10.14639/0392-100X-N2761
Objectives. In carotid paraganglioma surgery, magnification is crucial to properly evaluate the anatomical relationships between mass, carotid wall, cranial nerves, tumour vascular supply and fascial envelope. The aims of this study are to describe the microsurgical technique, along with the underlying microsurgical anatomy, and to assess outcomes in terms of disease control, complications and functional results. Methods. Twenty-six patients, accounting for 29 carotid paragangliomas, treated with microsurgery by the same senior surgeon over a 35-year period, were included. Results. No carotid injury requiring repair, nor peri- or post-operative stroke occurred in this series. No surgical injury of the main trunk of VII to XII cranial nerves occurred. Complete excision was obtained in all cases and no recurrence was observed during follow-up. Conclusions. The small study size and its retrospective nature suggests caution; however, our results show that microsurgery can allow a safe and precise dissection of the carotids and nerves.
text/xml
1827-675X
2761
en
Elisabetta Zanoletti
http://creativecommons.org/licenses/by-nc-nd/4.0
ACTA Otorhinolaryngologica Italica
surgical technique
Microsurgery in carotid body paraganglioma
Text.Serial.Journal
https://www.actaitalica.it/
44
Head and neck
2024-04-22
2023-09-24
2024-04-23
2024-04-23
76-82
1
Elisabetta Zanoletti
2024/04/22
10.14639/0392-100X-N2761
76
Otolaryngology Section, Department of Neuroscience DNS, University of Padua, Padua, Italy. Corrisponding author - elisabetta.zanoletti@unipd.it
1827-675X
surgical technique
en
82
Microsurgery in carotid body paraganglioma
https://www.actaitalica.it/article/download/2761/1085
44
ACTA OTORHINOLARYNGOLOGICA ITALICA 2024;44:76-82; doi: 10.14639/0392-100X-N2761




Head and neck


Microsurgery in carotid body paraganglioma
Antonio Mazzoni1, Leonardo Franz1,2, Elisabetta Zanoletti1
1
 Otolaryngology Section, Department of Neuroscience DNS, University of Padua, Padua, Italy; 2 Phoniatrics and Audiology Section,
Department of Neuroscience DNS, University of Padua, Treviso, Italy


SUMMARY
Objectives. In carotid paraganglioma surgery, magnification is crucial to properly evaluate
the anatomical relationships between mass, carotid wall, cranial nerves, tumour vascular
supply and fascial envelope. The aims of this study are to describe the microsurgical tech-
nique, along with the underlying microsurgical anatomy, and to assess outcomes in terms
of disease control, complications and functional results.
Methods. Twenty-six patients, accounting for 29 carotid paragangliomas, treated with mi-
crosurgery by the same senior surgeon over a 35-year period, were included.
Results. No carotid injury requiring repair, nor peri- or post-operative stroke occurred in
this series. No surgical injury of the main trunk of VII to XII cranial nerves occurred. Com-
plete excision was obtained in all cases and no recurrence was observed during follow-up.
Conclusions. The small study size and its retrospective nature suggests caution; however,
our results show that microsurgery can allow a safe and precise dissection of the carotids
and nerves.
KEY WORDS: carotid paraganglioma, microsurgery, carotid body, surgical anatomy,
surgical technique



Introduction
Carotid paraganglioma is a rare tumour accounting for 0.6% of head and neck
tumours and 65% of head and neck paragangliomas 1-3, which originates from
the paraganglia, a cluster of neuroendocrine cells, located on the postero-
medial side of the common carotid bifurcation 4,5. Treatment choices include
surgical excision, radiation therapy, or a conservative wait and see approach,                  Received: September 23, 2023
depending on parameters such as patient’s age, comorbidities, surgical risk,                    Accepted: November 4, 2023
size of the tumour, tumour extension, localisation, and multicentricity 6.
                                                                                                Correspondence
Surgical excision currently represents the only option for definitive treatment 7.              Elisabetta Zanoletti
However, surgery is challenging and faces two major technical issues, separa-                   E-mail: elisabetta.zanoletti@unipd.it
tion of the tumour from the carotid wall and preservation of the cranial nerves,
which are directly related to the functional outcome. Surgical resection can be                   How to cite this article: Mazzoni A,
associated with important morbidities, including massive bleeding, periopera-                     Franz L, Zanoletti E. Microsurgery in ca-
                                                                                                  rotid body paraganglioma. Acta Otorhi-
tive stroke and nerve loss 3,8-12.                                                                nolaryngol Ital 2024;44:76-82. https://doi.
Performing a safe and effective surgical approach to carotid paragangliomas                       org/10.14639/0392-100X-N2761
involves a thorough understanding of the anatomical relationship between the
                                                                                                © Società Italiana di Otorinolaringoiatria
carotid adventitia, tumour, cranial nerves and the fascial apparatus wrapping                   e Chirurgia Cervico-Facciale
around the tumour-carotid complex. The paraganglion lies on the carotid wall
adventitia, under the cervical fascial sheet that individually invests carotids,                               OPEN ACCESS
internal jugular vein, and vagal nerve 13,14. The tumour originates from the                    This is an open access article distributed in accordance with
                                                                                                the CC-BY-NC-ND (Creative Commons Attribution-Non-
paraganglion and grows on the wall of the artery. It appears as a unique mass                   Commercial-NoDerivatives 4.0 International) license. The
with the carotids, as the cervical fascia invests both tumour and carotid arter-                article can be used by giving appropriate credit and mentio-
                                                                                                ning the license, but only for non-commercial purposes and
ies in a single envelop and often fuses with the deep cervical fascia on the tu-                only in the original version. For further information: https://
mour’s posterior side. Here it is thick and highly vascular, as it carries most of              creativecommons.org/licenses/by-nc-nd/4.0/deed.en




