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Research

Original Investigation

Analysis of Postoperative Bleeding and Risk Factors


in Transoral Surgery of the Oropharynx
Taylor R. Pollei, MD; Michael L. Hinni, MD; Eric J. Moore, MD; Richard E. Hayden, MD; Kerry D. Olsen, MD;
John D. Casler, MD; Logan C. Walter, BS

IMPORTANCE With an increasing incidence of oropharyngeal carcinoma and prevalence of


transoral surgical techniques, postoperative bleeding, with its associated risk factors,
deserves evaluation.

OBJECTIVE To classify and review postoropharyngectomy hemorrhage rates and associated


risk factors.

DESIGN, SETTING, AND PARTICIPANTS Single-institution, multicenter retrospective medical


chart review analyzing surgical procedures in 906 patients treated with transoral surgery for
oropharyngeal carcinoma at a tertiary care, academic referral center from 1994 to 2012.
Tumor stage, previous treatment, resection method, and transcervical external carotid
branch ligation were analyzed in relationship to postoperative hemorrhage rate, and severity.
A novel classification system was created, grading bleeding episodes as minor, intermediate,
major, or severe based on management method and related sequelae.

RESULTS Postoperative bleeding occurred in 5.4% of patients (49 of 906) with 67.3% of
these (33 of 49) requiring operative intervention. Severe bleeding episodes were very rare
(1.1% of patients). Transcervical external carotid system vessel ligation was performed with
the primary resection in 15.6% of patients with no overall difference in bleeding rate or
severity of bleeding in patients who underwent ligation vs those who did not (P = .21 and
P = .66, respectively). Vessel ligation was performed more frequently in patients with a
higher T stage (P = .002). In previously treated patients, severity of bleeding was decreased if
vessels were ligated (P > .05). Higher T-stage tumors had a higher bleeding rate (P = .02).
Bleeding rates were similar between those treated with laser (5.6%) and robotic (5.9%)
oropharyngectomy (P = .80); however, patients with significantly higher T-stage tumors were
treated with laser vs robot techniques (P < .001).

CONCLUSIONS AND RELEVANCE Transoral resection of oropharyngeal carcinoma is safe, and


severe life-threatening hemorrhage is rare. Although transcervical vessel ligation did not
result in an overall decrease in bleeding rate, there is a trend toward reduced
postoropharyngectomy bleeding severity with ligation. We recommend ligation for higher
T-stage tumors, primary tonsil tumors, and patients undergoing revision surgery.

Author Affiliations: Department of


Otolaryngology–Head and Neck
Surgery, Mayo Clinic Arizona, Phoenix
(Pollei, Hinni, Hayden, Walter);
Department of
Otorhinolaryngology–Head and Neck
Surgery, Mayo Clinic Rochester,
Rochester, Minnesota (Moore,
Olsen); Department of
Otolaryngology–Head and Neck
Surgery, Mayo Clinic Jacksonville,
Jacksonville, Florida (Casler).
Corresponding Author: Taylor R.
Pollei, MD, Department of
Otolaryngology–Head and Neck
Surgery, Mayo Clinic Arizona, 5777 E
JAMA Otolaryngol Head Neck Surg. 2013;139(11):1212-1218. doi:10.1001/jamaoto.2013.5097 Mayo Blvd, Phoenix, AZ 85054
Published online October 10, 2013. (pollei.taylor@mayo.edu).

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Transoral Surgery of the Oropharynx Original Investigation Research

