Partial Horizontal Supracricoid Laryngectomy: Which Factors Impact on Post-decannulation Swallowing Outcomes? A Prospective Single-Center Experience

Abstract

Early decannulation, performed within the first ten days after supracricoid partial laryngectomy, can result in a more rapid recovery of swallowing function with a semisolid bolus in the short term, about 30 days. We selected 20 patients with squamous cell carcinoma of larynx, who underwent supracricoid laryngectomies: 10 cricohyoidopexy (CHP) and 10 cricohyoidoepiglottopexy (CHEP). Staging was pT2 (10 pts), and pT3 (10 pts). Fiberoptic endoscopic evaluation of swallowing was used to assess postoperative swallowing function after a mean of 12 and 22 days from surgery. A modified PAS score (penetration-aspiration scale) was assigned for subtotal laryngectomies. Decannulation occurred after 6.7 ± 2.1 days. Univariate analysis showed that the type of surgery (CHP or CHEP), pT, resection of one arytenoid, and decannulation time are significantly associated with the 12-day PAS score. The 22-day PAS score is significantly associated with only 3 variables: type of surgery, pT, and resection of one arytenoid. From the data presented, the factors that most delay an effective recovery of swallowing are T3 and the resection of one arytenoid. Early decannulation has been shown statistically to improve PAS score in the short term, but not in the long term.

Introduction

Horizontal supracricoid partial laryngectomy with crico-hyoid-epiglottopexy (CHEP) or with crico-hyoid-pexy (CHP) are meant to remove the oncological pathology of the larynx and, at the same time, preserving its three functions: breathing, swallowing and phonation. This kind of surgery results in a less efficient neoglottis, leading to loss of air during speech, problems of swallowing, and insufficient respiratory space for safe decannulation. A previous study has shown that the average time of removal of the nasogastric tube (SNG) ranges from 10 to 88 days, while the average decannulation time ranges from 8 to 105 days, with a percentage of decannulation ranging from 85.7 to 100% of patients [1]. The time necessary to recover laryngeal functions depends on factors such as the stage of the tumor, the preservation of one or both arytenoids, the type of laryngeal surgery, radiotherapy prior to surgery, the mobility of the base of the tongue, and the patient’s age [1–4].

The main goal of this prospective work is to analyze the role of several factors affecting the restoration of correct swallowing in patients undergoing supracricoyd laryngetomy.

Materials and Methods

20 patients who underwent supracricoid partial laryngectomy for squamous cell carcinoma of the larynx were evaluated at the Head and Neck Department of the “Policlinico Umberto I” Hospital, Sapienza University of Rome, between January, 2021 and September, 2022; 10 patients undergoing CHP and 10 patients undergoing CHEP. Exclusion criteria were: dehiscence of the surgical wound with pharyngeal fistula, neurological pathologies, and post-operative infections. 4 patients were excluded from the study (post-operative infections, n = 1; pharyngeal fistula, n = 2; neurological pathology, n = 1). 14 males and 6 females were enrolled with a mean age of 69.1 yr (range: 62–77 yr). Among them, 10 were staged as pT3 and 10 as pT2; 18 of them had no post-operative lymph nodes involvement and were classified as pN0, unlike 2 of them with lymph node metastases were considered pN1. According to the staging of the disease, none of these patients required adjuvant radiotherapy plus/or chemotherapy after surgery. 4 patients undergoing CHEP surgery received preoperative radiotherapy 9–10 before surgery. 14 patients underwent a selective neck dissection (SND) (levels II-IV); among these, 8 patients received unilateral SND, 6 bilateral SND. 10 patients undergoing CHP underwent a SND, 4 of them unilateral SND, and 6 of them bilateral SND. Among the patients undergoing CHEP, 4 of them underwent unilateral SN, while 6 of them received no SND. Both arytenoids were preserved in 12 patients (8 CHEP, and 4 CHP), while only one arytenoid was resected in 8 patients (2 CHEP, and 6 CHP). The staging and the therapeutic actions performed on the patients (preoperative radiotherapy, type of surgery, resection of one arytenoid, neck dissection, decannulation) were considered as delaying factors in the resumption of swallowing, and therefore counted for each patient. Each of these was assigned a value of 1. A score as 1 was assigned to those patietns who received decannulation after the 5th post-operative day (Table 1).

Table 1.

