four of six had a recurrence. The aim had been to reduce the dose to the parotid glands and avoid the toxicity of chemotherapy. However, it is possible that patients with T3 tumors that are not resectable would have an improved outcome with chemoradiation. Future attention needs to be given to the management of the neck. Twenty patients who were N0 initially developed nodal disease, and only 7 were salvaged. There was no ECS in the seven node-positive neck dissections done initially, but 10 of 11 neck dissections for subsequent nodes had ECS. Of the 50 T2N0 patients, 31 had the draining lymph nodes treated with surgery or EBRT and 4 developed nodal disease (12.9%). Of the remaining 17 T2N0 patients who did not have the neck treated for the current tumor, 7 developed nodal disease (41%). This raises the question posed by Mazeron et al. (11) as to whether all necks should be treated prophylactically. There were 6 patients (3 T1 and 3 T2) in whom the tumors appeared to be confined, yet who developed an

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extensive recurrence adjacent to the brachytherapy site, 2e14 months later. Although regarded as recurrences because of the time of appearance, the question arises as to whether they were understaged initially or were second primaries. How necessary are ancillary radiological investigations with a tumor that can be delineated clinically and in a situation where resources are limited? Is brachytherapy in the head and neck area here to stay or is it a dying art? It would be a great pity if it was neglected in favor of intensity-modulated RT or other highly sophisticated methods of RT delivery when a relatively small volume can be treated very effectively (33) with simpler, cheaper, and quicker methods as well as acceptable side effects. Although PDR combines the radiobiological advantages of LDR with the physical advantages of HDR, it is more demanding on staff time. 125I combines the advantages of LDR with minimum staff exposure and time expenditure and is therefore a viable alternative. In addition, the brachytherapy techniques can be adapted to various sites.

Conclusion 125

I can be used as the sole treatment or a boost to EBRT, with or without surgery, for early mouth cancer. It combines the radiobiological advantages of LDR brachytherapy with minimum staff exposure. It is a flexible system, local control is excellent with acceptable morbidity, and the treatment time is short. References [1] Shibuya H, Hoshina M, Takeda M, et al. Brachytherapy for stage I & II oral tongue cancer: An analysis of past cases focussing on control and complications. Int J Radiat Oncol Biol Phys 1993; 26:51e58. [2] Simon JM, Mazeron JJ, Pohar S, et al. Effect of intersource spacing on local control and complications in brachytherapy of mobile tongue and floor of mouth. Radiother Oncol 1993;26:19e25. [3] Mazeron JJ, Belkacemi Y, Simon JM, et al. Place of iridium-192 implantation in definitive irradiation of faucial arch squamous cell carcinomas. Int J Radiat Oncol Biol Phys 1993;27:251e257. [4] Pernot M, Malissard L, Hoffstetter S, et al. Influence of tumoral, radiobiological and general factors on local control and survival of a series of 361 tumors of the velotonsillar area treated by exclusive irradiation (external beam irradiation þ brachytherapy or brachytherapy alone). Int J Radiat Oncol Biol Phys 1994;30: 1051e1057. [5] Pernot M, Hoffstetter S, Peiffert D. Epidermoid carcinoma of the floor of mouth treated by exclusive irradiation: Statistical study of a series of 207 cases. Radiother Oncol 1995;35:177e185. [6] Pernot M, Hoffstetter S, Peiffert D, et al. Role of interstitial brachytherapy in oral and oropharyngeal carcinoma: Reflection of a series of 1344 patients treated at the time of initial presentation. Otolaryngol Head Neck Surg 1996;115:519e526. [7] Grabenbauer GG, Rodel C, Brunner T, et al. Interstitial brachytherapy with Ir-192 low-dose-rate in the treatment of primary and recurrent cancer of the oral cavity and oropharynx. Review of 318 patients treated between 1985 and 1997. Strahlenther Onkol 2001;177: 338e344.