H
ead and neck squamous cell carcinoma (SCC) repre-
Table 1. Classification System for Postoperative Hemorrhage
sents the sixth most common cancer diagnosed
worldwide.1 While the incidence of cancer in all non- Classification Description
oropharyngeal subsites has been steadily decreasing, over the Normal Patient noting the presence of blood-tinged mucus, flecks
of blood, brown mucus, or red streaks
past few decades, incidence of oropharyngeal squamous cell Minor Any description of bright red blood or blood clots
carcinoma (OPSCC) has been increasing.2,3 This has resulted Resolved without operative management whether or not
physician evaluation or hospitalization occurred.
in the identification of a causative relationship between hu-
Intermediate Diffuse venous oozing or small arterial source bleeding
man papillomavirus and OPSCC. Human papillomavirus– resulting in operating room evaluation or intervention
associated OPSCC presents in younger patients with less cor- Managed with monopolar or bipolar cautery
relation to tobacco use, responds more effectively to current Major Brisk or copious bleeding requiring operative intervention
Managed with transoral or transcervical vessel ligation, or
treatment modalities, and has high disease-specific and over- interventional radiology embolization
all survival rates.4,5 Severe Bleeding resulting in life-threatening medical
Transoral surgery (TOS) has been well established as a complications such as:
Hypoxia/airway compromise requiring tracheostomy
safe, effective treatment modality for cancer of the upper Cardiopulmonary arrest
Hemodynamic instability requiring blood transfusion
aerodigestive tract, yielding excellent functional and onco-
logic outcomes.6-9 Additional advantages of TOS techniques
include shorter length of hospitalization, decreased patient included patient demographics, tumor pathologic findings, lo-
morbidity, and lower surgical complication rates.7,10 Initial cation and T stage, surgical technique, external carotid branch
descriptions utilizing electrocautery and diathermy were vessel ligation, and presence of postoperative bleeding with
further expanded as laser dissection methods or transoral its associated severity and management.
laser microsurgery (TLM) was recognized.11,12 More recently, Postoperative hemorrhage was graded, using a newly cre-
transoral robotic surgery (TORS) has been popularized.13-15 ated classification system, as minor, intermediate, major, or
The use of both TLM and TORS to treat the increasing num- severe. This was based on quantity of blood loss, type of sur-
bers of palatine tonsil and tongue base SCC has been well gical management required, and development of life-
documented.16-19 threatening complications or need for emergent life-saving in-
Surgical complications, including bleeding, trismus, dys- tervention (Table 1).
phagia, aspiration, taste disturbance, and infection, can occur
as a result of both the traditional open approach and transoral
oropharyngectomy. Post–transoral surgery hemorrhage is un-
predictable and potentially catastrophic, with published rates
Results
for all head and neck subsite malignant neoplasms of 1.4% to All 906 patients met inclusion criteria, with 4 surgeons per-
9%.6,10,14,20,21 Bleeding rates following transoral oropharyn- forming 87.5% of all procedures (793 of 906). The average age
gectomy of 3% to 10% have been documented, which corre- was 59 years, and 83% were male and 17% were female. Pre-
late with published postoperative tonsillectomy bleeding rates vious treatment was documented in 7.6% of all patients (69 of
of 0.5% to 10%.10,22,23 A direct correlation between previous can- 906) with 58 previously treated with irradiation and 11 under-
cer treatment (surgery or radiation therapy) and all head and going revision surgery. Primary tumor T stage was docu-
neck subsite bleeding rates has been shown.10 Whether exter- mented according to the 2010 American Joint Committee on
nal carotid artery branch ligation at the time of TOS (typically Cancer (AJCC) TNM staging system.24 Of the 906 patients re-
performed with concurrent neck dissection) has any effect on viewed, 36.4% had stage T1 tumors; 41.6%, stage T2; 14.9%,
postoropharyngectomy bleeding rates has not been ad- stage T3; and 7.2%, stage T4. All of the resections were per-
dressed. The relationship between bleeding rates and tumor size formed transorally without reconstruction. When appropri-
and a comparison between bleeding rates in TLM and TORS mo- ate, neck dissection and vessel ligation were performed con-
dalities were questions that this study also addressed. currently with primary site resection. Significantly higher
T stages were treated with TLM when compared with TORS
with pairwise comparison methods. This was seen when look-
ing at the group with stage T1 tumors vs the group with stage
Methods T3 tumors (P < .001) and the group with stage T2 tumors vs the
Institutional review board approval from the Mayo Clinic Ari- group with stage T3 tumors (P < .001).
zona was obtained, and a secure database was created that in- All 906 primary tumors were located in the oropharynx,
cluded 906 patients with oropharyngeal cancer treated from with a specific subsite documented in 88.5% of patients (802
May 12, 1994, to May 31, 2012. Patients undergoing transoral of 906). When the tumors were documented, we found most
oropharyngectomy (TLM, TORS, or handheld electrocautery) to be located in the palatine tonsil (51.0%) followed by loca-
with or without previous cancer treatment at Mayo Clinic sites tion in the tongue base (46.0%), with the remaining 3.0% lo-
in Phoenix, Arizona; Rochester, Minnesota; and Jacksonville, cated in the soft palate or pharyngeal wall. Pathologic results
Florida; were included. Patients were excluded if they under- were present in all 906 patients, showing SCC in 97.8%, with
went an open cancer resection, the defect required reconstruc- the remaining 18 cases consisting of mucoepidermoid carci-
tion, or they lacked follow-up data. Standard, informed writ- noma (7), lymphoma (4), adenocarcinoma (3), adenoid cystic
ten consent was received at the time of surgery. Data collection carcinoma (2), and plasmacytoma (2).

