Presentation of oropharyngeal dysphagia and rehabilitative intervention following esophagectomy: a systematic review

Presentation of oropharyngeal dysphagia and rehabilitative intervention following esophagectomy:... SUMMARY No study has systematically reviewed the evidence on presentation of oropharyngeal dysphagia and swallowing rehabilitation following esophagectomy. The purposes of this systematic review are to 1) qualitatively synthesize the current findings on oropharyngeal swallowing abnormalities identified by instrumental swallowing evaluations, 2) describe the reported health-related outcomes in relation to swallowing abnormality following esophagectomy, and 3) examine the efficacy of reported rehabilitative interventions for oropharyngeal dysphagia in patients who underwent esophagectomy. Publications were searched using five electronic databases. No language or publication date restrictions were imposed. Two authors performed a blind review for published or unpublished studies that reported swallowing biomechanics and dysphagic symptoms using instrumental evaluation of swallowing, specifically the videofluoroscopic swallowing study and fiberoptic endoscopic evaluation of swallowing, and/or health-related outcomes in relation to swallowing abnormalities, and/or therapeutic interventions for oropharyngeal dysphagia following esophagectomy. Twelve studies out of 2,193 studies including 458 patients met the inclusion criteria. Reported abnormal swallowing biomechanics included vocal fold immobility, delayed onset of swallowing, reduced hyolaryngeal elevation, and reduced opening of the upper esophageal sphincter. Aspiration (0–81%) and pharyngeal residue (22–100%) were prevalent. Those abnormal swallowing biomechanics and swallowing symptoms were commonly reported following both transhiatal and transthoracic esophagectomy. Pneumonia presented in 5–25% of the study patients. One quasi-experimental study examined the effectiveness of swallowing exercises for postoperative oropharyngeal dysphagia; three case series reported a benefit of the chin-tuck maneuver in reducing aspiration and residue. This review revealed distinct swallowing impairments and increased pneumonia risks following esophagectomy. This review also found that evidence on the efficacy of therapeutic interventions was limited. Future studies are warranted to develop effective rehabilitative interventions for postesophagectomy patients with oropharyngeal dysphagia. INTRODUCTION Esophageal cancer is ranked as the eighth most common cancer worldwide and is the sixth most common cause of cancer-related death.1 Although the effectiveness of definitive chemotherapy,2 perioperative chemotherapy,3,4 and chemoradiotherapy5 has been reported, radical resection of the esophageal cancer has been the mainstay of treatment for this fatal malignancy.6 Meanwhile, complication rates for this highly invasive surgery have been reported to be as high as 22–29%.7-11 Unfavorable outcomes of the surgery can significantly impair patients’ long-term survival7 and quality of life.12-14 Major complications include anastomotic leakage, pulmonary complications, damage to the recurrent laryngeal nerve, dysphagia, strictures, reflux, and other gastrointestinal symptoms.10,11 Above all, the presence of dysphagia has been reported to increase the risk of pneumonia and mortality following esophagectomy.10 In addition, recent literature has found that patients who underwent surgical treatment for esophageal cancer had lower quality of life scores across many domains including swallowing impairments.15 Thus, it is crucial to provide patients with an adequate dysphagia assessment and therapeutic interventions in order to achieve better health outcomes and quality of life. When presence of dysphagia is suspected, two instrumental procedures are often used to assess the swallow function: the videofluoroscopic swallowing study (VFSS)16 and the fiberoptic endoscopic evaluation of swallowing (FEES).17 This study focused on impairments of the oropharyngeal stage of swallowing to investigate, given is prevalence in the postesophagectomy patient population. Understanding the oropharyngeal swallowing impairments as well as efficacy of behavior or postural modifications and exercises will improve our therapeutic intervention. To our knowledge, no research study has systematically examined the current findings about biomechanics of oropharyngeal swallowing and dysphagic symptoms following esophagectomy identified by instrumental evaluations. In order to better understand the underlying mechanism of postoperative oropharyngeal dysphagia, it will be valuable to synthesize the knowledge of pathophysiology and dysphagic symptoms associated with esophagectomy. It will also be important to understand the reported health-related outcomes in patients with oropharyngeal dysphagia following esophagectomy. Further, a summary of the reported rehabilitative interventions for oropharyngeal swallowing impairment will help develop a core set of swallowing exercises that may be most effective in treating this patient population. This review aims to qualitatively synthesize the current evidence on oropharyngeal swallowing abnormalities captured by instrumental evaluations of swallowing, specifically VFSS or FEES, in patients who underwent esophagectomy. Specific research questions of this systematic review are: What are the abnormalities in oropharyngeal swallowing biomechanics identified during VFSS or FEES following esophagectomy? What are the symptoms of oropharyngeal dysphagia identified during VFSS or FEES following esophagectomy? What are the reported health-related outcomes in relation to swallowing abnormality following esophagectomy? Is there any evidence to support that rehabilitative interventions are effective in improving swallowing function or health-related outcomes in patients with oropharyngeal dysphagia following esophagectomy? MATERIALS AND METHODS The review reported in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines.18 The predefined review protocol was registered at Center for Review and Dissemination (CRD42017056330). Search strategy Publications were searched from the August 30th, 2017 through the August 31st, 2017 using the MEDLINE [PubMed], Web of Science, CINAHL, Cochrane Database of Systematic Reviews, and Cochrane Central Register of Controlled Trials. To reduce investigator selection bias, all relevant search terms were defined a priori. The following is the search algorithm for searching MEDLINE: (esophageal cancer OR esophagus cancer) AND (esophagectomy OR esophageal surgery OR esophageal resection OR esophagus/surgery [MeSH Terms]) AND (dysphagia OR swallow OR deglutition OR deglutition disorders OR swallowing disorders OR oropharyngeal dysphagia) AND (modified barium swallow OR videofluoroscopy OR instrumental swallow OR VFSS OR FEES OR videofluoroscopic swallow study OR endoscopy OR videoendoscopy OR fiberoptic endoscopic evaluation of swallowing OR endoscopic evaluation of swallowing). Search was restricted to human studies. No language or publication date restriction was imposed. To ensure a comprehensive search, the first author scanned reference lists of included studies and previously published review articles. Study eligibility This review included studies that met the following criteria: 1) were published or unpublished original research articles; 2) retrospective and prospective studies; 3) studied adult (18 years or older) patients; 4) with a diagnosis of esophageal cancer; 5) treated with first-time esophagectomy (including both open esophagectomy and minimally invasive esophagectomy) with or without perioperative chemotherapy/chemoradiotherapy; 6) examined swallowing function of the patients using instrumental evaluations; and 7) reported swallowing biomechanical measurements and/or any symptoms of oropharyngeal dysphagia, rehabilitative interventions, and/or health-related outcomes in relation to oropharyngeal dysphagia using clearly described method(s). Studies that did not utilize VFSS or FEES to assess swallowing function were excluded because clinical swallowing evaluations do not allow researchers to objectively measure swallowing biomechanics or to accurately identify presence of swallowing symptoms.19 Further, case reports and case series that profiled fewer than five patients were excluded given the limited information provided by those studies. In this review, swallowing biomechanical measurements referred to any displacement measures of relevant structures for swallowing and time variables of swallowing motion identified by using VFSS or FEES.20,21Symptoms and signs of oropharyngeal dysphagia included penetration, aspiration, pharyngeal residue, and other abnormalities due to their frequent reporting in the literature.22,23Health-related outcomes in relation to swallowing abnormality included pneumonia, nutrition status, diet levels, and the use of alternative nutrition.24Rehabilitative interventions included exercise therapies that can be executed with or without accompanying food25,26 and compensatory swallowing strategies. Literature review Two review authors independently screened the abstracts of the identified studies for eligibility. The two authors then read full articles of potentially eligible studies for determining the eligibility. When publications were written in languages other than English, speech language pathologists, or medical doctors native to those languages reviewed the articles. Discrepancies in the inclusion between the two authors were resolved by discussion. Data extraction One review author extracted the following data from the included studies and the second reviewer checked the extracted data: 1) study characteristics, 2) the features of esophageal cancer treatment provided, 3) the key findings on biomechanical measurements and swallowing symptoms identified in the swallowing assessment performed, 4) health-related outcomes of esophagectomy in relation to swallowing abnormality; and 5) types of rehabilitative intervention and the effect of those interventions reported. Meta-analysis of the data was not possible due to high level of heterogeneity in subjects, research design, cancer treatment protocols, or swallowing assessment protocols across the included studies. Therefore, the extracted data were presented descriptively. Quality assessment Two review authors independently appraised the methodological quality of identified studies using the JBI Critical Appraisal Checklists for case series, diagnostic test accuracy studies, and quasi-experimental studies.27 Disagreements in the judgment between the two authors were resolved by discussion. RESULTS A total of 2193 records were identified from all sources (Fig. 1). After excluding duplicates, 2117 titles and abstracts were screened for eligibility. Of those, 34 studies (31 studies written in English, two in French, and one in German) were read in full for eligibility. Twelve studies consisting of 458 patients met all inclusion criteria and were included in the final systematic review. Fig. 1 View largeDownload slide PRISMA flowchart. Fig. 1 View largeDownload slide PRISMA flowchart. Characteristics of included studies Table 1 displays the characteristics of the 12 studies included in this review. One quasi-experimental study,28 one test accuracy study,29 and ten case series were included.30-39 Table 2 shows the features of cancer treatment provided in the included studies by surgical approach. Four studies from North America reported oropharyngeal dysphagia following transhiatal esophagectomy;32,33,37,38 seven studies from East Asia reported oropharyngeal dysphagia following transthoracic esophagectomy with lymph node dissection.28-31,34,35,39 One study involved patients who received either transhiatal or transthoracic esophagectomy.36 Table 3 summarizes the swallowing assessment performed in the included studies. Two of 12 studies performed VFSS both before and after esophagectomy.28,30,33 However, two of the three studies performed VFSS only on a part of their study participants,28,33 resulting in an unclear comparison between pre- and postoperative swallowing functions. No study performed longitudinal follow-up evaluations for swallowing. Table 1 Characteristics of the included studies (n = 12). References Country Study design Subject Mean or median age (range in years) % male Main purpose(s) of the study Easterling et al.32 USA Case series Patient 8 Healthy adult 8 NR (51–78) Age-matched NR to correlate the swallowing biomechanics with aspiration in patients with dysphagia after transhiatal esophagectomy Martin et al.33 Canada Case series 10 66.7 (49–76) 90.0 to compare pre- and postoperative swallowing patterns in patients who underwent transhiatal esophagectomy Lewin et al.36 USA Case series 26 66.0 (52–82) 88.5 to evaluate the use of chin tuck maneuver to alleviate aspiration during videofluoroscopy in patients who underwent esophagectomy Koh et al.37 Canada Case series 9 63.0 (52–76) 88.9 to investigate the function of the oral and pharyngeal phases of deglutition, and of the cervical esophagus, in patients who underwent transhiatal esophagectomy Leder et al.38 USA Case series 73 60.0 (39–74) 83.6 to characterize laryngeal physiology in patients who underwent transhiatal esophagectomy and to identify patients who are at high aspiration risk Kato et al.30 Japan Case series 27 64.3 (53–78) 100.0 to analyze the relationship between oropharyngeal swallowing and the alimentary reconstruction route after transthoracic esophagectomy Yasuda et al.31 Japan Case series 2FL 10 3FL 10 3FL + CDBIMS 20 61.4 (51–76) 61.3 (54–68) 61.5 (54–71) 80. 0100. 0 90.0 to compare swallowing function in patients who underwent esophagectomy with 2FL and 3FL, and to evaluate the preventative effect of the addition of CDBIMS for post-operative dysphagia Okumura et al.28 Japan Quasi-experimental Experiment 14 Control 12 65.9 ± 9.7 68.0 ± 5.1 92. 9100. 0 to assess the preventative and therapeutic effects of perioperative swallowing rehabilitation in patients undergoing esophagectomy Kim et al.34 Korea Case series Aspiration 23 No aspiration 24 Control 27 62.7 ± 8.2 63.3 ± 7.1 64.7 ± 10.1 100. 0100. 0100.0 to analyze the swallowing biomechanics in patients with oropharyngeal dysphagia after esophagectomy compared to healthy adults Lee et al.29 Korea Diagnostic test accuracy 118 63.4 ± 8.5 93.2 to assess the usefulness of clinical bedside swallowing tests for detecting aspiration after esophagectomy Kumai et al.35 Japan Case series 25 64.8 NR to identify the main factors associated with aspiration in patients with pharyngeal dysphagia following esophagectomy with 3FL and to assess the effectiveness of the chin-down maneuver Kumai et al.39 Japan Case series 14 65.9 ± 1.9 100.0 to determine the efficacy of the chin-down maneuver after esophagectomy with 3FL on pharyngeal residue, UES opening, and laryngeal closure References Country Study design Subject Mean or median age (range in years) % male Main purpose(s) of the study Easterling et al.32 USA Case series Patient 8 Healthy adult 8 NR (51–78) Age-matched NR to correlate the swallowing biomechanics with aspiration in patients with dysphagia after transhiatal esophagectomy Martin et al.33 Canada Case series 10 66.7 (49–76) 90.0 to compare pre- and postoperative swallowing patterns in patients who underwent transhiatal esophagectomy Lewin et al.36 USA Case series 26 66.0 (52–82) 88.5 to evaluate the use of chin tuck maneuver to alleviate aspiration during videofluoroscopy in patients who underwent esophagectomy Koh et al.37 Canada Case series 9 63.0 (52–76) 88.9 to investigate the function of the oral and pharyngeal phases of deglutition, and of the cervical esophagus, in patients who underwent transhiatal esophagectomy Leder et al.38 USA Case series 73 60.0 (39–74) 83.6 to characterize laryngeal physiology in patients who underwent transhiatal esophagectomy and to identify patients who are at high aspiration risk Kato et al.30 Japan Case series 27 64.3 (53–78) 100.0 to analyze the relationship between oropharyngeal swallowing and the alimentary reconstruction route after transthoracic esophagectomy Yasuda et al.31 Japan Case series 2FL 10 3FL 10 3FL + CDBIMS 20 61.4 (51–76) 61.3 (54–68) 61.5 (54–71) 80. 0100. 0 90.0 to compare swallowing function in patients who underwent esophagectomy with 2FL and 3FL, and to evaluate the preventative effect of the addition of CDBIMS for post-operative dysphagia Okumura et al.28 Japan Quasi-experimental Experiment 14 Control 12 65.9 ± 9.7 68.0 ± 5.1 92. 9100. 