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Effects of Chin-Down Maneuver on the Parameters of Swallowing Function After Esophagectomy With 3-Field Lymphadenectomy Examined by Videofluoroscopy
Accepted Manuscript Effects of chin-down maneuver on the parameters of swallowing function following esophagectomy with three-field lymphadenectomy examined by videofluoroscopy Yoshihiko Kumai, MD, PhD, Naoya Yoshida, MD, PhD, Yuta Kamenosono, BSc, Keigo Matsubara, BSc, Yasuhiro Samejima, MD, PhD, Hideo Baba, MD, PhD, Eiji Yumoto, MD, PhD PII:
S0003-9993(16)31295-3
DOI:
10.1016/j.apmr.2016.11.005
Reference:
YAPMR 56736
To appear in:
ARCHIVES OF PHYSICAL MEDICINE AND REHABILITATION
Received Date: 29 July 2016 Revised Date:
26 September 2016
Accepted Date: 4 November 2016
Please cite this article as: Kumai Y, Yoshida N, Kamenosono Y, Matsubara K, Samejima Y, Baba H, Yumoto E, Effects of chin-down maneuver on the parameters of swallowing function following esophagectomy with three-field lymphadenectomy examined by videofluoroscopy, ARCHIVES OF PHYSICAL MEDICINE AND REHABILITATION (2017), doi: 10.1016/j.apmr.2016.11.005. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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Running Title: Chin-down maneuver following esophagectomy
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Effects of chin-down maneuver on the parameters of swallowing function following esophagectomy with three-field lymphadenectomy examined by videofluoroscopy
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Yoshihiko Kumai, MD, PhD: Department of Otolaryngology Head and Neck Surgery, Kumamoto University School of Medicine, Kumamoto Japan Naoya Yoshida MD, PhD: Department of Gastroenterological surgery, Kumamoto
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University Graduate School of medicine, Kumamoto Japan Yuta Kamenosono BSc: Department of Otolaryngology Head and Neck Surgery, Kumamoto University School of Medicine, Kumamoto Japan Keigo Matsubara BSc: Department of Otolaryngology Head and Neck Surgery, Kumamoto University School of Medicine, Kumamoto Japan
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Yasuhiro Samejima MD, PhD: Department of Otolaryngology Head and Neck Surgery, Kumamoto University, Graduate School of Medicine, Kumamoto Japan Hideo Baba MD, PhD: Department of Gastroenterological surgery, Kumamoto University Graduate School of medicine, Kumamoto Japan
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Eiji Yumoto, MD, PhD: Department of Otolaryngology Head and Neck Surgery, Kumamoto University School of Medicine, Kumamoto Japan This work was presented at the American Broncho-Esophagological
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Association at COSM, Boston MA April 22th, 2015 as a poster presentation. Correspondence and Reprints: Yoshihiko Kumai, MD, PhD Department of Otolaryngology Head and Neck Surgery Kumamoto University School of Medicine 860-8556 1-1-1 Honjo Kumamoto City, Kumamoto, Japan Business Phone: +81-96-373-5255, Home Phone: +81-96-371-6499 Email:[email protected] We disclose here that
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(1)Each of the authors has contributed to, read and approved this manuscript.
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(2)None of the authors has any conflict of interest, financial or otherwise.
1 ACCEPTED Chin-down maneuver MANUSCRIPT following esophagectomy
Effects of the chin-down maneuver on parameters of
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swallowing function following esophagectomy with three-field
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lymphadenectomy examined by videofluoroscopy
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Abstract
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Objectives: This study quantitatively determined the effect of the chin-down maneuver
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following esophagectomy with three-field lymphadenectomy (3FL) on pharyngeal
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residue, upper esophageal sphincter (UES) opening, and laryngeal closure.
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Design: Prospective data were collected from a pharyngeal videofluoroscopic
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swallowing study.
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Setting: Dysphagia clinics at the ENT Department of Kumamoto University Hospital.
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Participants: A total 14 patients (mean age, 65.9 y) selected according to the inclusion
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criteria from a total of 43 patients who underwent esophagectomy with 3FL at the
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Department of Gastroenterological Surgery, Kumamoto University Hospital from May
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to December 2014 were enrolled.
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Interventions: Videoflurorscopy was conducted in head- neutral and chin-down
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positions to measure the pharyngeal constriction ratio (PCR), amount of residue in the
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vallecula and pyriform sinus after the first swallow, UES opening diameter, duration of
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UES opening, and duration of laryngeal vestibule closure.
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Main Outcome Measures: The above parameters were compared statistically, between
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the neutral and chin-down positions.
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Results: In comparison with the neutral group, the PCR and residue in the pyriform
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sinus were significantly smaller in the chin-down group (p < 0.01). However, the
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residue in the vallecula did not differ significantly from that of the neutral group (p =
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0.44). The UES opening diameter, duration of UES opening, and duration of laryngeal
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vestibule closure were all significantly larger in the chin-down group than in the neutral
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group (p < 0.05).
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Conclusion: This study demonstrates that use of the chin-down maneuver after
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esophagectomy with 3FL can help expedite swallowing by strengthening pharyngeal
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constriction, widening the UES, and enhancing laryngeal closure.
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Key words: swallowing dysfunction, chin-down maneuver, esophagectomy, three-field
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lymph node dissection, pharyngeal constriction ratio, upper esophageal sphincter
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List of abbreviation
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3FL: three-field lymphadenectomy RLN: recurrent laryngeal nerve VFSS: videofluoroscopic swallowing studies
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VESS: video endoscopic swallowing study UES: upper esophageal sphincter PCR: pharyngeal constriction ratio
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Introduction
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Respiratory complications are the most common causes of postoperative death after
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esophagectomy, with postoperative pneumonia having a mortality rate of 20% 1.
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Three-field lymphadenectomy (3FL) in esophagectomy for esophageal cancer, which is
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common in Japan, is a surgical procedure to completely dissect the lymph nodes
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surrounding the recurrent laryngeal nerve (RLN) in the cervicothoracic region, an area
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in which there is a high rate of metastasis 2–4. Aspiration is a common swallowing
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abnormality in patients following this procedure because resultant factors such as RLN
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paralysis, impaired epiglottic eversion, pharyngeal paralysis, and incomplete laryngeal
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elevation 5, 6 generally result in inefficient bolus transit and impaired airway protection 7,
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In addition, 3FL has displayed a relatively high RLN paralysis rate of around 25% of all
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patients who underwent the surgical procedure 10, 11. Dumont et al. 24 studied 309
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patients who were surgically treated for esophageal cancer. They recorded 28 (9%)
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deaths that occurred within 1 month postoperatively and reported that respiratory
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complications accounted for 64% of all postoperative deaths. The postoperative
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complication rate was high (37% of their patients), with the major causes being fistulae
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(35 cases) and RLN paralysis (26 cases). These observations indicated that reducing the
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. Laryngeal penetration or aspiration has been observed in 47% 5 or 33% 9 of patients.
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occurrence of aspiration is crucial to improve the postoperative morbidity of patients
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with advanced esophageal cancer. Swallowing abnormalities following esophagectomy
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with 3FL can induce aspiration and laryngeal penetration, which arise from multiple
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pathological factors including RLN paralysis, reduced laryngeal elevation, reduced
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upper esophageal sphincter (UES) opening, and deficient airway protection due to
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insufficient eversion of the epiglottis 2-9. In the present study, a video endoscopic
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swallow study (VESS) showed a significant amount of pharyngeal residue in the
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pyriform sinus following esophagectomy with 3FL in the neutral position, and this was
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demonstrably reduced when the chin-down maneuver was used. This observation
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prompted us to focus on the modulation of pharyngeal clearance, UES opening, and
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laryngeal closure post-esophagectomy with 3FL, with or without the chin-down
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maneuver. In the rehabilitation of patients with oropharyngeal dysphagia, the chin-down
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maneuver has been widely applied to reduce the occurrence of aspiration. Previous
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videofluoroscopic swallowing studies (VFSS) demonstrated that this maneuver
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facilitated closure of the laryngeal vestibule and downward movement of the epiglottis.
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Moreover, this maneuver decreased the distance and increased the duration of contact
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between the base of the tongue and the pharyngeal wall. Therefore, the chin-down
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maneuver contributed to both airway protection and improvement of the bolus pathway
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swallowing function of post-esophagectomy patients. Lewin et al. 13 used qualitative
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VFSS to demonstrate that the chin-down maneuver is effective for patients with
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oropharyngeal dysphagia who have undergone esophagectomy with 3FL. However, in
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addition to qualitative assessment, clinicians should perform quantitative assessment,
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especially for pharyngeal residue, laryngeal closure, and modulation of (UES) opening,
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to determine the efficacy of the chin-down maneuver for such patients.
