Langenbeck's Archives of Surgery (2022) 407:2059–2066

https://doi.org/10.1007/s00423-022-02493-w

ORIGINAL ARTICLE

Papillary thyroid cancer: the value of bilateral diagnostic

lymphadenectomy
Jagdeep Singh Bhangu1 · Christoph Bichler1 · Julia Altmeier1 · Lindsay Hargitai1 · Andreas Selberherr1 ·
Peter Mazal2 · Jonas Brugger3 · Christian Scheuba1 · Philipp Riss1 · Bruno Niederle1

Received: 11 October 2021 / Accepted: 9 March 2022 / Published online: 17 March 2022
© The Author(s) 2022

Abstract
Purpose Papillary thyroid carcinoma (PTC) spreads early to lymph nodes (LN). However, prophylactic central (CND) and
lateral neck dissection (LND) is controversially discussed in patients with clinically negative nodes (cN0). The preoperative
prediction of LN metastasis is desirable as re-operation is associated with higher morbidity and poor prognosis. The study
aims to analyse possible benefits of a systemic bilateral diagnostic lateral lymphadenectomy (DLL) for intraoperative LN
staging.
Methods Preoperative prediction of LN metastasis by conventional ultrasound (US) was correlated with the results of DLL
and intra-/postoperative complications in 118 consecutive patients with PTC (cN0) undergoing initial thyroidectomy and
bilateral CND and DLL.
Results Lateral LNs (pN1b) were positive in 43/118 (36.4%) patients, including skip lesions (n = 6; 14.0%). Preoperative US
and intraoperative DLL suspected lateral LN metastasis in 19/236 (TP: 8.1%) and 54/236 (TP: 22.9%) sides at risk, which
were confirmed by histology. Sixty-seven out of 236 (FN: 28.4%) and 32/236 (FN: 13.6%) sides at risk with negative pre-
operative US and intraoperative DLL lateral LN metastasis were documented. DLL was significantly superior compared to
US regarding sensitivity (62.8% vs 22.1%; p < 0.002), positive predictive value (100% vs 76.0%), negative predictive value
(82.4% vs 68.2%), and accuracy (86.4% vs 69.1%), but not specificity (100% vs 96.0%; p = 0.039). DLL-related complica-
tions (haematoma) occurred in 6/236 [2.5%] sides at risk, including chylous fistula in 2/118 [1.7%] patients.
Conclusion DLL can be recommended for LN staging during initial surgery in patients with PTC to detect occult lateral LN
metastasis not suspected by US in order to plan lateral LN dissection.

Keywords Papillary thyroid carcinoma · Thyroidectomy · Lymph node dissection · Diagnostic lateral lymphadenectomy

Introduction

Papillary thyroid carcinoma (PTC) is the most common

endocrine tumour with a gradually increasing incidence
over the past 20 years [1]. PTC accounts for almost 80%
of all well-differentiated thyroid carcinomas [2]. At initial
* Philipp Riss diagnosis, regional lymph node (LN) metastasis occurs in
[email protected] 30–80%, depending on diagnostic modalities [3]. While LN
1
Division of General Surgery, Department of Surgery, metastasis not removed during primary surgery and its role
Medical University of Vienna, Waehringer Guertel 18‑20, in recurrence is currently a subject of extended discussion
1090 Vienna, Austria [2, 4], recent studies have shown that metastasis in the lateral
2
Division of Clinical Pathology, Department of Pathology, neck (levels 2 to 5 Robbins [5]; compartments C2/C3 Dralle
Medical University of Vienna, Waehringer Guertel 18‑20, [6]; staged as N1b according to the TNM classification) is,
1090 Vienna, Austria in addition to tumour size and extrathyroidal tumour infiltra-
3
Centre of Medical Statistics, Informatics and Intelligent tion, a further independent risk factor for negative prognosis
Systems, Medical University of Vienna, Waehringer Guertel [3, 7–9]. To date, the dissection of lateral LN ipsilateral or
18‑20, 1090 Vienna, Austria

