Submandibular Gland Transfer for Prevention of Xerostomia After Radiation Therapy Swallowing Outcomes

ORIGINAL ARTICLE Submandibular Gland Transfer for Prevention of Xerostomia After Radiation Therapy Swallowing Outcomes

Jana Rieger, PhD; Hadi Seikaly, MD; Naresh Jha, MBBS; Jeffrey Harris, MD; David Williams, MD; Richard Liu, MD; Tim McGaw, DDS; John Wolfaardt, PhD

Objective: To assess swallowing outcomes in patients had preservation of 1 submandibular gland (SJP group) with oropharyngeal carcinoma in relation to the Seikaly- and 11 who did not (control group). Jha procedure for submandibular gland transfer (SJP). The SJP has recently been described as beneficial in the Main Outcome Measures: Quantitative and qualita- prevention of xerostomia induced by radiation therapy tive aspects of swallowing were obtained to determine in patients with head and neck cancer. whether patients in the SJP group performed more op- timally than those in the control group. Design: Inception cohort. Results: Baseline and stimulated salivary flow rates were Setting: University-affiliated primary care center. significantly different between groups. Patients in the SJP group were able to move the bolus through the oral cavity Patients: A phase 2 clinical trial was conducted from and into the pharynx faster than those in the control group. February 1, 1999, through February 28, 2002, to evalu- In addition, patients in the SJP group swallowed less often ate SJP in patients with head and neck cancer. During per bolus than patients in the control group. The com- that period, a consecutive sample of 51 patients who un- plete swallowing sequence was twice as long in controls. derwent surgical resection and reconstruction with a radial forearm free flap for oropharyngeal carcinoma were Conclusions: The SJP for submandibular gland trans- referred for functional assessment of swallowing after fer appears to be beneficial in promoting more time- completion of adjuvant radiation therapy. At 6 months efficient swallowing behaviors. This efficiency has im- after surgery, swallowing assessments for 24 patients were plications for the overall well-being and nutritional status available. of patients with head and neck cancer.

Intervention: The cohort of 24 patients included 13 who Arch Otolaryngol Head Neck Surg. 2005;131:140-145

EROSTOMIA IS A CONDI- for lubrication, and therefore comfort, of Author Affiliations: tion in which the function the mouth and oral pharynx, but is also Craniofacial Osseointegration of the salivary glands has necessary for modulation of microbial or- and Maxillofacial Prosthetic been altered such that the ganisms in the mouth, remineralization of Rehabilitation Unit, Caritas oral cavity lacks saliva, re- teeth, maintenance of the mucosal im- Health Group (Drs Rieger, Seikaly, and Wolfaardt), Faculty sulting in subjective complaints of dry mune system, and preparation of a bolus X 1 of Rehabilitation Medicine mouth. Xerostomia resulting from can- of food during mastication. When sali- (Dr Rieger), Division of cer treatment has a devastating impact on vary function is compromised, the result- Otolaryngology Head and Neck quality of life. Individuals diagnosed as ing sequelae include oral discomfort, mu- Surgery (Drs Seikaly, Harris, having cancer of the head and neck are cositis, periodontal disease, dental caries, and Liu), Division of General overwhelmed by the notion of treatment loss of teeth, fissures of the tongue, de- Surgery (Dr Williams), and potentially involving surgery, radiation creased taste acuity, inability to wear Department of Dentistry therapy, and chemotherapy. The com- dentures if needed, and difficulty with mas- (Drs McGaw and Wolfaardt), mon experience of the patients is that sur- tication and deglutition.1-9 The develop- University of Alberta; Division viving these therapies is the primary mor- ment of xerostomia in survivors of head of Surgical Oncology (Dr Seikaly) and Department of bid challenge to regaining quality of life. and neck cancer, therefore, is of serious Radiation Oncology (Dr Jha), However, the common clinical experi- consequence to their nutritional status and Cross Cancer Institute, ence is that where xerostomia occurs, this their overall quality of life. Edmonton, Alberta. condition becomes a primary threat to re- Because of the location of primary tu- Financial Disclosure: None. gaining quality of life. Saliva is important mors of the head and neck, the major sali-