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. VFSS may provide objective documentation of the structural integrity of the
The objective of this study was to quantitatively determine the efficacy of the chin-down maneuver following esophagectomy with 3FL on pharyngeal residue, UES
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opening, and laryngeal closure. We hypothesized that pharyngeal clearance and UES
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opening would be improved and that laryngeal closure would consequently be
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guaranteed with use of the chin-down maneuver to prevent aspiration.
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Materials and Methods
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A total of 43 patients underwent esophagectomy with lymphadenectomy at the
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Department of Gastroenterological Surgery, Kumamoto University Hospital from May
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to December 2014. Esophagectomy was defined in the present study as esophagectomy
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with lymphadenectomy requiring chest manipulation. When tumors were located in the
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upper or middle thoracic esophagus, 3FL was performed. Cervical lymph node
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dissection was omitted for lower esophageal tumors, and when the tumor depth was
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within clinical stage T1. The exclusion criteria for this study were as follows:
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performance of two-field lymphadenectomy (2FL, n=4), refusal to participants in VFSS
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(n = 8), previous glossectomy for tongue cancer (n = 1), tracheotomy during the
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perioperative period (n = 1), performance of the chin-down maneuver by the patient
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themselves at the time of the VFSS (n = 5), discharge within 12 postoperative
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days(meaning the patient was not able to undergo VFSS ;n = 6), esophageal
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reconstruction performed using the colon not the gastric tube as was the case in all other
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patients (n=1), and late postoperative VFSS at 22 days (n =2) and 34 days (n =1)
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because of respiratory complications in two patients and anastomotic leakage in one
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patient. Twenty-nine patients were therefore excluded from the study. Consequently,
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fourteen patients (all males) were enrolled in the study. Table I shows the characteristics
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of the enrolled patients including age, tumor location, tumor stage, , RLN paralysis and
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postoperative days of the VFSS. .All patients were male, did not receive radiation
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therapy to the neck, received retrosternal route reconstruction with gastric tube after
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subtotal esophagectomy with a cervical anastomotic site, and showed neither
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anastomotic leakage nor anastomotic stenosis as complications.
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At one week postoperatively, gastroenterologists routinely performed VFSS to
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identify anastomotic leakage and aspiration. If no major problems were found, patients
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were allowed to begin oral food intake after the examination. Following approval by the
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institutional review board (Study No. 1359) of our institution, VFSS in these 14 patients
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(mean age ± standard deviation, 65.9 ± 1.9 y) were performed prospectively at the
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Department of Otolaryngology–Head and Neck Surgery, Kumamoto University
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Hospital. Prior to the VFSS, the patients underwent a VESS to examine the presence of
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RLN paralysis, penetration, and aspiration by an ENT surgeon. VFSS were performed
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using radiographic equipment (collimator type R-50 model; Shimadzu Corp Medical
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Systems, Tokyo, Japan) by two speech pathologists and a board-certified
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otolaryngologist subspecializing in dysphagia. VFSS were conducted in the lateral
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projection, with the patient in the upright position. A 120% barium sulfate suspension
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was administered as a 3- or 5-mm bolus in a cup or syringe (n = 12). If aspiration was
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detected in the VESS, iopamiron was administered as a 3- or 5-mL bolus in a cup or
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syringe (n = 2). Before the actual swallow for the VFSS, we first asked the patients to
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swallow “naturally” without any specific instruction, stating “Please swallow with your
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neck in a comfortable position, as normal.” We then instructed them on how to perform
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the chin-down maneuver with the following command: “First, please bend only your
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neck forward as if taking a bow, and then swallow in that position.” During the actual
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swallow, we monitored whether they could hold the barium or iopamiron orally for a
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few seconds and then swallow in the correct position, as instructed. Procedures were
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always performed with the head in a neutral position first and then in the chin-down
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position with a single swallow for each position. In addition, to clear the residue from
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the neutral position, patients were asked to drink a cup of water before moving to the
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chin-down position for swallowing.
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We undertook the following steps to analyze the images from the VFSS. First, we
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recorded movies of the VFSS with each maneuver in the lateral view using a Mini DV
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(Mini DV & S-VHS dual format SR-VS30; Victor Company of Japan Ltd., Yokohama, Japan). Second, we connected the digital video camera (DCR-HC90; Sony, Tokyo,
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Japan) containing the Mini DV to a personal computer (dc7800MT-E6850/Windows
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XP; HP Inc., Palo Alto, CA, USA) with IEEE 1394 cables. Following this, data
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recorded by the Mini DV were converted into AVI format with video editing software
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(Corel Video Studio 12; E Frontier, Inc., Tokyo, Japan). The data comprised 30 frames
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per second. We then randomly selected 44 recoded data (22 × 2 maneuvers). Finally, we
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assessed the usefulness of these selected movies with a digitized video imaging
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software program (DIPP Motion Pro 2D; Ditect, Tokyo, Japan) and evaluated the
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swallowing function after the first swallow. Details of the examination procedures were
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described in our previous paper 14. We performed quantitative assessment using four parameters for the modulation of the oropharyngeal swallowing function in both the neutral and chin-down positions.
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Before analysis, a calibration marker (a coin of 23.5-mm diameter) was positioned on
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the lateral neck. To compensate for the varied magnification images among the patients,
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the marker length was measured in millimeters and adjusted to be the same value
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among the patients. The four parameters were as follows:
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• The pharyngeal constriction ratio (PCR), which was calculated by dividing the pharyngeal area at the point of maximum constriction during a swallow (neutral position, Fig. 1A; chin-down, Fig. 1B) by the area with a 1-mL bolus
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held in the oral cavity (Fig. 1C). The PCR appeared to be a valid objective
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surrogate measure of the strength of pharyngeal constriction 15.
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• The areas of pharyngeal residue in the vallecula and pyriform sinus,
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respectively (in units of mm2) (Fig. 2). These areas represent the clearance of pharyngeal residue. To clear the residue from the neutral position, patients
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were asked to drink a cup of water before moving to the the chin-down
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position for swallowing.
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• The UES opening diameter (in units of mm) (Fig. 3) and the duration of UES opening
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level of the sub-vocal fold (following the method described in Kumakura’s
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paper 16, the Y axis was drawn from the anterior and superior tip of the third
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cervical vertebra to the anterior and inferior tip of the fifth cervical vertebra,
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and the X axis was drawn orthogonal to the Y axis at the level of the anterior
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and inferior border of the thyroid cartilage. The length of the white bar at the
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sub-vocal fold level on the x axis was calculated as the UES opening diameter.
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(Fig. 3). The duration of UES opening was calculated by dividing the number
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of image frames by 30 (because 1 sec included 30 frames). These parameters
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represent the smoothness of the bolus passage at the UES. The first frame was
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taken when the tip of the barium or iopamiron reached the UES before its
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opening, and the last frame was taken when the UES had just closed after the
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(in units of sec). The UES opening diameter was calculated at the
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barium or iopamiron passed through the UES.
• The duration of laryngeal vestibule closure (in units of sec), which was defined
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as the duration of contact between the tip of the arytenoid and the base of the
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epiglottis during the first swallow and was calculated using the same method
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as that used for the duration of UES opening. A longer duration of laryngeal
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vestibule closure suggests that aspiration is unlikely to occur. Figure. 4 shows
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before (Fig. 4A) and during (Fig. 4B) contact of the two structures. Among the fourteen patients who underwent VFSS, two (14.2%) demonstrated
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aspiration in the neutral position. As the amount of aspirated barium or iopamiron could
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not be calculated precisely, these patients were excluded from the calculation of the area
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of the vallecula, area of the pyriform sinus, and duration of laryngeal vestibule closure.
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These two patients received jelly alone as an oral diet with compensation by tube
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feeding. However, the remaining twelve patients tolerated a full oral diet of rice
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porridge at the time of the VFSS without dysphagia after postoperative week 1. One
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patient who demonstrated aspiration during VESS but not during the VFSS was,
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however, included in the evaluation of these three parameters. Evaluation was repeated
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on different days by a single speech pathologist with a wealth of experience in rating
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VFSS. The intra-rater reliability of each parameter was examined using an intra-rater
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correlation coefficient between each pair of data obtained on different days. The
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inter-rater reliability of each parameter was examined using an inter-rater correlation
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coefficient between each pair of data evaluated by two speech pathologists and a
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board-certified otolaryngologist subspecializing in dysphagia. Each parameter was
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averaged among the three raters and statistically compared between the neutral and
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chin-down positions using a paired t-test. (p<0.05 was taken to indicate statistical
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significance).