0 to assess the preventative and therapeutic effects of perioperative swallowing rehabilitation in patients undergoing esophagectomy Kim et al.34 Korea Case series Aspiration 23 No aspiration 24 Control 27 62.7 ± 8.2 63.3 ± 7.1 64.7 ± 10.1 100. 0100. 0100.0 to analyze the swallowing biomechanics in patients with oropharyngeal dysphagia after esophagectomy compared to healthy adults Lee et al.29 Korea Diagnostic test accuracy 118 63.4 ± 8.5 93.2 to assess the usefulness of clinical bedside swallowing tests for detecting aspiration after esophagectomy Kumai et al.35 Japan Case series 25 64.8 NR to identify the main factors associated with aspiration in patients with pharyngeal dysphagia following esophagectomy with 3FL and to assess the effectiveness of the chin-down maneuver Kumai et al.39 Japan Case series 14 65.9 ± 1.9 100.0 to determine the efficacy of the chin-down maneuver after esophagectomy with 3FL on pharyngeal residue, UES opening, and laryngeal closure 2FL, two-field lymphadenectomy; 3FL, three-field lymphadenectomy; CDBIMS, complete division of the bilateral infrahyoid muscles attached to the sternum; NR, not recorded. View Large Table 1 Characteristics of the included studies (n = 12). References Country Study design Subject Mean or median age (range in years) % male Main purpose(s) of the study Easterling et al.32 USA Case series Patient 8 Healthy adult 8 NR (51–78) Age-matched NR to correlate the swallowing biomechanics with aspiration in patients with dysphagia after transhiatal esophagectomy Martin et al.33 Canada Case series 10 66.7 (49–76) 90.0 to compare pre- and postoperative swallowing patterns in patients who underwent transhiatal esophagectomy Lewin et al.36 USA Case series 26 66.0 (52–82) 88.5 to evaluate the use of chin tuck maneuver to alleviate aspiration during videofluoroscopy in patients who underwent esophagectomy Koh et al.37 Canada Case series 9 63.0 (52–76) 88.9 to investigate the function of the oral and pharyngeal phases of deglutition, and of the cervical esophagus, in patients who underwent transhiatal esophagectomy Leder et al.38 USA Case series 73 60.0 (39–74) 83.6 to characterize laryngeal physiology in patients who underwent transhiatal esophagectomy and to identify patients who are at high aspiration risk Kato et al.30 Japan Case series 27 64.3 (53–78) 100.0 to analyze the relationship between oropharyngeal swallowing and the alimentary reconstruction route after transthoracic esophagectomy Yasuda et al.31 Japan Case series 2FL 10 3FL 10 3FL + CDBIMS 20 61.4 (51–76) 61.3 (54–68) 61.5 (54–71) 80. 0100. 0 90.0 to compare swallowing function in patients who underwent esophagectomy with 2FL and 3FL, and to evaluate the preventative effect of the addition of CDBIMS for post-operative dysphagia Okumura et al.28 Japan Quasi-experimental Experiment 14 Control 12 65.9 ± 9.7 68.0 ± 5.1 92. 9100. 0 to assess the preventative and therapeutic effects of perioperative swallowing rehabilitation in patients undergoing esophagectomy Kim et al.34 Korea Case series Aspiration 23 No aspiration 24 Control 27 62.7 ± 8.2 63.3 ± 7.1 64.7 ± 10.1 100. 0100. 0100.0 to analyze the swallowing biomechanics in patients with oropharyngeal dysphagia after esophagectomy compared to healthy adults Lee et al.29 Korea Diagnostic test accuracy 118 63.4 ± 8.5 93.2 to assess the usefulness of clinical bedside swallowing tests for detecting aspiration after esophagectomy Kumai et al.35 Japan Case series 25 64.8 NR to identify the main factors associated with aspiration in patients with pharyngeal dysphagia following esophagectomy with 3FL and to assess the effectiveness of the chin-down maneuver Kumai et al.39 Japan Case series 14 65.9 ± 1.9 100.0 to determine the efficacy of the chin-down maneuver after esophagectomy with 3FL on pharyngeal residue, UES opening, and laryngeal closure References Country Study design Subject Mean or median age (range in years) % male Main purpose(s) of the study Easterling et al.32 USA Case series Patient 8 Healthy adult 8 NR (51–78) Age-matched NR to correlate the swallowing biomechanics with aspiration in patients with dysphagia after transhiatal esophagectomy Martin et al.33 Canada Case series 10 66.7 (49–76) 90.0 to compare pre- and postoperative swallowing patterns in patients who underwent transhiatal esophagectomy Lewin et al.36 USA Case series 26 66.0 (52–82) 88.5 to evaluate the use of chin tuck maneuver to alleviate aspiration during videofluoroscopy in patients who underwent esophagectomy Koh et al.37 Canada Case series 9 63.0 (52–76) 88.9 to investigate the function of the oral and pharyngeal phases of deglutition, and of the cervical esophagus, in patients who underwent transhiatal esophagectomy Leder et al.38 USA Case series 73 60.0 (39–74) 83.6 to characterize laryngeal physiology in patients who underwent transhiatal esophagectomy and to identify patients who are at high aspiration risk Kato et al.30 Japan Case series 27 64.3 (53–78) 100.0 to analyze the relationship between oropharyngeal swallowing and the alimentary reconstruction route after transthoracic esophagectomy Yasuda et al.31 Japan Case series 2FL 10 3FL 10 3FL + CDBIMS 20 61.4 (51–76) 61.3 (54–68) 61.5 (54–71) 80. 0100. 0 90.0 to compare swallowing function in patients who underwent esophagectomy with 2FL and 3FL, and to evaluate the preventative effect of the addition of CDBIMS for post-operative dysphagia Okumura et al.28 Japan Quasi-experimental Experiment 14 Control 12 65.9 ± 9.7 68.0 ± 5.1 92. 9100. 0 to assess the preventative and therapeutic effects of perioperative swallowing rehabilitation in patients undergoing esophagectomy Kim et al.34 Korea Case series Aspiration 23 No aspiration 24 Control 27 62.7 ± 8.2 63.3 ± 7.1 64.7 ± 10.1 100. 0100. 0100.0 to analyze the swallowing biomechanics in patients with oropharyngeal dysphagia after esophagectomy compared to healthy adults Lee et al.29 Korea Diagnostic test accuracy 118 63.4 ± 8.5 93.2 to assess the usefulness of clinical bedside swallowing tests for detecting aspiration after esophagectomy Kumai et al.35 Japan Case series 25 64.8 NR to identify the main factors associated with aspiration in patients with pharyngeal dysphagia following esophagectomy with 3FL and to assess the effectiveness of the chin-down maneuver Kumai et al.39 Japan Case series 14 65.9 ± 1.9 100.0 to determine the efficacy of the chin-down maneuver after esophagectomy with 3FL on pharyngeal residue, UES opening, and laryngeal closure 2FL, two-field lymphadenectomy; 3FL, three-field lymphadenectomy; CDBIMS, complete division of the bilateral infrahyoid muscles attached to the sternum; NR, not recorded. View Large Table 2 Treatment features of the included studies by surgical approach (n = 12). Reference Surgical approach Cancer type Pathological stage Reconstruction route Lymph node dissection Anastomosis site Neoadjuvant therapy Adjuvant therapy Easterling et al.32 TH AD NR Posterior mediastinum NR Cervical NR NR Martin et al.33 SCC 3 AD 7 T1N0M0 1 T2N0M0 4 T3N0M0 1 T3N1M0 4 Posterior mediastinum One node 3 Two nodes 1 Cervical None None Koh et al.37 AD NR Posterior mediastinum NR Cervical NR NR Leder et al.38 NR NR NR NR Cervical Neoadjuvant therapy 57(Detail was not shown) NR Kato et al.30 TT NR NR Posterior mediastinum 3FL 16 2FL 11 Cervical 16 Intrathoracic 11 None None Yasuda et al.31 NR I 4 IIA 8 IIB 11 III 10 IVA 1 IVB 6 Retrosternal 39 Orthotopic 1 2FL 4–12 3FL 8–21 3FL + CDBIMS 4–37 Cervical CT 14 CRT 2 NR Okumura et al.28 NR I/II 20 III/IV 6 Retrosternal 20 Subcutaneous 6 Dissected Cervical CT 6 CRT 1 NR Kim et al.34 SCC T2–3 N0–1 M0 NR 3FL Cervical NR CRT 10 Lee et al.29 NR NR NR Cervical lymph node dissection 27 Cervical 33 Noncervical 85 CRT 24 NR Kumai et al.35 NR NR Retrosternal 25 3FL 25 Cervical 25 NR NR Kumai et al.39 NR II 3 III 10 IVa 1 Retrosternal 14 3FL 14 Cervical 14 None NR Lewin et al.36 TH 16 TT 10 SCC 5 AD 19 Barrett's esophagus + HGD 2 NR NR NR Cervical 21 Thoracic 5 CRT 12 Photodynamic 1 NR Reference Surgical approach Cancer type Pathological stage Reconstruction route Lymph node dissection Anastomosis site Neoadjuvant therapy Adjuvant therapy Easterling et al.32 TH AD NR Posterior mediastinum NR Cervical NR NR Martin et al.33 SCC 3 AD 7 T1N0M0 1 T2N0M0 4 T3N0M0 1 T3N1M0 4 Posterior mediastinum One node 3 Two nodes 1 Cervical None None Koh et al.37 AD NR Posterior mediastinum NR Cervical NR NR Leder et al.38 NR NR NR NR Cervical Neoadjuvant therapy 57(Detail was not shown) NR Kato et al.30 TT NR NR Posterior mediastinum 3FL 16 2FL 11 Cervical 16 Intrathoracic 11 None None Yasuda et al.31 NR I 4 IIA 8 IIB 11 III 10 IVA 1 IVB 6 Retrosternal 39 Orthotopic 1 2FL 4–12 3FL 8–21 3FL + CDBIMS 4–37 Cervical CT 14 CRT 2 NR Okumura et al.28 NR I/II 20 III/IV 6 Retrosternal 20 Subcutaneous 6 Dissected Cervical CT 6 CRT 1 NR Kim et al.34 SCC T2–3 N0–1 M0 NR 3FL Cervical NR CRT 10 Lee et al.29 NR NR NR Cervical lymph node dissection 27 Cervical 33 Noncervical 85 CRT 24 NR Kumai et al.35 NR NR Retrosternal 25 3FL 25 Cervical 25 NR NR Kumai et al.39 NR II 3 III 10 IVa 1 Retrosternal 14 3FL 14 Cervical 14 None NR Lewin et al.36 TH 16 TT 10 SCC 5 AD 19 Barrett's esophagus + HGD 2 NR NR NR Cervical 21 Thoracic 5 CRT 12 Photodynamic 1 NR 2FL, two-field lymphadenectomy; 3FL, three-field lymphadenectomy; AD, adenocarcinoma; CRT, chemoradiation therapy; CT, chemotherapy; HGD high-grade dysplasia; NR, not recorded; SCC, squamous cell carcinoma; TH, transhiatal; TT, transthoracic. View Large Table 2 Treatment features of the included studies by surgical approach (n = 12). Reference Surgical approach Cancer type Pathological stage Reconstruction route Lymph node dissection Anastomosis site Neoadjuvant therapy Adjuvant therapy Easterling et al.32 TH AD NR Posterior mediastinum NR Cervical NR NR Martin et al.33 SCC 3 AD 7 T1N0M0 1 T2N0M0 4 T3N0M0 1 T3N1M0 4 Posterior mediastinum One node 3 Two nodes 1 Cervical None None Koh et al.37 AD NR Posterior mediastinum NR Cervical NR NR Leder et al.38 NR NR NR NR Cervical Neoadjuvant therapy 57(Detail was not shown) NR Kato et al.30 TT NR NR Posterior mediastinum 3FL 16 2FL 11 Cervical 16 Intrathoracic 11 None None Yasuda et al.31 NR I 4 IIA 8 IIB 11 III 10 IVA 1 IVB 6 Retrosternal 39 Orthotopic 1 2FL 4–12 3FL 8–21 3FL + CDBIMS 4–37 Cervical CT 14 CRT 2 NR Okumura et al.28 NR I/II 20 III/IV 6 Retrosternal 20 Subcutaneous 6 Dissected Cervical CT 6 CRT 1 NR Kim et al.34 SCC T2–3 N0–1 M0 NR 3FL Cervical NR CRT 10 Lee et al.29 NR NR NR Cervical lymph node dissection 27 Cervical 33 Noncervical 85 CRT 24 NR Kumai et al.35 NR NR Retrosternal 25 3FL 25 Cervical 25 NR NR Kumai et al.39 NR II 3 III 10 IVa 1 Retrosternal 14 3FL 14 Cervical 14 None NR Lewin et al.36 TH 16 TT 10 SCC 5 AD 19 Barrett's esophagus + HGD 2 NR NR NR Cervical 21 Thoracic 5 CRT 12 Photodynamic 1 NR Reference Surgical approach Cancer type Pathological stage Reconstruction route Lymph node dissection Anastomosis site Neoadjuvant therapy Adjuvant therapy Easterling et al.32 TH AD NR Posterior mediastinum NR Cervical NR NR Martin et al.33 SCC 3 AD 7 T1N0M0 1 T2N0M0 4 T3N0M0 1 T3N1M0 4 Posterior mediastinum One node 3 Two nodes 1 Cervical None None Koh et al.37 AD NR Posterior mediastinum NR Cervical NR NR Leder et al.38 NR NR NR NR Cervical Neoadjuvant therapy 57(Detail was not shown) NR Kato et al.30 TT NR NR Posterior mediastinum 3FL 16 2FL 11 Cervical 16 Intrathoracic 11 None None Yasuda et al.31 NR I 4 IIA 8 IIB 11 III 10 IVA 1 IVB 6 Retrosternal 39 Orthotopic 1 2FL 4–12 3FL 8–21 3FL + CDBIMS 4–37 Cervical CT 14 CRT 2 NR Okumura et al.28 NR I/II 20 III/IV 6 Retrosternal 20 Subcutaneous 6 Dissected Cervical CT 6 CRT 1 NR Kim et al.34 SCC T2–3 N0–1 M0 NR 3FL Cervical NR CRT 10 Lee et al.29 NR NR NR Cervical lymph node dissection 27 Cervical 33 Noncervical 85 CRT 24 NR Kumai et al.35 NR NR Retrosternal 25 3FL 25 Cervical 25 NR NR Kumai et al.39 NR II 3 III 10 IVa 1 Retrosternal 14 3FL 14 Cervical 14 None NR Lewin et al.36 TH 16 TT 10 SCC 5 AD 19 Barrett's esophagus + HGD 2 NR NR NR Cervical 21 Thoracic 5 CRT 12 Photodynamic 1 NR 2FL, two-field lymphadenectomy; 3FL, three-field lymphadenectomy; AD, adenocarcinoma; CRT, chemoradiation therapy; CT, chemotherapy; HGD high-grade dysplasia; NR, not recorded; SCC, squamous cell carcinoma; TH, transhiatal; TT, transthoracic. View Large Table 3 Swallowing biomechanics and dysphagic symptoms in the included studies by surgical approach (n = 12). Reference Surgical approach Methods Test materials Timing of swallowing evaluation Vocal fold immobility Key findings regarding swallowing biomechanics and dysphagic symptoms Before surgery After surgery Easterling et al.32 TH VFSS 5 mL thin barium N/A 1. 7–10 days 2. 17–29 days 3.42–105 days 25.0% • Aspiration (5 of 8; 62.5%) • Residue in the pyriform sinus (5 of 8; 62.5%) • The maximum UES anterior–posterior diameter and maximum anterior hyoid elevation in patients who aspirated were significantly smaller than those of age-matched normal controls Martin et al.33 VFSS 2,5,10mL thin and thick barium, 1 tsp cookie 2–21 days 44–134 days NR • Penetration/aspiration (2 of 5; 40%) • Residue in the valleculae, pyriform sinuses, and/or coating the posterior pharyngeal wall (5 of 5; 100%) • Anterior hyoid elevation was significantly decreased postoperatively for one subject and significantly increased for one subject. Superior hyoid elevation did not differ significantly. • Mild oropharyngeal dysphagia was observed before surgery (delayed initiation of swallowing, abnormal bolus formation, postswallow residue). Koh et al.37 VFSS Barium bolus, volume unspecified N/A 6–40 months (median 18 months) NR • Aspiration (0/9; 0%) • Residue in the valleculae (2 of 9; 22%) Leder et al.38 FEES 5mL custard, milk, cracker N/A 5 days 33.0% • Aspiration (15 of 73; 21%), penetration (24 of 73; 33%) • Pooling (9 of 73; 12%), spillage (4 of 73; 5%), residue (19 of 73; 26%) • Vocal fold immobility was associated with aspiration. Kato 200730 TT VFSS 10ml thin barium days not specified 14–21days NR • Superior/anterior hyoid elevation significantly decreased in patients who underwent intrathoracic esophagectomy with retrosternal reconstruction. Yasuda et al.31 VFSS Thin barium, volume unspecified N/A 7–62 days 20.0% • Laryngeal elevation was significantly impaired after 3FL as compared to 2FL. • A significant improvement of laryngeal elevation, compared with the 3FL group, was observed in the 3FL + CDBIMS group • Incomplete airway protection was observed in 25% of the 3FL + CDBIMS group, which was significantly lower than the 3FL group (70%), and was not different from the 2FL group (20%). Okumura et al.28 VFSS Thin iopamidol, volume unspecified N/A 4 time points for the experiment group, days after surgery not specified 28.6% • The maximum anterior/superior hyoid elevation and the anteroposterior diameters of the UES opening during swallows did not differ significantly among the four time points. Reference Surgical approach Methods Test materials Timing of swallowing evaluation Vocal fold immobility Key findings regarding swallowing biomechanics and dysphagic symptoms Before surgery After surgery • The volume of residue in the laryngeal vestibule and the pyriform sinus decreased significantly. Kim et al.34 VFSS 3ml thin barium N/A Aspiration group 8.2 ± 1.6 days No aspiration group 8.0 ± 1.8 days 14.9% • Aspiration (23 of 47; 48.9%) • Maximal anterior displacement of the hyoid, maximal rotation of the epiglottis, and pharyngeal delay time in normal group were significantly different from patients who underwent esophagectomy. • Pharyngeal delay time was significantly correlated with vocal cord palsy and aspiration. Lee et al.29 VFSS 3,6,9 mL thin barium, barium pudding, 1tsp of barium coated cookie N/A 7–10 days 12.7% • Aspiration (38/118; 32.2%), silent aspiration (17/118; 14.4%) • Vocal cord paralysis were risk factors for subglottic aspiration. • The clinical bedside swallowing test had a sensitivity of 68.4%. Kumai et al.35 VFSS NR N/A 2–3 weeks 76.0% • Aspiration (9/25; 36.0%), penetration (2/25; 8.0%). • Laryngeal aspiration was significantly correlated with reduced laryngeal elevation. • The penetration-aspiration scale score was significantly improved after training in chin-down swallowing. Kumai et al.39 FEES VFSS 3- or 5-mm thin barium or iopamidol N/A 14.8 ± 0.4 days 42.9% • Aspiration (2/14; 14.2%) • The pharyngeal constriction ratio and residue in the pyriform sinus for the chin-down position were significantly smaller than those in the neutral position. • The residue in the valleculae was not significantly different between the neutral and chin-down positions. • The UES opening diameter, duration of UES opening, and duration of laryngeal vestibule closure in the chin-down position were all significantly prolonged compared with those in the neutral position. Lewin et al.36 TH/TT VFSS 5 mL thin, 5mL thick barium, 5 mL applesauce 1/4 cracker N/A 6–43 days NR • Aspiration on thin liquid (21 of 26; 81.0%); both thin and thickened liquids (8 of 26; 30.8%); puree as well as thin and thickened liquids (3 of 26; 11.5%) • Chin-tuck swallow eliminated aspiration in 17/21 patients (80%). Reference Surgical approach Methods Test materials Timing of swallowing evaluation Vocal fold immobility Key findings regarding swallowing biomechanics and dysphagic symptoms Before surgery After surgery Easterling et al.32 TH VFSS 5 mL thin barium N/A 1. 