Characteristics of the patients included in the present analysis

Patient/surgery	Preoperative RT	pT	pN	Resection of one arytenoid (side)	Neck dissection (side-levels)	Decannulation time (post operative day)	PAS score 12 days	PAS score 22 days
1/CHP	No	T3	N0	1 (right)	right (II–IV levels)	5	4	4
2/CHP	No	T3	N0	No	unilateral	8	4	3
3/CHP	No	T3	N0	1 (right)	right (II–IV levels)	5	4	4
4/CHP	No	T2	N0	No	unilateral	6	4	3
5/CHP	No	T3	N0	No	bilateral (II–IV levels)	6	2	1
6/CHP	No	T3	N0	1	bilateral (II–IV levels)	8	4	4
7/CHP	No	T3	N0	No	bilateral (II–IV levels)	6	2	1
8/CHP	No	T3	N0	1 (right)	bilateral (II–IV levels)	10	4	4
9/CHP	No	T2	N0	1	bilateral (II–IV levels)	6	4	3
10/CHP	No	T3	N0	1 (right)	bilateral (II–IV levels)	10	4	4
11/CHEP	No	T2	N0	No	No	3	1	1
12/CHEP	No	T2	N0	No	No	6	1	1
13/CHEP	No	T2	N0	No	No	3	1	1
14/CHEP	No	T2	N0	No	No	6	1	1
15/CHEP	No	T2	N0	No	No	7	2	2
16/CHEP	No	T2	N0	No	No	7	3	2
17/CHEP	yes	T3	N1	No	left (II–IV levels)	6	4	4
18/CHEP	yes	T3	N1	No	left (II–IV levels)	6	4	4
19/CHEP	yes	T2	N0	1 (left)	left (II–IV levels)	10	3	2
20/CHEP	yes	T2	N0	1 (left)	left (II–IV levels)	10	3	2

FEES (fiberoptic endoscopic evaluation of swallowing) [5] was used to evaluate postoperative swallowing function, and a modified PAS score (penetration-aspiration scale) was assigned for subtotal laryngectomies as already presented by Alicandri-Ciufelli M et al. (2015), and adopted for this study. The modified PAS score ranges from 1 (when, through the fiberscope placed in the oropharynx, we observe that the material does not enter the airways, and does not penetrate through the neoglottic space) to 6 (when in endoscopy we observe that the material enters in the airways, it falls below the neoglottis, and no effort is made to expel it) (Table 2). The first evaluation of swallowing was performed on average on the 12 postoperative day (range: 8–15 days), while the second evaluation was performed on average on the 22 post-operative day (range: 17–30 day). For the evaluation, Acquagel or semisolid bolus was used.

Table 2.

Modified PAS (penetration-aspiration scale) for subtotal laryngectomies

1	Material does not enter the airway
2	Material enters the airway, contacts the neoglottis, stimulates cough reflex, and is ejected completely
3	Material enters the airway, contacts the neoglottis, stimulates cough reflex, and is not completely ejected
4	Material enters the airway, passes below the neoglottis, stimulates cough reflex, and is ejected completely
5	Material enters the airway, passes below the neoglottis, stimulates cough reflex, and is not completely ejected
6	Material enters the airway, passes below the neoglottis, and no effort is made to reject

Statistycal Analysis

The sample was analyzed using descriptive statistics, using mean and standard deviation for the quantitative variables, and absolute frequencies and percentages for categorical variables. The results were summarized in Tables 3, 4 and 5. Univariate and multivariate linear regression models were implemented to estimate the PAS score at a mean of 12 and 22 days after surgery. Only the significant predictors in univariate were included in the multivariate analysis. The significance level was set at p < 0.05, all analyzes were conducted with the software STATA vers.13 (StataCorp Release 13. College Station, TX).

Table 3.

Descriptive analysis of statistical frequencies of the examined features

	Frequency	Percentage (%)
Gender
Female	6	30
Male	14	70
Type of surgery
CHEP	10	50
CHP	10	50
Preoperative RT
No	16	80
Yes	4	20
pT
T2	10	50
T3	10	50
pN
N0	18	90
N1	2	10
Resection of one arytenoid
No	12	60
Yes	8	40
Decannulation time (post operative days)
3	2	10
5	2	10
6	8	40
7	2	10
8	2	10
10	4	20

Table 4.

Univariate and multivariate regression model of 12th-day PAS score

	Univariate analysis		Multivariate analysis
	β	p value	β	p value
Gender
female	Ref
male	0.16	0.797
Type of surgery
CHEP	Ref
CHP	− 1.1	0.05
Post-operative RT
no	Ref
yes	0.56	0.445
pT
T2	Ref
T3	1.5	0.005	1.27	0.007
pN
N0	Ref
N1	1.6	0.09
Resection of one arytenoid
No	Ref
Yes	1.375	0.014	1.46	0.018
Decannulation time (post operative days)	0.19	0.13

Table 5.