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Results
All patients enrolled in the present study underwent retrosternal route reconstruction
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using a gastric tube (all anastomosis sites were in the cervical lesion) after subtotal
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esophagectomy with 3L without preoperative radiation therapy to the neck. None of the
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patients demonstrated any major complications such as respiratory complications,
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anastomotic leakage or anastomotic stenosis. Six patients (42.9%) exhibited unilateral
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vocal fold paralysis. Bilateral vocal fold paralysis was not present in any patient. The
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period between surgery and the VFSS ranged from 12 to 16 days (14.8 ± 0.4 days).
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The intra-rater correlation coefficient of each parameter was 0.78 to 0.95 (p < 0.01),
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and the inter-rater correlation coefficient of each parameter was 0.76 to 0.96 (p < 0.01),
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which demonstrated consistency in the evaluation of the 2D VFSS images. The value of
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each of the parameters (mean ± standard deviation) and the presence or absence of the
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significant difference between neutral and chin-down positions for each parameter,
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t-value, degree of freedom, effect sizes and exact p-value are shown in Table II. The
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PCR and residue in the pyriform sinus for the chin-down position were significantly
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smaller than those in the neutral position (p < 0.01). However, the residue in the
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vallecula was not significantly different between the neutral and chin-down positions (p
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= 0.44). The UES opening diameter, duration of UES opening and duration of laryngeal
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vestibule closure in the chin-down position were all significantly prolonged compared
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with those in the neutral position (p < 0.05).
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Discussion
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The chin-down, or chin-tuck, maneuver is widely used to reduce the occurrence of
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aspiration and is effective for various dysphagic populations. Okada et al. 17 stated that
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in consideration of both biomechanics and functional anatomy, flexion and extension
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movements of the cervical spine involve coordinated motions in two anatomical areas:
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the occipito-atlanto (C1)-axial (C2) complex and the lower cervical (C2-C7) region.
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Flexion of the occipito-atlanto and atlanto-axial joints is referred to as flexion of the
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head at the neck (head flexion [HF]), whereas flexion of the lower cervical region is
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termed neck flexion (NF) 18. A previous Japanese article 19 pointed out that NF is a very
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physiologically natural position; on the other hand, HF compresses the pharyngeal
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cavity in the anterior-to-posterior direction, which helps to increase the pharyngeal
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pressure and restricts mobility of the epiglottis. Our previous study 20 and McCulloch's
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group demonstrated that in young healthy adults (different from the older
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esophagecomized patients in the present study), the NF maneuver resulted in
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significantly decreased pressure and a longer duration of lowered pressure at the UES
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without modulation of pharyngeal pressure, which may have been due to compensated
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laryngeal elevation in the anterior-superior direction combined with consequent UES
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opening by NF, thus assisting bolus passage through the UES. Therefore, in the
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present study, we used NF as the chin-down maneuver.
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Pearson et al. 21 demonstrated that the accurate quantification of post-swallow
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pharyngeal residue is an important clinical challenge that is limited by currently available methods such as the perceptual method, the three-point ordinal scale 22 and
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quantitative computer-based measurement of post-swallow pharyngeal residue, and the
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vallecula residue ratio 23. These papers demonstrated that experienced VFSS raters
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might be able to enhance the calculation of the area of pharyngeal residue using the true
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amount of pharyngeal residue. However, the accuracy of the quantitative measurement
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of pharyngeal residue using 2D VFSS still images in the present study was limited. With
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respect to this limitation, we validated the quantitative measurement of the area outlined
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in the lateral view of the VFSS still image by calculating inter- and intra-rater
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correlation coefficients, which were all found to be in the excellent range (0.76–0.96),
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demonstrating high consistency and stability in the evaluation. Leonard et al. 15 demonstrated that there was a high inverse correlation between the
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PCR and peak pharyngeal pressure, suggesting that the PCR (normal range, within 0.25)
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appears to be a valid objective surrogate measure of pharyngeal strength and, moreover,
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that decreased pharyngeal constriction contributes to an increased prevalence of
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aspiration 15, 25. The present study demonstrated that the chin-down maneuver
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significantly decreased the PCR and pharyngeal residue in the pyriform sinus rather
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than in the vallecula, suggesting that this maneuver has a positive effect on the
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reduction of post-swallow aspiration of residue in the pyriform sinus in postoperative
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patients with advanced esophageal cancer.
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Yasuda et al. 26 demonstrated that swallowing dysfunctions in patients who have
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undergone esophagectomy with 3FL might be caused by the defective relaxation of
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scarred sternohyoid and sternothyroid muscles during the pharyngeal phase. They stated
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that both muscles were subjected to considerable damage in cervical LN dissection
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because of retraction and partial division to allow visualization of the cervicothoracic
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area. Postoperatively, these muscles predictably become scarred, and these scarred
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fibers might work antagonistically against laryngeal elevation 26. Swallowing
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dysfunction following esophagectomy has also been thought to result from inadvertent
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damage to the pharyngeal plexus 26. Although we did not directly investigate the
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modulation of hyoid and laryngeal elevation, as Steel et al. 27 demonstrated previously,
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reductions in anterior hyoid and laryngeal movement are associated with an increased
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risk of penetration–aspiration and post-swallow residues in patients who have
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undergone esophagectomy with 3FL. Bülow et al. 12 reported that the chin-down
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maneuver significantly narrowed the distance between the mandible and hyoid bone
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(i.e., hyoid excursion with relative descent of the mandible). Previous papers have noted
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that sub-atmospheric pressure acts as a hypopharyngeal suction pump and that it is
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necessary for adequate bolus transport 28, 29. The present study demonstrated that the
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chin-down maneuver worked positively to promote not only the duration of UES
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opening but also UES opening. Moreover, the maneuver worked to increase the duration
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of laryngeal closure. Taken together, these three parameters suggest that the chin-down
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maneuver promotes widening of the UES, possibly by narrowing the distance between
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the mandible and hyoid bone which can compensate laryngeal elevation in the
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anterior-superior direction combined with consequent UES opening and increasing
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greater sub-atmospheric pressure in the UES, consequently improving bolus passage.
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This process definitely helps to decrease pharyngeal residue and reduce aspiration with
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laryngeal closure. As patients that underwent esophagectomy with 3FL had impaired
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laryngeal elevation during swallowing due to chest manipulation, the chin-down
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maneuver may be helpful especially as temporary compensation until the patient fully
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recovered from surgery.
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Study Limitations
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VFSS were conducted in the lateral projection alone as all parameters except the
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areas of pharyngeal residue (vallecula and pyriform sinus) must be measured in the
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lateral position, and not in the anterior-posterior position. Therefore, we were unable to
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compare the area of pharyngeal residue between right and left sides. Moreover, this
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study had additional limitations, including the relative short evaluation period, lack of
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follow-up, the relatively small number of patients, and lack of females included in the
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study population.
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Conclusion
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The chin-down maneuver after esophagectomy with 3FL might help expedite the
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ability to swallow by increasing pharyngeal constriction, minimizing pharyngeal residue,
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widening the UES, and enhancing laryngeal closure.
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References 1. Atkins BZ, Shah AS, Hutcheson KA et al. Reducing hospital morbidity and
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mortality following esophagectomy. Ann Thorac Surg. 2004; 78:1170-6.
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cancer of the thoracic esophagus. Ann Surg.1994; 220:364–373
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2. Akiyama H, Tsurumaru M, Udagawa H et al. Radical lymph node dissection for
3. Fujita H, Kakegawa T, Yamana H et al. Lymph node metastasis and recurrence in
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patients with a carcinoma of the thoracic esophagus who underwent three-field
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dissection. World J Surg.1994; 18:266–272
4. Altorki N, Kent M, Ferrara C et al. Three-field lymph node dissection for
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squamous cell and adenocarcinoma of the esophagus. Ann Surg.2002;
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236:177–183
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5. Heitmiller RF, Jones B. Transient diminished airway protection after transhiatal esophagectomy. Am J Surg. 1991;162:442-6
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6. Gandhi SK, Naunheim KS. Complications of transhiatal esophagectomy. Chest Surg Clin N Am. 1997;7:601-10
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7. Ekberg O, Nylander G. Pharyngeal dysfunction after treatment for pharyngeal
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cancer with surgery and radiotherapy. Gastrointest Radiol. 1983;8:97-104
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8. Hambraeus GM, Ekberg O, Fletcher R. Pharyngeal dysfunction after total and
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1
2
subtotal oesophagectomy. Acta Radiol. 1987; 28:409-13. 9. Leder SB, Bayar S, Sasaki CT et al. Fiberoptic endoscopic evaluation of swallowing in assessing aspiration after transhiatal esophagectomy. J Am Coll
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Surg 2007; 205:581–585
10. Kinugasa S, Tachibana M, Yoshimura H et al. Postoperative pulmonary
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complications are associated with worse shortand long-term outcomes after
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extended esophagectomy. J Surg Oncol 2004;88:71–77
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11. Fang WT, Chen WH, Chen Y Jiang Y. Selective three field lymphadenectomy for
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thoracic esophageal squamous carcinoma. Dis Esophagus 2007; 20:206–211 12. Bülow M, Olsson R, Ekberg O. Videomanometric analysis of supraglottic
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swallow, effortful swallow, and chin tuck in patients with pharyngeal dysfunction.