76
                                                                                               Carotid paraganglioma microsurgery




the blood supply to the tumour. The carotids have a simple      sification was confirmed intra-operatively. When there was
contact with the tumour, but, as the latter grows, they be-     a discrepancy between the pre- and intraoperative appear-
come lodged in a groove on the tumour. Growth and depth         ance, Shamblin’s class was assigned according to intraop-
of the groove increase simultaneously up to the point that      erative findings. Genetic assessment was systematically
the groove borders fuse around the artery and, through fur-     performed on each patient since 2005, and 68Ga-DOTA-
ther growth and fusion, they achieve complete encasement.       TATE PET imaging was added, to rule out multiple or me-
A thin layer of loose connective tissue remains between         tachronous tumours.
tumour and artery. The blood supply is simple and obvi-         A clinical evaluation of cranial nerves VII to XII was per-
ous in a small tumour, while it remains basically the same,     formed in each case. No patient underwent preoperative
but richer, in a large tumour. In a small tumour there are      tumour embolisation of a carotid tumour.
two hila. The lower one carries the glomic artery originat-     The clinical outcomes considered were disease control (in-
ing from the dorsal aspect of the carotid bifurcation and       cluding local recurrence and distant metastasis) and post-
running across connective tissue it ramifies to the tumour’s    operative complications including early/late death, stroke,
lower pole 15,16. The cranial pole of the tumour receives       newly onset permanent cranial nerves loss, Horner’s syn-
branches from the ascending pharyngeal and external ca-         drome, bleeding and cervical haematoma.
rotid artery 15. As the tumour grows cranially, the superior    Clinical and radiological follow-up was scheduled as fol-
vessels take on most of the blood supply. These vessels         lows: clinical examination and head and neck contrast-en-
reach the dorsal and, to a lesser extent, medial aspects of     hanced MRI every year for the first five years, then every
the tumour, ramifying on the fascial surface and thereby        two years until the 10th year for sporadic tumours, then
entering the tumour. In large tumours, such a distribution      every 5 years during the following years for familial or
of tumour vessels on the fascial layer may be visualised at     syndromic cases 19. In these latter cases of familial or mul-
imaging as a thick, contrast enhanced, hyper-vascular halo.     tiple tumours, follow-up was completed with chest x-ray,
Intra-operatively, the use of magnification tools is key to     contrast-enhanced total-body CT scan and, more recently,
properly evaluate the complex anatomical relationships be-      68
                                                                   Ga-DOTATATE PET.
tween tumour, carotid wall, cranial nerves, tumour vascular     Follow-up ranged from 2 to 23 years, mean 11 years. All
supply and fascial envelope. Recently, a few reports regard-    but one case had more than 5 years of follow-up.
ing the use of microsurgical dissection in carotid paragan-
glioma have appeared in the literature, a single case report    Surgical technique
by Ceccato et al. 2019 17, and a series of 31 cases by Degol-   Several microsurgical steps of resection were common in
lado-García et al. 18. However, a thorough discussion of the    head and neck paragangliomas. Our experience, gained
technical issues and anatomical considerations related to       with tympano-jugular (TJ) paraganglioma (156 surgical
the microsurgical approach to carotid paraganglioma is still    cases with concomitant internal carotid artery involve-
needed.                                                         ment), was applied to the present series of carotid body
The aims of this study are: i) to describe the microsurgical    paraganglioma.
technique, along with the underlying microsurgical anato-       The surgical microscope was set up with a 250 mm front
my; ii) to assess the outcomes in terms of disease control,     lens. The microsurgical instrumentation included a Freer-
complications and functional results.                           type elevator with semi-sharp straight and curved ends, bi-
                                                                polar coagulation forceps and two-way suction-irrigation
                                                                tubes (Fig. 1).
Materials and methods                                           The patient was positioned supine, with the head contralat-
Patients                                                        erally turned by 30°. Level II-III cervical lymph nodes
A cohort of 26 patients, accounting for 29 consecutive ca-      were removed to rule out the presence of metastasis. Ini-
rotid paragangliomas, was selected out of the overall se-       tial steps involved skin incision on the sternocleidomastoid
ries of 228 cases of head and neck paragangliomas (175          area, raising of the skin-platysma flap, exposure of carotid
jugular, 29 carotid and 24 vagal paragangliomas), that were     arteries, internal jugular vein and cranial nerves X to XII,
surgically treated by the same senior surgeon (AM) over a       as well as facial nerve main trunk in the case of a high-ly-
35-year period (1985 to 2020).                                  ing tumour. If in contact with the tumour, the vagal and
Each patient had undergone preoperative imaging with            hypoglossal nerves were separated, and their fascial sheet
contrast-enhanced CT and, since 1990, with gadolinium-          preserved.
enhanced MRI. Tumours were radiologically classified            Resection of the carotid paraganglioma involved opening
according to Shamblin’s classes, and imaging-based clas-        the common fascia (tumour-carotid fascia), dissecting fas-