Univariate and multivariate regression model of 22th-day PAS score

	Univariate analysis		Multivariate analysis
	β	p value	β	p value
Gender
Female	Ref
Male	0.16	0.797
Type of surgery
CHEP	Ref
CHP	− 1.1	0.05
Post-operative RT
No	Ref
Yes	0.56	0.445
pT
T2	Ref
T3	1.5	0.005	1.27	0.007
pN
N0	Ref
N1	1.6	0.09
Resection of one arytenoid
No	Ref
Yes	1.375	0.014	1.46	0.018
Decannulation time (post operative days)	0.19	0.13

Results

Demographic Data

The cohort consisted of 20 patients, mostly males (70%), half treated with CHEP and half with CHP. Most of them did not undergo radiotherapy before the operation (80%). The tumors treated were staged 50% as pT2, and 50% as T3. Only 10% was staged as pN1, while 90% were staged as pN0. One arytenoid was resected in 8 patients. Decannulation occurred on average after 6.7 ± 2.1 days. (Table 3). The PAS score was assessed after a mean of 12 days from surgery, and the average score was 2.95 ± 1.23, and after a mean of 22 days when the average was 2.55 ± 1.27. First, the univariate analysis was carried out. The 12-day PAS score was related to all the collected factors (Table 4) and it was assessed whether the association was statistically significant (p value < 0.05) or not. Only the statistically significant factors not associated with them were included in the multiple regression analysis. The β coefficient, or the regression coefficient, indicates the increase in the PAS score in the presence of that modality compared to the other. For example: being male increases the PAS score by 0.07 points compared to being female; for each additional day with the cannula, the PAS score increases by 0.26 points. The p value indicates whether that variable is significantly associated with the PAS score. If p > 0.05 the association is not statistically significant.

Statistical Analysis

After the univariate analysis, it can be concluded that type of surgery, pT, resection of one arytenoid, and decannulation time are significantly associated with the 12-day PAS score, so we could include all 4 in the multivariate analysis (Table 4). However, the model will lose significance if the 4 variables related to the PAS score are not correlated with each other. Of the 4 variables with significant p value, only 2 were included in the multivariate analysis: pT and resection of one arytenoid, which are those with the greatest β value. At this point the multivariate model will have only two variables and will indicate that:

• T3 tumor increases the PAS score at 12 days by 1.07 points compared to a T2, in a statistically significant way (p = 0.022);

• Resection of one arytenoid increases the PAS score at 12 days by 1.11 points compared to not having resected it, in a statistically significant manner (p = 0.021).

Consequently, a patient with T3 and an arytenoid resected starts from a PAS score of 2.18 (1.07 + 1.11), higher than a patient with T2 and a non-resected arytenoid. This multivariate model, despite having only two explanatory variables, is still a good model, in fact the R2 (goodness of fit of the model) is equal to 48%. For the 22-week PAS score, in which the same procedure was performed, the reference is Table 5. The 22-day PAS score is significantly associated with only 3 variables: type of surgery, pT, and resection of one arytenoid. Particularly, in a T3 tumor there is an increase of 1.27 (p = 0.007) points in the PAS score compared to a T2 tumor, while the resection of one arytenoid leads to an increase of 1.46 points in the same score (p = 0.018). This is a fairly accurate model, in fact it has an R2 = 54%. Only 4 patients experienced aspiration pneumonia.

Decannulation Versus Other Factors

Patients Undergoing CHP

Mean decannulation in patients undergoing CHP surgery occurred on the 7th postoperative day (5–10 days).

• Both arytenoids preserved (4 patients), decannulation on average in the 6th postoperative day,

• only one preserved arytenoid (6 patients), decannulation on average in the 7th postoperative day

• Unilateral neck dissection (4 patients) average decannulation in the 6th postoperative day

• Bilateral neck dissection (6 patients) decannulation on average in 7.6th postoperative day

• Bilateral neck dissection + 1 arytenoid (4 patients), decannulation on average in 8.5th post-operative day

• Neck dissection + 1 arytenoid (4 patients), decannulation on average in 5.5th post-operative day

• Neck dissection or 1 arytenoid (2 patients), decannulation on average in the 7th postoperative day

Patients Undergoing CHEP

Mean decannulation in patients undergoing CHEP occurred in 6.4th postoperative day (3–10 days).

• Both arytenoids preserved (8 patients), decannulation on average in 5.5th postoperative day,

• One preserved arytenoid (2 patients), decannulation on average in the 10th post-operative day.

• Neck dissection not performed (6 patients) mean decannulation in 5.3th postoperative day

• Neck dissection performed (4 patients) decannulation on average in the 8th postoperative day

• Neck dissection + 1 arytenoid (2 patients), decannulation on average in 10th postoperative day

• Neck dissection + 0 arytenoids (2 patients), decannulation on average in the 6th post-operative day

• No neck dissection + 0 arytenoid (6 patients), decannulation on average in the 7th postoperative day

Discussion

Our results showed that the factors that most delay an effective recovery of swallowing after supracricoid laryngectomy are pT3 and resection of one arytenoid. A pT3 tumor increases the PAS score at 12 days by 1.07 points compared to T2 and by 1.27 at 22 days. But the factor that most negatively affects the resumption of swallowing is the resection of the arytenoid with an increase in the PAS score of 1.11 at 12 days and of 1.46 at 22 days. It follows that in T3 patients with the arytenoid resected the score is even higher.

