- Email: [email protected]
Comparison of ultrasound frequency in laryngeal ultrasound for vocal cord evaluation
ARTICLE IN PRESS
Comparison of ultrasound frequency in laryngeal ultrasound for vocal cord evaluation Jung-Woo Woo, MD,a,b Inhye Park, MD,a Jun Ho Choe, MD, PhD,a Jung-Han Kim, MD, PhD,a and Jee Soo Kim, MD, PhD,a Seoul and Changwon, South Korea
Background. Laryngeal ultrasound is a new method of vocal cord evaluation in patients at risk for vocal cord palsy. However, the previously described laryngeal ultrasound reportedly has a high failure rate of vocal cord visualization in male patients. We compared 2 ultrasound frequencies in laryngeal ultrasound to improve on the limitations of this method. Method. A total of 301 (55 male, 246 female) consecutive laryngeal ultrasound and direct laryngoscopy exams were performed for patients with thyroidectomy and other neck operations. High-frequency transducer (12–5 MHz broad band spectrum) and low-frequency transducer (9–3 MHz broad band spectrum) were used for all laryngeal ultrasound. Findings were independently cross-validated with direct laryngoscopy. Results. High-frequency and low-frequency laryngeal ultrasound had 88.4% and 97.7% visualization rates, respectively. In addition, low-frequency laryngeal ultrasound showed improved sensitivity of 97.6% and specificity of 96.5%, compared with a sensitivity of 92.9% and specificity of 86.5% for high-frequency laryngeal ultrasound in vocal cord evaluation. Conclusion. The low-frequency laryngeal ultrasound method significantly enhances the visualization of vocal cords, especially in patients who have diffuse thyroid cartilage calcification interrupting laryngeal ultrasound, and therefore enhances the overall efficacy of laryngeal ultrasound as a perioperative diagnostic tool for vocal cord palsy. Hence, we recommend using a low-frequency transducer (about 9–3 MHz) for laryngeal ultrasound if it is available. (Surgery 2016;j:j-j.) From the Department of Surgery,a Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, South Korea; and Department of Surgery,b Gyeongsang National University Changwon Hospital and Gyeongsang National University School of Medicine, Changwon, South Korea
VOCAL CORD PALSY (VCP) is an important complication of thyroid and parathyroid operation that affects patient quality of life.1 Direct laryngoscopy is the gold standard for vocal cord assessment.2 Although laryngoscopy is safe, it is an invasive procedure and can cause patient discomfort and fear.3 Laryngeal ultrasound (LUS) is a noninvasive method of vocal cord (VC) evaluation in patients at risk for VCP.4,5 However, the previously described LUS reportedly has a high failure rate when visualizing VC in male patients.6 In male
patients, the thyroid cartilage has a tendency to be sharp in angle and show diffuse calcification. The sharp angle of the thyroid cartilage does not allow close contact of the ultrasound (US) transducer with the skin, and this prevents simultaneous evaluation of both VCs. Diffuse calcification of the thyroid cartilage blocks penetration of US through the thyroid cartilage. We compared 2 US frequencies (12–5 MHz and 9–3 MHz broad band spectrum) in LUS. The aim of this study was to determine the optimal LUS frequency for VC evaluation.
Presented as a poster at the 67th Congress of the Korean Surgical Society in Seoul, Korea, November 5–7, 2015.
METHODS Patients. A total of 301 (55 male, 246 female) consecutive LUS, and direct laryngoscopy (DL) examinations were performed in patients who underwent thyroidectomy and other neck operations pre- and postoperatively. A high-frequency (HF) transducer (12–5 MHz broad band spectrum) and low frequency (LF) transducer (9–3 MHz broad band spectrum) were used in all
Accepted for publication October 12, 2016. Reprint requests: Jun Ho Choe, MD, PhD, Department of Surgery, Samsung Medical Center, Sungkyunkwan, University School of Medicine, 81 Irwon-ro, Gangnam-gu, Seoul 135-710, South Korea. E-mail: [email protected]. 0039-6060/$ - see front matter Ó 2016 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.surg.2016.10.013
SURGERY 1
ARTICLE IN PRESS 2 Woo et al
Surgery j 2016
Fig. (A) LUS. (B) HF transducer (right, 12–5 MHz broad band spectrum) and LF transducer (left, 9–3 MHz broad band spectrum) were used for all LUS in this study. (C) HF and (D) LF LUS for the same patient. HS LUS shows only FC, while LF LUS shows all 3 landmarks; FC, TC, and AR.