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Dysphagia. 2001; 16:190-5.
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13. Lewin J, Hebert T, Putnam J Jr et al. Experience with the chin tuck maneuver in
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postesophagectomy aspirators. Dysphagia. 2001; 16:216-9.
14. Narajos N, Samejima Y, Kumai Y et al. Postdeglutitive residue in idiopathic
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unilateral vocal fold paralysis: a quantitative videofluoroscopic study.
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Laryngoscope. 2013; 123:2776-9.
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15. Leonard R, Belafsky PC, Rees CJ. Relationship between fluoroscopic and
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manometric measures of pharyngeal constriction: the pharyngeal constriction
2
ratio. Ann Otol Rhinol Laryngol. 2006; 115:897-901. 16. Kumakura M, Baba T, Dozono K. The effect of tongue position during swallow
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on the mobility of hyoid bone, larynx and on the opening of upper esophageal
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sphincter. Japanese journal of Dysphagia Rehabilitation. 2011; 15:
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165-173.(Japanese article)
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17. Okada S, Saitoh E, Palmer JB et al. What is the chin-down posture? A
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questionnaire survey of speech language pathologists in Japan and the United
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States. Dysphagia. 2007; 22:204-9.
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of manual examination.7th ed: 2002, W.B.Saunders:Philadelphia 19. Official publication of the Japanese society of dysphagia rehabilitation. Summary
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18. Hislop HJ, Montgomery J. Daniels and Worthigham’s muscle testing: techniques
of the training method .The Japanese journal of dysphagia rehabilitation.
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2014;18:55-89
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20. Matsubara K, Kumai Y, Kamenosono Y et al. Effect of three different chin-down
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maneuvers on swallowing pressure in healthy young adults. Laryngoscope. 2015
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Aug 12.
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21. Pearson WG Jr, Molfenter SM, Smith ZM et al.
Image-based measurement of
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post-swallow residue: the normalized residue ratio scale. Dysphagia.
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2013;28:167-77 22. Rosenbek JC, Roecker EB, Wood JL. Thermal application reduces the duration of
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stage transition in dysphagia after stroke. Dysphagia. 1996;11:225–33
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23. Dyer JC, Leslie P, Drinnan MJ. Objective computer-based assessment of
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valleculae residue: Is it useful? Dysphagia.2008;23:7–15.
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24. Dumont P, Wihlm JM, Hentz JG et al. Respiratory complications after surgical
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treatment of esophageal cancer. A study of 309 patients according to the type of
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resection. Eur J Cardiothorac Surg. 1995;9:539-43
25. Easterling CS, Bousamra M, Lang IM et al. Pharyngeal dysphagia in
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postesophagectomy patients: correlation with deglutitive biomechanics. Ann
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Thorac Surg. 2000; 69:989-92.
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15
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26. Yasuda T, Yano M, Miyata H et al. Evaluation of dysphagia and diminished
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airway protection after three-field esophagectomy and a remedy. World J Surg. 2013; 37:416-23.
27. Steele CM, Bailey GL, Chau T et al. The relationship between hyoid and
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laryngeal displacement and swallowing impairment. Clin Otolaryngol. 2011;
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36:30-6.
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3
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28. McConnel FM. Analysis of pressure generation and bolus transit during pharyngeal swallowing. Laryngoscope 1988; 98:71-78. 29. Cook IJ, Dodds WJ, Dantas RO et al. Opening mechanisms of the human upper esophageal sphincter. Am J Physiol 1989; 257: 748-59.
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23 ACCEPTED Chin-down maneuver MANUSCRIPT following esophagectomy
Suppliers
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a. collimator type R-50 model; Shimadzu Corporation Medical Systems, Tokyo, Japan
3
b. Mini DV : Mini DV & S-VHS dual format SR-VS30; Victor Company of Japan Ltd.,
4
Yokohama, Japan
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c. Digital video camera (DCR-HC90; Sony, Tokyo, Japan)
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d. Personal computer (dc7800MT-E6850/Windows XP; HP Inc., Palo Alto, CA, USA)
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e. Video editing software (Corel Video Studio 12; E Frontier, Inc., Tokyo, Japan).
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f. Digitized video imaging software program (DIPP Motion Pro 2D; Ditect, Tokyo,
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Japan)
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Figure legends
2
Figure 1 Pharyngeal constriction ratio (PCR)
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The pharyngeal constriction ratio (PCR) was calculated by dividing the pharyngeal area
4
at the point of maximum constriction during a swallow in the neutral position (A) or
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chin-down position (B) by the area with a 1-mL bolus held in the oral cavity (C).
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Figure 2 Area of pharyngeal residue in the pyriform sinus and vallecula,
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The area of pharyngeal residue in the pyriform sinus and vallecula, surrounded by a
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white line, was measured in the lateral view of the still VFSS images using a digitized video imaging software program (DIPP Motion Pro 2D; Tokyo, Japan) (units: mm2).
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Figure 3 Upper Esophagus Sphincter opening diameter
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The UES opening diameter (length of the white portion) (units: mm) was measured at
14
the level of the sub-vocal fold (the Y axis was drawn from the anterior and superior tip
15
of the third cervical vertebra to the anterior and inferior tip of the fifth vertebra). The X
16
axis was drawn, orthogonal to the Y axis, at the level of the anterior and inferior border
17
of the thyroid cartilage.
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Figure 4 Duration of laryngeal vestibule closure The duration of laryngeal vestibule
2
closure (units: sec), which was defined as the duration of contact between the tip of the
3
arytenoids and the base of the epiglottis during the first swallow, was calculated by
4
dividing the number of image frames by 30 (because 1 sec included 30 frames). (A)
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Before and (B) during contact of the two structures.
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The English in this document has been checked by at least two professional editors, both
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native speakers of English.
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Table 1 Characteristics of the enrolled patients
Tumor
Tumor
RLN
Day of VFSS
Location
Stage
paralysis
(days)
73
M～L
III
-
16
2
58
M～L
III
-
16
3
65
M
III
+
15
4
71
M～L
III
+
13
5
69
U～M
IVa
-
16
6
73
M
II
-
15
7
57
M～L
III
-
16
8
61
M
II
-
15
9
71
U～M
II
+
16
10
76
M
III
+
15
11
60
M
III
+
16
12
53
M
III
-
13
70
M
III
+
14
65
M
III
-
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13
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Sex: M: Male, Location: U: Upper, M: Middle, L: Lower
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RLN: recurrent laryngeal nerve
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Age
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Table 2 Each value of the parameters and the presence or absence of the significant ACCEPTED MANUSCRIPT difference between neutral and chin-down positions for each parameter
parameters
Neutral
Chin-down
P-value
t-value
degree
effect
of
sizes
freedom 0.21 ±0.10
0.17 ±0.09
P=0.007
0
14
0.42
Residue in the vallecula
60.52 ±37.15
59.05 ±36.88
P=0.442
0
14
0.04
70.31 ±55.98
40.86 ±58.55
P=0.001
UESD mm(mean ± SD)
6.01 ±2.43
8.04 ±1.87
P=0.003
DUES second(mean ± SD)
0.43 ±0.13
0.48 ±0.06
P=0.006
DLVC second(mean ±
0.37 ±0.21
0.51 ±0.20
2
mm (mean ± SD) Residue in the pyriform 2
P=0.038
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SD)
0
14
3.18
0
14
0.94
0
14
0.49
0
14
0.68
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sinus mm (mean ± SD)
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PCR ratio(mean ± SD)
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S0003-9993(16)31295-3
DOI:
10.1016/j.apmr.2016.11.005
Reference:
YAPMR 56736
To appear in:
ARCHIVES OF PHYSICAL MEDICINE AND REHABILITATION
Received Date: 29 July 2016 Revised Date:
26 September 2016
Accepted Date: 4 November 2016
Please cite this article as: Kumai Y, Yoshida N, Kamenosono Y, Matsubara K, Samejima Y, Baba H, Yumoto E, Effects of chin-down maneuver on the parameters of swallowing function following esophagectomy with three-field lymphadenectomy examined by videofluoroscopy, ARCHIVES OF PHYSICAL MEDICINE AND REHABILITATION (2017), doi: 10.1016/j.apmr.2016.11.005. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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Running Title: Chin-down maneuver following esophagectomy
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Effects of chin-down maneuver on the parameters of swallowing function following esophagectomy with three-field lymphadenectomy examined by videofluoroscopy
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Yoshihiko Kumai, MD, PhD: Department of Otolaryngology Head and Neck Surgery, Kumamoto University School of Medicine, Kumamoto Japan Naoya Yoshida MD, PhD: Department of Gastroenterological surgery, Kumamoto
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University Graduate School of medicine, Kumamoto Japan Yuta Kamenosono BSc: Department of Otolaryngology Head and Neck Surgery, Kumamoto University School of Medicine, Kumamoto Japan Keigo Matsubara BSc: Department of Otolaryngology Head and Neck Surgery, Kumamoto University School of Medicine, Kumamoto Japan
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Yasuhiro Samejima MD, PhD: Department of Otolaryngology Head and Neck Surgery, Kumamoto University, Graduate School of Medicine, Kumamoto Japan Hideo Baba MD, PhD: Department of Gastroenterological surgery, Kumamoto University Graduate School of medicine, Kumamoto Japan
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Eiji Yumoto, MD, PhD: Department of Otolaryngology Head and Neck Surgery, Kumamoto University School of Medicine, Kumamoto Japan This work was presented at the American Broncho-Esophagological
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Association at COSM, Boston MA April 22th, 2015 as a poster presentation. Correspondence and Reprints: Yoshihiko Kumai, MD, PhD Department of Otolaryngology Head and Neck Surgery Kumamoto University School of Medicine 860-8556 1-1-1 Honjo Kumamoto City, Kumamoto, Japan Business Phone: +81-96-373-5255, Home Phone: +81-96-371-6499 Email:[email protected] We disclose here that
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(1)Each of the authors has contributed to, read and approved this manuscript.