Although the partial supracricoid laryngectomy preserves a cricoarytenoid unit, the incomplete closure of the glottis with inhalation may remain [6]. The closure of the neoglottis can be achieved thanks to the posterior movement of the base of the tongue and the epiglottis (only in CHEP) and the forward and inward rotation movement of the residual arytenoid. It follows that the conservation of both arytenoids, collaborating with each other, allows a better closure of the neoglottis.

In this surgery, patients undergoing early rehabilitation are fed orally, without aspiration, on average 8–13 days earlier than the ones not undergoing rehabilitation [7]; although dietary choices alone do not reduce aspiration, it is reduced through the use of swallowing strategies that the patient learns during early post-operative rehabilitation [8]. Early rehabilitation and swallowing strategies can reduce the recovery time of dysphagia but, according to our data, they have a subordinate role to the preservation of the second arytenoid and the degree of T.

The type of surgery performed (CHP vs CHEP) is a factor that causes a delay in the recovery of swallowing at 12 and 22 days, but its effectiveness in representing the dysphagia problem, according to the univariate analysis, is lower than the degree of pT or resection of the arytenoid.

It is obvious, however, that the resection of one arytenoid and the degree of pT are closely related to the type of surgery. Among our patients, 8 CHEP retained both arytenoids, while only 4 were CHP patients.

Early decannulation has been shown statistically to improve the PAS score in the short but not in the long term, not confirming our initial hypothesis. Unlike our experience, where decannulation took place between 3 and 10 days, other authors [1–3] had average decannulation times, evaluated with MDADI, and “Pearson and Leipzig scale”, between 8 and 10 days, with better recovery from dysphagia but the types of surgery performed were predominantly CHEP (90%), and only the remaining 10% CHP. Therefore, their experience is not fully comparable with ours for 2 reasons: 50% of our patients had undergone CHP, and our dysphagia assessment procedures were different [9].

Bussi M et al. [9] analyzed a cohort of 39 patients, who underwent supracricoid laryngectomy, who recovered swallowing function free of disease after a minimum 3-year follow-up period with the Pearson’s Scale and MDADI and FEES; the authors demonstrated chronic aspiration, clinically, in 33.3% and, instrumentally, in 35.9% of patients, and found that aspiration was influenced by advanced age at surgery. The prevalence of aspiration was not influenced by the type of surgical procedure, resection of 1 arytenoid cartilage, postoperative rehabilitation with a speech-language therapist, radiotherapy, age at consultation, and length of follow-up. Among this cohort, five patients had pulmonary complications, whose incidence was related to aspiration and was favored by poor laryngeal sensation/cough reflex. Since incidence of pulmonary complications was low, the authors recommended that oral feeding should not be contraindicated for aspirating patients. Preservation of laryngeal sensation and cough reflex is mandatory to prevent pulmonary complications. Also in this case, since these methods of assessing dysphagia are different from ours, it is not possible to make a comparison with our study. However, the authors found that only 1 out of 3 patients who had episodes of subglottic aspiration, had aspiration pneumonia. The value was also confirmed in our study: 4 of 13 patients with PAS score ≤ 3 at 12 days had aspiration pneumonia. The conclusions reached by the authors, which we agree with, is that the probability that aspiration phenomena cause aspiration pneumonia, is modest.

Limits of the Study

This study shows several limits. First, the cohort of the study is too small to draw definitive conclusions. Second, a longer follow-up time should be required to confirm the present results. Third, the lack of a control group with a different decannulation time could affect the conclusion; for this, we used previous literature to compare our results.

Despite these limitations, the prospective nature of the study, and the rigorous statistics are the strengths of this work.

Conclusions

CHEP or CHP horizontal supracricoid laryngectomies require a period of time for swallowing recovery, which is longer in T3 patients who have had an arytenoid resected. The choice of the type of surgery (CHEP vs CHP), preoperative radiotherapy, neck dissection are variables subordinated to T. Early decannulation has been shown to improve the PAS score in the short but not in the long term, not confirming our initial hypothesis. While early decannulation inherently reduces splinting of the trachea, later effects subjectively may be due to the complexities of surgery and pathology.

Funding

No funding to declare.

Declarations

Conflict of interest

No conflict of interests to disclose.

Ethical Approval

This study was conducted according to the principles of the Helsinki Declaration and in accordance with the regulations of the Ethical Committee for prospective studies of the involved institution—Dipartimento Organi di Senso, Sapienza Università di Roma CE2021, who approved the present work without releasing an approval number.

Informed Consent

Informed consent was obtained from all the participants before their inclusion in the study.