7–10 days 2. 17–29 days 3.42–105 days 25.0% • Aspiration (5 of 8; 62.5%) • Residue in the pyriform sinus (5 of 8; 62.5%) • The maximum UES anterior–posterior diameter and maximum anterior hyoid elevation in patients who aspirated were significantly smaller than those of age-matched normal controls Martin et al.33 VFSS 2,5,10mL thin and thick barium, 1 tsp cookie 2–21 days 44–134 days NR • Penetration/aspiration (2 of 5; 40%) • Residue in the valleculae, pyriform sinuses, and/or coating the posterior pharyngeal wall (5 of 5; 100%) • Anterior hyoid elevation was significantly decreased postoperatively for one subject and significantly increased for one subject. Superior hyoid elevation did not differ significantly. • Mild oropharyngeal dysphagia was observed before surgery (delayed initiation of swallowing, abnormal bolus formation, postswallow residue). Koh et al.37 VFSS Barium bolus, volume unspecified N/A 6–40 months (median 18 months) NR • Aspiration (0/9; 0%) • Residue in the valleculae (2 of 9; 22%) Leder et al.38 FEES 5mL custard, milk, cracker N/A 5 days 33.0% • Aspiration (15 of 73; 21%), penetration (24 of 73; 33%) • Pooling (9 of 73; 12%), spillage (4 of 73; 5%), residue (19 of 73; 26%) • Vocal fold immobility was associated with aspiration. Kato 200730 TT VFSS 10ml thin barium days not specified 14–21days NR • Superior/anterior hyoid elevation significantly decreased in patients who underwent intrathoracic esophagectomy with retrosternal reconstruction. Yasuda et al.31 VFSS Thin barium, volume unspecified N/A 7–62 days 20.0% • Laryngeal elevation was significantly impaired after 3FL as compared to 2FL. • A significant improvement of laryngeal elevation, compared with the 3FL group, was observed in the 3FL + CDBIMS group • Incomplete airway protection was observed in 25% of the 3FL + CDBIMS group, which was significantly lower than the 3FL group (70%), and was not different from the 2FL group (20%). Okumura et al.28 VFSS Thin iopamidol, volume unspecified N/A 4 time points for the experiment group, days after surgery not specified 28.6% • The maximum anterior/superior hyoid elevation and the anteroposterior diameters of the UES opening during swallows did not differ significantly among the four time points. Reference Surgical approach Methods Test materials Timing of swallowing evaluation Vocal fold immobility Key findings regarding swallowing biomechanics and dysphagic symptoms Before surgery After surgery • The volume of residue in the laryngeal vestibule and the pyriform sinus decreased significantly. Kim et al.34 VFSS 3ml thin barium N/A Aspiration group 8.2 ± 1.6 days No aspiration group 8.0 ± 1.8 days 14.9% • Aspiration (23 of 47; 48.9%) • Maximal anterior displacement of the hyoid, maximal rotation of the epiglottis, and pharyngeal delay time in normal group were significantly different from patients who underwent esophagectomy. • Pharyngeal delay time was significantly correlated with vocal cord palsy and aspiration. Lee et al.29 VFSS 3,6,9 mL thin barium, barium pudding, 1tsp of barium coated cookie N/A 7–10 days 12.7% • Aspiration (38/118; 32.2%), silent aspiration (17/118; 14.4%) • Vocal cord paralysis were risk factors for subglottic aspiration. • The clinical bedside swallowing test had a sensitivity of 68.4%. Kumai et al.35 VFSS NR N/A 2–3 weeks 76.0% • Aspiration (9/25; 36.0%), penetration (2/25; 8.0%). • Laryngeal aspiration was significantly correlated with reduced laryngeal elevation. • The penetration-aspiration scale score was significantly improved after training in chin-down swallowing. Kumai et al.39 FEES VFSS 3- or 5-mm thin barium or iopamidol N/A 14.8 ± 0.4 days 42.9% • Aspiration (2/14; 14.2%) • The pharyngeal constriction ratio and residue in the pyriform sinus for the chin-down position were significantly smaller than those in the neutral position. • The residue in the valleculae was not significantly different between the neutral and chin-down positions. • The UES opening diameter, duration of UES opening, and duration of laryngeal vestibule closure in the chin-down position were all significantly prolonged compared with those in the neutral position. Lewin et al.36 TH/TT VFSS 5 mL thin, 5mL thick barium, 5 mL applesauce 1/4 cracker N/A 6–43 days NR • Aspiration on thin liquid (21 of 26; 81.0%); both thin and thickened liquids (8 of 26; 30.8%); puree as well as thin and thickened liquids (3 of 26; 11.5%) • Chin-tuck swallow eliminated aspiration in 17/21 patients (80%). View Large Table 3 Swallowing biomechanics and dysphagic symptoms in the included studies by surgical approach (n = 12). Reference Surgical approach Methods Test materials Timing of swallowing evaluation Vocal fold immobility Key findings regarding swallowing biomechanics and dysphagic symptoms Before surgery After surgery Easterling et al.32 TH VFSS 5 mL thin barium N/A 1. 7–10 days 2. 17–29 days 3.42–105 days 25.0% • Aspiration (5 of 8; 62.5%) • Residue in the pyriform sinus (5 of 8; 62.5%) • The maximum UES anterior–posterior diameter and maximum anterior hyoid elevation in patients who aspirated were significantly smaller than those of age-matched normal controls Martin et al.33 VFSS 2,5,10mL thin and thick barium, 1 tsp cookie 2–21 days 44–134 days NR • Penetration/aspiration (2 of 5; 40%) • Residue in the valleculae, pyriform sinuses, and/or coating the posterior pharyngeal wall (5 of 5; 100%) • Anterior hyoid elevation was significantly decreased postoperatively for one subject and significantly increased for one subject. Superior hyoid elevation did not differ significantly. • Mild oropharyngeal dysphagia was observed before surgery (delayed initiation of swallowing, abnormal bolus formation, postswallow residue). Koh et al.37 VFSS Barium bolus, volume unspecified N/A 6–40 months (median 18 months) NR • Aspiration (0/9; 0%) • Residue in the valleculae (2 of 9; 22%) Leder et al.38 FEES 5mL custard, milk, cracker N/A 5 days 33.0% • Aspiration (15 of 73; 21%), penetration (24 of 73; 33%) • Pooling (9 of 73; 12%), spillage (4 of 73; 5%), residue (19 of 73; 26%) • Vocal fold immobility was associated with aspiration. Kato 200730 TT VFSS 10ml thin barium days not specified 14–21days NR • Superior/anterior hyoid elevation significantly decreased in patients who underwent intrathoracic esophagectomy with retrosternal reconstruction. Yasuda et al.31 VFSS Thin barium, volume unspecified N/A 7–62 days 20.0% • Laryngeal elevation was significantly impaired after 3FL as compared to 2FL. • A significant improvement of laryngeal elevation, compared with the 3FL group, was observed in the 3FL + CDBIMS group • Incomplete airway protection was observed in 25% of the 3FL + CDBIMS group, which was significantly lower than the 3FL group (70%), and was not different from the 2FL group (20%). Okumura et al.28 VFSS Thin iopamidol, volume unspecified N/A 4 time points for the experiment group, days after surgery not specified 28.6% • The maximum anterior/superior hyoid elevation and the anteroposterior diameters of the UES opening during swallows did not differ significantly among the four time points. Reference Surgical approach Methods Test materials Timing of swallowing evaluation Vocal fold immobility Key findings regarding swallowing biomechanics and dysphagic symptoms Before surgery After surgery • The volume of residue in the laryngeal vestibule and the pyriform sinus decreased significantly. Kim et al.34 VFSS 3ml thin barium N/A Aspiration group 8.2 ± 1.6 days No aspiration group 8.0 ± 1.8 days 14.9% • Aspiration (23 of 47; 48.9%) • Maximal anterior displacement of the hyoid, maximal rotation of the epiglottis, and pharyngeal delay time in normal group were significantly different from patients who underwent esophagectomy. • Pharyngeal delay time was significantly correlated with vocal cord palsy and aspiration. Lee et al.29 VFSS 3,6,9 mL thin barium, barium pudding, 1tsp of barium coated cookie N/A 7–10 days 12.7% • Aspiration (38/118; 32.2%), silent aspiration (17/118; 14.4%) • Vocal cord paralysis were risk factors for subglottic aspiration. • The clinical bedside swallowing test had a sensitivity of 68.4%. Kumai et al.35 VFSS NR N/A 2–3 weeks 76.0% • Aspiration (9/25; 36.0%), penetration (2/25; 8.0%). • Laryngeal aspiration was significantly correlated with reduced laryngeal elevation. • The penetration-aspiration scale score was significantly improved after training in chin-down swallowing. Kumai et al.39 FEES VFSS 3- or 5-mm thin barium or iopamidol N/A 14.8 ± 0.4 days 42.9% • Aspiration (2/14; 14.2%) • The pharyngeal constriction ratio and residue in the pyriform sinus for the chin-down position were significantly smaller than those in the neutral position. • The residue in the valleculae was not significantly different between the neutral and chin-down positions. • The UES opening diameter, duration of UES opening, and duration of laryngeal vestibule closure in the chin-down position were all significantly prolonged compared with those in the neutral position. Lewin et al.36 TH/TT VFSS 5 mL thin, 5mL thick barium, 5 mL applesauce 1/4 cracker N/A 6–43 days NR • Aspiration on thin liquid (21 of 26; 81.0%); both thin and thickened liquids (8 of 26; 30.8%); puree as well as thin and thickened liquids (3 of 26; 11.5%) • Chin-tuck swallow eliminated aspiration in 17/21 patients (80%). Reference Surgical approach Methods Test materials Timing of swallowing evaluation Vocal fold immobility Key findings regarding swallowing biomechanics and dysphagic symptoms Before surgery After surgery Easterling et al.32 TH VFSS 5 mL thin barium N/A 1. 7–10 days 2. 17–29 days 3.42–105 days 25.0% • Aspiration (5 of 8; 62.5%) • Residue in the pyriform sinus (5 of 8; 62.5%) • The maximum UES anterior–posterior diameter and maximum anterior hyoid elevation in patients who aspirated were significantly smaller than those of age-matched normal controls Martin et al.33 VFSS 2,5,10mL thin and thick barium, 1 tsp cookie 2–21 days 44–134 days NR • Penetration/aspiration (2 of 5; 40%) • Residue in the valleculae, pyriform sinuses, and/or coating the posterior pharyngeal wall (5 of 5; 100%) • Anterior hyoid elevation was significantly decreased postoperatively for one subject and significantly increased for one subject. Superior hyoid elevation did not differ significantly. • Mild oropharyngeal dysphagia was observed before surgery (delayed initiation of swallowing, abnormal bolus formation, postswallow residue). Koh et al.37 VFSS Barium bolus, volume unspecified N/A 6–40 months (median 18 months) NR • Aspiration (0/9; 0%) • Residue in the valleculae (2 of 9; 22%) Leder et al.38 FEES 5mL custard, milk, cracker N/A 5 days 33.0% • Aspiration (15 of 73; 21%), penetration (24 of 73; 33%) • Pooling (9 of 73; 12%), spillage (4 of 73; 5%), residue (19 of 73; 26%) • Vocal fold immobility was associated with aspiration. Kato 200730 TT VFSS 10ml thin barium days not specified 14–21days NR • Superior/anterior hyoid elevation significantly decreased in patients who underwent intrathoracic esophagectomy with retrosternal reconstruction. Yasuda et al.31 VFSS Thin barium, volume unspecified N/A 7–62 days 20.0% • Laryngeal elevation was significantly impaired after 3FL as compared to 2FL. • A significant improvement of laryngeal elevation, compared with the 3FL group, was observed in the 3FL + CDBIMS group • Incomplete airway protection was observed in 25% of the 3FL + CDBIMS group, which was significantly lower than the 3FL group (70%), and was not different from the 2FL group (20%). Okumura et al.28 VFSS Thin iopamidol, volume unspecified N/A 4 time points for the experiment group, days after surgery not specified 28.6% • The maximum anterior/superior hyoid elevation and the anteroposterior diameters of the UES opening during swallows did not differ significantly among the four time points. Reference Surgical approach Methods Test materials Timing of swallowing evaluation Vocal fold immobility Key findings regarding swallowing biomechanics and dysphagic symptoms Before surgery After surgery • The volume of residue in the laryngeal vestibule and the pyriform sinus decreased significantly. Kim et al.34 VFSS 3ml thin barium N/A Aspiration group 8.2 ± 1.6 days No aspiration group 8.0 ± 1.8 days 14.9% • Aspiration (23 of 47; 48.9%) • Maximal anterior displacement of the hyoid, maximal rotation of the epiglottis, and pharyngeal delay time in normal group were significantly different from patients who underwent esophagectomy. • Pharyngeal delay time was significantly correlated with vocal cord palsy and aspiration. Lee et al.29 VFSS 3,6,9 mL thin barium, barium pudding, 1tsp of barium coated cookie N/A 7–10 days 12.7% • Aspiration (38/118; 32.2%), silent aspiration (17/118; 14.4%) • Vocal cord paralysis were risk factors for subglottic aspiration. • The clinical bedside swallowing test had a sensitivity of 68.4%. Kumai et al.35 VFSS NR N/A 2–3 weeks 76.0% • Aspiration (9/25; 36.0%), penetration (2/25; 8.0%). • Laryngeal aspiration was significantly correlated with reduced laryngeal elevation. • The penetration-aspiration scale score was significantly improved after training in chin-down swallowing. Kumai et al.39 FEES VFSS 3- or 5-mm thin barium or iopamidol N/A 14.8 ± 0.4 days 42.9% • Aspiration (2/14; 14.2%) • The pharyngeal constriction ratio and residue in the pyriform sinus for the chin-down position were significantly smaller than those in the neutral position. • The residue in the valleculae was not significantly different between the neutral and chin-down positions. • The UES opening diameter, duration of UES opening, and duration of laryngeal vestibule closure in the chin-down position were all significantly prolonged compared with those in the neutral position. Lewin et al.36 TH/TT VFSS 5 mL thin, 5mL thick barium, 5 mL applesauce 1/4 cracker N/A 6–43 days NR • Aspiration on thin liquid (21 of 26; 81.0%); both thin and thickened liquids (8 of 26; 30.8%); puree as well as thin and thickened liquids (3 of 26; 11.5%) • Chin-tuck swallow eliminated aspiration in 17/21 patients (80%). View Large Abnormalities in swallowing biomechanics and swallowing symptoms after esophagectomy Table 3 also displays the reported key findings on swallowing biomechanics and swallowing symptoms following esophagectomy. In patients who received transhiatal esophagectomy, several abnormal swallowing biomechanics were reported: vocal fold immobility (25.0%32–33.0%38), delayed onset of swallowing,33 reduced hyolaryngeal elevation during swallowing,32,33 and reduced maximum anterior–posterior diameter of the UES during swallowing.33 As for swallowing symptoms, overt aspiration (0%37–81.0%29) and pharyngeal residue (22.0%37 in the pyriform sinus and 62.5%32 in the valleculae) presented. Reported abnormalities in swallowing biomechanics after transthoracic esophagectomy were similar to those presented after transhiatal esophagectomy: vocal fold immobility (12.7%29–76.0%35), delayed onset of swallowing,34 reduced hyolaryngeal elevation during swallowing,31,35 particularly in patients who underwent three-field lymphadenectomy,31 and reduced maximum anterior–posterior diameter of the UES during swallowing particularly with reconstruction via the retrosternal route.30 Overt aspiration (12.7%29–76.0%35), silent aspiration (14.4%29), and pharyngeal residue (100%) were also reported.39 Aspiration was found to be significantly associated with vocal fold immobility,29,38 decreased excursion of the hyoid,32,35 reduced UES anterior–posterior opening,32 the three-field lymphadenectomy,31 and operation time greater than or equal to six hours in postesophagectomy patients.29 Thickening liquids decreased the occurrence of aspiration during the swallowing evaluation.36 Additive complete division of the bilateral infrahyoid muscles attached to the sternum was found to be a significant suppressor of penetration and aspiration after esophagectomy with three-field lymphadenectomy.31 Health-related outcomes after esophagectomy Three studies reported the occurrence of pneumonia,28,29,31 which ranged between 5%31 and 25%28 of the patients who underwent transthoracic