Evaluation of postoperative function in patients undergoing reconstruction following resection of superior and lateral oropharyngeal cancer: long-term outcomes of reconstruction with the Gehanno method

Article Outline

• Abstract
• Materials and methods
• Procedure for reconstruction
• Evaluation of postoperative function
• Results
  • Nasal breathing
  • Articulation
  • Swallowing
  • Nasopharyngeal cavity closing function
• Discussion
• Funding
• Competing interests
• Ethical approval
• References
• Copyright

Abstract 

Resection of the superior or lateral wall of the cancer-affected oropharynx can often lead to disturbed nasal breathing, dysphagia, and dysarthria. The authors used the Gehanno method to reconstruct these surgical defects and achieved favourable functional recovery soon after surgery. The present study was undertaken to analyze the long-term outcome and usefulness of this method. Reconstruction was carried out using the Gehanno method in 36 patients during the 10-year period between 1997 and 2007. Both short-term and long-term evaluations of the postoperative function were performed in 12 of the 36 cases. The postoperative function was favourably maintained in all 12 cases, but gradual deterioration was noted in some cases in which the forearm flap had been used for reconstruction. Conventionally, the forearm flap is considered suitable for the reconstruction of complex structures such as the oropharynx because of its excellent flexibility. The results suggest that if the forearm flap is used for reconstruction using the Gehanno method, the surrounding tissue is likely to undergo change over time. The rectus abdominis myocutaneous flap should be considered as the first-choice flap for reconstruction using the Gehanno method.

Keywords: Oropharynx, Reconstruction, Postoperative function, Long-term results

The oropharynx and its surrounding structures such as the soft palate and tonsils play important roles in articulation and swallowing. Surgery in this region should be performed carefully to prevent loss of the physiological function of these structures.

For functional recovery after resection of superior and lateral oropharyngeal cancer, the authors applied a technique in which a narrow border is created between the superior pharynx and the oropharynx (whilst avoiding disturbance in nasal breathing), similar to the velopharyngoplasty reported by Gehanno et al.², and the technique reported by Omura et al. was used to reconstruct the lower part of the fauces such that it is narrow and high¹¹. The authors have reported that reconstruction with this technique (hereafter called Gehanno method) enables favourable functional recovery soon after surgery⁴. To date, several cases have reported short-term (less than 1 year) evaluations of functional recovery after reconstruction performed using various techniques⁴, ¹¹, ¹², but few studies have reported the long-term outcomes of these techniques¹⁰. Only 1 study (published by the authors) has reported the long-term outcomes of reconstruction performed using the Gehanno method⁵. In this study, the authors have evaluated functional recovery more than 2 years after reconstruction with the Gehanno method and compared the long-term results with the short-term results to analyze the long-term usefulness of this method.

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Materials and methods 

During the 10-year period between 1997 and 2007, 36 patients underwent oropharyngeal reconstruction using the Gehanno method. In 12 of these 36 patients, follow-up was continued for 2 years or longer after surgery. The postoperative function (described later) was evaluated for these patients, and this allowed comparison of the long-term and short-term outcomes. These 12 patients were analyzed in this study. The survival data for these 12 patients did not correlate with the survival data of all the patients who underwent the operation at the authors’ facilities. Of the 24 patients for whom postoperative function could not be evaluated, 5 died of an underlying disease, 3 died of other causes, 3 could not be followed up, and 13 could not be evaluated. The reasons for the 13 not being evaluated were: lack of cooperation in 4; accompanying disease in 2 (1 postoperative cerebral infarction and 1 depression); combined resection of some organs in 7 (3 subtotal glossectomy, 3 resection of the mandible and 1 total laryngectomy). Neither short-term nor long-term evaluation of function was possible for the 13 patients who could not be evaluated.