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2060 Langenbeck's Archives of Surgery (2022) 407:2059–2066

contralateral the primary tumour is only recommended in and analysed preoperatively by one radiologist. A suspicious
patients with clinically suspected or histologically proven LN was described with a solid content, sometimes necrotic
lateral LN metastasis [2, 10]. or cystic, ovoid to round shape in the longitudinal plane but
Prophylactic central or lateral LN dissection is still a mat- taller-than-wide in the transverse plane, hypoechogenic,
ter of discussion and is currently not recommended [11]. with microcalcifications, irregular margins, loss of the nodal
However, recent studies indicate that patients with lateral LN hilum, and peripheral vascularity [13].
metastases are at higher risk for developing local recurrence
[11, 12]. The preoperative prediction of LN metastasis in Surgery
the central and lateral neck in their initial dissection would
be valuable to avoid re-operations with higher morbidity Surgical treatment consisted of (total) thyroidectomy, ini-
and poor prognosis [3]. Furthermore, systematic LN dis- tial bilateral central LN dissection (CND; extirpation of
section during initial surgery permits an accurate staging the lymphatic tissue along both recurrent laryngeal nerves
of disease, may decrease the rate of complications, guide a without neuromonitoring [14] concerning Robbins level VI
more appropriate subsequent treatment [8], and improve the [5]; Dralle compartments C1a and C1b [6]), and bilateral
prognosis of PTC. diagnostic lateral lymph node extirpation (DLL = extirpa-
The aim of this study was to evaluate the value of sys- tion of the central jugular lymph nodes = lymphatic tis-
tematic extirpation of central jugular LNs (diagnostic lat- sue lateral the internal jugular vein above and below the
eral lymphadenectomy (DLL)) compared to the results of omohyoid muscle) [15] through a shortened Kocher’s skin
preoperative ultrasound (US) to predict uni- and/or bilateral incision (length dependent of the thyroid; between 30 and
lateral LN metastasis. Furthermore, the value of DLL for 40 mm). Independent of the preoperative US results, bilat-
intraoperative LN staging for planning the extent of lateral eral DLL was performed in all patients as part of the well-
LN dissection should be analysed. defined prospective SOP, as previous studies [15] have
shown that positive LNs were histologically proven in 96%
within this region independent of the size and the site of
Patients and methods the primary thyroid tumour in patients with differentiated
thyroid cancer and LN metastasis.
Demography If LN metastasis was documented in lateral LNs by
intraoperative frozen (DLL positive) section, an ipsilat-
A total of 118 patients (females: 79/118 (66.9%); males: eral (if both DLL were positive: bilateral) functional lat-
39/118 (33.1%)), undergoing initial surgery for differenti- eral neck dissection (FLND) was performed. FLND was
ated thyroid carcinoma at the Department of Surgery, Med- defined as complete removal of the lymphatic tissue from
ical University of Vienna, were included in this analysis. the base of the skull down to the upper thoracic outlet
Inclusion criteria were histologically confirmed PTC (clini- (Robins levels II to IV; Dralle C2 or C3) saving the strap
cally without LN metastasis [cN0]) and patients older than muscles, the jugular vein, and all cervical nerves.
18 years of age. Patients with follicular, anaplastic, or med- The results of US, intraoperative frozen sections of
ullary thyroid cancer were excluded. DLL, and the definitive histology were evaluated and cor-
All patients with the pre- and intraoperative diagnosis of related retrospectively with each other to assess the value
PTC were managed according to a prospective and standard- of the methods to predict LN metastasis.
ized diagnostic, surgical, and pathohistological and follow- Intra- and postoperative complications of CND, DLL,
up protocol (standard operating procedure [SOP]). and FLND were documented.
The prospective data collection and the retrospective Following the SOP, postoperative treatment consisted
correlation analysis were approved by the Ethics Commit- of radioiodine ablation (80–100 mCi) 4 to 6 weeks after
tee of the Medical University of Vienna (study protocol no. surgery. This allowed to document persisting disease in
1351/2017). All patients gave their written informed consent the lateral neck or distant metastasis at the time of surgery.
for all diagnostic and surgical procedures. All patients were monitored annually as outpatients in
accordance with a standardized follow-up protocol that
Preoperative ultrasound included clinical examination, ultrasonography of the
neck, biochemical measurements of thyroglobulin levels,
All patients underwent a preoperative neck US of the central and radiography of the lungs. However, long-term follow-
and both lateral cervical regions from the skull down to the up results were not the subject of this presentation [16,
supraclavicular region (General Electric [GE] LOGIQ E9 17].
device; 9 MHz probe). The left and right sides were docu- Concerning the extent of LN dissection, patients were
mented separately. The US examinations were performed assigned into three groups: group 1: patients with bilateral