esophagectomy. Occurrence of pneumonia was higher in patients who aspirated during VFSS trials (13.2%) than in patients who did not aspirate (0%);29 in patients who underwent the three-field lymphadenectomy (20%) than in patients who underwent the two-field lymphadenectomy (10%) or the three-field lymphadenectomy with complete division of the bilateral infrahyoid muscles attached to the sternum (5%).31 One study reported patients’ diet levels following transthoracic esophagectomy.35 Majority of patients were temporarily dependent on tube-feeding or total parenteral nutrition at the time of postoperative VFSS, and had learned the chin tuck as a compensatory swallowing maneuver. Nearly 100% of the study patients were fed orally at discharge, which was at 29.5 ± 2.5 days after the postoperative VFSS was performed.35 Rehabilitative interventions for postesophagectomy oropharyngeal dysphagia Four studies, one quasi-experimental trial28 and three case series,35,36,39 reported rehabilitative interventions provided with this patient population. Okumura and colleagues provided perioperative nonswallowing exercises to patients who were undergoing esophagectomy.28 The rehabilitative program included pursed lip breathing, a cervical range of motion exercise, shoulder stretches, jaw opening, tongue exercises, and submental muscle training. The authors reported that the exercises did not change swallowing biomechanics of the patients, but the volume of laryngeal and pharyngeal residue after esophagectomy decreased significantly in patients who underwent perioperative swallowing exercises.28 Three case series observed immediate positive effect of the chin-tuck maneuver for improving airway protection by effectively eliminating aspiration after surgery.35,36,39 Pyriform sinus residue was significantly reduced when postesophagectomy patients implemented the chin tuck maneuver compared to the neutral position.39 The chin-tuck maneuver also increased UES opening diameter and prolonged duration of UES opening and duration of laryngeal vestibule closure compared with those in the neutral position.39 Quality assessment The JBI Critical Appraisal Checklists scores were low for quasi-experimental study28 (4 out of 9 points) and diagnostic accuracy study29 (4 out of 10 points), and were varied for case series (532,33,36,37–835,40 out of 10 points). The methodological quality of the majority of the included studies was not sufficient. DISCUSSION This systematic review revealed several pathological patterns in swallowing biomechanics after transhiatal and transthoracic esophagectomy. The abnormalities in swallowing included delayed onset of swallowing, reduced hyoid or hyolaryngeal elevation, and reduced UES opening. Both overt and silent aspiration and pharyngeal residue were commonly reported following esophagectomy. The abnormal biomechanics found in this review may explain the underlying mechanism of swallowing symptoms in postesophagectomy patients. In this population, initiation of swallowing tends to be delayed.41 Thus, the bolus can be propelled into the pharynx before the hyoid and larynx are pulled up and the epiglottis is passively retroflexed to its maximally lowered position to cover the laryngeal vestibule. 42 As a result, the bolus can be misdirected into the laryngeal vestibule. Vocal fold immobility due to the injury to the recurrent nerve during esophagectomy allows the penetrated materials to be easily aspirated to the trachea. Further, the damage to the pharyngeal plexus33,43 or scarring at the anastomotic area30 may reduce pharyngeal muscle contraction and UES opening. These pharyngeal dysfunctions may lead to pharyngeal residue, which can be aspirated when the patient attempts to clear them with additional clearing swallows.44 This review also aimed to examine the reported health-related outcomes in relation to swallowing abnormality following esophagectomy. Increased risk for pneumonia was found in patients who aspirated during VFSS trials.29 The high incidence of silent aspiration reported in this patient population29,36 and low sensitivity of the bedside screening test against VFSS29 emphasize the importance of instrumental evaluations when assessing patients who received esophagectomy. Only one study reported diet outcomes of the study patients.35 This lack of evidence suggests the need for future studies examining health-related outcomes of postesophagectomy oropharyngeal dysphagia, including length of time for dependence on alternative means of nutrition such as jejunostomy. Alternative means of nutrition along with a systematic and gradual introduction of the least restrictive diet can improve patient's health related outcomes. This can help set expectations for the healing processing, and rehabilitation postesophagectomy. Finally, this review revealed that evidence was scant regarding rehabilitative interventions for postesophagectomy oropharyngeal dysphagia. One study provided perioperative swallowing rehabilitation to patients who were undergoing esophagectomy.28 However, the study did not observe any improvement in swallowing biomechanics. This may be because its rehabilitative program did not target the pharyngeal abnormalities, which have now been identified in this review. The pharyngeal muscle training45,46 as well as the submental muscle training47 may be more relevant to restore the impaired hyolaryngeal excursion and pharyngeal contraction that could occur following esophagectomy. Three small case series indicated the potential efficacy of chin-tuck maneuver in reducing aspiration35 and pharyngeal residue39 (in both pyriform and valleculae structures). The chin-tuck maneuver appears to be a reasonable strategy to trial during postesophagectomy recovery since this swallowing technique has been found to alleviate aspiration48 and pharyngeal residue49 by decreasing distance between the hyoid bone and larynx,50,51 prolonging the duration of laryngeal vestibule closure52 and UES opening,53,54 all of which were often limited in this patient population. Other potential management strategies include thickening liquids, which may also prevent aspiration of this patient population.36 Since thickened liquids tend to flow more slowly, it can provide patients with delayed initiation of swallowing more control during swallowing.36 Although not discussed in the reviewed studies, postural modifications such as head turns and head tilts are compensatory strategies, which could be trialed during swallowing evaluations. The studies reviewed found a wide range of vocal fold immobility rates between 25.0%32 and 33.0%38 for patients who underwent transhiatal esophagectomy, and between 12.7%29 and 76.0%35 for patients who underwent transthoracic esophagectomy. In these instances, surgical interventions, both injection medialization and thyroplasty may alleviate swallowing symptoms in patients with vocal fold immobility,55 which was prevalent in this patient population. Most of the included studies performed instrumental evaluation only after esophagectomy. Thus, it is difficult to determine if the observed swallowing abnormalities and dysphagic symptoms following esophagectomy are resultant of the surgery or are preexisting characteristics of the patients with esophageal cancer. Further, none of the included studies performed follow-up swallowing evaluation to understand the trajectory of swallowing rehabilitation. In order to understand the recovery process of oropharyngeal dysphagia, follow up evaluations may also assist future development of rehabilitative intervention. Our review has some limitations. The weak study designs with limited methodological quality of the included studies may make the results of our analyses less conclusive. There may be eligible studies archived in databases and search algorithms that we did not use for literature search and thus were not identified. In conclusion, our systematic review revealed that vocal fold immobility, delayed onset of swallowing, reduced hyolaryngeal elevation, and reduced UES opening during swallowing were frequently reported in the literature in the patients who underwent esophagectomy. These pathological swallowing patterns may contribute to incomplete airway closure and reduced bolus clearance, resulting in aspiration and pharyngeal residue observed in swallows after esophagectomy. Pneumonia and restricted diets were found in patients who received esophagectomy. Evidence was scant regarding the therapeutic interventions for postesophagectomy oropharyngeal dysphagia. These results indicate the urgent need for future studies for developing effective swallowing exercises and management strategies for oropharyngeal dysphagia secondary to esophagectomy. The results, however, should be interpreted with caution, given limited generalizability and potential biases inherent to the include studies. Notes Specific author contributions:Asako Kaneoka designed the study, searched, and reviewed the literature, acquired data of the publications, assessed the quality of the included studies, interpreted the data, and drafted the manuscript with the guidance of the co-authors. Sky Yang reviewed the literature, acquired the data, and edited the manuscript. Haruhi Inokuchi assessed the quality of included studies. All investigators contributed to the study design and interpretation of the results, and critically revised the manuscript and approved the final version. ACKNOWLEDGMENTS The authors are grateful for the assistance provided by Helena Vonville, MPH and for her expertise in systematic searching. The authors would also like to acknowledge, Dr. Hidetomi Yamada, PhD, MD, for reviewing a German article, Ms. Maxine Van Doren M.S., CCC-SLP, for reviewing French articles, and Margo Naraghi-Grcich, M.A., CCC-SLP, CBIS for editing this paper. Funding was not received for this study. 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Google Scholar CrossRef Search ADS PubMed 26 Martino R , McCulloch T . Therapeutic intervention in oropharyngeal dysphagia . Nat Rev Gastroenterol Hepatol 2016 ; 13 : 665 – 79 . Google Scholar CrossRef Search ADS PubMed 27 Pearson A , Field J , Jordan Z , Wiley InterScience (Online service). Evidence-Based Clinical Practice in Nursing and Healthcare: Assimilating Research, Experience and Expertise . Chicester, United Kingdom , Updated 2007 . 28 Okumura T , Shimada Y , Watanabe T , Nakamichi N , Nagata T , Tsukada K . Functional outcome assessment of swallowing (FOAMS) scoring and videofluoroscopic evaluation of perioperative swallowing rehabilitation in radical esophagectomy . Surg Today 2016 ; 46 : 543 – 51 . Google Scholar CrossRef Search ADS PubMed 29 Lee S Y , Cheon H J , Kim S J , Shim Y M , Zo J I , Hwang J H . Clinical predictors of aspiration after esophagectomy in esophageal cancer patients . Support Care Cancer 2016 ; 24 : 295 – 9 . Google Scholar CrossRef Search ADS PubMed 30 Kato H , Miyazaki T , Sakai M et al. Videofluoroscopic evaluation in oropharyngeal swallowing after radical esophagectomy with lymphadenectomy for esophageal cancer . Anticancer Res 2007 ; 27 ( 6C ): 4249 – 54 . Google Scholar PubMed 31 Yasuda T , Yano M , Miyata H et al. Evaluation of dysphagia and diminished airway protection after three-field esophagectomy and a remedy . World J Surg 2013 ; 37 : 416 – 23 . Google Scholar CrossRef Search ADS PubMed 32 Easterling CS , Bousamra M 2nd , Lang I M et al. Pharyngeal dysphagia in postesophagectomy patients: correlation with deglutitive biomechanics . Ann Thorac Surg 2000 ; 69 : 989 – 92 . Google Scholar CrossRef Search ADS PubMed 33 Martin R E , Letsos P , Taves D H , Inculet R I , Johnston H , Preiksaitis H G . Oropharyngeal dysphagia in esophageal cancer before and after transhiatal esophagectomy . Dysphagia 2001 ; 16 : 23 – 31 . Google Scholar CrossRef Search ADS PubMed 34 Kim S J , Cheon H J , Lee H N , Hwang J H . Kinematic analysis of swallowing in the patients with esophagectomy for esophageal cancer . J Electromyogr Kinesiol 2016 ; 28 : 208 – 13 . Google Scholar CrossRef Search ADS PubMed 35 Kumai Y , Samejima Y , Watanabe M , Yumoto E . Videofluoroscopic evaluation of pharyngeal swallowing dysfunction after esophagectomy with three-field lymph node dissection . Eur Arch Otorhinolaryngol 2017 ; 274 : 321 – 6 . Google Scholar CrossRef Search ADS PubMed 36 Lewin J S , Hebert T M , Putnam J B , Jr DuBrow R A . Experience with the chin tuck maneuver in postesophagectomy aspirators . Dysphagia 2001 ; 16 : 216 – 9 . Google Scholar CrossRef Search ADS PubMed 37 Koh P , Turnbull G , Attia E , LeBrun P , Casson A G . Functional assessment of the cervical esophagus after gastric transposition and cervical esophagogastrostomy . Eur J Cardiothorac Surg 2004 ; 25 : 480 – 5 . Google Scholar CrossRef Search ADS PubMed 38 Leder S B , Bayar S , Sasaki C T , Salem R R . Fiberoptic endoscopic evaluation of swallowing in assessing aspiration after transhiatal esophagectomy . J Am Coll Surg 2007 ; 205 : 581 – 5 . Google Scholar CrossRef Search ADS PubMed 39 Kumai Y , Yoshida N , Kamenosono Y et al. Effects of chin-down maneuver on the parameters of swallowing function after esophagectomy with 3-field lymphadenectomy examined by videofluoroscopy . Arch Phys Med Rehabil 2017 ; 98 : 1174 – 9 . Google Scholar CrossRef Search ADS PubMed 40 Kim J Y , Kim S G , Lim J H , Im J P , Kim J S , Jung H C . Clinical outcomes of esophageal stents in patients with malignant esophageal obstruction according to palliative additional treatment . J Dig Dis 2015 ; 16 : 575 – 84 . Google Scholar CrossRef Search ADS PubMed 41 Perlman A L , Booth B M , Grayhack J P . Videofluoroscopic predictors of aspiration in patients with oropharyngeal dysphagia . Dysphagia 1994 ; 9 : 90 – 95 . 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Effect of the Masako maneuver and neuromuscular electrical stimulation on the improvement of swallowing function in patients with dysphagia caused by stroke . J Phys Ther Sci 2016 ; 28 : 2069 – 71 . Google Scholar CrossRef Search ADS PubMed 47 Shaker R , Easterling C , Kern M et al. Rehabilitation of swallowing by exercise in tube-fed patients with pharyngeal dysphagia secondary to abnormal UES opening . Gastroenterology 2002 ; 122 : 1314 – 21 . Google Scholar CrossRef Search ADS PubMed 48 Ra J Y , Hyun J K , Ko K R , Lee S J . Chin tuck for prevention of aspiration: effectiveness and appropriate posture . Dysphagia 2014 ; 29 : 603 – 9 . Google Scholar CrossRef Search ADS PubMed 49 Nagy A , Peladeau-Pigeon M , Valenzano T J , Namasivayam A M , Steele C M . The effectiveness of the head-turn-plus-chin-down maneuver for eliminating vallecular residue . Codas 2016 ; 28 : 113 – 7 . Google Scholar CrossRef Search ADS PubMed 50 Bulow M , Olsson R , Ekberg O . Videomanometric analysis of supraglottic swallow, effortful swallow, and chin tuck in healthy volunteers . Dysphagia 1999 ; 14 : 67 – 72 . Google Scholar CrossRef Search ADS PubMed 51 Bulow M , Olsson R , Ekberg O . Videomanometric analysis of supraglottic swallow, effortful swallow, and chin tuck in patients with pharyngeal dysfunction . Dysphagia 2001 ; 16 : 190 – 5 . Google Scholar CrossRef Search ADS PubMed 52 Young J L , Macrae P , Anderson C , Taylor-Kamara I , Humbert I A . The sequence of swallowing events during the chin-down posture . Am J Speech Lang Pathol 2015 ; 24 : 659 – 70 . Google Scholar CrossRef Search ADS PubMed 53 Balou M , McCullough G H , Aduli F et al. Manometric measures of head rotation and chin tuck in healthy participants . Dysphagia 2014 ; 29 : 25 – 32 . Google Scholar CrossRef Search ADS PubMed 54 McCulloch T M , Hoffman M R , Ciucci M R . High-resolution manometry of pharyngeal swallow pressure events associated with head turn and chin tuck . Ann Otol Rhinol Laryngol 2010 ; 119 : 369 – 76 . Google Scholar CrossRef Search ADS PubMed 55 Cates D J , Venkatesan N N , Strong B , Kuhn M A , Belafsky P C . Effect of vocal fold medialization on dysphagia in patients with unilateral vocal fold immobility . Otolaryngol Head Neck Surg 2016 ; 155 : 454 – 7 . Google Scholar CrossRef Search ADS PubMed © The Author(s) 2018. Published by Oxford University Press on behalf of International Society for Diseases of the Esophagus. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Diseases of the Esophagus Oxford University Press

Presentation of oropharyngeal dysphagia and rehabilitative intervention following esophagectomy: a systematic review

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The International Society for Diseases of the Esophagus
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© The Author(s) 2018. Published by Oxford University Press on behalf of International Society for Diseases of the Esophagus.