The ages of the 12 patients at the time of surgery ranged from 51 to 68 years (mean 60.3 years). The ages of the patients at the time of evaluation of the long-term results ranged from 54 to 71 years (mean 64.2 years). All 12 patients were men. The site of the primary cancer was the lateral wall in 10 cases and the superior wall in 2 cases. At the first examination, the tumour was rated according to the T classification system: T1 in 1 case; T2, 4 cases; T3, 1 case; and T4, 6 cases. The authors adopted the draught classification system proposed by Miura et al.¹⁰ to classify the extent of the defects (Fig. 1) because the evaluation of postoperative function is closely dependent on the extent of the oropharyngeal defects.

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• Figure 1. 

  Classification of the extent of defects in the oropharynx (draught).

Source: Miura et al.¹⁰.

All 12 patients received preoperative radiation (about 40Gy). In the cases in which excision in the parapharyngeal space¹⁵ was required, the operative field was developed using a mandibular swing approach¹⁴, and reconstruction was performed using a rectus abdominis myocutaneous flap. In the cases in which excision in the parapharyngeal space was not required, reconstruction was performed using an intraoral technique with a forearm flap. The rectus abdominis myocutaneous flap was used for reconstruction in 7 cases, whereas the forearm flap was used in 5 cases (Table 1).

Table 1. Patient data.

FA: forearm flap, RAMC: rectus abdominis myocutaneous flap.

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Procedure for reconstruction 

The procedure is shown in Fig. 2. First, the pharyngeal mucosa was freed from the pharyngeal posterior wall stump over the prevertebral fascia, and the pharyngeal myomucosal flap, which was composed of mucosa and the superior pharyngeal constrictor, was raised. In this step, freeing of the mucosa was done to the minimum degree possible. Next, the pharyngeal myomucosal flap was everted in the superomedial direction and sequentially sutured to the residual soft palate stump.

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• Figure 2. 

  Procedure for reconstruction. (1) Resection of the lateral wall and superior wall (including a part of the lingual root) of the oropharynx. (2) Freeing of the pharyngeal myomucosal flap from the oropharyngeal posterior wall stump (*), followed by superomedial eversion. (3) Suturing of the pharyngeal myomucosal flap to the soft palate and hard palate stump in sequences, followed by suturing of the lingual root to the pharyngeal posterior wall stump. (4) Covering of the exposed mucosal defect with the free flap.

Thus, a new velopharyngeal port surrounded by the mucosal plane was formed, the border between the superior pharynx and the oropharynx having been decreased to less than half of its original size. At the lower end of the pharyngeal lateral wall, the pharyngeal posterior wall stump was sutured to the lingual root stump as far as possible to ensure that the lower part of the fauces was narrow and high. In the last step, the flap was sutured to the defective areas of the exposed superior pharynx constrictor, pharyngeal posterior wall, pharyngeal lateral wall, and other areas of the oral cavity and oropharynx, and the wound was covered. Covering the wound marked the end of the reconstruction procedure.

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Evaluation of postoperative function 

The presence or absence of disturbances in four functions (nasal breathing, articulation, swallowing, and nasopharyngeal cavity closing function) was evaluated at about 6 months and 2 years after the operation, and the results obtained at the two time points were compared. The long-term results were recorded between 25 and 76 months after surgery (median 41 months).

The presence or absence of disturbed nasal breathing was evaluated by checking for subjective symptoms of nasal congestion and by analyzing the inspired and expired air and the time course of subjective symptoms from immediately after surgery to the time of the long-term outcome evaluation.

The articulation function was evaluated by analyzing speech clarity whilst the patient read a paragraph of a story aloud and by calculating the clarity of 100 monosyllabic Japanese words selected for the oropharyngeal function test¹¹. The clarity of velar consonants for 16 of these 100 words (velar consonant clarity) was also evaluated.

The swallowing function was evaluated using a questionnaire survey of the diet menu, time taken for eating, and inconvenience encountered whilst swallowing. The swallowing function was also evaluated objectively using video fluorography (VF).

The nasopharyngeal closing function was evaluated on the basis of the results of the blowing test⁷, by calculating the ratio (%) of the duration of soft blowing during nasal opening to that during nasal closure per expiration (‘blowing ratio’).