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©2005 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/26/2021 vary glands are often in the field of the postoperative ra- poral measures of swallowing events. In contrast, an- diation therapy.1,10,11 For this reason, the potential for other report involving patients with head and neck cancer8 development of xerostomia in this patient population is found that patients with xerostomia took longer to mas- very real. Salivary dysfunction develops immediately when ticate a dry bolus and were left with greater oral and pha- the major salivary glands are in the radiation field, and ryngeal residues than a group of healthy controls. These such dysfunction is permanent with little chance for re- reports appear to provide conflicting information regard- covery.10,12 The prevalence of xerostomia in patients with ing the effect of xerostomia on objective measures of swal- head and neck cancer after radiation therapy, whether lowing function. However, the effect of xerostomia was that therapy is the primary or secondary treatment, has being compared differently, with one set of reports us- been reported to vary from 94% to 100%.13-15 ing salivary weight to understand the effect of xerosto- Treatment for xerostomia can be supportive or pre- mia on swallowing,7,9 and the other report using a group ventive. Supportive care for xerostomia includes the use of healthy controls for comparison with patients with xe- of saliva substitutes and moistening agents. Saliva sub- rostomia.8 Regardless, evidence is emerging that sup- stitutes duplicate the properties of normal saliva and pro- ports what has been largely anecdotal evidence of swal- vide relief for approximately 40% of patients who use lowing problems related to xerostomia. them.16 However, they are costly and provide only tem- From previous salivary flow studies, it has been dem- porary relief.1 Moistening agents include chewing gum, onstrated that the SJP has yielded beneficial results in pre- candy, and sips of water. Again, these provide only tem- venting xerostomia in patients undergoing radiation porary relief of xerostomia. Furthermore, the constant therapy of the head and neck region.10,17-19 The objec- intake of water during the course of a day is associated tives of the present study were to explore the benefits of with polyuria, often resulting in nocturnal wakefulness. the SJP beyond previously reported salivary flow rates.19 The use of candies is associated with increased dental car- Specifically, we compared measures of swallowing out- ies and mucosal damage stemming from pressure against comes obtained via videofluoroscopy after adjuvant ra- the soft tissues of the mouth when sucking on the candy.1 diation therapy between a group of patients who re- One modality of preventive care for xerostomia is the ceived the SJP and a group of controls (ie, patients who Seikaly-Jha procedure for submandibular gland transfer did not receive the SJP owing to oncological reasons). (SJP). One submandibular salivary gland is transferred into the submental space, using retrograde flow through the facial vessels. An incision is made from the mastoid METHODS process to the mentum. A flap is elevated, and the submandibular gland is released from surrounding struc- A phase 2 clinical trial was conducted from February 1, 1999, tures and then repositioned in the submental space un- through February 28, 2002, to evaluate the SJP for subman- der the anterior belly of the digastric muscle. The dibular gland transfer in patients with head and neck cancer. submental and sublingual space is then shielded during The trial was approved by the internal review board and the postoperative radiation therapy, thereby protecting and human ethics committee of the University of Alberta (Edmon- preserving the transferred submandibular and sublin- ton), and informed consent was obtained from each patient. gual salivary glands. If any facial, preglandular, or sub- During that period, 51 patients who underwent surgical resection and reconstruction with a radial forearm free flap for oro- mental nodes are found to be involved with metastatic pharyngeal carcinoma were referred for functional assessment cancer, the gland transfer is abandoned and the gland is of swallowing after completion of adjuvant radiation therapy resected. The surgical procedure is described as requir- (ie, at least 6 months after surgery). Of those patients, 8 died ing no special surgical skills and adds approximately 45 before a post–radiation therapy assessment could occur, 8 were minutes to the total surgical time.10 It is a relatively in- lost to follow-up, 4 did not receive conventional adjuvant post- expensive treatment modality, with recent reports dem- operative radiation therapy (ie, they received intensity- onstrating efficacious results in the prevention of xero- modulated radiation therapy), 4 had a history of previous sur- stomia after radiation therapy.10,17-19 Statistically significant gery or radiation therapy for head and neck cancer, and 3 differences in salivary flow between patients who have underwent videofluoroscopic swallow studies in which the im- received the SJP and a group of control subjects have been age was too dark for proper analysis. Thus, for the current study, 24 patients underwent assessment for swallowing ability via vid- demonstrated. The SJP prevented xerostomia in 83% of eofluoroscopy. patients undergoing that treatment, whereas all of those All patients underwent surgical resection of an oropharyn- 19 in the control group experienced severe xerostomia. Pre- geal tumor and reconstruction with a radial forearm free flap, vious publications provide a more detailed description followed by a standard course of conventional radiation therapy. of the surgical procedure.10,17-19 All patients were treated by a single medical rehabilitation team. Unlike well-documented evidence describing the im- The anatomical areas involved in oropharyngeal resections in- pact of xerostomia in the development of mucositis, peri- cluded the soft palate, lateral pharyngeal wall, tonsil, and base odontal disease, and dental caries,1,2,20 the impact on the of tongue (BOT). No individual was included who had involve- development of swallowing disorders in patients with head ment of the oral tongue, maxilla, nasopharynx, or larynx. Data and neck cancer has only recently been described.7-9 In were available for 4 women (17%) and 20 men (83%) who 7,9 ranged in age from 33 to 75 years (mean age, 57 years). Of the 2 related reports, a reduction in saliva weight after che- 24 patients, 13 underwent the SJP for submandibular gland trans- moradiation therapy was related to patient report of poorer fer (SJP group) and the remaining 11 did not (control group). swallowing outcomes. There was no relationship found All patients received 50 to 70 Gy of radiation in 2 Gy per frac- in either report between saliva weight and objective as- tion, with treatment once a day, 5 times a week, during the course sessment of swallowing function, which included tem- of 6 weeks. Radiation therapy was started 4 to 6 weeks after