ISSN
1120-8694
eISSN
1442-2050
D.O.I.
10.1093/dote/doy050
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Abstract

SUMMARY No study has systematically reviewed the evidence on presentation of oropharyngeal dysphagia and swallowing rehabilitation following esophagectomy. The purposes of this systematic review are to 1) qualitatively synthesize the current findings on oropharyngeal swallowing abnormalities identified by instrumental swallowing evaluations, 2) describe the reported health-related outcomes in relation to swallowing abnormality following esophagectomy, and 3) examine the efficacy of reported rehabilitative interventions for oropharyngeal dysphagia in patients who underwent esophagectomy. Publications were searched using five electronic databases. No language or publication date restrictions were imposed. Two authors performed a blind review for published or unpublished studies that reported swallowing biomechanics and dysphagic symptoms using instrumental evaluation of swallowing, specifically the videofluoroscopic swallowing study and fiberoptic endoscopic evaluation of swallowing, and/or health-related outcomes in relation to swallowing abnormalities, and/or therapeutic interventions for oropharyngeal dysphagia following esophagectomy. Twelve studies out of 2,193 studies including 458 patients met the inclusion criteria. Reported abnormal swallowing biomechanics included vocal fold immobility, delayed onset of swallowing, reduced hyolaryngeal elevation, and reduced opening of the upper esophageal sphincter. Aspiration (0–81%) and pharyngeal residue (22–100%) were prevalent. Those abnormal swallowing biomechanics and swallowing symptoms were commonly reported following both transhiatal and transthoracic esophagectomy. Pneumonia presented in 5–25% of the study patients. One quasi-experimental study examined the effectiveness of swallowing exercises for postoperative oropharyngeal dysphagia; three case series reported a benefit of the chin-tuck maneuver in reducing aspiration and residue. This review revealed distinct swallowing impairments and increased pneumonia risks following esophagectomy. This review also found that evidence on the efficacy of therapeutic interventions was limited. Future studies are warranted to develop effective rehabilitative interventions for postesophagectomy patients with oropharyngeal dysphagia. INTRODUCTION Esophageal cancer is ranked as the eighth most common cancer worldwide and is the sixth most common cause of cancer-related death.1 Although the effectiveness of definitive chemotherapy,2 perioperative chemotherapy,3,4 and chemoradiotherapy5 has been reported, radical resection of the esophageal cancer has been the mainstay of treatment for this fatal malignancy.6 Meanwhile, complication rates for this highly invasive surgery have been reported to be as high as 22–29%.7-11 Unfavorable outcomes of the surgery can significantly impair patients’ long-term survival7 and quality of life.12-14 Major complications include anastomotic leakage, pulmonary complications, damage to the recurrent laryngeal nerve, dysphagia, strictures, reflux, and other gastrointestinal symptoms.10,11 Above all, the presence of dysphagia has been reported to increase the risk of pneumonia and mortality following esophagectomy.10 In addition, recent literature has found that patients who underwent surgical treatment for esophageal cancer had lower quality of life scores across many domains including swallowing impairments.15 Thus, it is crucial to provide patients with an adequate dysphagia assessment and therapeutic interventions in order to achieve better health outcomes and quality of life. When presence of dysphagia is suspected, two instrumental procedures are often used to assess the swallow function: the videofluoroscopic swallowing study (VFSS)16 and the fiberoptic endoscopic evaluation of swallowing (FEES).17 This study focused on impairments of the oropharyngeal stage of swallowing to investigate, given is prevalence in the postesophagectomy patient population. Understanding the oropharyngeal swallowing impairments as well as efficacy of behavior or postural modifications and exercises will improve our therapeutic intervention. To our knowledge, no research study has systematically examined the current findings about biomechanics of oropharyngeal swallowing and dysphagic symptoms following esophagectomy identified by instrumental evaluations. In order to better understand the underlying mechanism of postoperative oropharyngeal dysphagia, it will be valuable to synthesize the knowledge of pathophysiology and dysphagic symptoms associated with esophagectomy. It will also be important to understand the reported health-related outcomes in patients with oropharyngeal dysphagia following esophagectomy. Further, a summary of the reported rehabilitative interventions for oropharyngeal swallowing impairment will help develop a core set of swallowing exercises that may be most effective in treating this patient population. This review aims to qualitatively synthesize the current evidence on oropharyngeal swallowing abnormalities captured by instrumental evaluations of swallowing, specifically VFSS or FEES, in patients who underwent esophagectomy. Specific research questions of this systematic review are: What are the abnormalities in oropharyngeal swallowing biomechanics identified during VFSS or FEES following esophagectomy? What are the symptoms of oropharyngeal dysphagia identified during VFSS or FEES following esophagectomy? What are the reported health-related outcomes in relation to swallowing abnormality following esophagectomy? Is there any evidence to support that rehabilitative interventions are effective in improving swallowing function or health-related outcomes in patients with oropharyngeal dysphagia following esophagectomy? MATERIALS AND METHODS The review reported in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines.18 The predefined review protocol was registered at Center for Review and Dissemination (CRD42017056330). Search strategy Publications were searched from the August 30th, 2017 through the August 31st, 2017 using the MEDLINE [PubMed], Web of Science, CINAHL, Cochrane Database of Systematic Reviews, and Cochrane Central Register of Controlled Trials. To reduce investigator selection bias, all relevant search terms were defined a priori. The following is the search algorithm for searching MEDLINE: (esophageal cancer OR esophagus cancer) AND (esophagectomy OR esophageal surgery OR esophageal resection OR esophagus/surgery [MeSH Terms]) AND (dysphagia OR swallow OR deglutition OR deglutition disorders OR swallowing disorders OR oropharyngeal dysphagia) AND (modified barium swallow OR videofluoroscopy OR instrumental swallow OR VFSS OR FEES OR videofluoroscopic swallow study OR endoscopy OR videoendoscopy OR fiberoptic endoscopic evaluation of swallowing OR endoscopic evaluation of swallowing). Search was restricted to human studies. No language or publication date restriction was imposed. To ensure a comprehensive search, the first author scanned reference lists of included studies and previously published review articles. Study eligibility This review included studies that met the following criteria: 1) were published or unpublished original research articles; 2) retrospective and prospective studies; 3) studied adult (18 years or older) patients; 4) with a diagnosis of esophageal cancer; 5) treated with first-time esophagectomy (including both open esophagectomy and minimally invasive esophagectomy) with or without perioperative chemotherapy/chemoradiotherapy; 6) examined swallowing function of the patients using instrumental evaluations; and 7) reported swallowing biomechanical measurements and/or any symptoms of oropharyngeal dysphagia, rehabilitative interventions, and/or health-related outcomes in relation to oropharyngeal dysphagia using clearly described method(s). Studies that did not utilize VFSS or FEES to assess swallowing function were excluded because clinical swallowing evaluations do not allow researchers to objectively measure swallowing biomechanics or to accurately identify presence of swallowing symptoms.19 Further, case reports and case series that profiled fewer than five patients were excluded given the limited information provided by those studies. In this review, swallowing biomechanical measurements referred to any displacement measures of relevant structures for swallowing and time variables of swallowing motion identified by using VFSS or FEES.20,21Symptoms and signs of oropharyngeal dysphagia included penetration, aspiration, pharyngeal residue, and other abnormalities due to their frequent reporting in the literature.22,23Health-related outcomes in relation to swallowing abnormality included pneumonia, nutrition status, diet levels, and the use of alternative nutrition.24Rehabilitative interventions included exercise therapies that can be executed with or without accompanying food25,26 and compensatory swallowing strategies. Literature review Two review authors independently screened the abstracts of the identified studies for eligibility. The two authors then read full articles of potentially eligible studies for determining the eligibility. When publications were written in languages other than English, speech language pathologists, or medical doctors native to those languages reviewed the articles. Discrepancies in the inclusion between the two authors were resolved by discussion. Data extraction One review author extracted the following data from the included studies and the second reviewer checked the extracted data: 1) study characteristics, 2) the features of esophageal cancer treatment provided, 3) the key findings on biomechanical measurements and swallowing symptoms identified in the swallowing assessment performed, 4) health-related outcomes of esophagectomy in relation to swallowing abnormality; and 5) types of rehabilitative intervention and the effect of those interventions reported. Meta-analysis of the data was not possible due to high level of heterogeneity in subjects, research design, cancer treatment protocols, or swallowing assessment protocols across the included studies. Therefore, the extracted data were presented descriptively. Quality assessment Two review authors independently appraised the methodological quality of identified studies using the JBI Critical Appraisal Checklists for case series, diagnostic test accuracy studies, and quasi-experimental studies.27 Disagreements in the judgment between the two authors were resolved by discussion. RESULTS A total of 2193 records were identified from all sources (Fig. 1). After excluding duplicates, 2117 titles and abstracts were screened for eligibility. Of those, 34 studies (31 studies written in English, two in French, and one in German) were read in full for eligibility. Twelve studies consisting of 458 patients met all inclusion criteria and were included in the final systematic review. Fig. 1 View largeDownload slide PRISMA flowchart. Fig. 1 View largeDownload slide PRISMA flowchart. Characteristics of included studies Table 1 displays the characteristics of the 12 studies included in this review. One quasi-experimental study,28 one test accuracy study,29 and ten case series were included.30-39 Table 2 shows the features of cancer treatment provided in the included studies by surgical approach. Four studies from North America reported oropharyngeal dysphagia following transhiatal esophagectomy;32,33,37,38 seven studies from East Asia reported oropharyngeal dysphagia following transthoracic esophagectomy with lymph node dissection.28-31,34,35,39 One study involved patients who received either transhiatal or transthoracic esophagectomy.36 Table 3 summarizes the swallowing assessment performed in the included studies. Two of 12 studies performed VFSS both before and after esophagectomy.28,30,33 However, two of the three studies performed VFSS only on a part of their study participants,28,33 resulting in an unclear comparison between pre- and postoperative swallowing functions. No study performed longitudinal follow-up evaluations for swallowing. Table 1 Characteristics of the included studies (n = 12). References Country Study design Subject Mean or median age (range in years) % male Main purpose(s) of the study Easterling et al.32 USA Case series Patient 8 Healthy adult 8 NR (51–78) Age-matched NR to correlate the swallowing biomechanics with aspiration in patients with dysphagia after transhiatal esophagectomy Martin et al.33 Canada Case series 10 66.7 (49–76) 90.0 to compare pre- and postoperative swallowing patterns in patients who underwent transhiatal esophagectomy Lewin et al.36 USA Case series 26 66.0 (52–82) 88.5 to evaluate the use of chin tuck maneuver to alleviate aspiration during videofluoroscopy in patients who underwent esophagectomy Koh et al.37 Canada Case series 9 63.0 (52–76) 88.9 to investigate the function of the oral and pharyngeal phases of deglutition, and of the cervical esophagus, in patients who underwent transhiatal esophagectomy Leder et al.38 USA Case series 73 60.0 (39–74) 83.6 to characterize laryngeal physiology in patients who underwent transhiatal esophagectomy and to identify patients who are at high aspiration risk Kato et al.30 Japan Case series 27 64.3 (53–78) 100.0 to analyze the relationship between oropharyngeal swallowing and the alimentary reconstruction route after transthoracic esophagectomy Yasuda et al.31 Japan Case series 2FL 10 3FL 10 3FL + CDBIMS 20 61.4 (51–76) 61.3 (54–68) 61.5 (54–71) 80. 0100. 0 90.0 to compare swallowing function in patients who underwent esophagectomy with 2FL and 3FL, and to evaluate the preventative effect of the addition of CDBIMS for post-operative dysphagia Okumura et al.28 Japan Quasi-experimental Experiment 14 Control 12 65.9 ± 9.7 68.0 ± 5.1 92. 9100. 0 to assess the preventative and therapeutic effects of perioperative swallowing rehabilitation in patients undergoing esophagectomy Kim et al.34 Korea Case series Aspiration 23 No aspiration 24 Control 27 62.7 ± 8.2 63.3 ± 7.1 64.7 ± 10.1 100. 0100. 