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Langenbeck's Archives of Surgery (2022) 407:2059–2066 2061

CND and negative bilateral DLL frozen sections (n = 77 27 (43.5%) as pT1b (11–20 mm)]). Twenty-three patients
patients); group 2: patients with bilateral CND and bilat- (19.5%) had a pT2 tumour (21–40 mm) and 20 patients
eral DLL and unilateral positive frozen sections, uni-/ipsi- (17.0%) a pT3 tumour (> 40 mm). In 13 (11.0%) patients,
lateral FLND (n = 28); and group 3: patients with bilateral the carcinoma had already grossly invaded the subcuta-
CND and bilateral DLL and bilateral positive frozen sec- neous fatty tissue, larynx, trachea, oesophagus, recurrent
tions on both FLND (n = 13). laryngeal nerve, prevertebral fascia, and carotid artery
(pT4 [8 (61.5%) subclassified as pT4a; 5 (38.5%) as
Statistical analyses pT4b]) (see Table 1).
In 32 patients (27.1%), PTC was localized in the left thy-
CND and DLL were performed in 118 patients on both roid lobe, in 41 patients (34.8%) in the right thyroid lobe,
sides. Therefore, 236 “nerves at risk” and 236 “sides at and in six cases (5.1%) in the area of the isthmus.
risk” were used for the statistical calculation. Unilateral multicentricity was identified in 14 patients
All statistical analyses were conducted in SPSS Sta- (11.9% [group 1 (n = 7), group 2 (n = 6), group 3 (n = 1)])
tistics 25.0 software (SPSS Inc., Chicago, IL, USA). We and bilateral multicentricity in 39 patients (33.1% [group 1
compared the results of preoperative US, DLL (frozen (n = 26), group 2 (n = 6), group 3 (n = 7)]).
section), and definitive histology among each other using The median size of PTC was 20 mm (range 2–70 mm;
McNemar’s test. The sensitivity, specificity, positive pre- group 1: median 15 mm (range 2–70 mm), group 2: 23 mm
dictive value (PPV), negative predictive value (NPV), and (range 2–70 mm), group 3: 45 mm (range 5–60 mm)).
the general accuracy were determined for US and DLL
and subsequently compared with a two-proportion Z-test. LN metastasis
The significance level was adjusted using the Bonferroni
method (p ≤ 0.01). In 46/118 patients (39.0%), neither central nor DLL revealed
LN metastasis (pN0). In 72/118 patients (61.0%), PTC
had metastasized to the cervical LNs (pN1). Twenty-nine
(40.3%) of these patients showed central LN only (pN1a)
Results and 43 patients (59.7%) lateral LN involvement (pN1b). Six
patients (6/43 [14.0%] cases) with lateral LNs presented
TNM classification with skip lesions.
Median 9 (range 0–45) and 10 (range 0–49) LNs were
According to the current UICC/TNM Classification 15, 62 removed from the left and right neck compartments, respec-
(52.5%) tumours were identified as pT1 (tumour diame- tively, via DLL.
ter: ≤ 20 mm [35 (56.5%) subclassified as pT1a (≤ 10 mm);

Table 1  TNM classification Classification

[18] of 118 patients with
papillary thyroid cancer (PTC) T n N0, n (%) N1a, n (%) N1b, n (%) M0, n (%) M1, n (%)

pT1 62 30 (48.4) 17 (27.4) 15 (24.2) 62 (100) 0

pT1a 35 21 (60.0) 7 (20.0) 7 (20.0) 35 (100) 0
pT1b 27 9 (33.3) 10 (37.0) 8 (29.6) 27 (100) 0
pT2 23 7 (30.4) 8 (34.8) 8 (34.8) 23 (100) 0
pT3 20 7 (35.0) 3 (15.0) 10 (50.0) 18 (90.0) 2 (10.0)
pT4 13 2 (15.4) 1 (7.7) 10 (76.9) 12 (92.3) 1 (7.7)
pT4a 8 2 (25.0) 0 6 (75.0) 8 (100%) 0
pT4b 5 0 1 (20.0) 4 (80.0) 5 (100%) 0
Total 118 46 (39.0) 29 (24.6) 43* (36.4) 115 (97.5) 3 (2.5)