patients (Fig). LUS and DL were performed in each patient on the same day by different, blinded assessors who did not have any information about the results of the other method. The Philips HD 15 ultrasound system (Philips Ultrasound Inc, Reedsville, PA) was used for LUS. DLs were performed with the Karl-Storz Endoskope full HD system with an 8700H rigid scope (Tuttlingen, Germany). Findings from LUS were independently cross-validated with results from DL. VC evaluations were performed on the day before and after operation. Patients with VCP were followed up continuously at the outpatient department until recovery. Methods. LUS techniques have been described in previous studies.4,5 During the LUS assessment, the patient was positioned flat on the bed with the neck slightly extended. After applying ample gel over the anterior neck, an US transducer was placed transversely over the middle portion of the thyroid cartilage and the area was scanned until both true and false vocal cords were visualized. The 3 laryngeal landmarks-arytenoids (ARs), true cords (TCs), and false cords (FCs) were used for VC evaluation (Fig). Patients were instructed to perform all 3 maneuvers (breathing, phonation,
and Valsalva).7 The movement of the vocal cords was assessed during the evaluation. The extent of movement of the VC was graded according to the following scale: grade I, full or normal symmetric movement; grade II, impaired or decreased movement; and grade III, no movement. Before or after the LUS, the patient was directed to the other center where DL was performed by an experienced surgeon who was unaware of the patient’s LUS findings. Using a grading system similar to the LUS, the extent of VC movement on DL was graded from I to III. Grade II or III on DL was defined as having VCP. Patients with VCP were followed up at the outpatient department continuously until recovery from VCP. Student t test in SPSS Statistics 22 (IBM, Chicago, IL) was used to compare the VC visualization rate of each evaluation method. RESULTS A total of 301 consecutive VC examinations were evaluated. Table I shows the demographics, indications, extent of the operation, and the various operative approaches including 140 conventional open cervical thyroidectomies (86.4%), 11 robotic (6.8%), and 11 endoscopic (6.8%)
ARTICLE IN PRESS Woo et al 3
Surgery Volume j, Number j
Table I. Patient characteristics (n = 301), indications, extent of the operation, operative approaches, and vocal cord findings Characteristics Median age, y (range) Male Female Sex, n (%) Male Female Preoperative patients, n (%) Postoperative patients, n (%) Indication of operation, n (%) Suspicious malignancy Thyrotoxicosis Benign goiter Others Type of operation, n (%) Total thyroidectomy Hemithyroidectomy Subtotal thyroidectomy Parathyroidectomy Neck dissection Approach of operation, n (%) Conventional BABA robotic BABA endoscopic Calcification of thyroid cartilage, n (%) Focal calcification Diffuse calcification Laryngoscopic VC findings, n (%) Grade I Grade II Grade III Unassessable HF LUS VC findings, n (%) Grade I Grade II Grade III Unassessable LF LUS VC findings, n (%) Grade I Grade II Grade III Unassessable
Table II. HF LUS and DL correlation HF LUS Normal
Value 48 (13–81) 49 (28–67) 47 (13–81) 55 246 139 162
(18.3) (82.7) (46.2) (53.8)
273 3 17 8
(90.7) (1.0) (5.6) (2.7)
79 72 3 3 5
(48.8) (44.4) (1.9) (1.9) (3.1)
DL
(86.4) (6.8) (6.8) (30.6) (12.3) (18.3)
259 (86.0) 19 (6.3) 23 (7.6) 0 225 19 22 35
(74.8) (6.3) (7.3) (11.6)
251 20 23 7
(83.4) (6.6) (7.6) (2.3)
BABA, Bilateral axillo-breast approach; Grade I, normal mobility; Grade II, diminished mobility; Grade III, no mobility.
bilateral axillo-breast approach thyroidectomies. Suspicion of thyroid cancer was the most common indication (90.7%) for operation. There were 3 cases of parathyroidectomy and 5 cases of neck dissection. The median age at operation was 48 years. The 301 VC examinations revealed that 42 (14.0%; 5 male, 37 female) patients had VCP on
Not Grade I Grade II Grade III assessable Total
Normal 224 2 Grade I VC palsy Grade II 1 17 Grade III 0 0 Total 225 19 Accessibility 88.4% (266/301) Sensitivity 92.9% (39/42) Specificity 86.5% (224/259)
0
33
259
0 22 23
1 1 35
19 23 301
Grade I, Normal mobility; Grade II, diminished mobility; Grade III, no mobility.
Table III. LF LUS and DL correlation LF LUS Normal
DL 140 11 11 92 37 55
VC palsy
VC palsy
Not Grade I Grade II Grade III assessable Total
Normal 250 2 Grade I VC palsy Grade II 1 18 Grade III 0 0 Total 251 20 Accessibility 97.7% (294/301) Sensitivity 97.6% (41/42) Specificity 96.5% (250/259)
0
7
259
0 23 23
0 0 7
19 23 301
Grade I, Normal mobility; Grade II, diminished mobility; Grade III, no mobility.