0100.0 to analyze the swallowing biomechanics in patients with oropharyngeal dysphagia after esophagectomy compared to healthy adults Lee et al.29 Korea Diagnostic test accuracy 118 63.4 ± 8.5 93.2 to assess the usefulness of clinical bedside swallowing tests for detecting aspiration after esophagectomy Kumai et al.35 Japan Case series 25 64.8 NR to identify the main factors associated with aspiration in patients with pharyngeal dysphagia following esophagectomy with 3FL and to assess the effectiveness of the chin-down maneuver Kumai et al.39 Japan Case series 14 65.9 ± 1.9 100.0 to determine the efficacy of the chin-down maneuver after esophagectomy with 3FL on pharyngeal residue, UES opening, and laryngeal closure References Country Study design Subject Mean or median age (range in years) % male Main purpose(s) of the study Easterling et al.32 USA Case series Patient 8 Healthy adult 8 NR (51–78) Age-matched NR to correlate the swallowing biomechanics with aspiration in patients with dysphagia after transhiatal esophagectomy Martin et al.33 Canada Case series 10 66.7 (49–76) 90.0 to compare pre- and postoperative swallowing patterns in patients who underwent transhiatal esophagectomy Lewin et al.36 USA Case series 26 66.0 (52–82) 88.5 to evaluate the use of chin tuck maneuver to alleviate aspiration during videofluoroscopy in patients who underwent esophagectomy Koh et al.37 Canada Case series 9 63.0 (52–76) 88.9 to investigate the function of the oral and pharyngeal phases of deglutition, and of the cervical esophagus, in patients who underwent transhiatal esophagectomy Leder et al.38 USA Case series 73 60.0 (39–74) 83.6 to characterize laryngeal physiology in patients who underwent transhiatal esophagectomy and to identify patients who are at high aspiration risk Kato et al.30 Japan Case series 27 64.3 (53–78) 100.0 to analyze the relationship between oropharyngeal swallowing and the alimentary reconstruction route after transthoracic esophagectomy Yasuda et al.31 Japan Case series 2FL 10 3FL 10 3FL + CDBIMS 20 61.4 (51–76) 61.3 (54–68) 61.5 (54–71) 80. 0100. 0 90.0 to compare swallowing function in patients who underwent esophagectomy with 2FL and 3FL, and to evaluate the preventative effect of the addition of CDBIMS for post-operative dysphagia Okumura et al.28 Japan Quasi-experimental Experiment 14 Control 12 65.9 ± 9.7 68.0 ± 5.1 92. 9100. 0 to assess the preventative and therapeutic effects of perioperative swallowing rehabilitation in patients undergoing esophagectomy Kim et al.34 Korea Case series Aspiration 23 No aspiration 24 Control 27 62.7 ± 8.2 63.3 ± 7.1 64.7 ± 10.1 100. 0100. 0100.0 to analyze the swallowing biomechanics in patients with oropharyngeal dysphagia after esophagectomy compared to healthy adults Lee et al.29 Korea Diagnostic test accuracy 118 63.4 ± 8.5 93.2 to assess the usefulness of clinical bedside swallowing tests for detecting aspiration after esophagectomy Kumai et al.35 Japan Case series 25 64.8 NR to identify the main factors associated with aspiration in patients with pharyngeal dysphagia following esophagectomy with 3FL and to assess the effectiveness of the chin-down maneuver Kumai et al.39 Japan Case series 14 65.9 ± 1.9 100.0 to determine the efficacy of the chin-down maneuver after esophagectomy with 3FL on pharyngeal residue, UES opening, and laryngeal closure 2FL, two-field lymphadenectomy; 3FL, three-field lymphadenectomy; CDBIMS, complete division of the bilateral infrahyoid muscles attached to the sternum; NR, not recorded. View Large Table 1 Characteristics of the included studies (n = 12). References Country Study design Subject Mean or median age (range in years) % male Main purpose(s) of the study Easterling et al.32 USA Case series Patient 8 Healthy adult 8 NR (51–78) Age-matched NR to correlate the swallowing biomechanics with aspiration in patients with dysphagia after transhiatal esophagectomy Martin et al.33 Canada Case series 10 66.7 (49–76) 90.0 to compare pre- and postoperative swallowing patterns in patients who underwent transhiatal esophagectomy Lewin et al.36 USA Case series 26 66.0 (52–82) 88.5 to evaluate the use of chin tuck maneuver to alleviate aspiration during videofluoroscopy in patients who underwent esophagectomy Koh et al.37 Canada Case series 9 63.0 (52–76) 88.9 to investigate the function of the oral and pharyngeal phases of deglutition, and of the cervical esophagus, in patients who underwent transhiatal esophagectomy Leder et al.38 USA Case series 73 60.0 (39–74) 83.6 to characterize laryngeal physiology in patients who underwent transhiatal esophagectomy and to identify patients who are at high aspiration risk Kato et al.30 Japan Case series 27 64.3 (53–78) 100.0 to analyze the relationship between oropharyngeal swallowing and the alimentary reconstruction route after transthoracic esophagectomy Yasuda et al.31 Japan Case series 2FL 10 3FL 10 3FL + CDBIMS 20 61.4 (51–76) 61.3 (54–68) 61.5 (54–71) 80. 0100. 0 90.0 to compare swallowing function in patients who underwent esophagectomy with 2FL and 3FL, and to evaluate the preventative effect of the addition of CDBIMS for post-operative dysphagia Okumura et al.28 Japan Quasi-experimental Experiment 14 Control 12 65.9 ± 9.7 68.0 ± 5.1 92. 9100. 0 to assess the preventative and therapeutic effects of perioperative swallowing rehabilitation in patients undergoing esophagectomy Kim et al.34 Korea Case series Aspiration 23 No aspiration 24 Control 27 62.7 ± 8.2 63.3 ± 7.1 64.7 ± 10.1 100. 0100. 0100.0 to analyze the swallowing biomechanics in patients with oropharyngeal dysphagia after esophagectomy compared to healthy adults Lee et al.29 Korea Diagnostic test accuracy 118 63.4 ± 8.5 93.2 to assess the usefulness of clinical bedside swallowing tests for detecting aspiration after esophagectomy Kumai et al.35 Japan Case series 25 64.8 NR to identify the main factors associated with aspiration in patients with pharyngeal dysphagia following esophagectomy with 3FL and to assess the effectiveness of the chin-down maneuver Kumai et al.39 Japan Case series 14 65.9 ± 1.9 100.0 to determine the efficacy of the chin-down maneuver after esophagectomy with 3FL on pharyngeal residue, UES opening, and laryngeal closure References Country Study design Subject Mean or median age (range in years) % male Main purpose(s) of the study Easterling et al.32 USA Case series Patient 8 Healthy adult 8 NR (51–78) Age-matched NR to correlate the swallowing biomechanics with aspiration in patients with dysphagia after transhiatal esophagectomy Martin et al.33 Canada Case series 10 66.7 (49–76) 90.0 to compare pre- and postoperative swallowing patterns in patients who underwent transhiatal esophagectomy Lewin et al.36 USA Case series 26 66.0 (52–82) 88.5 to evaluate the use of chin tuck maneuver to alleviate aspiration during videofluoroscopy in patients who underwent esophagectomy Koh et al.37 Canada Case series 9 63.0 (52–76) 88.9 to investigate the function of the oral and pharyngeal phases of deglutition, and of the cervical esophagus, in patients who underwent transhiatal esophagectomy Leder et al.38 USA Case series 73 60.0 (39–74) 83.6 to characterize laryngeal physiology in patients who underwent transhiatal esophagectomy and to identify patients who are at high aspiration risk Kato et al.30 Japan Case series 27 64.3 (53–78) 100.0 to analyze the relationship between oropharyngeal swallowing and the alimentary reconstruction route after transthoracic esophagectomy Yasuda et al.31 Japan Case series 2FL 10 3FL 10 3FL + CDBIMS 20 61.4 (51–76) 61.3 (54–68) 61.5 (54–71) 80. 0100. 0 90.0 to compare swallowing function in patients who underwent esophagectomy with 2FL and 3FL, and to evaluate the preventative effect of the addition of CDBIMS for post-operative dysphagia Okumura et al.28 Japan Quasi-experimental Experiment 14 Control 12 65.9 ± 9.7 68.0 ± 5.1 92. 9100. 0 to assess the preventative and therapeutic effects of perioperative swallowing rehabilitation in patients undergoing esophagectomy Kim et al.34 Korea Case series Aspiration 23 No aspiration 24 Control 27 62.7 ± 8.2 63.3 ± 7.1 64.7 ± 10.1 100. 0100. 0100.0 to analyze the swallowing biomechanics in patients with oropharyngeal dysphagia after esophagectomy compared to healthy adults Lee et al.29 Korea Diagnostic test accuracy 118 63.4 ± 8.5 93.2 to assess the usefulness of clinical bedside swallowing tests for detecting aspiration after esophagectomy Kumai et al.35 Japan Case series 25 64.8 NR to identify the main factors associated with aspiration in patients with pharyngeal dysphagia following esophagectomy with 3FL and to assess the effectiveness of the chin-down maneuver Kumai et al.39 Japan Case series 14 65.9 ± 1.9 100.0 to determine the efficacy of the chin-down maneuver after esophagectomy with 3FL on pharyngeal residue, UES opening, and laryngeal closure 2FL, two-field lymphadenectomy; 3FL, three-field lymphadenectomy; CDBIMS, complete division of the bilateral infrahyoid muscles attached to the sternum; NR, not recorded. View Large Table 2 Treatment features of the included studies by surgical approach (n = 12). Reference Surgical approach Cancer type Pathological stage Reconstruction route Lymph node dissection Anastomosis site Neoadjuvant therapy Adjuvant therapy Easterling et al.32 TH AD NR Posterior mediastinum NR Cervical NR NR Martin et al.33 SCC 3 AD 7 T1N0M0 1 T2N0M0 4 T3N0M0 1 T3N1M0 4 Posterior mediastinum One node 3 Two nodes 1 Cervical None None Koh et al.37 AD NR Posterior mediastinum NR Cervical NR NR Leder et al.38 NR NR NR NR Cervical Neoadjuvant therapy 57(Detail was not shown) NR Kato et al.30 TT NR NR Posterior mediastinum 3FL 16 2FL 11 Cervical 16 Intrathoracic 11 None None Yasuda et al.31 NR I 4 IIA 8 IIB 11 III 10 IVA 1 IVB 6 Retrosternal 39 Orthotopic 1 2FL 4–12 3FL 8–21 3FL + CDBIMS 4–37 Cervical CT 14 CRT 2 NR Okumura et al.28 NR I/II 20 III/IV 6 Retrosternal 20 Subcutaneous 6 Dissected Cervical CT 6 CRT 1 NR Kim et al.34 SCC T2–3 N0–1 M0 NR 3FL Cervical NR CRT 10 Lee et al.29 NR NR NR Cervical lymph node dissection 27 Cervical 33 Noncervical 85 CRT 24 NR Kumai et al.35 NR NR Retrosternal 25 3FL 25 Cervical 25 NR NR Kumai et al.39 NR II 3 III 10 IVa 1 Retrosternal 14 3FL 14 Cervical 14 None NR Lewin et al.36 TH 16 TT 10 SCC 5 AD 19 Barrett's esophagus + HGD 2 NR NR NR Cervical 21 Thoracic 5 CRT 12 Photodynamic 1 NR Reference Surgical approach Cancer type Pathological stage Reconstruction route Lymph node dissection Anastomosis site Neoadjuvant therapy Adjuvant therapy Easterling et al.32 TH AD NR Posterior mediastinum NR Cervical NR NR Martin et al.33 SCC 3 AD 7 T1N0M0 1 T2N0M0 4 T3N0M0 1 T3N1M0 4 Posterior mediastinum One node 3 Two nodes 1 Cervical None None Koh et al.37 AD NR Posterior mediastinum NR Cervical NR NR Leder et al.38 NR NR NR NR Cervical Neoadjuvant therapy 57(Detail was not shown) NR Kato et al.30 TT NR NR Posterior mediastinum 3FL 16 2FL 11 Cervical 16 Intrathoracic 11 None None Yasuda et al.31 NR I 4 IIA 8 IIB 11 III 10 IVA 1 IVB 6 Retrosternal 39 Orthotopic 1 2FL 4–12 3FL 8–21 3FL + CDBIMS 4–37 Cervical CT 14 CRT 2 NR Okumura et al.28 NR I/II 20 III/IV 6 Retrosternal 20 Subcutaneous 6 Dissected Cervical CT 6 CRT 1 NR Kim et al.34 SCC T2–3 N0–1 M0 NR 3FL Cervical NR CRT 10 Lee et al.29 NR NR NR Cervical lymph node dissection 27 Cervical 33 Noncervical 85 CRT 24 NR Kumai et al.35 NR NR Retrosternal 25 3FL 25 Cervical 25 NR NR Kumai et al.39 NR II 3 III 10 IVa 1 Retrosternal 14 3FL 14 Cervical 14 None NR Lewin et al.36 TH 16 TT 10 SCC 5 AD 19 Barrett's esophagus + HGD 2 NR NR NR Cervical 21 Thoracic 5 CRT 12 Photodynamic 1 NR 2FL, two-field lymphadenectomy; 3FL, three-field lymphadenectomy; AD, adenocarcinoma; CRT, chemoradiation therapy; CT, chemotherapy; HGD high-grade dysplasia; NR, not recorded; SCC, squamous cell carcinoma; TH, transhiatal; TT, transthoracic. View Large Table 2 Treatment features of the included studies by surgical approach (n = 12). Reference Surgical approach Cancer type Pathological stage Reconstruction route Lymph node dissection Anastomosis site Neoadjuvant therapy Adjuvant therapy Easterling et al.32 TH AD NR Posterior mediastinum NR Cervical NR NR Martin et al.33 SCC 3 AD 7 T1N0M0 1 T2N0M0 4 T3N0M0 1 T3N1M0 4 Posterior mediastinum One node 3 Two nodes 1 Cervical None None Koh et al.37 AD NR Posterior mediastinum NR Cervical NR NR Leder et al.38 NR NR NR NR Cervical Neoadjuvant therapy 57(Detail was not shown) NR Kato et al.30 TT NR NR Posterior mediastinum 3FL 16 2FL 11 Cervical 16 Intrathoracic 11 None None Yasuda et al.31 NR I 4 IIA 8 IIB 11 III 10 IVA 1 IVB 6 Retrosternal 39 Orthotopic 1 2FL 4–12 3FL 8–21 3FL + CDBIMS 4–37 Cervical CT 14 CRT 2 NR Okumura et al.28 NR I/II 20 III/IV 6 Retrosternal 20 Subcutaneous 6 Dissected Cervical CT 6 CRT 1 NR Kim et al.34 SCC T2–3 N0–1 M0 NR 3FL Cervical NR CRT 10 Lee et al.29 NR NR NR Cervical lymph node dissection 27 Cervical 33 Noncervical 85 CRT 24 NR Kumai et al.35 NR NR Retrosternal 25 3FL 25 Cervical 25 NR NR Kumai et al.39 NR II 3 III 10 IVa 1 Retrosternal 14 3FL 14 Cervical 14 None NR Lewin et al.36 TH 16 TT 10 SCC 5 AD 19 Barrett's esophagus + HGD 2 NR NR NR Cervical 21 Thoracic 5 CRT 12 Photodynamic 1 NR Reference Surgical approach Cancer type Pathological stage Reconstruction route Lymph node dissection Anastomosis site Neoadjuvant therapy Adjuvant therapy Easterling et al.32 TH AD NR Posterior mediastinum NR Cervical NR NR Martin et al.33 SCC 3 AD 7 T1N0M0 1 T2N0M0 4 T3N0M0 1 T3N1M0 4 Posterior mediastinum One node 3 Two nodes 1 Cervical None None Koh et al.37 AD NR Posterior mediastinum NR Cervical NR NR Leder et al.38 NR NR NR NR Cervical Neoadjuvant therapy 57(Detail was not shown) NR Kato et al.30 TT NR NR Posterior mediastinum 3FL 16 2FL 11 Cervical 16 Intrathoracic 11 None None Yasuda et al.31 NR I 4 IIA 8 IIB 11 III 10 IVA 1 IVB 6 Retrosternal 39 Orthotopic 1 2FL 4–12 3FL 8–21 3FL + CDBIMS 4–37 Cervical CT 14 CRT 2 NR Okumura et al.28 NR I/II 20 III/IV 6 Retrosternal 20 Subcutaneous 6 Dissected Cervical CT 6 CRT 1 NR Kim et al.34 SCC T2–3 N0–1 M0 NR 3FL Cervical NR CRT 10 Lee et al.29 NR NR NR Cervical lymph node dissection 27 Cervical 33 Noncervical 85 CRT 24 NR Kumai et al.35 NR NR Retrosternal 25 3FL 25 Cervical 25 NR NR Kumai et al.39 NR II 3 III 10 IVa 1 Retrosternal 14 3FL 14 Cervical 14 None NR Lewin et al.36 TH 16 TT 10 SCC 5 AD 19 Barrett's esophagus + HGD 2 NR NR NR Cervical 21 Thoracic 5 CRT 12 Photodynamic 1 NR 2FL, two-field lymphadenectomy; 3FL, three-field lymphadenectomy; AD, adenocarcinoma; CRT, chemoradiation therapy; CT, chemotherapy; HGD high-grade dysplasia; NR, not recorded; SCC, squamous cell carcinoma; TH, transhiatal; TT, transthoracic. View Large Table 3 Swallowing biomechanics and dysphagic symptoms in the included studies by surgical approach (n = 12). Reference Surgical approach Methods Test materials Timing of swallowing evaluation Vocal fold immobility Key findings regarding swallowing biomechanics and dysphagic symptoms Before surgery After surgery Easterling et al.32 TH VFSS 5 mL thin barium N/A 1. 7–10 days 2. 