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(2)None of the authors has any conflict of interest, financial or otherwise.
1 ACCEPTED Chin-down maneuver MANUSCRIPT following esophagectomy
Effects of the chin-down maneuver on parameters of
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swallowing function following esophagectomy with three-field
3
lymphadenectomy examined by videofluoroscopy
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Abstract
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Objectives: This study quantitatively determined the effect of the chin-down maneuver
6
following esophagectomy with three-field lymphadenectomy (3FL) on pharyngeal
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residue, upper esophageal sphincter (UES) opening, and laryngeal closure.
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Design: Prospective data were collected from a pharyngeal videofluoroscopic
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swallowing study.
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Setting: Dysphagia clinics at the ENT Department of Kumamoto University Hospital.
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Participants: A total 14 patients (mean age, 65.9 y) selected according to the inclusion
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criteria from a total of 43 patients who underwent esophagectomy with 3FL at the
13
Department of Gastroenterological Surgery, Kumamoto University Hospital from May
14
to December 2014 were enrolled.
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Interventions: Videoflurorscopy was conducted in head- neutral and chin-down
16
positions to measure the pharyngeal constriction ratio (PCR), amount of residue in the
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vallecula and pyriform sinus after the first swallow, UES opening diameter, duration of
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UES opening, and duration of laryngeal vestibule closure.
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2 ACCEPTED Chin-down maneuver MANUSCRIPT following esophagectomy
Main Outcome Measures: The above parameters were compared statistically, between
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the neutral and chin-down positions.
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Results: In comparison with the neutral group, the PCR and residue in the pyriform
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sinus were significantly smaller in the chin-down group (p < 0.01). However, the
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residue in the vallecula did not differ significantly from that of the neutral group (p =
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0.44). The UES opening diameter, duration of UES opening, and duration of laryngeal
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vestibule closure were all significantly larger in the chin-down group than in the neutral
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group (p < 0.05).
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Conclusion: This study demonstrates that use of the chin-down maneuver after
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esophagectomy with 3FL can help expedite swallowing by strengthening pharyngeal
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constriction, widening the UES, and enhancing laryngeal closure.
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Key words: swallowing dysfunction, chin-down maneuver, esophagectomy, three-field
13
lymph node dissection, pharyngeal constriction ratio, upper esophageal sphincter
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List of abbreviation
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3FL: three-field lymphadenectomy RLN: recurrent laryngeal nerve VFSS: videofluoroscopic swallowing studies
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VESS: video endoscopic swallowing study UES: upper esophageal sphincter PCR: pharyngeal constriction ratio
3 ACCEPTED Chin-down maneuver MANUSCRIPT following esophagectomy
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Introduction
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Respiratory complications are the most common causes of postoperative death after
3
esophagectomy, with postoperative pneumonia having a mortality rate of 20% 1.
5
Three-field lymphadenectomy (3FL) in esophagectomy for esophageal cancer, which is
6
common in Japan, is a surgical procedure to completely dissect the lymph nodes
7
surrounding the recurrent laryngeal nerve (RLN) in the cervicothoracic region, an area
8
in which there is a high rate of metastasis 2–4. Aspiration is a common swallowing
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abnormality in patients following this procedure because resultant factors such as RLN
10
paralysis, impaired epiglottic eversion, pharyngeal paralysis, and incomplete laryngeal
11
elevation 5, 6 generally result in inefficient bolus transit and impaired airway protection 7,
12
8
13
In addition, 3FL has displayed a relatively high RLN paralysis rate of around 25% of all
14
patients who underwent the surgical procedure 10, 11. Dumont et al. 24 studied 309
15
patients who were surgically treated for esophageal cancer. They recorded 28 (9%)
16
deaths that occurred within 1 month postoperatively and reported that respiratory
17
complications accounted for 64% of all postoperative deaths. The postoperative
18
complication rate was high (37% of their patients), with the major causes being fistulae
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(35 cases) and RLN paralysis (26 cases). These observations indicated that reducing the
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. Laryngeal penetration or aspiration has been observed in 47% 5 or 33% 9 of patients.
4 ACCEPTED Chin-down maneuver MANUSCRIPT following esophagectomy
occurrence of aspiration is crucial to improve the postoperative morbidity of patients
2
with advanced esophageal cancer. Swallowing abnormalities following esophagectomy
3
with 3FL can induce aspiration and laryngeal penetration, which arise from multiple
4
pathological factors including RLN paralysis, reduced laryngeal elevation, reduced
5
upper esophageal sphincter (UES) opening, and deficient airway protection due to
6
insufficient eversion of the epiglottis 2-9. In the present study, a video endoscopic
7
swallow study (VESS) showed a significant amount of pharyngeal residue in the
8
pyriform sinus following esophagectomy with 3FL in the neutral position, and this was
9
demonstrably reduced when the chin-down maneuver was used. This observation
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prompted us to focus on the modulation of pharyngeal clearance, UES opening, and
11
laryngeal closure post-esophagectomy with 3FL, with or without the chin-down
12
maneuver. In the rehabilitation of patients with oropharyngeal dysphagia, the chin-down
13
maneuver has been widely applied to reduce the occurrence of aspiration. Previous
14
videofluoroscopic swallowing studies (VFSS) demonstrated that this maneuver
15
facilitated closure of the laryngeal vestibule and downward movement of the epiglottis.
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Moreover, this maneuver decreased the distance and increased the duration of contact
17
between the base of the tongue and the pharyngeal wall. Therefore, the chin-down
18
maneuver contributed to both airway protection and improvement of the bolus pathway
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12
2
swallowing function of post-esophagectomy patients. Lewin et al. 13 used qualitative
3
VFSS to demonstrate that the chin-down maneuver is effective for patients with
4
oropharyngeal dysphagia who have undergone esophagectomy with 3FL. However, in
5
addition to qualitative assessment, clinicians should perform quantitative assessment,
6
especially for pharyngeal residue, laryngeal closure, and modulation of (UES) opening,
7
to determine the efficacy of the chin-down maneuver for such patients.
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. VFSS may provide objective documentation of the structural integrity of the
The objective of this study was to quantitatively determine the efficacy of the chin-down maneuver following esophagectomy with 3FL on pharyngeal residue, UES
10
opening, and laryngeal closure. We hypothesized that pharyngeal clearance and UES
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opening would be improved and that laryngeal closure would consequently be
12
guaranteed with use of the chin-down maneuver to prevent aspiration.