DL, and 55 patients had diffuse thyroid cartilage calcification interrupting LUS. On HF LUS, 19 patients had grade II findings and 22 patients had grade III findings; meanwhile, on LF LUS, 20 patients had grade II findings and 23 patients had grade III findings (Table I). All VCP cases were unilateral. HF and LF LUS showed 88.4% and 97.7% visualization rate, 92.9% and 97.6% sensitivity, and 86.5% and 96.5% specificity, respectively (Tables II and III). There were 2 false positive cases and 1 false negative case in both HF and LF LUS. Table IV presents the visualization rates of VC landmarks by HF and LF LUS. Visualization rates of laryngeal landmarks by HF LUS compared with LF LUS were 88.0% (265) vs 97.3% (293) for FC, 50.5% (152) vs 78.7% (237) for TC, and 50.2% (151) vs 89.7% (270) for AR, respectively. FC was the most visible landmark by both HF
ARTICLE IN PRESS 4 Woo et al
Surgery j 2016
Table IV. Visualization rates of vocal cord landmarks in 301 LUS Frequency of LUS HF (%) LF (%) P value
FC
TC
AR
Overall
265 (88.0) 152 (50.5) 151 (50.2) 266 (88.4) 293 (97.3) 237 (78.7) 270 (89.7) 294 (97.7) <.001 <.001 <.001 <.001
and LF LUS. AR and TC were the least visible landmark by HF and LF LUS, respectively. LF LUS showed significantly greater visualization rates of all 3 VC landmarks than HF LUS (P < .001). DISCUSSION VCP has the maximum medicolegal and cost implications in thyroid and parathyroid operation.8 Therefore, the new 2015 American Thyroid Association Guidelines placed an emphasis on perioperative VC evaluation even in cases involving loss of voice.1 Nevertheless, controversies about routine VC evaluation are ongoing. DL, which is the gold standard for VC evaluation, frequently causes unnecessary discomfort and gag reflex in patients, especially in the immediate postoperative period. Since the introduction of LUS in 1992,9 LUS has improved with advancements in US technology. Wong et al4,5 compared the accuracy of LUS and DL in order to investigate the potential of using LUS as a VC evaluation tool. LUS can be performed pre- and postoperatively simultaneously during thyroid US; hence, it has its own unique benefit of reducing the additional medical cost and avoiding patient discomfort caused by DL.10,11 In the early period, LUS was limited to female patients because LUS was not appropriate for VCs in male patients due to the prominent protrusion and frequent diffuse calcification of thyroid cartilage, blocking US penetration.6 Although in a previous study, a novel attempt was made to improve VC visualization with LUS in male patients using a lateral approach, this method also had its own limitation of nonsynchronous 2-step evaluation of both VCs.11 LF LUS can evaluate VCs in male patients by a 1-step procedure using LF to improve US penetration. In our study, 47 patients were men among 55 patients with diffuse calcification on thyroid cartilage. Most calcifications in thyroid cartilage were thin and light calcifications, not thick and bony calcifications. Therefore, they were penetrated easily by LF LUS. The LF US transducer originally was manufactured for deep
vascular evaluations such as visualization of the carotid artery. We applied the LF US transducer to LUS for the first time to improve VC visualization. The sonographic view with LF LUS showed more VC landmarks compared with HF LUS but sacrificed the high definition of HF LUS at the same time. LUS is a motion-based diagnostic tool; therefore, visualization of the VC landmarks is more important than high definition. Previous studies used various frequencies in the range of 3–12 MHz. However, there was no research about optimal frequency for LUS4,5; the purpose of our research is to discover the optimal frequency for LUS. When using broadband spectrum frequency US system, which all most recent medical US systems have adopted, a user cannot select or adjust specific frequency because broadband spectrum frequency uses all frequencies within the given range. Therefore, we compared 2 different transducers with different frequency ranges. In the case of using adjustable frequency, simply decreasing the frequency may have the same effect of changing to LF transducer. The accuracy of LUS still is controversial. Although our previous study and the present study performed in Asia demonstrated high accuracy of LUS,4,5,11 another study performed in the United States reported a comparatively poor accuracy of LUS.12 This discrepancy might be due to differences in body habitus of different races or differences in LUS assessor’s skills. Wong et al13 reported that surgeons needed LUS experience of about 40 cases to perform LUS accurately. Other well-trained LUS assessors in the United States reported high accuracy of LUS and demonstrated their LUS skills at the 2014 American Association of Endocrine Surgeons annual meeting.14 Therefore, we can assume that LUS is a reliable VC evaluation tool based on