17–29 days 3.42–105 days 25.0% • Aspiration (5 of 8; 62.5%) • Residue in the pyriform sinus (5 of 8; 62.5%) • The maximum UES anterior–posterior diameter and maximum anterior hyoid elevation in patients who aspirated were significantly smaller than those of age-matched normal controls Martin et al.33 VFSS 2,5,10mL thin and thick barium, 1 tsp cookie 2–21 days 44–134 days NR • Penetration/aspiration (2 of 5; 40%) • Residue in the valleculae, pyriform sinuses, and/or coating the posterior pharyngeal wall (5 of 5; 100%) • Anterior hyoid elevation was significantly decreased postoperatively for one subject and significantly increased for one subject. Superior hyoid elevation did not differ significantly. • Mild oropharyngeal dysphagia was observed before surgery (delayed initiation of swallowing, abnormal bolus formation, postswallow residue). Koh et al.37 VFSS Barium bolus, volume unspecified N/A 6–40 months (median 18 months) NR • Aspiration (0/9; 0%) • Residue in the valleculae (2 of 9; 22%) Leder et al.38 FEES 5mL custard, milk, cracker N/A 5 days 33.0% • Aspiration (15 of 73; 21%), penetration (24 of 73; 33%) • Pooling (9 of 73; 12%), spillage (4 of 73; 5%), residue (19 of 73; 26%) • Vocal fold immobility was associated with aspiration. Kato 200730 TT VFSS 10ml thin barium days not specified 14–21days NR • Superior/anterior hyoid elevation significantly decreased in patients who underwent intrathoracic esophagectomy with retrosternal reconstruction. Yasuda et al.31 VFSS Thin barium, volume unspecified N/A 7–62 days 20.0% • Laryngeal elevation was significantly impaired after 3FL as compared to 2FL. • A significant improvement of laryngeal elevation, compared with the 3FL group, was observed in the 3FL + CDBIMS group • Incomplete airway protection was observed in 25% of the 3FL + CDBIMS group, which was significantly lower than the 3FL group (70%), and was not different from the 2FL group (20%). Okumura et al.28 VFSS Thin iopamidol, volume unspecified N/A 4 time points for the experiment group, days after surgery not specified 28.6% • The maximum anterior/superior hyoid elevation and the anteroposterior diameters of the UES opening during swallows did not differ significantly among the four time points. Reference Surgical approach Methods Test materials Timing of swallowing evaluation Vocal fold immobility Key findings regarding swallowing biomechanics and dysphagic symptoms Before surgery After surgery • The volume of residue in the laryngeal vestibule and the pyriform sinus decreased significantly. Kim et al.34 VFSS 3ml thin barium N/A Aspiration group 8.2 ± 1.6 days No aspiration group 8.0 ± 1.8 days 14.9% • Aspiration (23 of 47; 48.9%) • Maximal anterior displacement of the hyoid, maximal rotation of the epiglottis, and pharyngeal delay time in normal group were significantly different from patients who underwent esophagectomy. • Pharyngeal delay time was significantly correlated with vocal cord palsy and aspiration. Lee et al.29 VFSS 3,6,9 mL thin barium, barium pudding, 1tsp of barium coated cookie N/A 7–10 days 12.7% • Aspiration (38/118; 32.2%), silent aspiration (17/118; 14.4%) • Vocal cord paralysis were risk factors for subglottic aspiration. • The clinical bedside swallowing test had a sensitivity of 68.4%. Kumai et al.35 VFSS NR N/A 2–3 weeks 76.0% • Aspiration (9/25; 36.0%), penetration (2/25; 8.0%). • Laryngeal aspiration was significantly correlated with reduced laryngeal elevation. • The penetration-aspiration scale score was significantly improved after training in chin-down swallowing. Kumai et al.39 FEES VFSS 3- or 5-mm thin barium or iopamidol N/A 14.8 ± 0.4 days 42.9% • Aspiration (2/14; 14.2%) • The pharyngeal constriction ratio and residue in the pyriform sinus for the chin-down position were significantly smaller than those in the neutral position. • The residue in the valleculae was not significantly different between the neutral and chin-down positions. • The UES opening diameter, duration of UES opening, and duration of laryngeal vestibule closure in the chin-down position were all significantly prolonged compared with those in the neutral position. Lewin et al.36 TH/TT VFSS 5 mL thin, 5mL thick barium, 5 mL applesauce 1/4 cracker N/A 6–43 days NR • Aspiration on thin liquid (21 of 26; 81.0%); both thin and thickened liquids (8 of 26; 30.8%); puree as well as thin and thickened liquids (3 of 26; 11.5%) • Chin-tuck swallow eliminated aspiration in 17/21 patients (80%). Reference Surgical approach Methods Test materials Timing of swallowing evaluation Vocal fold immobility Key findings regarding swallowing biomechanics and dysphagic symptoms Before surgery After surgery Easterling et al.32 TH VFSS 5 mL thin barium N/A 1. 7–10 days 2. 17–29 days 3.42–105 days 25.0% • Aspiration (5 of 8; 62.5%) • Residue in the pyriform sinus (5 of 8; 62.5%) • The maximum UES anterior–posterior diameter and maximum anterior hyoid elevation in patients who aspirated were significantly smaller than those of age-matched normal controls Martin et al.33 VFSS 2,5,10mL thin and thick barium, 1 tsp cookie 2–21 days 44–134 days NR • Penetration/aspiration (2 of 5; 40%) • Residue in the valleculae, pyriform sinuses, and/or coating the posterior pharyngeal wall (5 of 5; 100%) • Anterior hyoid elevation was significantly decreased postoperatively for one subject and significantly increased for one subject. Superior hyoid elevation did not differ significantly. • Mild oropharyngeal dysphagia was observed before surgery (delayed initiation of swallowing, abnormal bolus formation, postswallow residue). Koh et al.37 VFSS Barium bolus, volume unspecified N/A 6–40 months (median 18 months) NR • Aspiration (0/9; 0%) • Residue in the valleculae (2 of 9; 22%) Leder et al.38 FEES 5mL custard, milk, cracker N/A 5 days 33.0% • Aspiration (15 of 73; 21%), penetration (24 of 73; 33%) • Pooling (9 of 73; 12%), spillage (4 of 73; 5%), residue (19 of 73; 26%) • Vocal fold immobility was associated with aspiration. Kato 200730 TT VFSS 10ml thin barium days not specified 14–21days NR • Superior/anterior hyoid elevation significantly decreased in patients who underwent intrathoracic esophagectomy with retrosternal reconstruction. Yasuda et al.31 VFSS Thin barium, volume unspecified N/A 7–62 days 20.0% • Laryngeal elevation was significantly impaired after 3FL as compared to 2FL. • A significant improvement of laryngeal elevation, compared with the 3FL group, was observed in the 3FL + CDBIMS group • Incomplete airway protection was observed in 25% of the 3FL + CDBIMS group, which was significantly lower than the 3FL group (70%), and was not different from the 2FL group (20%). Okumura et al.28 VFSS Thin iopamidol, volume unspecified N/A 4 time points for the experiment group, days after surgery not specified 28.6% • The maximum anterior/superior hyoid elevation and the anteroposterior diameters of the UES opening during swallows did not differ significantly among the four time points. Reference Surgical approach Methods Test materials Timing of swallowing evaluation Vocal fold immobility Key findings regarding swallowing biomechanics and dysphagic symptoms Before surgery After surgery • The volume of residue in the laryngeal vestibule and the pyriform sinus decreased significantly. Kim et al.34 VFSS 3ml thin barium N/A Aspiration group 8.2 ± 1.6 days No aspiration group 8.0 ± 1.8 days 14.9% • Aspiration (23 of 47; 48.9%) • Maximal anterior displacement of the hyoid, maximal rotation of the epiglottis, and pharyngeal delay time in normal group were significantly different from patients who underwent esophagectomy. • Pharyngeal delay time was significantly correlated with vocal cord palsy and aspiration. Lee et al.29 VFSS 3,6,9 mL thin barium, barium pudding, 1tsp of barium coated cookie N/A 7–10 days 12.7% • Aspiration (38/118; 32.2%), silent aspiration (17/118; 14.4%) • Vocal cord paralysis were risk factors for subglottic aspiration. • The clinical bedside swallowing test had a sensitivity of 68.4%. Kumai et al.35 VFSS NR N/A 2–3 weeks 76.0% • Aspiration (9/25; 36.0%), penetration (2/25; 8.0%). • Laryngeal aspiration was significantly correlated with reduced laryngeal elevation. • The penetration-aspiration scale score was significantly improved after training in chin-down swallowing. Kumai et al.39 FEES VFSS 3- or 5-mm thin barium or iopamidol N/A 14.8 ± 0.4 days 42.9% • Aspiration (2/14; 14.2%) • The pharyngeal constriction ratio and residue in the pyriform sinus for the chin-down position were significantly smaller than those in the neutral position. • The residue in the valleculae was not significantly different between the neutral and chin-down positions. • The UES opening diameter, duration of UES opening, and duration of laryngeal vestibule closure in the chin-down position were all significantly prolonged compared with those in the neutral position. Lewin et al.36 TH/TT VFSS 5 mL thin, 5mL thick barium, 5 mL applesauce 1/4 cracker N/A 6–43 days NR • Aspiration on thin liquid (21 of 26; 81.0%); both thin and thickened liquids (8 of 26; 30.8%); puree as well as thin and thickened liquids (3 of 26; 11.5%) • Chin-tuck swallow eliminated aspiration in 17/21 patients (80%). View Large Table 3 Swallowing biomechanics and dysphagic symptoms in the included studies by surgical approach (n = 12). Reference Surgical approach Methods Test materials Timing of swallowing evaluation Vocal fold immobility Key findings regarding swallowing biomechanics and dysphagic symptoms Before surgery After surgery Easterling et al.32 TH VFSS 5 mL thin barium N/A 1. 7–10 days 2. 17–29 days 3.42–105 days 25.0% • Aspiration (5 of 8; 62.5%) • Residue in the pyriform sinus (5 of 8; 62.5%) • The maximum UES anterior–posterior diameter and maximum anterior hyoid elevation in patients who aspirated were significantly smaller than those of age-matched normal controls Martin et al.33 VFSS 2,5,10mL thin and thick barium, 1 tsp cookie 2–21 days 44–134 days NR • Penetration/aspiration (2 of 5; 40%) • Residue in the valleculae, pyriform sinuses, and/or coating the posterior pharyngeal wall (5 of 5; 100%) • Anterior hyoid elevation was significantly decreased postoperatively for one subject and significantly increased for one subject. Superior hyoid elevation did not differ significantly. • Mild oropharyngeal dysphagia was observed before surgery (delayed initiation of swallowing, abnormal bolus formation, postswallow residue). Koh et al.37 VFSS Barium bolus, volume unspecified N/A 6–40 months (median 18 months) NR • Aspiration (0/9; 0%) • Residue in the valleculae (2 of 9; 22%) Leder et al.38 FEES 5mL custard, milk, cracker N/A 5 days 33.0% • Aspiration (15 of 73; 21%), penetration (24 of 73; 33%) • Pooling (9 of 73; 12%), spillage (4 of 73; 5%), residue (19 of 73; 26%) • Vocal fold immobility was associated with aspiration. Kato 200730 TT VFSS 10ml thin barium days not specified 14–21days NR • Superior/anterior hyoid elevation significantly decreased in patients who underwent intrathoracic esophagectomy with retrosternal reconstruction. Yasuda et al.31 VFSS Thin barium, volume unspecified N/A 7–62 days 20.0% • Laryngeal elevation was significantly impaired after 3FL as compared to 2FL. • A significant improvement of laryngeal elevation, compared with the 3FL group, was observed in the 3FL + CDBIMS group • Incomplete airway protection was observed in 25% of the 3FL + CDBIMS group, which was significantly lower than the 3FL group (70%), and was not different from the 2FL group (20%). Okumura et al.28 VFSS Thin iopamidol, volume unspecified N/A 4 time points for the experiment group, days after surgery not specified 28.6% • The maximum anterior/superior hyoid elevation and the anteroposterior diameters of the UES opening during swallows did not differ significantly among the four time points. Reference Surgical approach Methods Test materials Timing of swallowing evaluation Vocal fold immobility Key findings regarding swallowing biomechanics and dysphagic symptoms Before surgery After surgery • The volume of residue in the laryngeal vestibule and the pyriform sinus decreased significantly. Kim et al.34 VFSS 3ml thin barium N/A Aspiration group 8.2 ± 1.6 days No aspiration group 8.0 ± 1.8 days 14.9% • Aspiration (23 of 47; 48.9%) • Maximal anterior displacement of the hyoid, maximal rotation of the epiglottis, and pharyngeal delay time in normal group were significantly different from patients who underwent esophagectomy. • Pharyngeal delay time was significantly correlated with vocal cord palsy and aspiration. Lee et al.29 VFSS 3,6,9 mL thin barium, barium pudding, 1tsp of barium coated cookie N/A 7–10 days 12.7% • Aspiration (38/118; 32.2%), silent aspiration (17/118; 14.4%) • Vocal cord paralysis were risk factors for subglottic aspiration. • The clinical bedside swallowing test had a sensitivity of 68.4%. Kumai et al.35 VFSS NR N/A 2–3 weeks 76.0% • Aspiration (9/25; 36.0%), penetration (2/25; 8.0%). • Laryngeal aspiration was significantly correlated with reduced laryngeal elevation. • The penetration-aspiration scale score was significantly improved after training in chin-down swallowing. Kumai et al.39 FEES VFSS 3- or 5-mm thin barium or iopamidol N/A 14.8 ± 0.4 days 42.9% • Aspiration (2/14; 14.2%) • The pharyngeal constriction ratio and residue in the pyriform sinus for the chin-down position were significantly smaller than those in the neutral position. • The residue in the valleculae was not significantly different between the neutral and chin-down positions. • The UES opening diameter, duration of UES opening, and duration of laryngeal vestibule closure in the chin-down position were all significantly prolonged compared with those in the neutral position. Lewin et al.36 TH/TT VFSS 5 mL thin, 5mL thick barium, 5 mL applesauce 1/4 cracker N/A 6–43 days NR • Aspiration on thin liquid (21 of 26; 81.0%); both thin and thickened liquids (8 of 26; 30.8%); puree as well as thin and thickened liquids (3 of 26; 11.5%) • Chin-tuck swallow eliminated aspiration in 17/21 patients (80%). Reference Surgical approach Methods Test materials Timing of swallowing evaluation Vocal fold immobility Key findings regarding swallowing biomechanics and dysphagic symptoms Before surgery After surgery Easterling et al.32 TH VFSS 5 mL thin barium N/A 1. 7–10 days 2. 