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Results 

Nasal breathing 

In the evaluation of subjective symptoms, none of the patients complained of disturbed nasal breathing during inspiration or expiration, and none of the patients experienced nasal congestion from the time immediately after surgery to the time of the long-term outcome evaluation. Intensification of snoring during sleep was observed in some patients but this finding was not considered a subjective symptom.

Articulation 

On the basis of the criteria for the evaluation of speech function proposed by Hirose (a member of the Ministry of Health and Welfare cancer study group ‘59-8: Establishment of treatment methods for oral and oropharyngeal cancer and evaluation of post-treatment function’)³, speech clarity was rated as excellent (score 8–10) in all 12 patients. When the changes in speech clarity were analyzed in the same patients, the score tended to worsen slightly in patients who had undergone reconstruction with the forearm flap (cases 1, 2 and 8; Fig. 3).

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• Figure 3. 

  Results for speech clarity.

The clarity of 100 monosyllabic Japanese words in the oropharyngeal function test ranged from 75% to 92% (mean 84%) in the short-term outcome evaluation, but it ranged from 64% to 91% (mean: 81%) in the long-term outcome evaluation. Velar consonant clarity showed a greater variance, ranging from 56% to 94% (mean 75%) in the short-term outcome evaluation and from 44% to 94% (mean 72%) in the long-term outcome evaluation. These parameters were analyzed in relation to the extent of defects. In Group II (defects in palate+lateral wall), the monosyllabic word clarity ranged from 86% to 92% (velar consonant clarity 63–75%) in the short-term outcome evaluation and from 80% to 83% (velar consonant clarity 44–81%) in the long-term outcome evaluation. In Group III (defects in palate+lateral wall+lingual root), the monosyllabic word clarity ranged from 75% to 92% (velar consonant clarity 56–94%) in the short-term outcome evaluation and from 64% to 91% (velar consonant clarity 44–94%) in the long-term outcome evaluation. The extent of surgical resection was not associated with marked reduction in monosyllabic word clarity or velar consonant clarity. When the changes over time were analyzed in the same patients, 5 of the 12 patients showed a tendency for deterioration in articulation, and 3 patients (cases 2, 4 and 8) showed 15% or more reduction in velar consonant clarity after reconstruction with the forearm flap (Fig. 4).

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• Figure 4. 

  Results for monosyllabic word clarity (a) 100 words for the oropharynx test; (b) 16 velar consonants.

Swallowing 

At the time of short-term and long-term outcome evaluations, all patients were capable of ingesting foods orally. Although the questionnaire survey revealed 1 patient who had been receiving tube feeding as an auxiliary means of nourishment in addition to oral ingestion (case 3), all patients were capable of ingesting an ordinary diet or soft diet orally. The time taken for a meal ranged from 20 to 60min. Regarding inconveniences related to eating, no patient complained of ‘difficulty in swallowing’, but 2 patients complained of ‘occasional outflow of food/drink through the nose’ (cases 2 and 8). When the changes in the swallowing function over time in the same patients were analyzed, no patient showed a marked change in this function, but 2 patients (cases 2 and 4) reported occasional ‘difficulty in swallowing’ and 1 patient (case 11) reported occasional ‘mis-swallowing symptom’ at the time of the long-term outcome evaluation.

In the analysis of VF data, the capability to retain barium within the oral cavity was favourable at both the short-term and long-term outcome evaluations. No patient showed regurgitation into the nasal cavity during swallowing or mis-swallowing into the trachea. Swallowing was smooth in all patients. Even the patient who had reported some inconveniences in the questionnaire survey (cases 2, 4, 8 and 11) showed sufficient closure of the nasopharyngeal cavity and no mis-swallowing in the objective evaluation.