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Research Original Investigation Transoral Surgery of the Oropharynx

Table 2. Postoperative Bleeding Details

Bleeding Severity
Patient/Surgical Characteristic Minor Intermediate Major Severe
Patients, No. 16 17 6 10
T-stage: unknown primary 1 1 1 0
T1 2 3 3 3
T2 6 8 1 3
T3 7 4 0 2
T4 0 1 1 2
Patients treated with revision surgery or radiation therapy, No. 1 1 0 3
Patients treated with transcervical ligation, No. 2 5 1 1
Postoperative day of bleeding, mean 11 10 10 9
Transoral laser microsurgery 11 6 3 6
Transoral robotic surgery 4 7 3 2
Handheld electrocautery 1 4 0 2

Tracheostomy was performed in 14.8% of patients (134 of Of bleeding episodes requiring operative intervention, 64% (21
906), and a nasogastric tube was placed intraoperatively in of 33) were treated by the patient’s primary surgeon with 36%
52.9% (479 of 906). Laser treatment was used in 53.0% surgi- (12 of 33) treated by either a local emergency department phy-
cal procedures, robotic surgery in 29.7%, and handheld elec- sician or otolaryngologist.
trocautery in 12.9%, with only 5 of 906 (0.55%) documented Transcervical external carotid system vessel ligation was
as laser-robotic or laser-cautery hybrid cases. No specific sur- performed in 15.6% of patients and was always performed at
gical technique was documented in 34 patients. Modified radi- the time of the primary resection. No significant difference in
cal neck dissection or selective neck dissection most often in- overall bleeding rate was found between the ligated (6.7%) and
cluded nodal levels II, III, and IV and was performed in 79.0% nonligated (5.5%) groups (P = .21). Regarding bleeding sever-
of all patients (717 of 906). These consisted of 569 ipsilateral ity, only 1 ligated patient developed severe bleeding. Ten per-
neck dissections (62.8%), 11 contralateral neck dissections cent of severely bleeding patients (1 of 10) underwent vessel
(1.2%), and 137 bilateral neck dissections (15.1%). Radical neck ligation vs 20.5% of nonseverely bleeding patients (8 of 39);
dissection was performed in 54 of 906 of all patients (6%). this difference was not statistically significant (P = .66). Higher
Documentation of single or multiple external carotid ar- T-stage tumors were more likely to bleed, as seen with pair-
tery branch ligation was present in 95.0% of medical charts and wise comparison methods. This was notable in T1 tumors vs
was performed in 15.6% of these cases (134 of 860). Ligation T3 tumors (P < .005) and T1 tumors vs T4 tumors (P = .001).
was performed at the time of concurrent neck dissection with The bleeding rate was no different between the TLM (5.6%) and
the ipsilateral lingual arteries (80 of 134) and facial arteries (71 TORS (5.9%) subgroups (P = .80); however, of the 2 surgical mo-
of 134) most frequently addressed. Also ligated were the ipsi- dalities, TLM T -stages were significantly higher (stage T1 vs
lateral superior thyroid (37 of 134), ascending pharyngeal (12 T3, P < .001; and stage T2 vs T3, P < .001).
of 134), superior laryngeal (2 of 134), occipital artery (2 of 134), Prior radiation therapy or surgery did not correlate with a sig-
or main external carotid trunk (28 of 134). Only once was a con- nificant increase in postoperative bleeding rate (7.8%) compared
tralateral vessel (lingual artery) ligated. There were no re- with previously untreated patients (5.4%) (P = .51). Although not
ported complications from vessel ligation. statistically significant, 3 of the 5 patients with previous radia-
tion and/or surgery that bled had severe bleeding (P = .15).
Postoperative Bleeding Details
The postoperative course in all patients revealed a 5.4% over- Bleeding Classification
all TOS resection site bleeding rate (49 of 906 patients). Opera- Minor Bleeding
tive intervention was required in 3.6% of all patients (33 of 906). Of all patients, minor bleeding occurred in 1.8% (16 of 906). The
Based on our classification system (Table 1), we found that 32.7% bleeding resolved without the need for operative intervention
of bleeding episodes were classified as minor, 34.7% as inter- whether or not a physician evaluation, emergency depart-
mediate, 12.2% as major, and 20.4% as severe. Therefore, 67% ment visit, or hospital admission occurred. In 5 of these pa-
of bleeding episodes required operative intervention. The mean tients, bleeding was managed via telephone conversation only.
postoperative day of bleeding was 10, broken down to day 11 for Reported estimated blood loss (EBL) ranged from 5 to 240 mL.
minor episodes, day 10 in intermediate episodes, day 10 in ma- Interestingly, 4 of the 16 cases documented use of an ice water
jor episodes, and day 9 in severe episodes (Table 2). gargle or placement of a cold compress neck to the anterior neck.
Tonsillar primaries were more likely to bleed (32 of 49
[65.3%]) compared with tongue base primaries (16 of 49 Intermediate Bleeding
[32.7%]) (P = .04). Male patients were more likely to require op- Intermediate bleeding occurred in 1.88% of patients (17 of 906),
erative intervention for bleeding than female patients (P = .02). with all taken to the operating room for control or evaluation.