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©2005 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/26/2021 A modified barium swallow procedure was completed in the Table 1. Patient Information presence of a radiologist within the radiology department of the hospital. Two consistencies of food were administered, in- % Resected cluding approximately 10 mL of pudding mixed with paste Patient No./ Dental barium (barium sulfate cream [Esobar]; Therapex, Montreal, Age, y/Sex SJP BOT SP Status Quebec) in a 3:1 ratio presented as a calibrated bolus on a tea- 1/M/51 Y 75 25 E spoon, and a quarter of a digestive cookie covered with barium 2/M/47 Y 0 25 PD paste. Two trials of each consistency were consumed and re- 3/M/71* Y250D corded on a videofluoroscopic study. Based on the methods of 4/M/45 N 75 50 D previous studies of swallowing,21-23 each swallow study was ana- 5/M/48 N 50 50 D lyzed in frame-by-frame slow motion using the Digital Swal- 6/M/68 Y 25 25 E lowing Workstation (Model 7200; Kay Elemetrics Corp, Lin- 7/M/71 N 50 25 E coln Park, NJ) for the following timing events: oral transit 8/M/42 Y 0 50 PD duration, pharyngeal transit duration, oral containment dura- 9/M/33 N 0 25 D tion, oropharyngeal transit duration, cricopharyngeal open du- 10/M/55 N 100 50 D ration, and sequence duration. We recorded the number of swal- 11/M/73 Y 100 0 D lows per each bolus consistency. In addition, we observed any 12/M/70 N 50 25 PD 13/M/68 Y 25 0 E occurrences of laryngeal penetration or pulmonary aspiration 14/M/55 N 0 100 E during the swallow study and rated them on the Penetration- 24 15/M/57 N 25 25 E Aspiration Scale. Observers also rated the degree of residue 16/M/55 Y 100 25 D remaining in the oral cavity after all swallows in a sequence of 17/M/60 Y 25 50 E swallows on 1 bolus. A rating of 1 was assigned in instances 18/F/55 Y 50 50 E where there was no or very mild oral residue. A rating of 2 was 19/F/75 N 50 50 E assigned in instances where there was considerable residue in 20/F/52 Y 25 50 PD the mouth, which was estimated to be no more than 25% of 21/M/45 N 25 25 D the original bolus. A rating of 3 was assigned in instances where 22/F/57 Y 50 0 D there was approximately 25% or more of the original bolus re- 23/M/66 N 75 50 E maining in the mouth. Finally, we judged the degree of pha- 24/M/50 Y 25 50 D ryngeal residue at the end of each swallowing sequence. A rating of 1 was assigned in instances where there was no or very Abbreviations: BOT, base of tongue; D, dentate (full natural or prosthetic mild pharyngeal residue. A rating of 2 was assigned in in- dentition); E, edentulous; PD, partially dentate (Ͻ75% of normal adult stances where there was considerable residue in the pharynx dentition); SJP, Seikaly-Jha procedure for submandibular gland transfer; SP, soft palate. that did not threaten the airway. A rating of 3 was assigned in *Patient 3 received nutrition orally and through a gastrostomy tube. instances where there was considerable residue in the pharynx that appeared to threaten the airway.