Nasopharyngeal cavity closing function 

The blowing ratio ranged from 81% to 96% (mean 90%) in the short-term outcome evaluation and from 60% to 100% (mean 85%) in the long-term outcome evaluation. The authors analyzed the blowing ratio in relation to the extent of defects. In Group II, the mean blowing ratio was 92% in the short-term outcome evaluation and 84% in the long-term outcome evaluation. In Group III, it was 89% and 85% in the short-term and long-term outcome evaluations, respectively. The blowing ratio did not differ according to the extent of surgical resection. In the analysis of the changes in the blowing ratio over time, a tendency to deterioration was seen in 4 patients (cases 1, 2, 4 and 8), all of whom had undergone reconstruction with the forearm flap. The changes in the blowing ratio over time were associated with the type of flap used for the reconstruction rather than the extent of surgical resection, which was similar to the changes observed in articulation (Fig. 5).

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• Figure 5. 

  Results for blowing ratio.

Table 2 summarizes all the patient data. Details are given for 2 patients: case 3 (a typical case) in Fig. 6; and case 2 (a case of deteriorated function after reconstruction with the forearm flap) in Fig. 7.

Table 2. Results of the outcome evaluations.

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• Figure 6. 

  Case 3: 57 months after surgery (reconstruction with the rectus abdominis myocutaneous flap). (a) The flap remains bulky and the pharyngeal cavity formed is narrow. (b) Complete closure of the nasopharyngeal cavity was achieved during swallowing. (c) Newly formed velopharyngeal port. (d) VF revealed no sign of nasopharyngeal regurgitation and mis-swallowing.

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• Figure 7. 

  Case 2: 58 months after surgery (reconstruction with the forearm flap). (a) Atrophy of the resected area caused extensive upward spread of the pharyngeal cavity. (b) Closure of nasopharyngeal cavity is slightly incomplete during swallowing. (c) VF revealed no sign of nasopharyngeal regurgitation and mis-swallowing.

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Discussion 

The soft palate has two functions that are contrary to each other (opening and closing of the nasopharyngeal cavity), so reconstruction of the soft palate after resection is difficult.

Various techniques have been reported for soft palate reconstruction⁶, ¹³. They are principally designed for static reconstruction, and functional reconstruction with these techniques seems to be difficult to achieve. The postoperative function of the soft palate is closely associated with the location and extent of surgical resection. If the lateral wall of the oropharynx is resected along with the soft palate, the pharyngeal lateral wall will lack mobility after reconstruction, and this lack of mobility is likely to cause dysphagia (e.g. mis-swallowing) and dysarthria (e.g. nasal voice). Kimata et al.⁸ compared four methods of reconstruction (patch method, jump method, denude method, and Gehanno method) after resection of the superior or lateral wall of the oropharynx and reported that reconstruction performed using the Gehanno method yielded excellent outcomes in cases in which two-thirds or less of the superior wall had defects. Attempts have been made to avoid surgery for cases of oropharyngeal cancer (particularly cancer that primarily affects the lateral wall of the oropharynx) and to select radiotherapy or chemoradiotherapy as the first-line therapy because of the high sensitivity of the cancer to these treatments¹. In the authors’ department, one strategy employed for the treatment of advanced lateral oropharyngeal cancer during the observation period is the administration of preoperative radiotherapy (about 40Gy) combined with chemotherapy (primarily using cis-diamminedichloroplatinum (CDDP) and 5-fluorouracil (5-FU)), followed by extended surgical resection and reconstruction. All patients enrolled in this study had received preoperative chemoradiotherapy.

The Gehanno method was originally reported in 1985 by Gehanno et al.² Later, Omura et al. modified the method of reconstruction of the lower part of the fauces¹¹. Kimata et al. were the first to use the term ‘Gehanno method’ for this reconstruction technique⁸. Morphologically, this technique is designed to form a narrow border between the superior pharynx and the oropharynx such that nasal breathing is not disturbed and to restore the closing function of the nasopharyngeal cavity through the contractility of the pharyngeal myomucosal flap. When used for the reconstruction of the oropharyngeal lateral wall, this technique is designed to allow reconstruction of the lower part of the fauces such that it is narrow and high, thereby preventing postoperative mis-swallowing (particularly mis-swallowing during the descending phase in the larynx).