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Transoral Surgery of the Oropharynx Original Investigation Research

Table 3. Patient Data Summary for Subgroup With Severe Bleeding


Patient
No. POD Site or Artery Duration/Amount Pretreatment Sequelae Operative Treatment Outcome
1 8 ND ND None Neck exploration with external carotid Good
ligation
Tracheostomy
2 10 Right external carotid “Brisk” None Urgent/awake tracheostomy Good
Transcervical EC ligation
3 10 Right tongue base 1 h, “Profuse” Pulse = 115 bpm Urgent/awake tracheostomy Good
Hg = 8.7 SBP = 60 s Transoral hemaclip
4 U PRBC Transcervical hemaclip to
Lingual/Facial
4 10 Right lingual “Copious” SPO2 = 40% Tracheostomy site cannulation Good
13 Right facial (aneurysm) “Large amounts” SBP = 180 s IR embolization-Lingual
Carina/right mainstem IR embolization-Facial
bronchus clot Bronchoscopy
5 12 Right tonsillar fossa 12 h, Hg decreased 2 U PRBC Urgent/awake tracheostomy Good
from 12 to 9 g/dL Transoral bipolar cautery, suture
ligature
6 6 ND ND Hypotension ND Good
2 U PRBC
7 1 Right floor of mouth ND None Urgent/awake tracheostomy Good
Transcervical external carotid ligation
8 10 Left tonsillar 2 h, “Off and on” 8 U PRBC Transoral monopolar cautery Good
fossa/Facial dopamine for hypotension
9 2 Lingual 30 min 6 U PRBC Urgent/awake tracheostomy Anoxic brain
Aspiration Transoral hemaclip injury; died
Code blue Transcervical external carotid ligation 8 mo later
10 14 Diffuse bleeding “Large amount” PEA Transoral monopolar cautery Good
“Pulsatile” epinephrine Bronchoscopy
Hg decreased from 15 Intubation
to 12 g/dL U PRBC
Abbreviations: Hg, hemoglobin; IR, interventional radiology; ND, not documented; PEA, pulseless electrical activity; POD postoperative day; PRBC, packed red
blood cells; SBP, systolic blood pressure; SPO2, blood oxygen saturation level.
SI conversion factor: To convert hemoglobin to grams per liter, multiply by 10.0.

