World J Surg (2016) 40:665–671 DOI 10.1007/s00268-015-3393-x

ORIGINAL SCIENTIFIC REPORT

Transcutaneous Ultrasonography in Early Postoperative Diagnosis of Vocal Cord Palsy After Total Thyroidectomy Fre´de´ric Borel1 • Anne-Sophie Delemazure2 • Florent Espitalier3 • Andrew Spiers1 Eric Mirallie1 • Claire Blanchard1

•

Published online: 7 January 2016 Ó Socie´te´ Internationale de Chirurgie 2016

Abstract Purpose This study evaluated the efficiency of transcutaneous laryngeal ultrasonography (TLUS) as an alternative to direct flexible laryngoscopy (DFL) in the early postoperative screening of vocal cord palsy (VCP) after total thyroidectomy, performed for benign and non-extensive malignant disease. Methods A prospective study was performed on patients who underwent total thyroidectomy between October 2013 and January 2015 at the Nantes University Hospital (France). Patients underwent DFL on postoperative day 1 performed by an otolaryngologist, followed by TLUS performed by a radiologist on postoperative day 1 or 2. Results One hundred and three (103) patients were included in this study, 17.5 % were male and 82.5 % were female, with a mean age of 51 ± 12 years. Nine patients (9.5 %) were diagnosed with postoperative VCP using DFL of these cases 2 were not completely resolved at 3 months postoperatively. Three cases of VCP (33 %) were diagnosed using TLUS. TLUS had a sensitivity of 33 % and a negative predictive value (NPV) of 95 % for the diagnosis of postoperative VCP. Vocal cords (VC) were unassessable in 27.2 % of patients. Unassessable VC were significantly associated with male gender (p = 0.0001), age (p = 0.0001), weight (p = 0.002), operating time (p = 0.032), postoperative drainage (p = 0.001), and thyroid weight (p = 0.001). Independent risk factors in the multivariate analysis were male gender (p = 0.0001) and age (p = 0.0001). In the group of women under 50-year old, TLUS had a sensitivity of 50 % and a NPV of 97.4 %. Conclusion TLUS sensitivity is insufficient in early postoperative screening of VCP after thyroid surgery. Ultrasonographic VCP diagnosis should be confirmed with DFL.

Introduction

& Claire Blanchard [email protected] 1

Service de Clinique Chirurgicale Digestive et Endocrinienne, CHU Nantes, 1 place Alexis Ricordeau, 44093 Nantes Cedex 1, France

2

Service de Radiologie et Imagerie Me´dicale, CHU Nantes, Nantes, France

3

Service d’Oto-Rhino-Laryngologie, CHU Nantes, Nantes, France

Thyroidectomy for benign disease is the most performed endocrine surgery worldwide. In cases of benign thyroid disease, surgery minimizes both mortality and morbidity [1]. The main complications associated with thyroidectomies are hypoparathyroidism, vocal cord palsy (VCP), and hematoma [2]. VCP is the major complication of thyroidectomies. The postoperative VCP rate varies between 0.5 and 20 % [3]. Unilateral VCP often leads to voice impairment but can also be asymptomatic [4]. On the other hand, up to 30 % of patients with no underlying recurrent laryngeal nerve (RLN) lesion, complain of