current evidences. There were 3 false positive cases and 1 false negative case with both LUS methods in the present study. All of these false positive and negative cases were of mild, grade II VCP (VC paresis), which sometimes leads to interobserver differences in other VC evaluation methods as well. There was no case of grade III VCP (VC paralysis) among the false positive and negative cases. We think that this mild interobserver variability in screening tools is acceptable. When VCP was detected before operation, we could expect the invasion of thyroid cancer to the recurrent laryngeal nerve. Therefore, we could prepare anastomosis of recurrent laryngeal nerve before operation. When VCP was detected after operation, we waited for spontaneous recovery for
ARTICLE IN PRESS Surgery Volume j, Number j
3 months. When permanent VCP was detected, we referred the patient to the voice clinic for more aggressive treatments, such as laryngoplasty. The proportion of VCP (14.0%) in the present study is different from the complication rate. Patients with VCP were followed up continuously until recovery; therefore, VCP findings were counted as multiple observations. There were 5 cases of permanent VCP after cutting of the recurrent laryngeal nerve invaded by a tumor. With the exception of these cases, all patients with VCP recovered within 3 months. All 7 patients who were not visualized by LF LUS were male patients with severe calcification of the thyroid cartilage, and all of these patients had normal VCs on DL evaluation. In conclusion, LF LUS significantly enhanced visualization of VCs in patients who had diffuse thyroid cartilage calcification interrupting LUS; therefore, this frequency increased the overall efficacy of LUS as a perioperative diagnostic tool for VCP. Hence, we recommend using a LF transducer (about 9–3 MHz) for LUS if it is available. We want to express our special gratitude to Dr Woo’s wife Min Hye Kim for her infinite understanding and devotion to this work. REFERENCES 1. Haugen BR, Alexander EK, Bible KC, Doherty GM, Mandel SJ, Nikiforov YE, et al. 2015 American Thyroid Association management guidelines for adult patients with thyroid nodules and differentiated thyroid cancer. Thyroid 2016;26:1-133. 2. Chandrasekhar SS, Randolph GW, Seidman MD, Rosenfeld RM, Angelos P, Barkmeier-Kraemer J, et al. Clinical practice guideline: improving voice outcomes after thyroid surgery. Otolaryngol Head Neck Surg 2013;148:S1-37. 3. Paul BC, Rafii B, Achlatis S, Amin MR, Branski RC. Morbidity and patient perception of flexible laryngoscopy. Ann Otol Rhinol Laryngol 2012;121:708-13.
Woo et al 5
4. Wong KP, Lang BH, Ng SH, Cheung CY, Chan CT, Lo CY. A prospective, assessor-blind evaluation of surgeonperformed transcutaneous laryngeal ultrasonography in vocal cord examination before and after thyroidectomy. Surgery 2013;154:1158-64; discussion 64-5. 5. Wong KP, Woo JW, Youn YK, Chow FC, Lee KE, Lang BH. The importance of sonographic landmarks by transcutaneous laryngeal ultrasonography in post-thyroidectomy vocal cord assessment. Surgery 2014;156:1590-6; discussion 6. 6. Wong KP, Lang BH, Chang YK, Wong KC, Chow FC. Assessing the validity of transcutaneous laryngeal ultrasonography (TLUSG) after thyroidectomy: what factors matter? Ann Surg Oncol 2015;22:1774-80. 7. Wong KP, Woo JW, Li JY, Lee KE, Youn YK, Lang BH. Using transcutaneous laryngeal ultrasonography (TLUSG) to assess post-thyroidectomy patients’ vocal cords: which maneuver best optimizes visualization and assessment accuracy? World J Surg 2016;40:652-8. 8. Singer MC, Iverson KC, Terris DJ. Thyroidectomy-related malpractice claims. Otolaryngol Head Neck Surg 2012; 146:358-61. 9. Ooi LL. B-mode real-time ultrasound assessment of vocal cord function in recurrent laryngeal nerve palsy. Ann Acad Med Singapore 1992;21:214-6. 10. Lang BH, Wong CK, Tsang RK, Wong KP, Wong BY. Evaluating the cost-effectiveness of laryngeal examination after elective total thyroidectomy. Ann Surg Oncol 2014;21: 3548-56. 11. Woo JW, Suh H, Song RY, Lee JH, Yu HW, Kim SJ, et al. A novel lateral-approach laryngeal ultrasonography for vocal cord evaluation. Surgery 2016;159:52-7. 12. Kandil E, Deniwar A, Noureldine SI, Hammad AY, Mohamed H, Al-Qurayshi Z, et al. Assessment of vocal fold function using transcutaneous laryngeal ultrasonography and flexible laryngoscopy. JAMA Otolaryngol Head Neck Surg 2015:1-6. 13. Wong KP, Lang BH, Lam S, Au KP, Chan DT, Kotewall NC. Determining the learning curve of transcutaneous laryngeal ultrasound in vocal cord assessment by CUSUM analysis of eight surgical residents: when to abandon laryngoscopy. World J Surg 2016;40:659-64. 14. Carneiro-Pla D, Miller BS, Wilhelm SM, Milas M, Gauger PG, Cohen MS, et al. Feasibility of surgeonperformed transcutaneous vocal cord ultrasonography in identifying vocal cord mobility: a multi-institutional experience. Surgery 2014;156:1597-602; discussion 602-4.