Eleven patients had a bleeding source identified; arterial in 4 pa- 2 to 8 U. Six patients underwent an urgently performed awake
tients and diffuse venous oozing in 7. The EBL ranged from 100 tracheostomy for airway compromise, and 5 underwent neck
to 500 mL. No patients experienced another episode of bleed- exploration with ligation of either the external carotid (4 pa-
ing following intervention. The only 2 patients to develop bleed- tients) or facial and lingual arteries (1 patient). All patients ex-
ing on the day of their primary resection fell into this group. perienced a return to preoperative function and quality of life
except for 1 patient who developed an anoxic brain injury and
Major Bleeding died 8 months postoperatively (Table 3).
Major bleeding occurred in 0.66% of patients (6 of 906). Four
of the 6 patients had “arterial spasm bleeding” or “sentinel
bleeding” episodes documented up to 2 days prior to defini-
tive intervention. The EBL leading up to and including explo-
Discussion
ration ranged from 500 to 700 mL, with the bleeding vessel Transoral surgical resection for oropharyngeal OPSCC carries
identified as an arterial vessel in 4 cases, twice as many as in many advantages, including its excellent oncologic and func-
the superior laryngeal artery. Two patients underwent inter- tional outcomes in addition to decreased hospitalization length
ventional radiologic embolization, 1 as primary hemorrhage and complication rate.15-17 Unfortunately, the risk of acute life-
management, and 1 owing to an unidentifiable bleeding source threatening postoperative hemorrhage is increased in TOS com-
on direct laryngoscopy. Two patients had arterial bleeding with pared with open surgery.10 This specifically applies to the oro-
vessels that were too large for bipolar cautery; therefore, he- pharynx, where an intricate network of named vessels exists
moclips were placed transorally. Owing to negative results from with multiple branches crossing tissue planes, accompany-
a transoral examination, the remaining 2 patients underwent ing nerves, and penetrating into various muscular, fascial, and
transcervical vessel ligation utilizing their neck dissection in- mucosal layers (Figure 1 and Figure 2). Unfortunately, the tra-
cision with ligation of the lingual, facial, and superior thyroid ditional anatomic dissection approach to head and neck struc-
artery performed. tures from the outside-in is reversed, and sound knowledge
of the inside-out anatomy is needed. As the oropharyngec-
Severe Bleeding tomy resection progresses deeper into the lateral pharyngeal
Severe bleeding occurred in 1.1% of patients (10 of 906). Three tissues, large vessels are cauterized, clipped, and ligated, and
had a history of radiation therapy, 2 also undergoing previous the open wound is left to heal by secondary intention. These
surgery. Six patients received a blood transfusion, ranging from insensate tissues with altered swallow and compromised air-

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Research Original Investigation Transoral Surgery of the Oropharynx

Figure 1. Blood Supply to the Lateral Oropharynx

Superior constrictor m.
Stylohyoid process
Ascending palatine branch
Descending palatine a. of Facial a.
Ascending pharyngeal a.
Palatoglossus m. Stylohyoid m.
Styloglossus m. Digastric m.
Tonsillar branch of Facial a.
Dorsal lingual a.‘s Facial a.
Palatopharyngeus m.
Stylohyoid ligament Stylopharyngeus m.
Lingual a.
Superior thyroid a.
Superior laryngeal a.

Superior constrictor m.
Styloglossus m.
Dorsal lingual a.‘s
Hyoglossus m. Tonsillar branch
of Facial a.
Middle constrictor m.
Facial a.
Lingual a. Stylopharyngeus m.
Hyoid bone Reproduced with permission of the
Mayo Foundation for Medical
Education and Research. a.’s indicates
arteries; m., muscle.

Figure 2. Facial and Lingual Artery Course

Genioglossus m.

Sublingual gland

Lingual n.

Submandibular gland
Mylohyoid m.
Facial a.
Geniohyoid m.
Stylohyoid ligament
Hyoglossus m.
Tonsillar branch Stylohyoid m.
of Facial a. Digastric m.
Ascending palatine Stylopharyngeus m.
branch of Facial a.