13
Materials and Methods
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A total of 43 patients underwent esophagectomy with lymphadenectomy at the
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Department of Gastroenterological Surgery, Kumamoto University Hospital from May
17
to December 2014. Esophagectomy was defined in the present study as esophagectomy
18
with lymphadenectomy requiring chest manipulation. When tumors were located in the
19
upper or middle thoracic esophagus, 3FL was performed. Cervical lymph node
6 ACCEPTED Chin-down maneuver MANUSCRIPT following esophagectomy
dissection was omitted for lower esophageal tumors, and when the tumor depth was
2
within clinical stage T1. The exclusion criteria for this study were as follows:
3
performance of two-field lymphadenectomy (2FL, n=4), refusal to participants in VFSS
4
(n = 8), previous glossectomy for tongue cancer (n = 1), tracheotomy during the
5
perioperative period (n = 1), performance of the chin-down maneuver by the patient
6
themselves at the time of the VFSS (n = 5), discharge within 12 postoperative
7
days(meaning the patient was not able to undergo VFSS ;n = 6), esophageal
8
reconstruction performed using the colon not the gastric tube as was the case in all other
9
patients (n=1), and late postoperative VFSS at 22 days (n =2) and 34 days (n =1)
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because of respiratory complications in two patients and anastomotic leakage in one
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patient. Twenty-nine patients were therefore excluded from the study. Consequently,
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fourteen patients (all males) were enrolled in the study. Table I shows the characteristics
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of the enrolled patients including age, tumor location, tumor stage, , RLN paralysis and
14
postoperative days of the VFSS. .All patients were male, did not receive radiation
15
therapy to the neck, received retrosternal route reconstruction with gastric tube after
16
subtotal esophagectomy with a cervical anastomotic site, and showed neither
17
anastomotic leakage nor anastomotic stenosis as complications.
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At one week postoperatively, gastroenterologists routinely performed VFSS to
7 ACCEPTED Chin-down maneuver MANUSCRIPT following esophagectomy
identify anastomotic leakage and aspiration. If no major problems were found, patients
2
were allowed to begin oral food intake after the examination. Following approval by the
3
institutional review board (Study No. 1359) of our institution, VFSS in these 14 patients
4
(mean age ± standard deviation, 65.9 ± 1.9 y) were performed prospectively at the
5
Department of Otolaryngology–Head and Neck Surgery, Kumamoto University
6
Hospital. Prior to the VFSS, the patients underwent a VESS to examine the presence of
7
RLN paralysis, penetration, and aspiration by an ENT surgeon. VFSS were performed
8
using radiographic equipment (collimator type R-50 model; Shimadzu Corp Medical
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Systems, Tokyo, Japan) by two speech pathologists and a board-certified
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otolaryngologist subspecializing in dysphagia. VFSS were conducted in the lateral
11
projection, with the patient in the upright position. A 120% barium sulfate suspension
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was administered as a 3- or 5-mm bolus in a cup or syringe (n = 12). If aspiration was
13
detected in the VESS, iopamiron was administered as a 3- or 5-mL bolus in a cup or
14
syringe (n = 2). Before the actual swallow for the VFSS, we first asked the patients to
15
swallow “naturally” without any specific instruction, stating “Please swallow with your
16
neck in a comfortable position, as normal.” We then instructed them on how to perform
17
the chin-down maneuver with the following command: “First, please bend only your
18
neck forward as if taking a bow, and then swallow in that position.” During the actual
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8 ACCEPTED Chin-down maneuver MANUSCRIPT following esophagectomy
swallow, we monitored whether they could hold the barium or iopamiron orally for a
2
few seconds and then swallow in the correct position, as instructed. Procedures were
3
always performed with the head in a neutral position first and then in the chin-down
4
position with a single swallow for each position. In addition, to clear the residue from
5
the neutral position, patients were asked to drink a cup of water before moving to the
6
chin-down position for swallowing.
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We undertook the following steps to analyze the images from the VFSS. First, we
8
recorded movies of the VFSS with each maneuver in the lateral view using a Mini DV
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(Mini DV & S-VHS dual format SR-VS30; Victor Company of Japan Ltd., Yokohama, Japan). Second, we connected the digital video camera (DCR-HC90; Sony, Tokyo,
11
Japan) containing the Mini DV to a personal computer (dc7800MT-E6850/Windows
12
XP; HP Inc., Palo Alto, CA, USA) with IEEE 1394 cables. Following this, data
13
recorded by the Mini DV were converted into AVI format with video editing software
14
(Corel Video Studio 12; E Frontier, Inc., Tokyo, Japan). The data comprised 30 frames
15
per second. We then randomly selected 44 recoded data (22 × 2 maneuvers). Finally, we
16
assessed the usefulness of these selected movies with a digitized video imaging
17
software program (DIPP Motion Pro 2D; Ditect, Tokyo, Japan) and evaluated the
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swallowing function after the first swallow. Details of the examination procedures were
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1
2
described in our previous paper 14. We performed quantitative assessment using four parameters for the modulation of the oropharyngeal swallowing function in both the neutral and chin-down positions.
4
Before analysis, a calibration marker (a coin of 23.5-mm diameter) was positioned on
5
the lateral neck. To compensate for the varied magnification images among the patients,
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the marker length was measured in millimeters and adjusted to be the same value
7
among the patients. The four parameters were as follows:
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• The pharyngeal constriction ratio (PCR), which was calculated by dividing the pharyngeal area at the point of maximum constriction during a swallow (neutral position, Fig. 1A; chin-down, Fig. 1B) by the area with a 1-mL bolus
11
held in the oral cavity (Fig. 1C). The PCR appeared to be a valid objective
12
surrogate measure of the strength of pharyngeal constriction 15.
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• The areas of pharyngeal residue in the vallecula and pyriform sinus,
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respectively (in units of mm2) (Fig. 2). These areas represent the clearance of pharyngeal residue. To clear the residue from the neutral position, patients
16
were asked to drink a cup of water before moving to the the chin-down
17
position for swallowing.
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• The UES opening diameter (in units of mm) (Fig. 3) and the duration of UES opening
3
level of the sub-vocal fold (following the method described in Kumakura’s
4
paper 16, the Y axis was drawn from the anterior and superior tip of the third
5
cervical vertebra to the anterior and inferior tip of the fifth cervical vertebra,
6
and the X axis was drawn orthogonal to the Y axis at the level of the anterior
7
and inferior border of the thyroid cartilage. The length of the white bar at the
8
sub-vocal fold level on the x axis was calculated as the UES opening diameter.
9
(Fig. 3). The duration of UES opening was calculated by dividing the number
10
of image frames by 30 (because 1 sec included 30 frames). These parameters
11
represent the smoothness of the bolus passage at the UES. The first frame was
12
taken when the tip of the barium or iopamiron reached the UES before its
13
opening, and the last frame was taken when the UES had just closed after the
15
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(in units of sec). The UES opening diameter was calculated at the
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barium or iopamiron passed through the UES.
• The duration of laryngeal vestibule closure (in units of sec), which was defined
16
as the duration of contact between the tip of the arytenoid and the base of the
17
epiglottis during the first swallow and was calculated using the same method
18
as that used for the duration of UES opening. A longer duration of laryngeal
11 ACCEPTED Chin-down maneuver MANUSCRIPT following esophagectomy
1
vestibule closure suggests that aspiration is unlikely to occur. Figure. 4 shows
2
before (Fig. 4A) and during (Fig. 4B) contact of the two structures. Among the fourteen patients who underwent VFSS, two (14.2%) demonstrated
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aspiration in the neutral position. As the amount of aspirated barium or iopamiron could
5
not be calculated precisely, these patients were excluded from the calculation of the area
6
of the vallecula, area of the pyriform sinus, and duration of laryngeal vestibule closure.
7
These two patients received jelly alone as an oral diet with compensation by tube
8
feeding. However, the remaining twelve patients tolerated a full oral diet of rice
9
porridge at the time of the VFSS without dysphagia after postoperative week 1. One
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patient who demonstrated aspiration during VESS but not during the VFSS was,
11
however, included in the evaluation of these three parameters. Evaluation was repeated
12
on different days by a single speech pathologist with a wealth of experience in rating
13
VFSS. The intra-rater reliability of each parameter was examined using an intra-rater
14
correlation coefficient between each pair of data obtained on different days. The
15
inter-rater reliability of each parameter was examined using an inter-rater correlation
16
coefficient between each pair of data evaluated by two speech pathologists and a
17
board-certified otolaryngologist subspecializing in dysphagia. Each parameter was
18
averaged among the three raters and statistically compared between the neutral and
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12 ACCEPTED Chin-down maneuver MANUSCRIPT following esophagectomy
1
chin-down positions using a paired t-test. (p<0.05 was taken to indicate statistical
2
significance).
5
Results
All patients enrolled in the present study underwent retrosternal route reconstruction
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using a gastric tube (all anastomosis sites were in the cervical lesion) after subtotal
7
esophagectomy with 3L without preoperative radiation therapy to the neck. None of the
8
patients demonstrated any major complications such as respiratory complications,
9
anastomotic leakage or anastomotic stenosis. Six patients (42.9%) exhibited unilateral
10
vocal fold paralysis. Bilateral vocal fold paralysis was not present in any patient. The
11
period between surgery and the VFSS ranged from 12 to 16 days (14.8 ± 0.4 days).