17–29 days 3.42–105 days 25.0% • Aspiration (5 of 8; 62.5%) • Residue in the pyriform sinus (5 of 8; 62.5%) • The maximum UES anterior–posterior diameter and maximum anterior hyoid elevation in patients who aspirated were significantly smaller than those of age-matched normal controls Martin et al.33 VFSS 2,5,10mL thin and thick barium, 1 tsp cookie 2–21 days 44–134 days NR • Penetration/aspiration (2 of 5; 40%) • Residue in the valleculae, pyriform sinuses, and/or coating the posterior pharyngeal wall (5 of 5; 100%) • Anterior hyoid elevation was significantly decreased postoperatively for one subject and significantly increased for one subject. Superior hyoid elevation did not differ significantly. • Mild oropharyngeal dysphagia was observed before surgery (delayed initiation of swallowing, abnormal bolus formation, postswallow residue). Koh et al.37 VFSS Barium bolus, volume unspecified N/A 6–40 months (median 18 months) NR • Aspiration (0/9; 0%) • Residue in the valleculae (2 of 9; 22%) Leder et al.38 FEES 5mL custard, milk, cracker N/A 5 days 33.0% • Aspiration (15 of 73; 21%), penetration (24 of 73; 33%) • Pooling (9 of 73; 12%), spillage (4 of 73; 5%), residue (19 of 73; 26%) • Vocal fold immobility was associated with aspiration. Kato 200730 TT VFSS 10ml thin barium days not specified 14–21days NR • Superior/anterior hyoid elevation significantly decreased in patients who underwent intrathoracic esophagectomy with retrosternal reconstruction. Yasuda et al.31 VFSS Thin barium, volume unspecified N/A 7–62 days 20.0% • Laryngeal elevation was significantly impaired after 3FL as compared to 2FL. • A significant improvement of laryngeal elevation, compared with the 3FL group, was observed in the 3FL + CDBIMS group • Incomplete airway protection was observed in 25% of the 3FL + CDBIMS group, which was significantly lower than the 3FL group (70%), and was not different from the 2FL group (20%). Okumura et al.28 VFSS Thin iopamidol, volume unspecified N/A 4 time points for the experiment group, days after surgery not specified 28.6% • The maximum anterior/superior hyoid elevation and the anteroposterior diameters of the UES opening during swallows did not differ significantly among the four time points. Reference Surgical approach Methods Test materials Timing of swallowing evaluation Vocal fold immobility Key findings regarding swallowing biomechanics and dysphagic symptoms Before surgery After surgery • The volume of residue in the laryngeal vestibule and the pyriform sinus decreased significantly. Kim et al.34 VFSS 3ml thin barium N/A Aspiration group 8.2 ± 1.6 days No aspiration group 8.0 ± 1.8 days 14.9% • Aspiration (23 of 47; 48.9%) • Maximal anterior displacement of the hyoid, maximal rotation of the epiglottis, and pharyngeal delay time in normal group were significantly different from patients who underwent esophagectomy. • Pharyngeal delay time was significantly correlated with vocal cord palsy and aspiration. Lee et al.29 VFSS 3,6,9 mL thin barium, barium pudding, 1tsp of barium coated cookie N/A 7–10 days 12.7% • Aspiration (38/118; 32.2%), silent aspiration (17/118; 14.4%) • Vocal cord paralysis were risk factors for subglottic aspiration. • The clinical bedside swallowing test had a sensitivity of 68.4%. Kumai et al.35 VFSS NR N/A 2–3 weeks 76.0% • Aspiration (9/25; 36.0%), penetration (2/25; 8.0%). • Laryngeal aspiration was significantly correlated with reduced laryngeal elevation. • The penetration-aspiration scale score was significantly improved after training in chin-down swallowing. Kumai et al.39 FEES VFSS 3- or 5-mm thin barium or iopamidol N/A 14.8 ± 0.4 days 42.9% • Aspiration (2/14; 14.2%) • The pharyngeal constriction ratio and residue in the pyriform sinus for the chin-down position were significantly smaller than those in the neutral position. • The residue in the valleculae was not significantly different between the neutral and chin-down positions. • The UES opening diameter, duration of UES opening, and duration of laryngeal vestibule closure in the chin-down position were all significantly prolonged compared with those in the neutral position. Lewin et al.36 TH/TT VFSS 5 mL thin, 5mL thick barium, 5 mL applesauce 1/4 cracker N/A 6–43 days NR • Aspiration on thin liquid (21 of 26; 81.0%); both thin and thickened liquids (8 of 26; 30.8%); puree as well as thin and thickened liquids (3 of 26; 11.5%) • Chin-tuck swallow eliminated aspiration in 17/21 patients (80%). View Large Abnormalities in swallowing biomechanics and swallowing symptoms after esophagectomy Table 3 also displays the reported key findings on swallowing biomechanics and swallowing symptoms following esophagectomy. In patients who received transhiatal esophagectomy, several abnormal swallowing biomechanics were reported: vocal fold immobility (25.0%32–33.0%38), delayed onset of swallowing,33 reduced hyolaryngeal elevation during swallowing,32,33 and reduced maximum anterior–posterior diameter of the UES during swallowing.33 As for swallowing symptoms, overt aspiration (0%37–81.0%29) and pharyngeal residue (22.0%37 in the pyriform sinus and 62.5%32 in the valleculae) presented. Reported abnormalities in swallowing biomechanics after transthoracic esophagectomy were similar to those presented after transhiatal esophagectomy: vocal fold immobility (12.7%29–76.0%35), delayed onset of swallowing,34 reduced hyolaryngeal elevation during swallowing,31,35 particularly in patients who underwent three-field lymphadenectomy,31 and reduced maximum anterior–posterior diameter of the UES during swallowing particularly with reconstruction via the retrosternal route.30 Overt aspiration (12.7%29–76.0%35), silent aspiration (14.4%29), and pharyngeal residue (100%) were also reported.39 Aspiration was found to be significantly associated with vocal fold immobility,29,38 decreased excursion of the hyoid,32,35 reduced UES anterior–posterior opening,32 the three-field lymphadenectomy,31 and operation time greater than or equal to six hours in postesophagectomy patients.29 Thickening liquids decreased the occurrence of aspiration during the swallowing evaluation.36 Additive complete division of the bilateral infrahyoid muscles attached to the sternum was found to be a significant suppressor of penetration and aspiration after esophagectomy with three-field lymphadenectomy.31 Health-related outcomes after esophagectomy Three studies reported the occurrence of pneumonia,28,29,31 which ranged between 5%31 and 25%28 of the patients who underwent transthoracic esophagectomy. Occurrence of pneumonia was higher in patients who aspirated during VFSS trials (13.2%) than in patients who did not aspirate (0%);29 in patients who underwent the three-field lymphadenectomy (20%) than in patients who underwent the two-field lymphadenectomy (10%) or the three-field lymphadenectomy with complete division of the bilateral infrahyoid muscles attached to the sternum (5%).31 One study reported patients’ diet levels following transthoracic esophagectomy.35 Majority of patients were temporarily dependent on tube-feeding or total parenteral nutrition at the time of postoperative VFSS, and had learned the chin tuck as a compensatory swallowing maneuver. Nearly 100% of the study patients were fed orally at discharge, which was at 29.5 ± 2.5 days after the postoperative VFSS was performed.35 Rehabilitative interventions for postesophagectomy oropharyngeal dysphagia Four studies, one quasi-experimental trial28 and three case series,35,36,39 reported rehabilitative interventions provided with this patient population. Okumura and colleagues provided perioperative nonswallowing exercises to patients who were undergoing esophagectomy.28 The rehabilitative program included pursed lip breathing, a cervical range of motion exercise, shoulder stretches, jaw opening, tongue exercises, and submental muscle training. The authors reported that the exercises did not change swallowing biomechanics of the patients, but the volume of laryngeal and pharyngeal residue after esophagectomy decreased significantly in patients who underwent perioperative swallowing exercises.28 Three case series observed immediate positive effect of the chin-tuck maneuver for improving airway protection by effectively eliminating aspiration after surgery.35,36,39 Pyriform sinus residue was significantly reduced when postesophagectomy patients implemented the chin tuck maneuver compared to the neutral position.39 The chin-tuck maneuver also increased UES opening diameter and prolonged duration of UES opening and duration of laryngeal vestibule closure compared with those in the neutral position.39 Quality assessment The JBI Critical Appraisal Checklists scores were low for quasi-experimental study28 (4 out of 9 points) and diagnostic accuracy study29 (4 out of 10 points), and were varied for case series (532,33,36,37–835,40 out of 10 points). The methodological quality of the majority of the included studies was not sufficient. DISCUSSION This systematic review revealed several pathological patterns in swallowing biomechanics after transhiatal and transthoracic esophagectomy. The abnormalities in swallowing included delayed onset of swallowing, reduced hyoid or hyolaryngeal elevation, and reduced UES opening. Both overt and silent aspiration and pharyngeal residue were commonly reported following esophagectomy. The abnormal biomechanics found in this review may explain the underlying mechanism of swallowing symptoms in postesophagectomy patients. In this population, initiation of swallowing tends to be delayed.41 Thus, the bolus can be propelled into the pharynx before the hyoid and larynx are pulled up and the epiglottis is passively retroflexed to its maximally lowered position to cover the laryngeal vestibule. 42 As a result, the bolus can be misdirected into the laryngeal vestibule. Vocal fold immobility due to the injury to the recurrent nerve during esophagectomy allows the penetrated materials to be easily aspirated to the trachea. Further, the damage to the pharyngeal plexus33,43 or scarring at the anastomotic area30 may reduce pharyngeal muscle contraction and UES opening. These pharyngeal dysfunctions may lead to pharyngeal residue, which can be aspirated when the patient attempts to clear them with additional clearing swallows.44 This review also aimed to examine the reported health-related outcomes in relation to swallowing abnormality following esophagectomy. Increased risk for pneumonia was found in patients who aspirated during VFSS trials.29 The high incidence of silent aspiration reported in this patient population29,36 and low sensitivity of the bedside screening test against VFSS29 emphasize the importance of instrumental evaluations when assessing patients who received esophagectomy. Only one study reported diet outcomes of the study patients.35 This lack of evidence suggests the need for future studies examining health-related outcomes of postesophagectomy oropharyngeal dysphagia, including length of time for dependence on alternative means of nutrition such as jejunostomy. Alternative means of nutrition along with a systematic and gradual introduction of the least restrictive diet can improve patient's health related outcomes. This can help set expectations for the healing processing, and rehabilitation postesophagectomy. Finally, this review revealed that evidence was scant regarding rehabilitative interventions for postesophagectomy oropharyngeal dysphagia. One study provided perioperative swallowing rehabilitation to patients who were undergoing esophagectomy.28 However, the study did not observe any improvement in swallowing biomechanics. This may be because its rehabilitative program did not target the pharyngeal abnormalities, which have now been identified in this review. The pharyngeal muscle training45,46 as well as the submental muscle training47 may be more relevant to restore the impaired hyolaryngeal excursion and pharyngeal contraction that could occur following esophagectomy. Three small case series indicated the potential efficacy of chin-tuck maneuver in reducing aspiration35 and pharyngeal residue39 (in both pyriform and valleculae structures). The chin-tuck maneuver appears to be a reasonable strategy to trial during postesophagectomy recovery since this swallowing technique has been found to alleviate aspiration48 and pharyngeal residue49 by decreasing distance between the hyoid bone and larynx,50,51 prolonging the duration of laryngeal vestibule closure52 and UES opening,53,54 all of which were often limited in this patient population. Other potential management strategies include thickening liquids, which may also prevent aspiration of this patient population.36 Since thickened liquids tend to flow more slowly, it can provide patients with delayed initiation of swallowing more control during swallowing.36 Although not discussed in the reviewed studies, postural modifications such as head turns and head tilts are compensatory strategies, which could be trialed during swallowing evaluations. The studies reviewed found a wide range of vocal fold immobility rates between 25.0%32 and 33.0%38 for patients who underwent transhiatal esophagectomy, and between 12.7%29 and 76.0%35 for patients who underwent transthoracic esophagectomy. In these instances, surgical interventions, both injection medialization and thyroplasty may alleviate swallowing symptoms in patients with vocal fold immobility,55 which was prevalent in this patient population. Most of the included studies performed instrumental evaluation only after esophagectomy. Thus, it is difficult to determine if the observed swallowing abnormalities and dysphagic symptoms following esophagectomy are resultant of the surgery or are preexisting characteristics of the patients with esophageal cancer. Further, none of the included studies performed follow-up swallowing evaluation to understand the trajectory of swallowing rehabilitation. In order to understand the recovery process of oropharyngeal dysphagia, follow up evaluations may also assist future development of rehabilitative intervention. Our review has some limitations. The weak study designs with limited methodological quality of the included studies may make the results of our analyses less conclusive. There may be eligible studies archived in databases and search algorithms that we did not use for literature search and thus were not identified. In conclusion, our systematic review revealed that vocal fold immobility, delayed onset of swallowing, reduced hyolaryngeal elevation, and reduced UES opening during swallowing were frequently reported in the literature in the patients who underwent esophagectomy. These pathological swallowing patterns may contribute to incomplete airway closure and reduced bolus clearance, resulting in aspiration and pharyngeal residue observed in swallows after esophagectomy. Pneumonia and restricted diets were found in patients who received esophagectomy. Evidence was scant regarding the therapeutic interventions for postesophagectomy oropharyngeal dysphagia. These results indicate the urgent need for future studies for developing effective swallowing exercises and management strategies for oropharyngeal dysphagia secondary to esophagectomy. The results, however, should be interpreted with caution, given limited generalizability and potential biases inherent to the include studies. Notes Specific author contributions:Asako Kaneoka designed the study, searched, and reviewed the literature, acquired data of the publications, assessed the quality of the included studies, interpreted the data, and drafted the manuscript with the guidance of the co-authors. Sky Yang reviewed the literature, acquired the data, and edited the manuscript. Haruhi Inokuchi assessed the quality of included studies. All investigators contributed to the study design and interpretation of the results, and critically revised the manuscript and approved the final version. ACKNOWLEDGMENTS The authors are grateful for the assistance provided by Helena Vonville, MPH and for her expertise in systematic searching. The authors would also like to acknowledge, Dr. Hidetomi Yamada, PhD, MD, for reviewing a German article, Ms. Maxine Van Doren M.S., CCC-SLP, for reviewing French articles, and Margo Naraghi-Grcich, M.A., CCC-SLP, CBIS for editing this paper. Funding was not received for this study. 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Diseases of the EsophagusOxford University Press

Published: May 21, 2018

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