This study delineated the longitudinal changes in swallowing physiology, dysphagic symptoms, and diet levels in patients undergoing esophagectomy. This study identified an association between pharyngeal residue and aspiration pneumonia after esophagectomy.

First, our preoperative VFSS assessment revealed that the swallowing functions of patients with esophageal cancer were intact before esophagectomy despite the assumption that presbyphagia [19] or sarcopenic dysphagia [28,29,30] may already exist owing to advanced age or malnutrition in patients with esophageal cancer preoperatively [18]. The study participants were younger (mean age = 64.4 years) than those with presbyphagia, which typically develops after 80 years of age [31]. In addition, they had a better nutritional status (mean PNI 49.3) than patients with sarcopenia preoperatively (mean PNI 46.0) [31]. Thus, preoperatively older or less-nourished patients may still be at risk of symptomatic or asymptomatic swallowing deficits, which could be exacerbated after surgery. Therefore, preoperative VFSS assessment remains valuable for identifying patients with baseline dysphagia and elevated risk of postoperative dysphagia.

Second, our longitudinal assessment demonstrated recovery of swallowing impairments after esophagectomy. Initiation of swallowing and PES opening were unchanged after surgery. Tongue base retraction and PCR worsened two weeks after surgery but returned to baseline levels three months after surgery. However, once impaired after surgery, hyoid displacement during swallowing and vocal fold immobility did not fully recover after three months.

The temporary decline in tongue base retraction and pharyngeal squeezing indicated by PCR were unexpected changes after surgery, as the surgical procedure involved in esophagectomy or lymphadenectomy does not typically affect these swallowing mechanisms. However, as previously reported, it is possible that exposure to physical stress during invasive surgery and prolonged postoperative nil per os status overwhelmed the participants' functional reserves, causing temporal weakness in the lingual or pharyngeal muscles [19]. Consequently, bolus transport was tentatively affected, increasing pharyngeal residue after esophagectomy. Another potential reason for the tentative impairment in pharyngeal squeezing is iatrogenic damage to the ansa cervicalis and nerve rootlets during neck dissection, although the impact of neck dissection on pharyngeal movement was likely limited [32, 33].

Contrary to the decline in tongue base retraction and PCR, the reduced hyoid displacement during swallowing and vocal fold immobility is likely due to the direct impact of surgical procedures on swallowing mechanisms and, therefore, is persistent. In cervical lymph node dissection during esophagectomy, the infrahyoid muscles are either retracted or partially divided [34]. The damaged infrahyoid muscles become scarred, thereby hindering the lifting of the hyolaryngeal complex [9]. Scar formation around the trachea may also produce a counterforce against the hyolaryngeal elevation [17]. Furthermore, damage to the recurrent laryngeal nerve during lymphadenectomy increases the risk of vocal fold immobility after esophagectomy [35]. All the study participants underwent lymphadenectomy, which may be a reason for the higher incidence of vocal fold immobility observed in our study compared to that in previous reports in which esophagectomy was performed without lymphadenectomy (12.7% [8], 14.9% [11]). These surgery-induced changes might have allowed postoperative airway invasion in the participants. As previously reported, reduced hyolaryngeal elevation [8, 17] and vocal fold immobility [11, 18] were associated with aspiration after esophagectomy.

Despite persistent deficits in the movement of the hyoid and vocal folds, no aspiration events occurred three months after surgery. One possible reason for this favorable outcome is that the participants may have acquired maneuvers for safe swallowing, such as super supraglottic swallow [36] or chin-tuck swallow [37]. Kumai et al. reported that patients who underwent esophagectomy with three-field lymph node dissection had already acquired a chin-down swallow at postoperative VFSS without specific guidance and thus showed lower PAS scores than those who did not [38]. Our longitudinal research added that the compromised airway protective mechanism could continue for up to three months, emphasizing the importance of postoperative education for patients with compensatory strategies for airway protection.

Finally, our study found that pharyngeal residue, among other swallowing-related abnormalities, identified through a thorough swallowing assessment, is the single postoperative change associated with aspiration pneumonia. The pharyngeal residue, specifically the residue in the vallecula, is related to post-swallow aspiration [39]. However, in our study, all penetration and aspiration events were observed during swallowing when the participants’ maximum laryngeal elevation seemed to be achieved; these were probably due to incomplete airway closure. No aspiration of post-swallow residue was observed during VFSS, which might be due to the limitation of the test bolus volume to 5 mL. As such, accumulated residue with larger bolus in real-life meals can result in aspiration, thereby leading to aspiration pneumonia. Therefore, managing pharyngeal residues is essential to decrease penetration and aspiration after esophagectomy.

The study did not specifically analyze the location of the residue. However, the significant postoperative impairments identified in this study are known contributors to pharyngeal residue [40]: reduced tongue base retraction, reduced pharyngeal contraction, and decreased hyoid displacement. This study could not examine the longitudinal changes in several other factors, such as hyolaryngeal approximation or pharyngeal shortening during swallowing, which might affect postoperative residue. Further kinematic analyses may reveal the detailed contributions of swallowing mechanisms to pharyngeal residue, which may, in turn, help identify potential targets for postoperative swallowing exercises.

The current study has several limitations, similar to other retrospective observational studies [41]. First, the results were based on a limited sample size from a single-center setting, hampering generalizability and limited univariate statistical analyses. For example, most participants had thoracic esophagus cancers. Other participant characteristics, such as pathological stage, surgical procedure, or reconstruction routes, may have influenced postoperative swallowing impairments. To our knowledge, no other comprehensive longitudinal analyses of the kinematics and dysphagic symptoms have been published. Therefore, our study provides unique findings regarding dysphagia associated with esophagectomy. Second, our inclusion criteria required three-time VFSS data, potentially limiting patients with severe medical conditions and prolonged serious dysphagia who could not undergo VFSS from participating in the study. Third, the analysis was restricted to swallowing of only 5 mL of thickened liquid in this study due to missing data regarding thin liquid trials resulting from VFSS discontinuation for swallowing safety. Thin-liquid swallowing trials might have revealed more penetration and aspiration events, leading to additional findings of dysphagia after esophagectomy. Similarly, decreased UES openings may be observed for larger bolus volumes, as UES opening is volume dependent [14]. However, as this study was performed postoperatively in an acute hospital setting, swallowing safety during the VFSS was prioritized. Finally, observer bias may be involved in assessing the MBSImP since only one SLP served as a rater. However, to minimize bias, we ensured that the scoring was performed by an MBSImP-certified rater. We also blinded the two raters when assessing the PAS.

Future large-scale studies are warranted to examine longitudinal changes in swallowing function, kinematics, and symptoms of other dysphagia-related variables. Studies should also investigate factors associated with patients with severe dysphagia using various test boluses after esophagectomy.