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Original Research
The incidence of vocal fold motion impairment after primary thyroid and T
parathyroid surgery for a single high-volume academic surgeon determined
by pre- and immediate post-operative fiberoptic laryngoscopy
Vaninder K. Dhillona, Eleni Rettiga, Salem I. Noureldinea, Dane J. Genthera, Ahmed Hassoonb,
Mai G. Al Khadema, Ozan B. Ozgursoya, Ralph P. Tufanoa,∗
a
Division of Head and Neck Endocrine Surgery, Department of Otolaryngology - Head and Neck Surgery, Johns Hopkins University School of Medicine, Baltimore, MD,
USA
b
Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA
A R T I C LE I N FO A B S T R A C T
Keywords: Background: Vocal fold motion impairment (VFMI) is a well-recognized complication of thyroid and parathyroid
Recurrent laryngeal nerve surgery. Preoperative counseling requires a thorough understanding of the incidence, risk factors, and value of
Thyroidectomy early diagnosis of postoperative VFMI. Our objective is to describe the incidence of and risk factors for VFMI for
Parathyroidectomy a single high-volume academic surgeon, and to assess the utility of immediate postoperative fiberoptic lar-
Vocal fold paralysis
yngoscopy (FOL) in early diagnosis of VFMI.
Palsy
Paresis
Methods: Retrospective cohort study of patients undergoing primary thyroid and parathyroid procedures by a
Hoarseness single high-volume surgeon at an academic tertiary care center. All patients underwent preoperative and im-
Complications mediate postoperative FOL. The primary outcome was incidence of VFMI, either temporary (< 1 year) or per-
Laryngoscopy manent (1 year or more). The unit of analysis was number of recurrent laryngeal nerves (RLN) at risk. Risk
factors for VFMI were analyzed using logistic regression, reporting unadjusted and adjusted odds ratios (OR and
aOR) and 95% confidence intervals (CI).
Results: The study population comprised 1547 patients undergoing 1580 procedures for a total of 2527 nerves at
risk, excluding the 27 nerves found to have motion impairment on preoperative FOL. Sixty-seven new incidents
of VFMI were identified on postoperative FOL, with an additional six new incidents detected after voice com-
plaints prompted FOL upon follow-up. Thus, the incidence of postoperative VFMI was 2.9% of RLNs at risk (73 of
2527). The sensitivity and negative predictive value of immediate postoperative FOL were 92% and 99.8%
respectively. Permanent VFMI occurred in 9 cases (0.4%), 3 of which were from intentional RLN transection for
malignancy. Odds of VFMI were significantly lower after parathyroidectomy (aOR = 0.1, 95%CI = 0.01–0.8
compared with hemithryoidectomy) and higher with central neck dissection (aOR = 2.4, 95CI = 1.0–5.9).
Among cases of malignancy, odds of VFMI increased significantly with increasing T-stage (adjusted
ptrend < 0.001).
Conclusion: VFMI is rare and usually temporary after primary thyroid and parathyroid procedures, with in-
creased risk associated with larger primary malignancies and the inclusion of central neck dissection. Immediate
postoperative FOL is useful for early detection of VFMI that may allow for clear definition of temporary and
permanent immobility rehabilitation especially if there is evidence to support early intervention.
∗
Corresponding author. Head and Neck Endocrine Surgery, Department of Otolaryngology-Head and Neck Surgery, The Johns Hopkins School of Medicine, Johns Hopkins Outpatient
Center, 601 N. Caroline Street, 6th floor, Baltimore, MD, 21287, USA.
E-mail address: rtufano1@jhmi.edu (R.P. Tufano).
https://doi.org/10.1016/j.ijsu.2018.06.014
Received 25 February 2018; Received in revised form 16 April 2018; Accepted 12 June 2018
Available online 14 June 2018
1743-9191/ © 2018 IJS Publishing Group Ltd. Published by Elsevier Ltd. All rights reserved.