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[8] Levendag P, Schmitz PI, Jansen PP, et al. Fractionated high-dose-rate and pulsed-dose-rate brachytherapy: First clinical experience in squamous cell carcinoma of the tonsillar fossa and soft palate. Int J Radiat Oncol Biol Phys 1997;38:497e506. [9] Brenner DJ, Schiff PB, Huang Y, et al. Pulsed-dose-rate brachytherapy: Design of convenient (daytime-only) schedules. Int J Radiat Oncol Biol Phys 1997;39:809e815. [10] Inoue T, Inoue T, Yamazaki M, et al. High dose rate versus low dose rate interstitial radiotherapy for carcinoma of the floor of mouth. Int J Radiat Oncol Biol Phys 1998;41:53e58. [11] Mazeron JJ, Noel G, Simon J-M. Head and neck brachytherapy. Semin Radiat Oncol 2002;12:95e108. [12] Sealy R, le Roux PLM, Rapley F, et al. The treatment of ophthalmic tumours with low-energy sources. Br J Radiol 1976;49:551e554. [13] Sealy R, Buret E, Cleminshaw H, et al. Progress in the use of iodine therapy for tumours of the eye. Br J Radiol 1980;53:1052e1060. [14] Stannard C, Sauerwein W, Maree G, et al. Radiotherapy for ocular tumours. Eye 2013;27:119e127. [15] Clarke DH, Edmundson GK, Martinez AA, et al. The utilisation of iodine-125 seeds as a substitute for iridium-192 seeds in temporary implants. An overview and a description of the William Beaumont Hospital Technique. Int J Radiat Oncol Biol Phys 1988;15: 1027e1033. [16] Clarke DH, Edmundson GK, Martinez AA, et al. The clinical advantages of iodine-125 seeds as a substitute for iridium-192 seeds in temporary plastic tube implants. Int J Radiat Oncol Biol Phys 1989;17: 859e863. [17] Horwitz EM, Frazier AJ, Vicini FA, et al. Excellent functional outcome in patients with squamous cell carcinoma of the base of tongue treated with external beam irradiation and interstitial iodine125 boost. Cancer 1996;78:948e957. [18] Vikram B, Strong EW, Shah JP, et al. Intraoperative radiotherapy in patients with recurrent head and neck cancer. Am J Surg 1985;150: 485e487. [19] Lee DJ, Liberman FZ, Park RI, et al. Intraoperative I-125 seed implantation for extensive recurrent head and neck carcinomas. Radiology 1991;178:879e882. [20] Vikram B, Mishra S. Permanent iodine-125 implants in postoperative radiotherapy for head and neck cancer with positive surgical margins. Head Neck 1994;16:155e157. [21] Beitler JJ, Smith RV, Silver CE, et al. Close or positive margins after surgical resection for the head and neck cancer patient: The addition of brachytherapy improves local control. Int J Radiat Oncol Biol Phys 1998;40:313e317. [22] Meng N, Jiang YL, Wang JJ, et al. Permanent implantation of iodine125 seeds as a salvage therapy for recurrent head and neck carcinoma after radiotherapy. Cancer Invest 2012;30:236e242. [23] Stannard CE, Hering E, Hough J, et al. Post-operative treatment of malignant salivary gland tumours of the palate with iodine-125 brachytherapy. Radiother Oncol 2004;73:307e311. [24] Edge SB, Byrd BR, Compton CC, et al, editors. American Joint Committee on Cancer Staging Manual. 7th ed. New York, NY: Springer; 2009. [25] Sealy R, Le Roux PLM, Hering E, et al. The treatment of cancer of the uvula and soft palate with interstitial radioactive wire implants. Int J Radiat Oncol Biol Phys 1984;10:1951e1955. [26] Inoue T, Inoue T, Yoshida K, et al. Phase III trial of high- vs. lowdose-rate interstitial radiotherapy for early mobile tongue cancer. Int J Radiat Oncol Biol Phys 2001;51:171e175. [27] Yamazaki H, Inoue T, Yoshida K, et al. Brachytherapy for early tongue cancer: LDR to high dose rate. J Radiat Res 2003;44:37e40. [28] Strnad V, Melzner W, Geiger M, et al. Role of interstitial PDR brachytherapy in the treatment of oral and oropharyngeal cancer. Strahlenther Onkol 2005;181:762e767. [29] Guinot JL, Santos M, Tortajada MI, et al. Efficacy of high-dose-rate interstitial brachytherapy in patients with oral tongue carcinoma. Brachytherapy 2010;9:227e234.

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[30] Lapeyre M, Bollet MA, Racadot S, et al. Postoperative brachytherapy alone and combined postoperative radiotherapy and brachytherapy boost for squamous cell carcinoma of the oral cavity, with positive or close margins. Head Neck 2004;26:216e223. [31] Benk V, Mazeron JJ, Grimard L, et al. Comparison of curietherapy versus external irradiation combined with curietherapy in stage II squamous carcinoma of the mobile tongue. Radiother Oncol 1990; 18:339e347.

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[32] Pernot M, Malissard L, Aletti P, et al. Iridium-192 brachytherapy in the management of 147 T2N0 oral tongue carcinomas treated with irradiation alone: Comparison of two treatment techniques. Radiother Oncol 1992;23:223e228. [33] Sresty NV, Ramanjappa T, Raju AK. Acquisition of equal or better planning results with interstitial brachytherapy when compared with intensity-modulated radiotherapy in tongue cancers. Brachytherapy 2010;9:235e238.

Iodine-125 brachytherapy in the management of squamous cell carcinoma of the oral cavity and oropharynx.

Brachytherapy is an acknowledged modality for treating head and neck cancers and has moved from low-dose-rate (LDR) to high-dose-rate remote afterload...
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