Glossopharyngeal n.
Lingual a. Middle constrictor m. Reproduced with permission of the
Mayo Foundation for Medical
Dorsal lingual a.‘s Education and Research. a.’s indicates
arteries; m., muscle; n., nerve.

way protection mechanisms can persist for several weeks to doing so we address many questions: specifically, the rela-
months as healing ensues. In the event of postoperative hem- tionship between bleeding rate and severity with patient sex,
orrhage, the mechanism of morbidity or mortality is typically previous treatment, tumor size, surgical technique, external
aspiration and asphyxiation, not exsanguination (as evi- carotid system vessel ligation, and concern about staged ophar-
denced by our description of patient 9 in Table 3). This occurs yngectomy with neck dissection or ligation.
as blood rapidly obscures visualization in the pharynx, im-
peding intubation and resulting in aspiration and hypoxia. The Risk Factors for Bleeding
aspirate coagulates then accumulates in the distal broncho- Age and sex have no effect on bleeding frequency; however,
pulmonary tree and can result in prolonged anoxia, acidosis, we found that males are more likely than females to have a
cardiac arrhythmia, cerebral hypoperfusion, anoxic encepha- bleeding episode requiring operative intervention (P = .02).
lopathy, and death. This is unlikely to be related to anatomy or pathologic find-
The main outcome measures of the study were to evalu- ings but could possibly be the result of increased postopera-
ate our experience of postoropharyngectomy hemorrhage, ad- tive exertion or activity. As anticipated, the greatest bleeding
dress factors associated with increased bleeding risk, and pro- risk is present 7 to 14 days postoperatively (mean [SD], 10.1
pose methods to treat these patients with an elevated risk. In [5.9] days).

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Transoral Surgery of the Oropharynx Original Investigation Research

Previous Treatment and Bleeding was not different between patients who had undergone liga-
We did not find that previous head and neck radiation and or tion and those who had not, we observed that tumors with
surgery increased the risk of postoperative bleeding (P = .41). higher T stages were more often ligated (P = .002). This com-
We found differences in bleeding severity, with a history of pre- parison is statistically significant when comparing T1 and T3
vious treatment present in 3 of 10 severe bleeding episodes tumors (P = .005) and comparing T1 and T4 tumors (P = .001).
(30.0%) vs 2 of 39 nonsevere bleeding episodes (5.1%) (P = .05). This likely represents the surgeon’s calculated effort to mini-
Diminished or delayed wound healing, radiation-induced blood mize the bleeding risk in a more complex wound that will take
vessel or microvasculature changes, fibrosis, or anatomic varia- longer to heal.
tions resulting from previous surgery are all possible factors Simultaneous neck dissection was performed in 79.1% of
leading to an increased severity of bleeding. Although based cases; therefore, most of our patients had accessible external
on a small number of patients, this difference in bleeding se- carotid artery branches at the time of the primary surgery, fa-
verity (30.0% vs 5.1%) seen with previous treatment warrants cilitating ligation. Despite this increased rate of ligation in larger
discussion of vascularized flap coverage. tumors and the increased rate of bleeding in higher T-stage tu-
mors, we are unable to measure the precise impact of vessel
Tumor Size and Bleeding ligation in this subgroup regarding the overall bleeding rate.
Higher T-stage tumors were more likely to bleed (P = .02) and While there are theoretic concerns about regional necrosis or
trended toward having a more severe episode of bleeding vascular insults with ligation, none were noted, even in pre-
(P = .07). This comparison was statistically significant when viously radiated patients. An additional risk with large resec-
looking at both T1 vs T3 tumors (P < .005) and T1 vs T4 tu- tions performed in conjunction with neck dissection is fis-
mors (P = .001). This difference likely results from larger tu- tula formation. Fistulas occurred rarely with neck dissection