surgery. In those patients who underwent the SJP, shielding STATISTICAL ANALYSIS covered more than 80% to 90% of the transferred submandibular salivary gland. The posterior border shielding always re- All statistical analyses were performed using SPSS (version 11.5 mained anterior to the hyoid bone. Disease areas or potential [2002]; SPSS Inc, Chicago, Ill). Preliminary statistical analy- sites of spread were not shielded. Primary target volume in- ses showed that patient age and percentage of the BOT re- cluded the major salivary glands (parotid and the nontrans- sected were significantly correlated with several of the depen- ferred submandibular salivary glands) and had greater than 50 dent variables. Therefore, age and percentage of BOT resected Gy of radiation delivered to that volume via external beam. were entered as covariates in the analysis. The data were ana- Patients underwent assessment for swallowing after the lyzed via a 1-way multivariate analysis of covariance with fixed completion of radiation therapy. Time elapsed from the sur- effects on the between-subjects factor. The between-subjects gery date to the swallowing assessment reported herein ranged factor was group and had 2 levels (SJP and control). An inde- from 155 to 398 days, with an average across patients of 220 pendent-samples t test was used to determine differences between baseline and stimulated flow rates. Approximately 20% days. A description of the patients is given in Table 1. Pre- liminary data analysis showed that there were no differences of the data were reanalyzed to establish interobserver reliabil- between the demographic characteristics (ie, sex, dental sta- ity. Intraclass correlation coefficients (average of raters) re- tus, degree of resection, and days since surgery) of patients with vealed a value of 0.96, with the upper and lower bounds of a or without the SJP. 95% confidence interval at 0.98 and 0.92, respectively.

DATA COLLECTION RESULTS

At the 6-month postoperative assessment time, saliva from the SALIVARY FLOW RATES anterior floor of the mouth was collected at least 1 hour after the most recent meal, between 9:30 AM and 12:30 PM, and was Baseline and stimulated salivary flow rates were avail- calculated as collected volume/collection time. An appliance able for all patients in the SJP group and for a subgroup consisting of a micropipette holder fitted with a latex dropper of controls. In the SJP group, mean baseline flow rate was bulb was used to collect the baseline and stimulated saliva samples. Baseline saliva samples were collected first, followed 0.07 mL/min (range, 0.01-0.17 mL/min), whereas in the by a 3-minute rest interval. Then, stimulated saliva samples were control group it was 0 mL/min. Mean stimulated sali- collected after administration of a 6% citric acid solution to the vary flow rate for the SJP group was 0.32 mL/min (range, posterior dorsal surface of the tongue. The details of this pro- 0.04-0.90 mL/min), whereas in the control group it was cedure are described more thoroughly elsewhere.19 0.07 mL/min (range, 0-0.21 mL/min). An independent-

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©2005 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/26/2021 Table 2. Statistical Results of Bolus Studies Table 2. Statistical Results of Bolus Studies (cont)