TNM classification—UICC 8th edition

T, tumour; LN, lymph node; N0, no LN metastasis; N1a, central LN; N1b, lateral/bilateral LN metasta-
sis; M0, no distant metastasis; M1, distant metastasis; p, pathological classification—pT1a: ≤ 10 mm and
intrathyroidal; pT1b: 11–20 mm and intrathyroidal; pT2: 21–40 mm and intrathyroidal; pT3: > 40 mm and
intrathyroidal or gross extrathyroidal extension; pT4a: any size and gross extrathyroidal extension; pT4b:
gross extrathyroidal extension or encasing the carotid artery, mediastinal vessels
*
Six out of 43 (14.0%) patients with LN metastasis had skip lesions

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2062 Langenbeck's Archives of Surgery (2022) 407:2059–2066

Thirty out of 118 (25.4%) patients with pT1 tumour negative (TN). US was unable to detect LN metastases in
(pT1a: 21/30 (70.0%); pT1b: 9/30 (30.0%)) were classi- 67/236 (28.4%) examinations (false negative [FN]) and
fied pN0. Seventeen patients (27.4%) with pT1 tumour incorrectly predicted LN metastasis in 6/236 (2.5%) scans
presented with central LN metastases (pT1a: 7/20 (20.0%) (false positive [FP]). The sensitivity of US was 22.1%,
and pT1b: 10/27 (37.0%)) and 15 patients (24.2%) lateral specificity 96.0%, PPV 76.0%, NPV 68.2%, and accuracy
LN metastases (pT1a: 7/35 (20.0%); pT1b: 8/27 (29.6%)). 69.1%. Data is summarized in Table 2.
Three out of 15 (20.0%) patients with pT1N1b tumours
showed skip lesions, two of them with multifocal micro- DLL and frozen section
carcinomas (pT1am) and one with pT1b tumour.
Furthermore, LN metastases were absent in patients The results of 54/236 (22.9%) positive (TP) and 150/236
with 7/23 (30.4%) pT2 and in 7/20 (35.0%) pT3 (n = 7) (63.6%) negative frozen section samples (TN) were subse-
and 2/13 (15.4%) pT4 tumours. PTC smaller than 40 mm quently confirmed by definitive histological examination.
and limited to the thyroid gland (pT2) equally infiltrated In 32/236 (13.6%) DLLs, the result of frozen section was
the central (pN1a: 34.8%, n = 8) and lateral LNs (pN1b: negative. However, LN metastases were found in the defini-
34.8%, n = 8), while pT3 carcinomas metastasized to the tive histological examination (FN). No false-positive frozen
lateral cervical compartment more frequently (pN1b: section results were found in this analysis. The DLL and
50.0%, n = 10) than to the central cervical compartment frozen section analysis displayed a sensitivity of 62.8% and
(pN1a: 15.0%, n = 3). Tumours with extension into adja- a specificity of 100%. PPV was 100% and NPV was 82.4%.
cent neck structures (pT4) showed metastasis in the cen- The accuracy was 86.4% (Table 2).
tral neck compartment in 1/13 (7.7%) patient and in the
lateral LNs in 10/13 (76.9%) patients, respectively. Comparison of US and DLL

US and DLL showed a significant difference in terms of sen-

Distant metastasis sitivity (p < 0.001), PPV (p = 0.001), NPV (p = 0.002), and
accuracy (p ≤ 0.001) but did not differ in regard to specificity
According to the postoperative radioiodine ablation, (p = 0.039) (Table 2).
whole-body scan distant metastases occurred in three
patients (2.5%; 2/20 [10.0%] patients with pT3 and 1/13 FLND
[7.7%] patient with a pT4 tumour). Distant metastasis
was not observed in patients with pT1 and pT2 tumours. Unilateral and bilateral FLNDs were conducted in 28/236
(11.9%) and 26/236 (11.0%) cases. Fifty percent (14/28) of
the unilateral and 65.4% (17/26) of the bilateral FLNDs were
Preoperative ultrasonography positive in the definitive histological examination. Only 1/13
(7.7%) patient, who underwent bilateral FLND (1/26 [3.8%])
Ultrasonography (US) predicted positive lateral LN in and showed no LN metastases in the definitive histological
25/236 (10.6%) and was negative in 211/236 (89.4%) examination, presented a postoperative complication (hae-
examinations, respectively. In 19/236 (8.1%) US scans, matoma). During unilateral and bilateral FLNDs, medians
lateral LN metastases were histologically confirmed of 21 (range 2–67) and 29 (range 9–87) LNs were removed.
(true positive [TP]) and 144/236 (61.1%) scans were true