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subjective voice symptoms after thyroid surgery [5]. Bilateral VCP can be responsible for acute respiratory distress, requiring temporary or permanent tracheostomy. VCP is also the most frequent cause of medicolegal litigation after thyroid surgery [6]. Malignant disease, previous thyroid surgery, anatomical variations and the experience of surgeon increase the risk of intraoperative lesion of the RLN [7, 8]. The pertinence of a vocal cord (VC) examination as part of thyroid surgery management is still debated. The most commonly practiced guidelines recommend a selective VC examination in case of thyroid cancer with suspected extrathyroidal extension and/or previous neck surgery or voice impairment. [9] Surgeons who recommend routine preoperative laryngeal examination argue that knowledge of preoperative VCP should lead to extra-care in the dissection and preservation of the controlateral RLN [10]. Furthermore, postoperative VC examinations detect damage to the RLN associated with surgery and inform surgeons of their postoperative complication rate. The gold standard examination of VC, and the most used examination tool, is direct flexible laryngoscopy (DFL). DFL allows for the visualization of 99 % of VC [11]. However, DFL remains an invasive examination and is often associated with pain and discomfort among patients [12]. Endocrine surgeons often address patients to a specialist for DFL, leading to extra expense and time loss. Other standard methods of assessing VC include indirect laryngoscopy, video-stroboscopy, or the review of a clinical history [13]. Considering the disadvantages of DFL, some authors propose transcutaneous laryngeal ultrasonography (TLUS) as an alternative to routine DFL after thyroid surgery. TLUS is a noninvasive and low-cost examination. Endocrine surgeons can perform TLUS during a preoperative or postoperative surgical consultation [14–17]. The efficacy of TLUS in the assessment of VC in adult patients or in the diagnosis of VCP is still under debate. We report in the present study our experience of early routine examination using TLUS for diagnosis of VCP following total thyroidectomy performed for benign or non-extensive malignant disease.

Materials and methods Patients admitted for both a total thyroidectomy and a postoperative ultrasound (US) VC examination, between October 2013 and January 2015, at University Hospital of Nantes (France), were included prospectively in this study. Exclusion criteria included age under 18, suspected or confirmed extensive malignant disease and preoperative voice abnormalities.

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All patients gave written consent prior to surgery. Surgical procedure Surgery was performed under general anesthesia with tracheal intubation. The surgical procedure was total thyroidectomy through a collar incision. Strap muscles were not cut unless required. Drainage was performed according to the surgeons’ indication. The closure of the surgical incision consisted of a two layer closure comprised a subcutaneous dissolvable continuous stitch and intradermal dissolvable single stitches. Surgical glue was applied on the incision site. Laryngeal examination No preoperative laryngeal examination was performed. Postoperative laryngeal examination was performed early postoperatively and during hospitalization. Patients first underwent a laryngeal examination with DFL performed by an otolaryngologist 1 day after the surgery. The existence and severity of a VCP was noted. TLUS was performed, after the DFL on postoperative day 1 or 2, by skilled radiologists who had no prior experience of TLUS. A single-ultrasound machine (ToshibaÒ Aplio 400) and probe (8 mHz high-frequency linear transducer) were used during the present study. Patients were positioned flat on their back during the exam, with no neck elevation. The ultrasound probe was placed above the collar incision and the VC axis was located via arytenoid landmarks (Fig. 1). The operator was able to directly visualize VC movement and airflow through the VC by asking the patient to phonate. The radiologists were blinded to the result of the DFL laryngeal examination. TLUS did not allow us to grade accurately the severity of VC dysfunction, we therefore associated both VC immobility, VC mobility decrease, and VC asymmetry [18], with diagnosis of VCP when these were detected by TLUS. The operator reported (i) if VC were assessable or not with TLUS, (ii) on the presence or absence of VCP, and (iii) tried to assess VCP severity. Patients with postoperative VCP were followed-up every month after surgery with a medical consultation and a DFL to assess the VCP evolution. Statistical analysis Patient data were compiled in a Microsoft ExcelÒ spreadsheet. Statistical analyses were performed with SPSS softwareÒ (version 22), using a 5 % p value. Univariate analysis was made with v2 tests and Student t tests. Multivariate analysis was made using logistic regression.

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Fig. 1 Ultrasonographic examination of VC adduction (a) and abduction (b) in plan of arytenoids (AR) landmarks

Results One hundred and three patients were included in this study; their characteristics and the outcomes of surgery are, respectively, summarized in Tables 1 and 2. Ninety-five patients (92.2 %) underwent DFL on postoperative day one. Eight patients (7.7 %) did not undergo DFL due to the impossibility to get a consultation with an otolaryngologist before the end of their hospitalization (n = 5, 4.8 %), a refusal motivated by fear of discomfort associated with DFL (n = 2, 1.9 %), and the occurrence of a vasovagal episode during the examination (n = 1, 1 %). All patients were examined by TLUS on postoperative day 1 (40 patients, 38.8 %) or 2 (63 patients, 61.2 %). Nine VCP (9.5 %) were diagnosed using DFL; 7 (7.4 %) of the VCP cases were transient, whereas 2 (2.1 %) of the VCP cases were incompletely resolved 3 months postoperatively.