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The intra-rater correlation coefficient of each parameter was 0.78 to 0.95 (p < 0.01),
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and the inter-rater correlation coefficient of each parameter was 0.76 to 0.96 (p < 0.01),
14
which demonstrated consistency in the evaluation of the 2D VFSS images. The value of
15
each of the parameters (mean ± standard deviation) and the presence or absence of the
16
significant difference between neutral and chin-down positions for each parameter,
17
t-value, degree of freedom, effect sizes and exact p-value are shown in Table II. The
18
PCR and residue in the pyriform sinus for the chin-down position were significantly
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13 ACCEPTED Chin-down maneuver MANUSCRIPT following esophagectomy
smaller than those in the neutral position (p < 0.01). However, the residue in the
2
vallecula was not significantly different between the neutral and chin-down positions (p
3
= 0.44). The UES opening diameter, duration of UES opening and duration of laryngeal
4
vestibule closure in the chin-down position were all significantly prolonged compared
5
with those in the neutral position (p < 0.05).
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Discussion
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The chin-down, or chin-tuck, maneuver is widely used to reduce the occurrence of
10
aspiration and is effective for various dysphagic populations. Okada et al. 17 stated that
11
in consideration of both biomechanics and functional anatomy, flexion and extension
12
movements of the cervical spine involve coordinated motions in two anatomical areas:
13
the occipito-atlanto (C1)-axial (C2) complex and the lower cervical (C2-C7) region.
14
Flexion of the occipito-atlanto and atlanto-axial joints is referred to as flexion of the
15
head at the neck (head flexion [HF]), whereas flexion of the lower cervical region is
16
termed neck flexion (NF) 18. A previous Japanese article 19 pointed out that NF is a very
17
physiologically natural position; on the other hand, HF compresses the pharyngeal
18
cavity in the anterior-to-posterior direction, which helps to increase the pharyngeal
19
pressure and restricts mobility of the epiglottis. Our previous study 20 and McCulloch's
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14 ACCEPTED Chin-down maneuver MANUSCRIPT following esophagectomy
group demonstrated that in young healthy adults (different from the older
2
esophagecomized patients in the present study), the NF maneuver resulted in
3
significantly decreased pressure and a longer duration of lowered pressure at the UES
4
without modulation of pharyngeal pressure, which may have been due to compensated
5
laryngeal elevation in the anterior-superior direction combined with consequent UES
6
opening by NF, thus assisting bolus passage through the UES. Therefore, in the
7
present study, we used NF as the chin-down maneuver.
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8
Pearson et al. 21 demonstrated that the accurate quantification of post-swallow
9
pharyngeal residue is an important clinical challenge that is limited by currently available methods such as the perceptual method, the three-point ordinal scale 22 and
11
quantitative computer-based measurement of post-swallow pharyngeal residue, and the
12
vallecula residue ratio 23. These papers demonstrated that experienced VFSS raters
13
might be able to enhance the calculation of the area of pharyngeal residue using the true
14
amount of pharyngeal residue. However, the accuracy of the quantitative measurement
15
of pharyngeal residue using 2D VFSS still images in the present study was limited. With
16
respect to this limitation, we validated the quantitative measurement of the area outlined
17
in the lateral view of the VFSS still image by calculating inter- and intra-rater
18
correlation coefficients, which were all found to be in the excellent range (0.76–0.96),
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15 ACCEPTED Chin-down maneuver MANUSCRIPT following esophagectomy
1
demonstrating high consistency and stability in the evaluation. Leonard et al. 15 demonstrated that there was a high inverse correlation between the
3
PCR and peak pharyngeal pressure, suggesting that the PCR (normal range, within 0.25)
4
appears to be a valid objective surrogate measure of pharyngeal strength and, moreover,
5
that decreased pharyngeal constriction contributes to an increased prevalence of
6
aspiration 15, 25. The present study demonstrated that the chin-down maneuver
7
significantly decreased the PCR and pharyngeal residue in the pyriform sinus rather
8
than in the vallecula, suggesting that this maneuver has a positive effect on the
9
reduction of post-swallow aspiration of residue in the pyriform sinus in postoperative
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patients with advanced esophageal cancer.
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Yasuda et al. 26 demonstrated that swallowing dysfunctions in patients who have
12
undergone esophagectomy with 3FL might be caused by the defective relaxation of
13
scarred sternohyoid and sternothyroid muscles during the pharyngeal phase. They stated
14
that both muscles were subjected to considerable damage in cervical LN dissection
15
because of retraction and partial division to allow visualization of the cervicothoracic
16
area. Postoperatively, these muscles predictably become scarred, and these scarred
17
fibers might work antagonistically against laryngeal elevation 26. Swallowing
18
dysfunction following esophagectomy has also been thought to result from inadvertent
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16 ACCEPTED Chin-down maneuver MANUSCRIPT following esophagectomy
damage to the pharyngeal plexus 26. Although we did not directly investigate the
2
modulation of hyoid and laryngeal elevation, as Steel et al. 27 demonstrated previously,
3
reductions in anterior hyoid and laryngeal movement are associated with an increased
4
risk of penetration–aspiration and post-swallow residues in patients who have
5
undergone esophagectomy with 3FL. Bülow et al. 12 reported that the chin-down
6
maneuver significantly narrowed the distance between the mandible and hyoid bone
7
(i.e., hyoid excursion with relative descent of the mandible). Previous papers have noted
8
that sub-atmospheric pressure acts as a hypopharyngeal suction pump and that it is
9
necessary for adequate bolus transport 28, 29. The present study demonstrated that the
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chin-down maneuver worked positively to promote not only the duration of UES
11
opening but also UES opening. Moreover, the maneuver worked to increase the duration
12
of laryngeal closure. Taken together, these three parameters suggest that the chin-down
13
maneuver promotes widening of the UES, possibly by narrowing the distance between
14
the mandible and hyoid bone which can compensate laryngeal elevation in the
15
anterior-superior direction combined with consequent UES opening and increasing
16
greater sub-atmospheric pressure in the UES, consequently improving bolus passage.
17
This process definitely helps to decrease pharyngeal residue and reduce aspiration with
18
laryngeal closure. As patients that underwent esophagectomy with 3FL had impaired
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17 ACCEPTED Chin-down maneuver MANUSCRIPT following esophagectomy
laryngeal elevation during swallowing due to chest manipulation, the chin-down
2
maneuver may be helpful especially as temporary compensation until the patient fully
3
recovered from surgery.
4
Study Limitations
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VFSS were conducted in the lateral projection alone as all parameters except the
6
areas of pharyngeal residue (vallecula and pyriform sinus) must be measured in the
7
lateral position, and not in the anterior-posterior position. Therefore, we were unable to
8
compare the area of pharyngeal residue between right and left sides. Moreover, this
9
study had additional limitations, including the relative short evaluation period, lack of
10
follow-up, the relatively small number of patients, and lack of females included in the
11
study population.
14 15
Conclusion
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The chin-down maneuver after esophagectomy with 3FL might help expedite the
16
ability to swallow by increasing pharyngeal constriction, minimizing pharyngeal residue,
17
widening the UES, and enhancing laryngeal closure.
18
19
18 ACCEPTED Chin-down maneuver MANUSCRIPT following esophagectomy
1
References 1. Atkins BZ, Shah AS, Hutcheson KA et al. Reducing hospital morbidity and
3
mortality following esophagectomy. Ann Thorac Surg. 2004; 78:1170-6.
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cancer of the thoracic esophagus. Ann Surg.1994; 220:364–373
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2. Akiyama H, Tsurumaru M, Udagawa H et al. Radical lymph node dissection for
3. Fujita H, Kakegawa T, Yamana H et al. Lymph node metastasis and recurrence in
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2
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patients with a carcinoma of the thoracic esophagus who underwent three-field
8
dissection. World J Surg.1994; 18:266–272
4. Altorki N, Kent M, Ferrara C et al. Three-field lymph node dissection for
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squamous cell and adenocarcinoma of the esophagus. Ann Surg.2002;
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236:177–183
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5. Heitmiller RF, Jones B. Transient diminished airway protection after transhiatal esophagectomy. Am J Surg. 1991;162:442-6
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6. Gandhi SK, Naunheim KS. Complications of transhiatal esophagectomy. Chest Surg Clin N Am. 1997;7:601-10
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7. Ekberg O, Nylander G. Pharyngeal dysfunction after treatment for pharyngeal
17
cancer with surgery and radiotherapy. Gastrointest Radiol. 1983;8:97-104
18
8. Hambraeus GM, Ekberg O, Fletcher R. Pharyngeal dysfunction after total and
19 ACCEPTED Chin-down maneuver MANUSCRIPT following esophagectomy
1
2
subtotal oesophagectomy. Acta Radiol. 1987; 28:409-13. 9. Leder SB, Bayar S, Sasaki CT et al. Fiberoptic endoscopic evaluation of swallowing in assessing aspiration after transhiatal esophagectomy. J Am Coll
4
Surg 2007; 205:581–585
10. Kinugasa S, Tachibana M, Yoshimura H et al. Postoperative pulmonary
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complications are associated with worse shortand long-term outcomes after
7
extended esophagectomy. J Surg Oncol 2004;88:71–77
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11. Fang WT, Chen WH, Chen Y Jiang Y. Selective three field lymphadenectomy for
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thoracic esophageal squamous carcinoma. Dis Esophagus 2007; 20:206–211 12. Bülow M, Olsson R, Ekberg O. Videomanometric analysis of supraglottic
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swallow, effortful swallow, and chin tuck in patients with pharyngeal dysfunction.