Table 2  Results of bilateral LN metastasis US 95% CI DLL 95% CI p value

ultrasound (US) and
bilateral diagnostic lateral True positive, n (%) 19/236 (8.1) 54/236 (22.9) < 0.001
lymphadenectomy (DLL) in
True negative, n (%) 144/236 (61.0) 150/236 (63.6) 0.635
patients
False positive, n (%) 6/236 (2.5) 0 0.040
False negative, n (%) 67/236 (28.4) 32/236 (13.6) < 0.001
Sensitivity 22.1% 0.146–0.319 62.8% 0.522–0.723 < 0.001
Specificity 96.0% 0.915–0.982 100% 0.975–1.000 0.039
PPV 76.0% 0.566–0.885 100% 0.934–1.000 0.001
NPV 68.2% 0.617–0.742 82.4% 0.762–0.873 0.002
Accuracy 69.1% 0.629–0.746 86.4% 0.815–0.902 < 0.001

LN, lymph node; CI, confidence interval; PPV, positive predictive value; NPV, negative predictive value

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Langenbeck's Archives of Surgery (2022) 407:2059–2066 2063

Postoperative complications Discussion

In total, 15 patients (12.7%) showed complications after In the current study, 29/118 (24.6%) patients with central
surgery. (pN1a) and 43/118 (36.4%) patients with lateral (pN1b)
After thyroidectomy and bilateral CND, unilateral paraly- metastases, including 6/118 (5.1%) patients with “skip
sis of the recurrent laryngeal nerve (RLN) was documented lesions”, were documented independent of the pT classifi-
in 7/118 (5.9%) patients (7/236 [3.0%] nerves at risk; uni- cation. Preoperatively, all patients were cN0. Intraoperative
lateral temporary paralysis of the RLN: 6/236 [2.5%] nerves frozen sections and definitive histological reports of diag-
at risk; unilateral permanent paralysis of the RLN: 1/236 nostic bilateral DLL were correlated with the findings of
[0.4%] nerve at risk). Combined with the FLND, no nerve preoperative US. An accurate preoperative evaluation of the
injuries to the accessory, hypoglossal, or vagal nerves, to central and lateral compartment is needed to locate suspi-
branches of the cervical or brachial plexus, or to the sympa- cious lymph nodes, given that prophylactic LN dissection is
thetic trunk were observed. recommended in patients with a high risk of LN metastasis
After DLL, postoperative bleeding or haematoma with [19].
surgical re-intervention were reported in 4/118 (3.4%) US is a non-invasive diagnostic modality that is recom-
patients (4/236 [1.7%] DLLs). Chylous fistula appeared fol- mended in the preoperative work-up of thyroid lesions and
lowing 2/118 (1.7%) DLLs on postoperative days 1 and 7. detection of abnormal LNs in the lateral compartment. How-
In the first patient, the thoracic duct showed an anatomical ever, varying sensitivity (37 to 93%) and specificity rates
variety on its course to the internal jugular vein. The thoracic (79 to 100%) have been reported in the literature and may
duct proceeded dorsally of the common carotid artery to the depend on the size and number of affected nodes [20–22].
middle of the neck, crossed the vagal nerve and the internal The current results demonstrate a lower sensitivity (22.1%),
jugular vein moving parallel down to the venous angle of specificity (96.0%), PPV (76.0%), and NPV (68.2%), indi-
internal jugular and left subclavian vein. In the second case, cating a weakness of US in detecting lateral LN metastasis.
the thoracic duct was injured due to preparation of lymphatic Other authors presented similar sensitivity and specificity
tissue near the upper thoracic outlet. In both cases, the fistu- rates for US diagnosing lateral LN metastasis [23].
las were occluded surgically plugging the leak with parts of In this study, DLL demonstrates a sensitivity of 62.8%,
the omohyoid muscle. Both patients were discharged 2 days specificity 100%, PPV 100%, NPV 82.4%, and accuracy
after re-intervention. 86.4% in identifying lateral LN metastasis. Compared to
After FLND, postoperative bleeding or haematoma with preoperative US, DLL presents significantly superior results.
surgical re-intervention occurred in 2/118 (1.7%) patients Notably, 27/98 (27.6%) patients in this study with negative
(1/28 [3.6%] unilateral FLND; 1/26 [3.8%] bilateral FLND; preoperative US presented with histological LN metastasis
Table 3). in the lateral compartment, emphasizing the importance of
Neither clinically nor sonographically lateral LN recur- DLL in thyroid cancer surgery. When taking the TP and TN
rences were documented during a 5-year follow-up in the rates into account, DLL influenced the extent of lateral neck
118 study patients. surgery in 86.5% of the patients. Therefore, the main advan-
tage of DLL lies in its ability to stage lateral LN metastasis