Table 2 Outcomes of surgery Outcomes

Value

Histological diagnosis Benign thyroid disease, n (%)

81 (78.4)

Malignant tumor, n (%)

22 (21.4)

Histological classification

Table 1 Patient characteristics Characteristic

Three VCP were diagnosed with TLUS (33 %), whereas 4 patients with mobile VC confirmed using DFL were found to have postoperative VCP using TLUS. TLUS had a sensitivity of 33 %, a specificity of 95 %, a positive predictive value of 42 %, and a negative predictive value of 89 % (Table 3). Four (66 %) out the 6 missed VCP at TLUS were graded as VC paresis with DFL. VC were not completely visible using TLUS in 28 patients (27.2 %). The quality of the TLUS examinations remained stable throughout the study and there was no difference in VC visualization rates between the 50 initial and final TLUS

Papillary thyroid cancer, n (%)

22 (100)

Value

Tumor size

51 ± 12

\10-mm-sized tumor, n (%)

15 (68.2)

Gender

C10-mm-sized tumor, n (%)

7 (31.8)

Male, n (%) Female, n (%)

Postoperatives complications Re-operation for hematomaa, n (%)

2 (1.9)

Mean age at surgery (year ± SD)

18 (17.5) 85 (82.5)

b

Hypocalcemia \ 2 mM , n (%)

Surgical indication

13 (12.6)

65 (63.1)

VCP, n (%)

9 (9.5)

Malignant tumor , n (%)

20 (19.4)

Transient VCP, n (%)

7 (7.4)

Grave’s disease, n (%)

17 (16.5)

Incompletely resolved VCPc, n (%)

2 (2.1)

1 (1)

Mean hospital stay, (days ± SD)

1.85 ± 0.47

Benign nodular goiter, n (%) a

b

Prophylactic thyroidectomy , n (%) a

a

b

b

Suspected papillary or follicular tumor on preoperative nodule fineneedle aspiration biopsy

Prophylactic thyroidectomy for familial medullary thyroid cancer history

Re-operation for bleeding or compressive hematoma during the first 24 h postoperatively

c

Hypocalcemia \2 mmol/L on hospital discharge Incompletely resolved VCP at 3 months postoperatively

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Table 3 Comparison of DFL and TLUS for VCP diagnosis TLUS

Table 5 Comparison of DFL and TLUS for diagnosis of VCP in women under 50 years of age

DFL

TLUS

DFL

VCP?

VCP-

VCP?

3

4

7

VCP-

6

82

88

VCP?

1

1

2

95

VCP-

1

38

39

2

39

41

VCP?

9

86

(28.8 % vs 25.5 %, p = 0.872), nor between the 25 initial and final TLUS (40.7 % vs 24 %, p = 0.322). Unassessable VC using TLUS were significantly associated with male gender (50 % vs 5.3 %, p = 0.0001), age (58 years vs 48 years, p = 0.0001), weight (78 kg vs 67 kg, p = 0.002), operating time (107 min vs 93 min, p = 0.032), postoperative drainage (25 % vs 4 %, p = 0.001), and thyroid weight (50.9 g vs 24.7 g, p = 0.001) in univariate statistical analysis (Table 4). Age and male gender remain significant independent risk factors of unassessable VC using TLUS according to logistic regression multivariate analysis (Table 4). In the sub-group of women under 50 years of age, TLUS had a sensitivity of 50 %, a specificity of 97.4 %, a positive predictive value of 50 %, and a negative predictive value of 97.4 % (Table 5). VC were not completely visible in 8.8 % of cases.