Comparison of ultrasound frequency in laryngeal ultrasound for vocal cord evaluation Jung-Woo Woo, MD,a,b Inhye Park, MD,a Jun Ho Choe, MD, PhD,a Jung-Han Kim, MD, PhD,a and Jee Soo Kim, MD, PhD,a Seoul and Changwon, South Korea
Background. Laryngeal ultrasound is a new method of vocal cord evaluation in patients at risk for vocal cord palsy. However, the previously described laryngeal ultrasound reportedly has a high failure rate of vocal cord visualization in male patients. We compared 2 ultrasound frequencies in laryngeal ultrasound to improve on the limitations of this method. Method. A total of 301 (55 male, 246 female) consecutive laryngeal ultrasound and direct laryngoscopy exams were performed for patients with thyroidectomy and other neck operations. High-frequency transducer (12–5 MHz broad band spectrum) and low-frequency transducer (9–3 MHz broad band spectrum) were used for all laryngeal ultrasound. Findings were independently cross-validated with direct laryngoscopy. Results. High-frequency and low-frequency laryngeal ultrasound had 88.4% and 97.7% visualization rates, respectively. In addition, low-frequency laryngeal ultrasound showed improved sensitivity of 97.6% and specificity of 96.5%, compared with a sensitivity of 92.9% and specificity of 86.5% for high-frequency laryngeal ultrasound in vocal cord evaluation. Conclusion. The low-frequency laryngeal ultrasound method significantly enhances the visualization of vocal cords, especially in patients who have diffuse thyroid cartilage calcification interrupting laryngeal ultrasound, and therefore enhances the overall efficacy of laryngeal ultrasound as a perioperative diagnostic tool for vocal cord palsy. Hence, we recommend using a low-frequency transducer (about 9–3 MHz) for laryngeal ultrasound if it is available. (Surgery 2016;j:j-j.) From the Department of Surgery,a Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, South Korea; and Department of Surgery,b Gyeongsang National University Changwon Hospital and Gyeongsang National University School of Medicine, Changwon, South Korea
VOCAL CORD PALSY (VCP) is an important complication of thyroid and parathyroid operation that affects patient quality of life.1 Direct laryngoscopy is the gold standard for vocal cord assessment.2 Although laryngoscopy is safe, it is an invasive procedure and can cause patient discomfort and fear.3 Laryngeal ultrasound (LUS) is a noninvasive method of vocal cord (VC) evaluation in patients at risk for VCP.4,5 However, the previously described LUS reportedly has a high failure rate when visualizing VC in male patients.6 In male
patients, the thyroid cartilage has a tendency to be sharp in angle and show diffuse calcification. The sharp angle of the thyroid cartilage does not allow close contact of the ultrasound (US) transducer with the skin, and this prevents simultaneous evaluation of both VCs. Diffuse calcification of the thyroid cartilage blocks penetration of US through the thyroid cartilage. We compared 2 US frequencies (12–5 MHz and 9–3 MHz broad band spectrum) in LUS. The aim of this study was to determine the optimal LUS frequency for VC evaluation.
Presented as a poster at the 67th Congress of the Korean Surgical Society in Seoul, Korea, November 5–7, 2015.
METHODS Patients. A total of 301 (55 male, 246 female) consecutive LUS, and direct laryngoscopy (DL) examinations were performed in patients who underwent thyroidectomy and other neck operations pre- and postoperatively. A high-frequency (HF) transducer (12–5 MHz broad band spectrum) and low frequency (LF) transducer (9–3 MHz broad band spectrum) were used in all
Accepted for publication October 12, 2016. Reprint requests: Jun Ho Choe, MD, PhD, Department of Surgery, Samsung Medical Center, Sungkyunkwan, University School of Medicine, 81 Irwon-ro, Gangnam-gu, Seoul 135-710, South Korea. E-mail: [email protected]. 0039-6060/$ - see front matter Ó 2016 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.surg.2016.10.013
SURGERY 1
ARTICLE IN PRESS 2 Woo et al
Surgery j 2016
Fig. (A) LUS. (B) HF transducer (right, 12–5 MHz broad band spectrum) and LF transducer (left, 9–3 MHz broad band spectrum) were used for all LUS in this study. (C) HF and (D) LF LUS for the same patient. HS LUS shows only FC, while LF LUS shows all 3 landmarks; FC, TC, and AR.