Table 3  Postoperative complications

CND, n (%) DLL, n (%) FLND unilateral, n (%) FLND bilateral, n (%)

Patients 118 (100) 118 (100) 28/118 (23.7) 13/118 (11.0)

RLN/sides at risk* 236 (100) 236 (100)
No complications 229/236 (97.0) 230/236 (97.5) 27/28 (96.4) 25/26 (96.2)
Overall local complications 7/236 (3.0) 6/236 (2.5) 1/28 (3.6) 1/26 (3.8)
Temporary unilateral VFP 6/236 (2.5) – – –
Permanent unilateral VFP 1/236 (0.4) – – –
Haematoma – 4/236 (1.7) 1/28 (3.6) 1/26 (3.8)
Chylous fistula—neck – 2/118 (1.7) 0/118 0/118

CND, central neck dissection; DLL, diagnostic lateral lymphadenectomy; FLND, functional lateral neck dissection; VFP, vocal fold paralysis;
RLN, recurrent laryngeal nerve
*
Nerves/sides at risk: n = 236

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2064 Langenbeck's Archives of Surgery (2022) 407:2059–2066

not predicted by preoperative US. Only DLL and intraopera- metastasis are located above and below the omohyoid mus-
tive frozen sections allow the planning of adequate lateral cle corresponding to the caudal parts of LN level 3 and cra-
LN surgery. nial parts of LN level 4 [36].
In PTC, prophylactic bilateral CND can lead to com- A therapeutic LN dissection is the fundamental treat-
plete remission of the disease in the central neck in patients ment for clinically evident cervical LN metastasis. Cervical
with clinically occult LN metastasis, reducing the chances LN dissection range from a “berry-picking” approach, in
of recurrence and subsequent morbidity of re-operations. which only grossly involved”, enlarged” LNs are excised, to
It also allows a definitive LN staging to plan further adju- “systematic” en bloc compartment-oriented LN dissection,
vant therapy. CND can be performed with an overall low where one or more LN levels (compartments) are removed.
morbidity [24]. Patients with metastasis in the lateral neck Today, the “berry-picking” approach has become obsolete,
show a poorer prognosis compared to those with metastasis given that in patients with clinically palpable LNs, the
in the central neck or those with no metastasis at all [1, tumour has always metastasized into smaller LNs, thereby
25]. Functional dissection in patients with documented lat- predisposing these patients to recurrent cancer [30, 37].
eral LN metastasis improves survival, given that lateral LN Furthermore, systematic compartment-oriented procedures
metastasis negatively influences overall survival [26, 27]. show a significant less local recurrence rate compared to
The knowledge of the pattern of cervical nodal metastasis the “berry-picking” procedure. There is no definitive evi-
is of great importance, as the central compartment (prelaryn- dence of decreased morbidity after applying this “selective”
geal, pre-/paratracheal, upper mediastinum) is known to be approach [38]. A “berry-picking approach” is only recom-
the first site of lymphatic spread in the majority of patients, mended in cases of local LN recurrence preceding system-
metastasizing next to the ipsilateral lateral compartment atic LN dissection or CND [32].
[28]. Generally, the caudal portion of the lateral compart- In the past decade, proposals for the establishment of
ment is affected more frequently than the cranial portion [29, a diagnostic pathway similar to the sentinel LN mapping
30], implicating that the cervical lymphatic flow is directed (SLNM) in breast cancer, cutaneous melanoma, and other
toward the ipsilateral lower jugular LNs and the venous malignant solid neoplasms in PTC have emerged. The con-
angle. In this study, 72/118 patients (61.0%; pT1–pT4) were cept of SLNM is a less invasive method to evaluate metasta-
identified in whom the PTC had metastasized to the cervical sis in clinically normal LN staging and indicates LN dissec-
LNs (pN1). The current findings emphasize the importance tion only in patients with histologically documented SLNM.
of CND in the initial surgery, given that the predictive value The thyroid gland possesses a rich lymphatic drainage sys-
of US in detecting LN metastases in the central compartment tem. There is an initial horizontal (central) and vertical (lat-
is very low [20, 31]. eral) lymphatic way of metastatic formation in cervical LN
Interestingly, some patients present with metastasis in metastasis. Both ways develop in parallel and the predic-
the lateral compartment without involving the central com- tion of SLNM in the central or lateral neck seems difficult