Discussion In the present study, we report our experience of early routine examination using TLUS for diagnosis of VCP following total thyroidectomy. We found the efficiency of TLUS as a means of diagnosis for VCP in the general population to be mediocre, with a sensitivity of 33 %, a

VCP-

specificity of 95 %, a positive predictive value of 42 %, and a negative predictive value of 89 %. TLUS assessment of VC was most efficient in premenopausal women, with a sensitivity of 50 %, a specificity of 97.4 %, a positive predictive value of 50 %, and a negative predictive value of 97.4 %, in relation with a globally easier visualization of VC. Authors have suggested that TLUS could be a key tool in postoperative VCP screening [14]. TLUS is a more convenient exam than DFL, which can be uncomfortable or even painful. In fact, in the present study, 3 patients did not undergo DFL for such reasons. Two patients refused DFL due to fear of discomfort, and one other had a vasovagal episode during the examination. On the contrary, no patient refused to undergo TLUS and there were no complaints during the procedure. Furthermore, the use of TLUS allows both cost and time reductions, especially if performed by endocrine surgeons during a pre- or postoperative consultation. In France, DFL costs twice as much as TLUS (73.92€ vs 35.91€), independent of laryngofiberscope sterilization costs. TLUS can be easily learnt and practiced by endocrine surgeons, thus reducing referral to other specialists [19]. The TLUS learning curve shortens with prior experience of neck ultrasonography (US) [16]. Examination duration is about 2–5 min.

Table 4 Risk factors of unassessable VC with TLUS examination Assessable VC, n (%) 75 (72.8 %)

Unassessable VC, n (%) 28 (27.2 %)

Univariate analysis p value

Multivariate analysis p value 0.009

Mean age at surgery, years ± SD

48.25 ± 11.99

58.14 ± 12.17

0.0001

Male gender, n (%)

4 (5.3)

14 (50)

0.0001

0.002

Weight, kg ± SD

67.6 ± 13.3

78.2 ± 18.9

0.002

0.77

BMI, kg/m2

25.03

26.85

0.189

Operative time, min

93

107

0.032

Curage, n (%)

7 (9.3)

0 (0)

0.185

Postoperative drainage, n (%)

3 (4)

7 (25)

0.001

Re-operationa, n (%)

1 (1.3)

1 (3.6)

0.142

Thyroid weight, g ± SD

24.7 ± 18.9

50.9 ± 47.6

0.001

Malignant tumor, n (%)

14 (18.7 %)

8 (28.6 %)

0.275

a

Re-operation for bleeding or compressive hematoma during the first 24 h postoperatively

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0.545 0.863 0.336

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The main goal of postoperative TLUS is to reliably detect and diagnose VCP, a rare but serious complication. Even if VCP diagnosis is made in excess, the examination should aim to prevent any failed VCP diagnosis. Available literature reports TLUS sensitivity at from 62 to 100 % and negative predictive value from 60 to 99.4 % [14, 16, 20, 21]. In line with most previous studies, we failed to diagnose all VCP cases using TLUS. We assessed TLUS sensitivity at 33 %, as 6 VCP cases were missed by TLUS in this study. TLUS show a negative predictive value of 89 %, which is relevant considering the low incidence of VCP after thyroidectomy. Only Dedecjus et al. reported a 100 % sensitivity of TLUS when comparing results of pre- and postoperative TLUS [21]. The proposed criterion of evaluation was a [50 % decrease in VC displacement velocity between pre- and postoperative TLUS. This method detected with a 100 % sensitivity patients with postoperative VCP. Even if TLUS performances depend upon operator skills, all authors agree that TLUS cannot accurately grade VC dysfunction severity. However, we were more likely to miss the less severe VC dysfunctions with TLUS. The main limit to TLUS efficiency is difficulty in visualizing VC. We report a 27 % unassessable VC rate whereas various studies report difficulties in VC visualization from 4 to 18 % [14, 17]. Known risk factors of difficult VC visualization are age, male gender, height, thyroid cartilage calcification, and a collar incision closer to the thyroid cartilage [22]. These risk factors are underlined by the poor results of TLUS in adults compared with children [23]. Moreover, in this study, operating time, postoperative drainage and thyroid weight appeared to be significantly associated with unassessable VC in univariate analysis. These factors can also be linked to more extensive surgeries, and a larger thyroid lodge associated with an increased risk of both hematoma and major postoperative laryngeal edema. Hematoma was the most frequent obstruction to the visualization of VC in this study, followed by thyroid cartilage calcification. Weight was also significantly associated with unassessable VC, whereas BMI was not. Neck adiposity, even in obese patients, did not hinder the US according to the operators. Wong et al. suggested the use of a saline-filled glove placed between the US probe and the thyroid cartilage to improve US conduction in case of difficulty in the visualization of VC [14]. We did not observe a learning curve effect leading to an improvement of the quality of the examination. A hypothesis to explain the poor visualization rates in the present study could be the time between surgery and TLUS. The best reported VC visualization rates concern TLUS performed on postoperative days 7–10, when patients have their dressings and steristrip removed [14]. Nevertheless, TLUS has been proven to be efficient immediately after surgery [24].