patients (Fig). LUS and DL were performed in each patient on the same day by different, blinded assessors who did not have any information about the results of the other method. The Philips HD 15 ultrasound system (Philips Ultrasound Inc, Reedsville, PA) was used for LUS. DLs were performed with the Karl-Storz Endoskope full HD system with an 8700H rigid scope (Tuttlingen, Germany). Findings from LUS were independently cross-validated with results from DL. VC evaluations were performed on the day before and after operation. Patients with VCP were followed up continuously at the outpatient department until recovery. Methods. LUS techniques have been described in previous studies.4,5 During the LUS assessment, the patient was positioned flat on the bed with the neck slightly extended. After applying ample gel over the anterior neck, an US transducer was placed transversely over the middle portion of the thyroid cartilage and the area was scanned until both true and false vocal cords were visualized. The 3 laryngeal landmarks-arytenoids (ARs), true cords (TCs), and false cords (FCs) were used for VC evaluation (Fig). Patients were instructed to perform all 3 maneuvers (breathing, phonation,
and Valsalva).7 The movement of the vocal cords was assessed during the evaluation. The extent of movement of the VC was graded according to the following scale: grade I, full or normal symmetric movement; grade II, impaired or decreased movement; and grade III, no movement. Before or after the LUS, the patient was directed to the other center where DL was performed by an experienced surgeon who was unaware of the patient’s LUS findings. Using a grading system similar to the LUS, the extent of VC movement on DL was graded from I to III. Grade II or III on DL was defined as having VCP. Patients with VCP were followed up at the outpatient department continuously until recovery from VCP. Student t test in SPSS Statistics 22 (IBM, Chicago, IL) was used to compare the VC visualization rate of each evaluation method. RESULTS A total of 301 consecutive VC examinations were evaluated. Table I shows the demographics, indications, extent of the operation, and the various operative approaches including 140 conventional open cervical thyroidectomies (86.4%), 11 robotic (6.8%), and 11 endoscopic (6.8%)
ARTICLE IN PRESS Woo et al 3
Surgery Volume j, Number j
Table I. Patient characteristics (n = 301), indications, extent of the operation, operative approaches, and vocal cord findings Characteristics Median age, y (range) Male Female Sex, n (%) Male Female Preoperative patients, n (%) Postoperative patients, n (%) Indication of operation, n (%) Suspicious malignancy Thyrotoxicosis Benign goiter Others Type of operation, n (%) Total thyroidectomy Hemithyroidectomy Subtotal thyroidectomy Parathyroidectomy Neck dissection Approach of operation, n (%) Conventional BABA robotic BABA endoscopic Calcification of thyroid cartilage, n (%) Focal calcification Diffuse calcification Laryngoscopic VC findings, n (%) Grade I Grade II Grade III Unassessable HF LUS VC findings, n (%) Grade I Grade II Grade III Unassessable LF LUS VC findings, n (%) Grade I Grade II Grade III Unassessable
Table II. HF LUS and DL correlation HF LUS Normal
Value 48 (13–81) 49 (28–67) 47 (13–81) 55 246 139 162
(18.3) (82.7) (46.2) (53.8)
273 3 17 8
(90.7) (1.0) (5.6) (2.7)
79 72 3 3 5
(48.8) (44.4) (1.9) (1.9) (3.1)
DL
(86.4) (6.8) (6.8) (30.6) (12.3) (18.3)
259 (86.0) 19 (6.3) 23 (7.6) 0 225 19 22 35
(74.8) (6.3) (7.3) (11.6)
251 20 23 7
(83.4) (6.6) (7.6) (2.3)
BABA, Bilateral axillo-breast approach; Grade I, normal mobility; Grade II, diminished mobility; Grade III, no mobility.
bilateral axillo-breast approach thyroidectomies. Suspicion of thyroid cancer was the most common indication (90.7%) for operation. There were 3 cases of parathyroidectomy and 5 cases of neck dissection. The median age at operation was 48 years. The 301 VC examinations revealed that 42 (14.0%; 5 male, 37 female) patients had VCP on
Not Grade I Grade II Grade III assessable Total
Normal 224 2 Grade I VC palsy Grade II 1 17 Grade III 0 0 Total 225 19 Accessibility 88.4% (266/301) Sensitivity 92.9% (39/42) Specificity 86.5% (224/259)
0
33
259
0 22 23
1 1 35
19 23 301
Grade I, Normal mobility; Grade II, diminished mobility; Grade III, no mobility.
Table III. LF LUS and DL correlation LF LUS Normal
DL 140 11 11 92 37 55
VC palsy
VC palsy
Not Grade I Grade II Grade III assessable Total
Normal 250 2 Grade I VC palsy Grade II 1 18 Grade III 0 0 Total 251 20 Accessibility 97.7% (294/301) Sensitivity 97.6% (41/42) Specificity 96.5% (250/259)
0
7
259
0 23 23
0 0 7
19 23 301
Grade I, Normal mobility; Grade II, diminished mobility; Grade III, no mobility.