Measure, Group Control SJP Significance* Measure, Group Control SJP Significance* Pudding Bolus Cookie Bolus Oral transit duration, s Oral transit duration, s Mean (SD) 1.10 (1.08) 0.59 (0.38) .19 Mean (SD) 3.93 (5.27) 0.80 (0.85) .47 Minimum 0.13 0.2 Minimum 0.2 0.18 Maximum 3.65 1.2 Maximum 7.7 2.27 Pharyngeal transit Pharyngeal transit duration, s duration, s Mean (SD) 2.25 (2.90) 1.22 (0.76) .31 Mean (SD) 2.85 (2.00) 2.68 (4.24) .72 Minimum 0.58 0.4 Minimum 1.44 0.43 Maximum 10.61 3 Maximum 4.27 10.24 Oropharyngeal transit Oropharyngeal transit duration, s duration, s Mean (SD) 3.35 (3.81) 1.81 (0.79) .23 Mean (SD) 6.28 (6.57) 3.48 (5.08) .94 Minimum 0.83 0.93 Minimum 1.64 0.62 Maximum 14.26 3.2 Maximum 10.93 12.51 Cricopharynx open Cricopharynx open duration, s duration, s Mean (SD) 0.45 (0.22) 0.37 (0.10) .30 Mean (SD) 0.80 (0.47) 0.35 (0.13) .12 Minimum 0.15 0.18 Minimum 0.47 0.23 Maximum 1.02 0.48 Maximum 1.13 0.57 Oral containment Oral containment duration, s duration, s Mean (SD) 4.13 (2.98) 1.97 (1.03) .02 Mean (SD) 14.16 (11.47) 14.87 (4.51) .69 Minimum 1.47 0.55 Minimum 6.06 8.74 Maximum 11.25 3.89 Maximum 22.27 20.58 Sequence duration, s Sequence duration, s Mean (SD) 20.99 (14.93) 10.65 (5.53) .054 Mean (SD) 29.81 (26.04) 34.98 (24.03) .74 Minimum 6.91 2.44 Minimum 11.4 12.62 Maximum 49.48 23.52 Maximum 48.21 66.48 No. of swallows No. of swallows Mean (SD) 4.36 (3.96) 2.50 (1.57) .18 Mean (SD) 4.00 (1.41) 3.60 (1.67) .65 Minimum 2 1 Minimum 3 1 Maximum 15 7 Maximum 5 5 Penetration-Aspiration Pharyngeal residue Scale level† Mean (SD) 1.50 (0.71) 1.40 (0.89) .95 Mean (SD) 1.36 (0.50) 1.75 (1.76) .57 Minimum 1 1 Minimum 1 1 Maximum 2 3 Maximum 2 7 Oral residue Pharyngeal residue Mean (SD) 2.00 (1.41) 1.20 (0.45) .09 Mean (SD) 1.64 (0.92) 1.50 (0.67) .89 Minimum 1 1 Minimum 1 1 Maximum 3 2 Maximum 3 3 Oral residue Abbreviation: SJP, Seikaly-Jha procedure for submandibular gland Mean (SD) 1.18 (0.40) 1.17 (0.39) .98 transfer. Minimum 1 1 *Based on estimated marginal means (covariates appearing in the model Maximum 2 2 were age and percentage of base of tongue resected) with adjustment for multiple comparisons via a Bonferroni correction. †On this scale, level 1 indicates no penetration or aspiration; (continued) 2, penetration above the vocal folds but no residue; 3, penetration above the vocal folds with residue; 4, bolus contacting the vocal folds but no residue; 5, bolus contacting the vocal folds with residue; 6, bolus passing the glottis samples t test showed that differences between the 2 without subglottic residue; 7, bolus passing the glottis with subglottic groups were significant for the baseline (P=.002) and residue and patient response; and 8, bolus passing the glottis with subglottic stimulated (P=.05) flow rates. residue and no patient response.

SWALLOWING OUTCOMES the dependent variables oral containment duration (ie, the Pudding Bolus interval from the start of the sequence until the tail of the bolus passes the posterior border of the ramus of the man- Means and SDs for all dependent variables are shown in dible) and sequence duration (ie, the interval between the Table 2. For the pudding bolus, 23 of 24 fluoroscopic stud- start and the end of the complete swallowing sequence). ies were analyzed (12 SJP and 11 control). A study from 1 Individuals in the SJP group had significantly shorter oral patient in the SJP group was not included because the im- containment duration (mean, 1.97 seconds) than those in age was not satisfactory for analysis. The results showed the control group (mean, 4.13 seconds). In addition, over- that, while controlling for age and percentage of BOT re- all swallowing sequence duration differed between the 2 sected, there were significant between-group differences for groups. Individuals in the SJP group took a mean of 10.65