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Difficulties in VC visualization are not the only limit to TLUS as a VC examination. We report 3 cases of an inaccurate TLUS examination, where VCP was missed although VC were assessable. The hypothesis of transient palsy, usually resolved after several weeks, cannot explain these results [25]. Radiologists with prior experience of neck US performed all TLUS in this study. However, they had no prior experience in US VC examinations. They were blinded to both the course of the surgery and to the results of previous DFL. The operating surgeon would most likely perform a postoperative TLUS with extra-care if he suspected a nerve to be at risk after difficult surgery, contrary to radiologists. VCP remains a rare event and our study was therefore underpowered. We report a postoperative VCP rate of 9.5 % in spite of surgical indications of mainly benign thyroid diseases performed in a high-volume center. No DFL was performed before surgery to exclude preoperative VCP, because our goal was to appraise TLUS performances in VC assessment and VCP diagnosis after thyroidectomy, whatever may have been the cause. Most of the VCP were transient, in accordance with the 9.8 % incidence reported in literature [13]. The origins of RLN palsy remain unclear and probably multifactorial, the macroscopic integrity of the RLN does not imply its functional integrity [26]. An extralaryngeal ramification of the RLN is the main risk factor of transient VCP. The transient VCP rate is no different when comparing benign and malignant surgery indications [25]. Due to the relatively poor performances of TLUS in the diagnosis and evaluation of VCP reported in our study, DFL should be performed whenever VCP is diagnosed using TLUS, to confirm the diagnosis and to assess the severity. Wong et al. suggested an algorithm using TLUS as a screening tool for selecting DFL candidates [14]. Both the US diagnoses of VCP and non-assessable VC should be indications for a secondary DFL. The application of the aforementioned algorithm to the present series would have improved the TLUS sensitivity and negative predictive value to respectively 66 and 95 %. Thirty-five patients would have undergone secondary DFL, and only 3 cases of VCP would have been missed. This two-phase algorithm would also decrease the cost of TLUS while saving time as only a third of patient would require secondary DFL. TLUS showed good performances in women under 50 years of age. Premenopausal women represent a significant proportion of patients requiring total thyroidectomy due to the great prevalence of goiters in this subgroup [27]. The low rate of thyroid cartilage calcification in women may explain the better rate of assessable VC using TLUS. However, one case of VCP was still missed using TLUS in this sub-group, despite the usage of the 2 phase algorithm proposed by Wong et al. [14].

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Conclusion The sensitivity of TLUS in our population is insufficient and excludes this method from being a recommended means of early postoperative screening of VCP after thyroid surgery. Moreover, DFL should be performed to confirm any diagnosis of VCP established using TLUS. TLUS efficiency is highly correlated with age and gender. Further prospective studies should be initiated concerning premenopausal women to confirm the efficiency of TLUS in this specific sub-group, using the French AFCE network. Acknowledgments The authors thank Dr Emmanuelle LangloisMourrain for her participation in performing the ultrasonographies. We also thank Pr Eric Frampas, Dr Ce´cile Caillard, and Dr Delphine Drui for critical insight and suggestions on this work, and Laurence Toque´ and Ludwig Pasquier for their help. Compliance with ethical standards Conflict of Interest The authors declare that they have no potential or real conflict of interest. Ethical approval All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Human and animal rights and informed consent Informed consent was obtained from all individual participants included in the study. This article does not contain any studies with animals performed by any of the authors.

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