V.K. Dhillon et al. International Journal of Surgery 56 (2018) 73–78
The reported incidence of VFMI varies significantly, which may be due performed at follow-up clinic visits for any patients with new voice
to variation in the methodologies used to diagnose RLN injury (e.g., complaints despite normal immediate postoperative FOL. Patients with
voice alone, indirect laryngoscopy, videostroboscopy, fiberoptic lar- VFMI and voice changes were offered functional voice therapy with a
yngoscopy [FOL], and more recently transcutaneous ultrasound), with speech pathologist to improve laryngeal function, and referred to a
each method having significantly different sensitivities and specificities laryngologist as indicated. Permanent VFMI was defined as absence of
[1]. Laryngoscopy for evaluation of vocal fold motion is the gold complete recovery of vocal fold mobility at one year after surgery or at
standard for assessment of VFMI [13], however few studies have in- the last follow-up visit for patients with less than one year of follow-up
corporated visualization of the vocal folds as part of routine post- time. Transient VFMI was defined as postoperative VFMI with recovery
operative assessment [8,10]. Notably, using voice quality alone has of spontaneous motion before one year or last follow-up visit for pa-
been shown to underestimate the true incidence of VFMI after thyroid tients with less than one year of follow-up time.
and parathyroid surgery, as unilateral VFMI can occur without voice
changes [11] (see Table 4). 2.4. Statistical analysis
The purposes of this study were to describe the incidence of VFMI
for a high volume surgeon in an academic teaching hospital after pri- Descriptive statistics were reported as N (%), mean (average) and
mary thyroidectomy and parathyroidectomy incorporating pre-opera- standard deviation (SD) and/or range and median. The primary out-
tive and immediate postoperative FOL, and to assess patient- and dis- come was VFMI, and the unit of analysis was number of RLNs at risk;
ease-related risk factors for VFMI. vocal folds that were found to be impaired preoperatively were con-
sidered not at risk and excluded from analysis. The sensitivity and ne-
2. Methods gative predictive value (NPV) of immediate post-extubation FOL ex-
amination were calculated. Characteristics associated with VFMI were
2.1. Data source and patient population compared using unadjusted and adjusted logistic regression analysis,
and unadjusted and adjusted odds ratios (OR and aOR) with 95%
We collected data from medical records of all consecutive patients confidence intervals (CI) were reported. Adjusted analyses were per-
who underwent primary thyroid procedures (with or without central formed separately for all RLNs at risk, and RLNs at risk in malignancy
neck dissection) or primary parathyroid procedures between March cases only. All reported p-values are two sided, and p < 0.05 was
2004 and December 2015. All procedures were performed by a single considered statistically significant. Data analysis was performed using
surgeon (R.P.T.) who had been performing high volume [16] thyroid Stata 14 (College Station, TX).
and parathyroid surgery independently, at a university-based tertiary The work has been reported in line with the STROCSS criteria [28].
care center, for more than 3 years prior to the data collection starting
point. We identified all patients who underwent primary para- 3. Results
thyroidectomy, hemithyroidectomy, total thyroidectomy, completion
thyroidectomy, substernal thyroidectomy with or without sternal split, 3.1. Patient population
and total or completion thyroidectomy with central neck dissection, in
which one or both RLNs were surgery-naïve and at risk of injury. A total of 1547 patients underwent 1580 primary surgical proce-
Completion thyroidectomy was considered a primary procedure and dures during the eleven-year study period, 308 (19%) of which were
included in this analysis if no prior dissection had been performed on parathyroidectomy procedures and 1272 (81%) of which were thyr-
the side in question, as the RLN would therefore be anatomically intact oidectomy procedures. Table 1 summarizes the characteristics of the
and undisturbed. Patients with confounding laryngotracheal invasion of patient population, thyroid diagnoses and procedures performed. The
thyroid cancer and those undergoing reoperative thyroid surgery with a mean patient age was 51 years (range, 6–90). The majority (81%) of
previously dissected RLN were excluded from the study. This retro- patients were younger than 65 years of age and predominantly (75%)
spective study was approved by the Institutional Review Board of XXX female. Most procedures were performed for either benign thyroid
Medicine, and informed consent was waived in accordance with the nodular disease (N = 581, 37%) or thyroid malignancy (N = 611,
Health Insurance Portability and Accountability Act. 39%), with relatively fewer cases of parathyroid adenomas (N = 310,
20%) and Graves' disease (N = 78, 5%). The most common procedure
2.2. Surgical technique was total thyroidectomy (N = 613, 39%). The overall average follow-
up duration was 7 weeks (range 0–122; median 3). Patients with VFMI
In all thyroidectomy cases, the RLNs at risk were identified using were followed for a longer period of time postoperatively, with an
direct visualization and dissected intraoperatively to the extent the average of 16 weeks (range 1–208; median 7.5).