This technique is simple and can achieve a favourable postoperative function. The authors have previously reported the usefulness of the Gehanno method⁴, ⁵ but during the postoperative follow-up of patients who underwent surgery with this technique, the authors occasionally encountered cases where the patient showed local atrophy and gradual deterioration of function after surgery, even though good functional recovery was seen immediately after the surgery. In the light of these findings, the authors decided to evaluate the usefulness of this technique. They conducted the present study to compare the long-term functional outcome with the short-term outcome in individual patients who had undergone surgery ≥2 years ago at the Kansai Medical University Hospital or its affiliated hospitals.

In general, the outcome for nasal breathing was favourable for a long time immediately after surgery. The newly formed velopharyngeal port at the border between the superior pharynx and the oropharynx was designed to have a size equivalent to the width of the little finger. Nasal breathing was not disturbed if a size of at least about 1/4 of the normal space was ensured (Fig. 6), and this space does not seem to be affected by the deformation of the flap (Fig. 6). Regarding articulation, patients showed favourable recovery of speech not only with family members but also with other individuals. Speech clarity differed depending on the location and extent of combined resection and on the type of flap used for reconstruction. A general evaluation of the effect of this technique on articulation was not possible. For this reason, the authors attempted to calculate and analyze the clarity of velar consonants in this study. The data on this parameter varied from case to case. When the background variables of the cases showing poor function were analyzed, gradual atrophy of the resected area after reconstruction with the forearm flap was found; this atrophy resulted in a gradual and upward spread of the fauces, which had initially enabled favourable articulation (Fig. 7).

Simple comparison was difficult because the number of patients who had undergone the same degree of resection was small, but this phenomenon was seldom associated with the extent of soft palate resection. This phenomenon was quite rare amongst the patients who had undergone reconstruction with the rectus abdominis myocutaneous flap, which suggested that such a postoperative change is unlikely to occur after reconstruction with this type of flap. This finding may be explained as follows. The muscular body, which can generally undergo atrophy, primarily fills the parapharyngeal space, and the pharynx and its surrounding structures retain an appropriate volume because of the presence of fat, which is less likely to be affected by atrophy. Regarding the swallowing function, none of the cases showed repeated mis-swallowing necessitating glottis closure or laryngectomy. The observed mis-swllowing rarely caused any disturbances in daily life. In the objective evaluation, none of the cases showed a deterioration in the swallowing function over time. In the above-mentioned case where the fauces expanded after reconstruction with the forearm flap, the patients showed adequate ingestion of diet (soft food). The VF examinations revealed no regurgitation into the nasal cavity in any patient. Combined with the favourable results in the blowing ratio (an indicator of the closing function of the nasopharyngeal cavity), this finding seems to reflect the fact that the function of the residual normal tissue could be maximally utilized (a characteristic of reconstruction with this technique).

Regarding the materials used for reconstruction, the forearm flap, which has previously been reported to be suitable for the preservation of the residual function because of its high flexibility⁹, was shown to be likely to undergo changes over time if used for reconstruction in the Gehanno method. The rectus abdominis myocutaneous flap has a larger volume, and seems to be suitable for oropharyngeal reconstruction in which a narrow cavity needs to be formed. This flap is relatively soft and does not seem markedly to suppress the mobility of the residual tissue. In the evaluation of the long-term outcome, the subcutaneous fat seemed to have undergone minimal changes over time. This finding also suggests that the rectus abdominis myocutaneous flap is superior to the forearm flap.

Conventionally, the necessity for the excision of a tumour in the parapharyngeal space served as a criterion for the selection of the type of flap used in the authors’ department. At present, it is relatively easy to adjust the muscular mass and it seems advisable to use the rectus abdominis myocutaneous flap as the first-choice flap, regardless of the necessity for the excision of a tumour in the parapharyngeal space.

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Funding 

This work was supported by a Fund from the Society for Research Aid in Otolaryngology, Kansai Medical University.

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Competing interests 

None declared.

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Ethical approval 

Not required.

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