mors involving multiple named arteries, such as the ascend- technique modified to prevent their occurrence. In the rare cir-
ing pharyngeal, facial, lingual, and superior laryngeal arteries. cumstance that a communication occurred between the oro-
In large resections required for advanced T-stage tonsillar and pharynx and neck following a large resection with neck dis-
tongue base tumors, the tonsillar and ascending palatine section, it was closed with local tissue or by suture impaction.
branches of the facial artery and dorsal lingual branch of the
lingual artery are typically encountered and ligated trans- Simultaneous vs Staged Resection With Neck Dissection
orally. Owing to time and facility constraints, the practice of staging
the margin-clearing resection and neck dissection with ves-
Surgical Modality and Bleeding sel ligation is becoming more frequent.18 With a hospital’s in-
Analysis comparing different techniques showed that no sta- vestment in expensive equipment, such as surgical robotic sys-
tistical difference in bleeding rate existed when comparing TLM tems, lasers, or microscopes, comes the pressure to maximize
resections (5.9%), TORS resections (6.3%), and handheld mo- productivity. This may result in scheduling multiple resec-
nopolar electrocautery resections (4.5%) (P = .80). Compari- tions around equipment or block time availability, which does
son of bleeding severity also showed no significant differ- not allow time for additional procedures, such as a neck dis-
ences among the 3 primary resection methods (P = .54). section. Patients then return to the operating room days to
Although no increase in bleeding rate or bleeding severity was weeks later for a second anesthetic and neck dissection with
present between the difference resection techniques, tumors or without vessel ligation. We report that postoperative day 10
with higher T stages were more often resected with laser than is the mean postoperative day for oropharyngeal hemor-
robotic techniques (P < .001). The 2 specific comparisons that rhage, with 83.6% of bleeding episodes occurring within 2
were statistically significant were between T1 and T3 tumors weeks or surgery.
as well as between T2 and T3 tumors (P < .001 for both com-
parisons). Although additional variables may be present, that Additional Recommendations
higher T-stage tumors have an increased bleeding rate, and Our standard practice during oropharyngectomy is to use he-
larger tumors more often resected by TLM warrants mention. moclips on all arteries 2 mm or larger and suture ligature on
This and other potential differences between resection mo- arteries larger than 4 mm. When cautery is needed, we find
dalities prompted further study. the bipolar hemoclip superior to the monopolar hemoclip ow-
ing to its ability to seal vessel ends rather than create a charred
Vessel Ligation and Bleeding coagulum that imitates a “spot weld.” If neck dissection is per-
All vessel ligations were performed transcervically at the time formed and there is concern for increased postoperative bleed-
of the primary transoral resection. The 15.6% documented li- ing or any question of exposed arterial vessels, we perform ves-
gation rate likely underrepresents the true frequency as a re- sel ligation. The specific branches of the external carotid artery
sult of variability in operative note dictation detail. Despite this to be ligated are those directly involved in the resection bed,
deficiency, vessel ligation was not found to be associated with typically including the lingual and facial arteries in oropha-
decreased overall rate of bleeding (P = .21), but it also was not ryngeal resections. If a large resection continues inferiorly near-
found to be related to increased bleeding. Although severe ing the hyoid bone, ligation of the superior thyroid artery is
bleeding seemed to be less frequent in patients with vessel li- also performed.
gation (1 of 9 [11.1%] vs 8 of 31 [25.8%]), this difference was not We prefer to not stage the neck dissection because we feel
statistically significant (P = .66). While the overall bleeding rate it allows for concurrent vessel ligation, is more efficient, and