surgeon felt it was necessary to allow for attempted preservation.
Intraoperative nerve monitoring of the RLNs was performed routinely 3.2. Pre- and immediate post-operative vocal fold motion impairment
using either the NIM 2.0 or the 3.0 intermittent nerve monitoring
system (Medtronic, Minneapolis, MN). Preoperatively, FOL examination was performed on all but two
patients. Twenty-seven (2%) vocal folds were found to be impaired on
2.3. Assessment of vocal folds preoperative assessment in 27 patients, with 15 involving the left vocal
fold and 12 involving the right. Eleven (41%) of these patients were
Vocal fold function was assessed by the operating surgeon (R.P.T.) preoperatively asymptomatic and noted no problems with their voice.
using FOL at the preoperative visit and immediately following ex- These 27 nerves were considered not at risk due to pre-existing im-
tubation in the operating room at the conclusion of the surgical pro- pairment, and excluded from further analysis. Of the 2527 RLNs at risk
cedure. The primary surgeon used a flexible nasolaryngoscope with an of injury, 2476 (98%) were visualized and dissected during the surgical
associated halogen light source over the time period by which this study procedures. Fifty-six RLNs were not visualized during resection of
was analyzed. The postoperative laryngeal examination included at a parathyroid adenomas via focused surgery, but nonetheless were at risk
minimum the analysis of the symmetry of arytenoid and true vocal fold for injury.
motion during respiration and active abduction and adduction, with Overall, at the conclusion of surgery, all but 7 (0.3%) RLNs were
phonation or cough when possible. VFMI was defined as a new motion visually intact. Four (0.2%) RLNs were unintentionally transected
impairment of a vocal fold or no discernible motion after surgery, as (Table 2). Three of these were anterior branches injured during dis-
compared to the preoperative examination. Repeat FOL was also section at Berry's ligament and noted to be adherent the respective
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V.K. Dhillon et al. International Journal of Surgery 56 (2018) 73–78
Table 1
N (%)
Total 1580
Age, mean (SD) 51.3 (14.5)
Age, categorical (years)
< 35 219 (14)
35-44 283 (18)
Motion impairment
Motion impairment
Motion impairment
Motion impairment
45-54 404 (26)
55-64 379 (24)
65+ 295 (19)
Sex
Immobile
Immobile
Immobile
Immobile
Immobile
Female 1183 (75)
Male 397 (25)
Race
White 1126 (71)
208
2 91 (15)
36
52
20
48
24
27
15
4
3 77 (13)
4 10 (2)
Intraoperative state of RLN at risk
Procedurea
Hemithyroidectomy 247 (16)
Total thyroidectomy 613 (39)
Intentional transection
Intentional transection
Intentional transection
Completion thyroidectomy 88 (6)
Iatrogenic transection
Iatrogenic transection
Iatrogenic transection
Iatrogenic transection
Substernal thyroidectomy, cervical approach 158 (10)
Substernal thyroidectomy, thoracic approach 8 (0.5)
Total thyroidectomy or completion thyroidectomy with 158 (10)
Intact RLN
Intact RLN
unilateral or bilateral central neck dissection
Parathyroidectomy 308 (19)
Characteristics of the ten patients with pre-op mobile vocal folds but permanent vocal fold immobility.