DL, and 55 patients had diffuse thyroid cartilage calcification interrupting LUS. On HF LUS, 19 patients had grade II findings and 22 patients had grade III findings; meanwhile, on LF LUS, 20 patients had grade II findings and 23 patients had grade III findings (Table I). All VCP cases were unilateral. HF and LF LUS showed 88.4% and 97.7% visualization rate, 92.9% and 97.6% sensitivity, and 86.5% and 96.5% specificity, respectively (Tables II and III). There were 2 false positive cases and 1 false negative case in both HF and LF LUS. Table IV presents the visualization rates of VC landmarks by HF and LF LUS. Visualization rates of laryngeal landmarks by HF LUS compared with LF LUS were 88.0% (265) vs 97.3% (293) for FC, 50.5% (152) vs 78.7% (237) for TC, and 50.2% (151) vs 89.7% (270) for AR, respectively. FC was the most visible landmark by both HF
ARTICLE IN PRESS 4 Woo et al
Surgery j 2016
Table IV. Visualization rates of vocal cord landmarks in 301 LUS Frequency of LUS HF (%) LF (%) P value
FC
TC
AR
Overall
265 (88.0) 152 (50.5) 151 (50.2) 266 (88.4) 293 (97.3) 237 (78.7) 270 (89.7) 294 (97.7) <.001 <.001 <.001 <.001
and LF LUS. AR and TC were the least visible landmark by HF and LF LUS, respectively. LF LUS showed significantly greater visualization rates of all 3 VC landmarks than HF LUS (P < .001). DISCUSSION VCP has the maximum medicolegal and cost implications in thyroid and parathyroid operation.8 Therefore, the new 2015 American Thyroid Association Guidelines placed an emphasis on perioperative VC evaluation even in cases involving loss of voice.1 Nevertheless, controversies about routine VC evaluation are ongoing. DL, which is the gold standard for VC evaluation, frequently causes unnecessary discomfort and gag reflex in patients, especially in the immediate postoperative period. Since the introduction of LUS in 1992,9 LUS has improved with advancements in US technology. Wong et al4,5 compared the accuracy of LUS and DL in order to investigate the potential of using LUS as a VC evaluation tool. LUS can be performed pre- and postoperatively simultaneously during thyroid US; hence, it has its own unique benefit of reducing the additional medical cost and avoiding patient discomfort caused by DL.10,11 In the early period, LUS was limited to female patients because LUS was not appropriate for VCs in male patients due to the prominent protrusion and frequent diffuse calcification of thyroid cartilage, blocking US penetration.6 Although in a previous study, a novel attempt was made to improve VC visualization with LUS in male patients using a lateral approach, this method also had its own limitation of nonsynchronous 2-step evaluation of both VCs.11 LF LUS can evaluate VCs in male patients by a 1-step procedure using LF to improve US penetration. In our study, 47 patients were men among 55 patients with diffuse calcification on thyroid cartilage. Most calcifications in thyroid cartilage were thin and light calcifications, not thick and bony calcifications. Therefore, they were penetrated easily by LF LUS. The LF US transducer originally was manufactured for deep
vascular evaluations such as visualization of the carotid artery. We applied the LF US transducer to LUS for the first time to improve VC visualization. The sonographic view with LF LUS showed more VC landmarks compared with HF LUS but sacrificed the high definition of HF LUS at the same time. LUS is a motion-based diagnostic tool; therefore, visualization of the VC landmarks is more important than high definition. Previous studies used various frequencies in the range of 3–12 MHz. However, there was no research about optimal frequency for LUS4,5; the purpose of our research is to discover the optimal frequency for LUS. When using broadband spectrum frequency US system, which all most recent medical US systems have adopted, a user cannot select or adjust specific frequency because broadband spectrum frequency uses all frequencies within the given range. Therefore, we compared 2 different transducers with different frequency ranges. In the case of using adjustable frequency, simply decreasing the frequency may have the same effect of changing to LF transducer. The accuracy of LUS still is controversial. Although our previous study and the present study performed in Asia demonstrated high accuracy of LUS,4,5,11 another study performed in the United States reported a comparatively poor accuracy of LUS.12 This discrepancy might be due to differences in body habitus of different races or differences in LUS assessor’s skills. Wong et al13 reported that surgeons needed LUS experience of about 40 cases to perform LUS accurately. Other well-trained LUS assessors in the United States reported high accuracy of LUS and demonstrated their LUS skills at the 2014 American Association of Endocrine Surgeons annual meeting.14 Therefore, we can assume that LUS is a reliable VC evaluation tool based on current evidences. There were 3 false positive cases and 1 false negative case with both LUS methods in the present study. All of these false positive and negative cases were of mild, grade II VCP (VC paresis), which sometimes leads to interobserver differences in other VC evaluation methods as well. There was no case of grade III VCP (VC paralysis) among the false positive and negative cases. We think that this mild interobserver variability in screening tools is acceptable. When VCP was detected before operation, we could expect the invasion of thyroid cancer to the recurrent laryngeal nerve. Therefore, we could prepare anastomosis of recurrent laryngeal nerve before operation. When VCP was detected after operation, we waited for spontaneous recovery for