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©2005 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/26/2021 seconds to swallow the pudding bolus, whereas those in appetizing, resulting in an unfinished meal. Finally, pa- the control group took 20.99 seconds. tients often report that they simply become tired after eating for extended periods of time. Because cachexia is often Cookie Bolus observed in individuals who have undergone treatment for head and neck cancer,25 increased meal duration is a Means and SDs for all dependent variables are shown in clinical concern that must be addressed, especially in the Table 2. For the cookie bolus, 7 of 24 fluoroscopic stud- xerostomic patient. ies were analyzed (5 SJP and 2 control patients). Seven One limitation of the present study that must be ad- studies were excluded from the analyses because the pa- dressed is the sample size that was available for analysis tients were given water to help propel the bolus into the of swallowing related to the cookie bolus. Although power pharynx before any swallow could be initiated (4 SJP and for the results obtained for the pudding bolus was mod- 3 control patients). Ten patients were not able to com- erate, that for the analysis of the cookie bolus was low. plete a cookie swallow owing to lack of dentition or diet Future studies of solid boluses, with a greater and equal restriction (4 SJP and 6 control patients). The results did number of patients in each group, may allow for conclu- not reveal any significant differences between groups. sions that could not be drawn from this study because of small subject numbers for that consistency of food. COMMENT CONCLUSIONS Xerostomia is a devastating consequence of radiation Prevention of xerostomia in persons with head and neck therapy associated with head and neck cancer treat- cancer is of great significance to the maintenance of ment. The sequelae of xerostomia have the potential to healthy oral structures, quality of life, and ability to eat. profoundly affect many aspects of quality of life in such The SJP for submandibular gland transfer in patients with patients. Recent surgical innovation, namely, the SJP for oropharyngeal cancer appears to be successful in main- submandibular gland transfer, has provided hope in the taining salivary flow in a large number of patients. The battle against xerostomia in patients who have been treated procedure appears to be beneficial also in promoting more for oropharyngeal cancer. Reports of this procedure sug- time-efficient swallowing behaviors. This efficiency has gest that it is successful in maintaining salivary flow in a implications for a patient’s overall well-being and nutri- high percentage of individuals receiving the treatment. tional status. For the patients in this study, significant differences in salivary flow rate existed between the 2 groups. Trans- lation of the importance of the maintenance of saliva to Submitted for Publication: June 23, 2004; final revision functional outcomes after the SJP has not been de- received September 22, 2004; accepted October 21, 2004. scribed previously. The results of the present research Correspondence: Jana Rieger, PhD, Craniofacial Osseo- show that the benefits of this procedure in maintaining integration and Maxillofacial Prosthetic Rehabilitation saliva extend to swallowing outcomes. Unit, Misericordia Community Hospital, 16940–87th Ave, With respect to the pudding bolus, patients in the SJP Edmonton, Alberta, Canada T5R 4H5 (jana.rieger group were able to move the bolus through the oral cav- @ualberta.ca). ity and into the pharynx faster than patients in the con- Financial Support: This study was supported by grants trol group. Patients in the SJP group also were able to from the Alberta Heritage Foundation for Medical Re- swallow the whole bolus in half the time of patients in search and the Caritas Hospitals Foundation, Edmonton. the control group. In addition, inspection of the means Acknowledgment: We acknowledge the participation of shows that patients in the SJP group did not need to swal- the Diagnostic Imaging and Radiology Department at the low as often per bolus as did patients in the control group. Misericordia Community Hospital, Edmonton. Although no significant differences in temporal measures were found for the cookie bolus, the means sug- REFERENCES gest that oral and oropharyngeal transit differences between groups may follow a similar pattern to that of the 1. Guchelaar HJ, Vermes A, Meerwaldt JH. Radiation-induced xerostomia: patho- pudding bolus. Overall, patients who undergo the SJP ap- physiology, clinical course and supportive treatment. Support Care Cancer. 1997; pear to transport food through the mouth and into the 5:281-288. 2. Vissink A, Panders AK, Gravenmade EJ, Vermey A. The causes and conse- pharynx more efficiently than do patients who do not un- quences of hyposalivation. Ear Nose Throat J. 1988;67:166-176. dergo the procedure. 3. Hughes CV, Baum BJ, Fox PC, Marmary Y, Yen CK, Sonies BC. Oral-pharyngeal The findings from this study have significant clinical dysphagia: a common sequela of salivary gland dysfunction. Dysphagia. 1987; implications for the population of patients treated for head 1:173-177. and neck cancer. Clinical anecdotes from these patients 4. Ohrn KE, Wahlin YB, Sjoden PO. Oral status during radiotherapy and chemotherapy: a descriptive study of patient experiences and the occurrence of oral will often disclose that increased meal durations result complications. Support Care Cancer. 2001;9:247-257. in less food being consumed by them. This occurs for sev- 5. Hamburger J. Sjogren’s syndrome as seen by an oral physician. Scand J Rheu- eral reasons. First, their eating companions may finish matol Suppl. 2001;115:34-38. their meals before them, and so patients may be reluc- 6. Young W, Khan F, Brandt R, Savage N, Razek AA, Huang Q. Syndromes with salivary dysfunction predispose to tooth wear: case reports of congenital dys- tant to continue to eat for extended periods beyond their function of major salivary glands, Prader-Willi, congenital rubella, and Sjo- companions. Second, patients often report that their food gren’s syndromes. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2001; cools off during lengthy eating times and becomes un- 92:38-48.