Year of surgery
2004–2005 40 (3)
2006–2007 97 (6)
Right
Right
Right
Right
Right
Right
Side
Left
Left
Left
Thyroid malignancy
Thyroid malignancy
Thyroid malignancy
Thyroid malignancy
Thyroid malignancy
Hemithyroidectomy (2013)
11
32
64
30
57
62
59
52
43
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V.K. Dhillon et al. International Journal of Surgery 56 (2018) 73–78
Table 3 Table 4
Characteristics associated with odds of postoperative VFMI for nerves at risk. Adjusted analysis of characteristics associated with odds of postoperative VFMI
for at-risk recurrent laryngeal nerves.
Characteristic Total Number of Odds of VFP p-value
nerves vocal folds Characteristic Adjusted odds of p-value
at riska with postoperative vocal cord
paresis immobility
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V.K. Dhillon et al. International Journal of Surgery 56 (2018) 73–78
contrast, odds of VFMI were significantly increased by the performance post-operative VFMI for any of the patients within this study. We
of central neck dissection (OR = 2.8, 95%CI = 1.7–4.8, p < 0.001 therefore we do no attribute any change to our results in particular from
compared with no central neck dissection) and, among patients with changes or abnormalities from the use of IONM. In an analysis of six
malignancies, higher T-stage (ptrend < 0.001). VFMI was not sig- studies with more than 100 nerves at risk, Dralle et al. demonstrated
nificantly associated with sex, race, thyroid pathology, or calendar that the rate of permanent recurrent laryngeal nerve palsy varied from
period in which the surgery was performed. 0% to 11% [18]. The study group showed that IONM can lower the rate
The only factors that remained significantly associated with VFMI of vocal fold paralysis, but it was not statistically significant as com-
upon adjusted analysis were the type of surgery, with lower risk from pared to RLN visualization alone [18]. IONM cannot substitute for vi-
parathyroidectomy (OR = 0.1, 95%CI = 0.01–0.8, p = 0.04) and sual identification and vigilant dissection of the RLN in thyroid surgery.
higher risk from inclusion of central neck dissection (OR = 2.4, Our data support the use of preoperative laryngoscopy to assess pre-
95%CI = 1.0–5.9, p = 0.05), and among malignancies, tumor stage existing VFMI in order to allow for accurate identification of iatrogenic
(OR 7.5, 95%CI = 1.2–48.3 for T4 versus T1; ptrend < 0.001 for higher complications, in agreement with previously published studies [12,13].
OR with increasing T stage). In this cohort, twenty-seven patients with preoperative VFMI were
identified, some of whom otherwise might have been erroneously
4. Discussion considered iatrogenic VFMI if only detected post-operatively, which
would have skewed our risk estimates considerably. It is important to
The overall risk of VFMI after thyroid or parathyroid surgery is low, note that the primary surgeon performed flexible laryngoscopy without
but is not insignificant even in experienced hands. Our data suggest that any significant technical or instrument adjustments over the time
VFMI risk is highest for patients undergoing central neck dissection or course of the study.
who have large tumors, while it is nearly zero for patients undergoing There is no current consensus on the optimal timing of post-
parathyroid surgery. These findings should inform patient counseling. operative FOL to assess iatrogenic VFMI [8]. We have incorporated
We also report that immediate postoperative FOL may be useful for immediate postoperative FOL into our practice and believe it is ad-
early identification of most VFMIs, allowing for improved commu- vantageous for several reasons. Most importantly, early FOL allows for
nication with patients and early voice and swallow rehabilitation. early patient counseling in order to set expectations and plan for in-
In our study, the incidence of postoperative VFMI was 2.9% of terventions that may improve voice and swallowing outcomes. Early
nerves at risk, which is consistent with the low rates reported in com- intervention by a Speech-Language Pathologist has been shown to im-
parison studies [10,13–15]. Preoperative discussions with patients prove patient satisfaction on subjective outcome measures [22,23], and
should include a discussion of this non-negligible risk and its implica- it is well established in laryngology literature that intervention in the
tions for speech and swallowing, and the potential need for re- form of early vocal fold augmentation is beneficial for select patients
habilitation. Importantly, there is evidence for an inverse association of with unilateral VFMI in improving voice related quality of life [24,25].