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3 months. When permanent VCP was detected, we referred the patient to the voice clinic for more aggressive treatments, such as laryngoplasty. The proportion of VCP (14.0%) in the present study is different from the complication rate. Patients with VCP were followed up continuously until recovery; therefore, VCP findings were counted as multiple observations. There were 5 cases of permanent VCP after cutting of the recurrent laryngeal nerve invaded by a tumor. With the exception of these cases, all patients with VCP recovered within 3 months. All 7 patients who were not visualized by LF LUS were male patients with severe calcification of the thyroid cartilage, and all of these patients had normal VCs on DL evaluation. In conclusion, LF LUS significantly enhanced visualization of VCs in patients who had diffuse thyroid cartilage calcification interrupting LUS; therefore, this frequency increased the overall efficacy of LUS as a perioperative diagnostic tool for VCP. Hence, we recommend using a LF transducer (about 9–3 MHz) for LUS if it is available. We want to express our special gratitude to Dr Woo’s wife Min Hye Kim for her infinite understanding and devotion to this work. REFERENCES 1. Haugen BR, Alexander EK, Bible KC, Doherty GM, Mandel SJ, Nikiforov YE, et al. 2015 American Thyroid Association management guidelines for adult patients with thyroid nodules and differentiated thyroid cancer. Thyroid 2016;26:1-133. 2. Chandrasekhar SS, Randolph GW, Seidman MD, Rosenfeld RM, Angelos P, Barkmeier-Kraemer J, et al. Clinical practice guideline: improving voice outcomes after thyroid surgery. Otolaryngol Head Neck Surg 2013;148:S1-37. 3. Paul BC, Rafii B, Achlatis S, Amin MR, Branski RC. Morbidity and patient perception of flexible laryngoscopy. Ann Otol Rhinol Laryngol 2012;121:708-13.
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4. Wong KP, Lang BH, Ng SH, Cheung CY, Chan CT, Lo CY. A prospective, assessor-blind evaluation of surgeonperformed transcutaneous laryngeal ultrasonography in vocal cord examination before and after thyroidectomy. Surgery 2013;154:1158-64; discussion 64-5. 5. Wong KP, Woo JW, Youn YK, Chow FC, Lee KE, Lang BH. The importance of sonographic landmarks by transcutaneous laryngeal ultrasonography in post-thyroidectomy vocal cord assessment. Surgery 2014;156:1590-6; discussion 6. 6. Wong KP, Lang BH, Chang YK, Wong KC, Chow FC. Assessing the validity of transcutaneous laryngeal ultrasonography (TLUSG) after thyroidectomy: what factors matter? Ann Surg Oncol 2015;22:1774-80. 7. Wong KP, Woo JW, Li JY, Lee KE, Youn YK, Lang BH. Using transcutaneous laryngeal ultrasonography (TLUSG) to assess post-thyroidectomy patients’ vocal cords: which maneuver best optimizes visualization and assessment accuracy? World J Surg 2016;40:652-8. 8. Singer MC, Iverson KC, Terris DJ. Thyroidectomy-related malpractice claims. Otolaryngol Head Neck Surg 2012; 146:358-61. 9. Ooi LL. B-mode real-time ultrasound assessment of vocal cord function in recurrent laryngeal nerve palsy. Ann Acad Med Singapore 1992;21:214-6. 10. Lang BH, Wong CK, Tsang RK, Wong KP, Wong BY. Evaluating the cost-effectiveness of laryngeal examination after elective total thyroidectomy. Ann Surg Oncol 2014;21: 3548-56. 11. Woo JW, Suh H, Song RY, Lee JH, Yu HW, Kim SJ, et al. A novel lateral-approach laryngeal ultrasonography for vocal cord evaluation. Surgery 2016;159:52-7. 12. Kandil E, Deniwar A, Noureldine SI, Hammad AY, Mohamed H, Al-Qurayshi Z, et al. Assessment of vocal fold function using transcutaneous laryngeal ultrasonography and flexible laryngoscopy. JAMA Otolaryngol Head Neck Surg 2015:1-6. 13. Wong KP, Lang BH, Lam S, Au KP, Chan DT, Kotewall NC. Determining the learning curve of transcutaneous laryngeal ultrasound in vocal cord assessment by CUSUM analysis of eight surgical residents: when to abandon laryngoscopy. World J Surg 2016;40:659-64. 14. Carneiro-Pla D, Miller BS, Wilhelm SM, Milas M, Gauger PG, Cohen MS, et al. Feasibility of surgeonperformed transcutaneous vocal cord ultrasonography in identifying vocal cord mobility: a multi-institutional experience. Surgery 2014;156:1597-602; discussion 602-4.