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Research Original Investigation Transoral Surgery of the Oropharynx

is cost-effective. Although not assessed in this study, in our ex- In conclusion, transoral resection of oropharyngeal carci-
perience, detailed appreciation of the inside-out anatomy is noma is safe and effective with a predictable rate of postop-
critical to performing safe TOS. Although rarely performed, erative hemorrhage. Severe life-threatening hemorrhage is very
planned tracheostomy is utilized in selected patients, often rare. Bleeding rates were equivalent between TLM- and TORS-
those undergoing concomitant TOS and bilateral neck dissec- treated patients. Although transcervical vessel ligation did not
tion with a history of radiation therapy or previous surgery. result in an overall decrease in bleeding rate, we feel it is a safe
Known study limitations include its retrospective na- technique to use in selected cases. For higher T-stage tumors,
ture, as well as lack of additional risk factor assessment, such primary tonsil tumors, or previously treated patients, simul-
as antiplatelet or anticoagulation therapy discontinuation, hu- taneous multivessel ligation may reduce the severity of a se-
man papillomavirus status, or smoking history. vere episode of bleeding.

ARTICLE INFORMATION 4. Gillison ML. Current topics in the epidemiology 15. Moore EJ, Olsen KD, Kasperbauer JL. Transoral
Submitted for Publication: February 27, 2013; final of oral cavity and oropharyngeal cancers. Head robotic surgery for oropharyngeal squamous cell
revision received July 30, 2013; accepted August Neck. 2007;29(8):779-792. carcinoma: a prospective study of feasibility and
23, 2013. 5. Chandarana SP, Lee JS, Chanowski EJ, et al. functional outcomes. Laryngoscope.
Prevalence and predictive role of p16 and epidermal 2009;119(11):2156-2164.
Published Online: October 10, 2013.
doi:10.1001/jamaoto.2013.5097. growth factor receptor in surgically treated 16. Grant DG, Salassa JR, Hinni ML, Pearson BW,
oropharyngeal and oral cavity cancer. Head Neck. Perry WC. Carcinoma of the tongue base treated by
Author Contributions: Drs Pollei and Hinni had full 2013;35(8):1083-1090. transoral laser microsurgery, part one: untreated
access to all of the data in the study and take tumors, a prospective analysis of oncologic and
responsibility for the integrity of the data and the 6. Steiner W, Ambrosch P. Endoscopic Laser
Surgery of the Upper Aerodigestive Tract: With functional outcomes. Laryngoscope.
accuracy of the data analysis. 2006;116(12):2150-2155.
Study concept and design: Pollei, Hinni, Moore, Special Emphasis on Cancer Surgery. New York, NY:
Hayden, Olsen. Thieme; 2000:112-113. 17. Canis M, Ihler F, Wolff HA, Christiansen H,
Acquisition of data: Pollei, Hinni, Hayden, Casler, 7. Ellies M, Steiner W. Peri- and postoperative Matthias C, Steiner W. Oncologic and functional
Walter. complications after laser surgery of tumors of the results after transoral laser microsurgery of tongue
Analysis and interpretation of data: Pollei, Hinni, upper aerodigestive tract. Am J Otolaryngol. base carcinoma. Eur Arch Otorhinolaryngol.
Olsen. 2007;28(3):168-172. 2012;270(3):1075-1083.
Drafting of the manuscript: Pollei, Hinni, Moore. 8. Kutter J, Lang F, Monnier P, Pasche P. Transoral 18. Moore EJ, Henstrom DK, Olsen KD,
Critical revision of the manuscript for important laser surgery for pharyngeal and pharyngolaryngeal Kasperbauer JL, McGree ME. Transoral resection of
intellectual content: All authors. carcinomas. Arch Otolaryngol Head Neck Surg. tonsillar squamous cell carcinoma. Laryngoscope.
Statistical analysis: Pollei, Hinni, Moore, Walter. 2007;133(2):139-144. 2009;119(3):508-515.
Administrative, technical, or material support: 19. Eckel HE, Volling P, Pototschnig C, Zorowka P,
Moore, Hayden, Olsen, Casler. 9. Grant DG, Salassa JR, Hinni ML, Pearson BW,
Hayden RE, Perry WC. Transoral laser microsurgery Thumfart W. Transoral laser resection with staged
Study supervision: Moore. discontinuous neck dissection for oral cavity and
for recurrent laryngeal and pharyngeal cancer.
Conflict of Interest Disclosures: None reported. Otolaryngol Head Neck Surg. 2008;138(5):606-613. oropharynx squamous cell carcinoma.
Previous Presentation: This study was presented Laryngoscope. 1995;105(1):53-60.
10. Salassa JR, Hinni ML, Grant DG, Hayden RE.
at the American Head and Neck Society 2013 Postoperative bleeding in transoral laser 20. Kremer B, Schlöndorff G. Late lethal secondary
Annual Meeting; April 10, 2013; Orlando, Florida. microsurgery for upper aerodigestive tract tumors. hemorrhage after laser supraglottic laryngectomy.
Additional Contributions: Yu-Hui Chang, PhD, Otolaryngol Head Neck Surg. 2008;139(3):453-459. Arch Otolaryngol Head Neck Surg.
Department of Research Biostatistics, Mayo Clinic 2001;127(2):203-205.
11. Rigby MH, Taylor SM. Review of transoral laser
Arizona, Phoenix, provided assistance with microsurgery for cancer of the upper aerodigestive 21. Vilaseca-González I, Bernal-Sprekelsen M,
statistical analysis. tract. J Otolaryngol Head Neck Surg. Blanch-Alejandro JL, Moragas-Lluis M.
2011;40(2):113-121. Complications in transoral CO2 laser surgery for
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