post-thyroidectomy complication rates with surgeon volume [16,17]. In addition, thyroid and parathyroid surgeries are becoming same day
We therefore recommend that thyroid and parathyroid surgeons should surgeries [26,27], with patients being discharged postoperatively and
endeavor to assess their own true rate of VFMI in order to appropriately seen weeks later in follow up. In such cases, VFMI may be missed in the
counsel patients. Interestingly, our data did not show a learning curve absence of early FOL and patient concerns not addressed, even if
as the rate of VFMI did not significantly change over the study period. normal function may be restored by the time of outpatient follow-up
This may be attributable to the fact that the senior author (R.P.T) was 1–2 weeks postoperatively [8]. Immediate postoperative FOL provides
performing a relatively high volume of thyroid surgery for several years timely feedback regarding surgical technique that is useful for the
prior to the study period, so any learning curve may not have been surgeon in identifying surgical nuances that affect RLN function. Fi-
captured in these data. nally, despite the challenges of FOL in a patient just awakened from
The primary determinants of postoperative VFMI in our study were general anesthesia, including airway secretions, laryngeal edema, and
type of surgery and, for malignancies, tumor size. The high risk for RLN variability in patient cooperativeness, the sensitivity and negative
injury in thyroidectomy with central neck dissection is related to the predictive value of immediate postoperative FOL were quite high at
dissection of the lymph node packet along the course of the entire RLN 92% and 99.8%, respectively, in our hands. This is consistent with other
in the neck. Considerable nerve manipulation may be required in order reports [8,9,20].
to achieve a comprehensive dissection [18]. The increased risk of VFMI Although this study represented a sizable patient cohort, its gen-
with larger tumor sizes is consistent with other studies, and may also eralizability is limited because it is retrospective and describes a single
suggest a higher rate of nerve manipulation [6,19–21]. Furthermore, six surgeon's experience. The retrospective nature of this study has its
out of nine permanent RLN paralyses were on the right side compared limitations, including incomplete patient information and loss of follow
to left, and while non-significant, can be inferred that there is a higher up for patients beyond sixteen weeks. Furthermore, only patients with
likelihood of neurophysiologic injury along a longer coursing right RLN symptoms had subsequent follow up FOL after the immediate post-
during dissection. The low risk of VFMI with parathyroidectomy sup- operative FOL on extubation. We recognize that only those with
ports the practice of not always identifying and dissecting out the RLN symptoms had repeated FOL and the incidence of VFMI post-opera-
during parathyroid surgery [3,7]. tively may be under-represented. Clinically, we only perform FOL those
While we universally utilize IONM for all thyroid and parathyroid with symptoms, but for a future prospective study FOL should be done
cases within our group, we acknowledge that four RLNs were unin- for all patients including those without symptoms. A prospective study
tentionally transected despite the use of nerve monitoring. All of these would standardize a pre-operative FOL as well as a post-operative FOL
dissections were performed by the primary surgeon (R.P.T.) with the and serial follow up for all patients regardless of symptomatology, ac-
assistance of a fellow or senior resident trainee; it is important to note curately predicting the NPV and PPV of FOL for thyroid surgery. A
that iatrogenic injury in the form of transection with permanent vocal prospective study would also eliminate the incidence of patients lost to
fold paralysis, though rare, can still occur despite extensive surgical follow up. We acknowledge that the assessment of VFMI by the oper-
experience and best efforts to prevent it with standardized operative ating surgeon introduces a possibility of unconscious bias to these re-
technique and IONM. IONM is a universal component to all thyroid and sults. The time-period by which the data was reviewed also may accrue
parathyroid cases that have spanned the lifetime of the primary sur- some heterogeneity for the gaps in data. Our study aim is to exemplify
geon's (R.P.T.) practice. While we do not establish the details of our set how FOL in a pre-operative and immediate post-operative setting, can
up and standard protocol for using the IONM, it is important to note play a critical role in identifying the true incidence of VFMI in patients,
that we had no correlative data between an observed signal loss and and that incidence may actually be higher than we currently recognize.
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V.K. Dhillon et al. International Journal of Surgery 56 (2018) 73–78
78