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©2005 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/26/2021 7. Logemann JA, Smith CH, Pauloski BR, et al. Effects of xerostomia on perception of postradiation xerostomia in patients with head and neck cancer. Support Care and performance of swallow function. Head Neck. 2001;23:317-321. Cancer. 2000;8:203-208. 8. Hamlet S, Faull J, Klein B, et al. Mastication and swallowing in patients with post- 17. Jha N, Seikaly H, McGaw T, Coulter L. Submandibular salivary gland transfer pre- irradiation xerostomia. Int J Radiat Oncol Biol Phys. 1997;37:789-796. vents radiation-induced xerostomia. Int J Radiat Oncol Biol Phys. 2000;46: 9. Logemann JA, Pauloski BR, Rademaker AW, et al. Xerostomia: 12-month changes 7-11. in saliva production and its relationship to perception and performance of swal- 18. Jha N, Seikaly H, Harris J, et al. Prevention of radiation-induced xerostomia by low function, oral intake, and diet after chemoradiation. Head Neck. 2003;25: surgical transfer of submandibular salivary gland into the submental space. 432-437. Radiother Oncol. 2003;66:283-289. 10. Seikaly H, Jha N, McGaw T, Coulter L, Liu R, Oldring D. Submandibular gland 19. Seikaly H, Jha N, Barnaby P, et al. Long-term outcomes of submandibular gland transfer: a new method of preventing radiation-induced xerostomia. Laryngoscope. transfer for prevention of postradiation xerostomia. Arch Otolaryngol Head Neck 2001;111:347-352. Surg. 2004;130:956-961. 11. Specht L. Oral complications in the head and neck radiation patient: introduc- 20. Izutsu KT, Truelove EL, Bleyer WA, Anderson WM, Schubert MM, Rice JC. tion and scope of the problem. Support Care Cancer. 2002;10:36-39. Whole saliva albumin as an indicator of stomatitis in cancer therapy patients. 12. Wescott WB, Mira JG, Starcke EN, Shannon IL, Thornby JI. Alterations in whole Cancer. 1981;48:1450-1454. saliva flow rate induced by fractionated radiotherapy. AJR Am J Roentgenol. 1978; 21. Stachler RJ, Hamlet SL, Mathog RH, et al. Swallowing of bolus types by post- 130:145-149. surgical head and neck cancer patients. Head Neck. 1994;16:413-419. 13. Hughes PJ, Scott PM, Kew J, et al. Dysphagia in treated nasopharyngeal cancer. 22. Lazarus CL, Logemann JA, Pauloski BR, et al. Swallowing disorders in head and Head Neck. 2000;22:393-397. neck cancer patients treated with radiotherapy and adjuvant chemotherapy. 14. Ramirez-Amador V, Silverman S Jr, Mayer P, Tyler M, Quivey J. Candidal colo- Laryngoscope. 1996;106:1157-1166. nization and oral candidiasis in patients undergoing oral and pharyngeal radia- 23. Lof GL, Robbins J. Test-retest variability in normal swallowing. Dysphagia. 1990; tion therapy. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 1997;84:149- 4:236-242. 153. 24. Robbins J, Coyle J, Rosenbek J, Roecker E, Wood J. Differentiation of normal 15. Kies MS, Haraf DJ, Rosen F, et al. Concomitant infusional paclitaxel and fluoro- and abnormal protection during swallowing using the Penetration-Aspiration Scale. uracil, oral hydroxyurea, and hyperfractionated radiation for locally advanced squa- Dysphagia. 1999;14:228-232. mous head and neck cancer. J Clin Oncol. 2001;19:1961-1969. 25. Davis MP, Dickerson D. Cachexia and anorexia: cancer’s covert killer. Support 16. Warde P, Kroll B, O’Sullivan B, et al. A phase II study of Biotene in the treatment Care Cancer. 2000;8:180-187.

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