partment (“skip lesions”) [32]. Forty-three of 72 patients and varies individually. Up to 70% of patients demonstrate
(59.7%) showed lateral LN involvement (pN1b), including a SLN in more than one location. By definition [32], skip
six patients (14.0%) with skip lesions. This rate lies within lesions were revealed as positive SLNM in 14% in the cur-
the range of 4 to 38% of patients documented in the lit- rent analysis. Studies have reported an accuracy of SLNM
erature [8, 33]. This finding is quite relevant, given that in in detecting LN in the central compartment in up to 97%,
the absence of DLL, these patients would have been falsely though only up to 33% in the lateral compartment [39].
classified as pN0 [34, 35]. DLL documented clinically occult The presence of cervical LN metastasis seems to be the
“skip lesions” in all patients. most significant prognostic factor for patients with PTC.
In terms of the surgical strategy applied in this study, Locoregional recurrences tend to occur more often in
CND and bilateral DLL are always performed prophylacti- patients with LN metastases and result in poor prognosis
cally [15], followed by FLND only in the case that positive and decreased survival. Studies have indicated an age > 45
lateral LN metastasis is diagnosed by frozen section dur- and an increasing primary tumour size as further independ-
ing initial surgery for PTC [16, 17]. CND demonstrates an ent factors predicting worse prognosis, whereas gender, mul-
overall low rate of morbidity and is recommended in various tifocality, and operative strategy did not reach prognostic
international guidelines [24]. Bilateral DLL is performed significance [16, 17, 40, 41].
using the typical transverse skin incision without additional Respecting the results of TP and TN rates, DLL influ-
extension and poses no additional risk when conducted in enced the extent of lateral neck surgery in 86.5% of the
combination with initial thyroidectomy and CND. Moreo- patients. Therefore, the main benefit of DLL is the possibil-
ver, DLL and the subsequent frozen section examination ity to stage lateral LN metastasis not predicted by preopera-
are important tools in the intraoperative staging of PTC. tive US. Only DLL and intraoperative frozen sections allow
In the case of lateral LN involvement, the majority of LN the planning of an adequate lateral LN surgery.

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Langenbeck's Archives of Surgery (2022) 407:2059–2066 2065

DLL did not significantly increase the risk for postop- Declarations
erative complications when performed in addition to initial
(total) thyroidectomy and CND. In the current study, the Conflict of interest The authors declare no competing interests.
overall complication rate was 2.5%, including one patient
with local haematoma and two others with a chylous fistula Open Access This article is licensed under a Creative Commons Attri-
bution 4.0 International License, which permits use, sharing, adapta-
(2/118 [1.7%]). The reason for these uncharacteristic com- tion, distribution and reproduction in any medium or format, as long
plications was, on the one hand, an anatomical variety of the as you give appropriate credit to the original author(s) and the source,
thoracic duct, and, on the other hand, a dissection of the lym- provide a link to the Creative Commons licence, and indicate if changes
were made. The images or other third party material in this article are
phatic tissue too close to the confluence of the thoracic duct
included in the article’s Creative Commons licence, unless indicated
into the internal jugular vein in the upper thoracic outlet (not otherwise in a credit line to the material. If material is not included in
the typical region of DDL). The risk for such complications the article’s Creative Commons licence and your intended use is not
can be minimized with an even more meticulous prepara- permitted by statutory regulation or exceeds the permitted use, you will
need to obtain permission directly from the copyright holder. To view a
tion. Other authors have reported a similar complication rate
copy of this licence, visit http://​creat​iveco​mmons.​org/​licen​ses/​by/4.​0/.
in patients undergoing thyroidectomy in combination with
CND, indicating that DLL does not necessarily increase the
risk for postoperative compilations [42]. Furthermore, DLL
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Vienna.

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