12
Dysphagia. 2001; 16:190-5.
14
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13. Lewin J, Hebert T, Putnam J Jr et al. Experience with the chin tuck maneuver in
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postesophagectomy aspirators. Dysphagia. 2001; 16:216-9.
14. Narajos N, Samejima Y, Kumai Y et al. Postdeglutitive residue in idiopathic
16
unilateral vocal fold paralysis: a quantitative videofluoroscopic study.
17
Laryngoscope. 2013; 123:2776-9.
18
15. Leonard R, Belafsky PC, Rees CJ. Relationship between fluoroscopic and
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1
manometric measures of pharyngeal constriction: the pharyngeal constriction
2
ratio. Ann Otol Rhinol Laryngol. 2006; 115:897-901. 16. Kumakura M, Baba T, Dozono K. The effect of tongue position during swallow
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on the mobility of hyoid bone, larynx and on the opening of upper esophageal
5
sphincter. Japanese journal of Dysphagia Rehabilitation. 2011; 15:
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165-173.(Japanese article)
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17. Okada S, Saitoh E, Palmer JB et al. What is the chin-down posture? A
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questionnaire survey of speech language pathologists in Japan and the United
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States. Dysphagia. 2007; 22:204-9.
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14
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of manual examination.7th ed: 2002, W.B.Saunders:Philadelphia 19. Official publication of the Japanese society of dysphagia rehabilitation. Summary
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18. Hislop HJ, Montgomery J. Daniels and Worthigham’s muscle testing: techniques
of the training method .The Japanese journal of dysphagia rehabilitation.
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2014;18:55-89
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20. Matsubara K, Kumai Y, Kamenosono Y et al. Effect of three different chin-down
16
maneuvers on swallowing pressure in healthy young adults. Laryngoscope. 2015
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Aug 12.
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21. Pearson WG Jr, Molfenter SM, Smith ZM et al.
Image-based measurement of
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post-swallow residue: the normalized residue ratio scale. Dysphagia.
2
2013;28:167-77 22. Rosenbek JC, Roecker EB, Wood JL. Thermal application reduces the duration of
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stage transition in dysphagia after stroke. Dysphagia. 1996;11:225–33
5
23. Dyer JC, Leslie P, Drinnan MJ. Objective computer-based assessment of
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valleculae residue: Is it useful? Dysphagia.2008;23:7–15.
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24. Dumont P, Wihlm JM, Hentz JG et al. Respiratory complications after surgical
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treatment of esophageal cancer. A study of 309 patients according to the type of
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resection. Eur J Cardiothorac Surg. 1995;9:539-43
25. Easterling CS, Bousamra M, Lang IM et al. Pharyngeal dysphagia in
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postesophagectomy patients: correlation with deglutitive biomechanics. Ann
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Thorac Surg. 2000; 69:989-92.
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15
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26. Yasuda T, Yano M, Miyata H et al. Evaluation of dysphagia and diminished
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airway protection after three-field esophagectomy and a remedy. World J Surg. 2013; 37:416-23.
27. Steele CM, Bailey GL, Chau T et al. The relationship between hyoid and
17
laryngeal displacement and swallowing impairment. Clin Otolaryngol. 2011;
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36:30-6.
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3
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28. McConnel FM. Analysis of pressure generation and bolus transit during pharyngeal swallowing. Laryngoscope 1988; 98:71-78. 29. Cook IJ, Dodds WJ, Dantas RO et al. Opening mechanisms of the human upper esophageal sphincter. Am J Physiol 1989; 257: 748-59.
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23 ACCEPTED Chin-down maneuver MANUSCRIPT following esophagectomy
Suppliers
2
a. collimator type R-50 model; Shimadzu Corporation Medical Systems, Tokyo, Japan
3
b. Mini DV : Mini DV & S-VHS dual format SR-VS30; Victor Company of Japan Ltd.,
4
Yokohama, Japan
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c. Digital video camera (DCR-HC90; Sony, Tokyo, Japan)
6
d. Personal computer (dc7800MT-E6850/Windows XP; HP Inc., Palo Alto, CA, USA)
7
e. Video editing software (Corel Video Studio 12; E Frontier, Inc., Tokyo, Japan).
8
f. Digitized video imaging software program (DIPP Motion Pro 2D; Ditect, Tokyo,
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Japan)
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24 ACCEPTED Chin-down maneuver MANUSCRIPT following esophagectomy
Figure legends
2
Figure 1 Pharyngeal constriction ratio (PCR)
3
The pharyngeal constriction ratio (PCR) was calculated by dividing the pharyngeal area
4
at the point of maximum constriction during a swallow in the neutral position (A) or
5
chin-down position (B) by the area with a 1-mL bolus held in the oral cavity (C).
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Figure 2 Area of pharyngeal residue in the pyriform sinus and vallecula,
8
The area of pharyngeal residue in the pyriform sinus and vallecula, surrounded by a
9
white line, was measured in the lateral view of the still VFSS images using a digitized video imaging software program (DIPP Motion Pro 2D; Tokyo, Japan) (units: mm2).
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Figure 3 Upper Esophagus Sphincter opening diameter
13
The UES opening diameter (length of the white portion) (units: mm) was measured at
14
the level of the sub-vocal fold (the Y axis was drawn from the anterior and superior tip
15
of the third cervical vertebra to the anterior and inferior tip of the fifth vertebra). The X
16
axis was drawn, orthogonal to the Y axis, at the level of the anterior and inferior border
17
of the thyroid cartilage.
18
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25 ACCEPTED Chin-down maneuver MANUSCRIPT following esophagectomy
Figure 4 Duration of laryngeal vestibule closure The duration of laryngeal vestibule
2
closure (units: sec), which was defined as the duration of contact between the tip of the
3
arytenoids and the base of the epiglottis during the first swallow, was calculated by
4
dividing the number of image frames by 30 (because 1 sec included 30 frames). (A)
5
Before and (B) during contact of the two structures.
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6
The English in this document has been checked by at least two professional editors, both
8
native speakers of English.
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Table 1 Characteristics of the enrolled patients
Tumor
Tumor
RLN
Day of VFSS
Location
Stage
paralysis
(days)
73
M～L
III
-
16
2
58
M～L
III
-
16
3
65
M
III
+
15
4
71
M～L
III
+
13
5
69
U～M
IVa
-
16
6
73
M
II
-
15
7
57
M～L
III
-
16
8
61
M
II
-
15
9
71
U～M
II
+
16
10
76
M
III
+
15
11
60
M
III
+
16
12
53
M
III
-
13
70
M
III
+
14
65
M
III
-
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13
13
12
Sex: M: Male, Location: U: Upper, M: Middle, L: Lower
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RLN: recurrent laryngeal nerve
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ACCEPTED MANUSCRIPT
Table 2 Each value of the parameters and the presence or absence of the significant ACCEPTED MANUSCRIPT difference between neutral and chin-down positions for each parameter
parameters
Neutral
Chin-down
P-value
t-value
degree
effect
of
sizes
freedom 0.21 ±0.10
0.17 ±0.09
P=0.007
0
14
0.42
Residue in the vallecula
60.52 ±37.15
59.05 ±36.88
P=0.442
0
14
0.04
70.31 ±55.98
40.86 ±58.55
P=0.001
UESD mm(mean ± SD)
6.01 ±2.43
8.04 ±1.87
P=0.003
DUES second(mean ± SD)
0.43 ±0.13
0.48 ±0.06
P=0.006
DLVC second(mean ±
0.37 ±0.21
0.51 ±0.20
2
mm (mean ± SD) Residue in the pyriform 2
P=0.038
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SD)
0
14
3.18
0
14
0.94
0
14
0.49
0
14
0.68
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sinus mm (mean ± SD)
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PCR ratio(mean ± SD)
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