                                                                                                                             77
A. Mazzoni et al.




                                                                        A      A                                         B




                                                                        B




                                                                              Figure 2. Pre-operative MRI of a left-sided carotid body tumour: A) contrast
                                                                              enhanced axial T1 sequence (arrow: external carotid artery; arrowhead: inter-
                                                                        C     nal carotid artery); B) axial T2 sequence (arrow: external carotid artery; arrow-
                                                                              head: internal carotid artery).

Figure 1. Microsurgical instrumentation: A) bipolar coagulation forceps; B)
Freer-type elevators with semi-sharp straight and curved ends; C) two-way
suction-irrigation tube.


cia from tumour, dissecting tumour from carotid(s), dis-                       A                                        B
secting lower pole of tumour from carotid bifurcation and
coagulating the glomic artery. In detail, the surgical proce-
dure was performed as follows.
Figures 2 and 3 show an exemplary case, describing surgi-
cal details.
The body of the tumour-carotid complex, along with its                        C                                         D
common fascia envelop (Fig. 3A), was exposed on its an-
terior, medial, and lateral sides. The superior pole of the
tumour, previously freed from the hypoglossal nerve, was
followed up to the transition to the dorsal side. In Sham-
blin 2-3 paragangliomas, while dissecting the dorsal side of                   E                                        F
the tumour, a thick, tight, highly vascularised tissue can be
encountered and dissected, as allowed by a safe carotid re-
traction manoeuver. Sometimes such a dissection might be
stopped and left for a later step. The vessels branching on
the exposed surface of the common fascia were coagulated.
The anterior side of the fascia was opened vertically (Fig. 3B)               G                                         H
and the cleavage plane between fascia and tumour was de-
veloped with further coagulation on bleeding spots between
fascia and tumour. Intra-fascial dissection reached the inter-
nal (Fig. 3C,D) and external (Fig. 3E) carotids, where the tu-
mour-artery interface was clearly visible. This interface was
dissected with the Freer elevator in a cranio-caudal direction,               Figure 3. Surgical steps of carotid dissection from paraganglioma (PGL)
also along its dorsal aspect (Fig. 3F), and stopped at the tu-                (same case of left-sided carotid body tumour): A) initial view of the tumuor
mour’s lower pole to avoid injury to the glomic artery. Dis-                  (T), enveloped by common tumour-carotid fascia (IC: internal carotid; V: vagus
                                                                              nerve); B) opening of common fascia (*common fascia; T: tumour); C) elevator
secting the lower pole of the tumour at the carotid bifurcation               on tumour-carotid interface; D) internal carotid artery freed from tumour on
may be a difficult step of resection due to the risk of bleeding              antero-lateral aspect; E) dissection of external carotid (EC) completes separa-
and lack of a landmark of the glomic artery. Bleeding may                     tion of the ventral part of tumour; F) dorsal aspect of internal carotid freed from
                                                                              tumour (T: tumour; IC: internal carotid; V: vagus nerve); G) blood spilling from
arise from the supplying arteries on the tumour’s posterior
                                                                              origin of glomic artery on the posterior wall of carotid bifurcation, where the
side as well as the glomic artery. Cranial displacement of the                common carotid (CC) divides into external (EC) and internal carotid (IC) arteries;
freed tumour, to reach the glomic artery, involved the risk of                H) the same after bipolar coagulation.



78
                                                                                                    Carotid paraganglioma microsurgery




tearing its origin, thus causing a carotid fenestration. Bipo-     accounting for 29 carotid paragangliomas were included in
lar coagulation was feasible, as the adventitia was preserved      this study. All cases were treated with microsurgical excision.
(Fig. 3G,H). A better option was to gain a good control of         Of the 29 paragangliomas, 11 tumours were unilateral, while
the glomic artery root area by fully freeing both carotids.        18 in 14 patients were multiple, either unilateral or bilateral
Gently retracting external carotid and tumour revealed the         tumours. Three patients, belonging to the same family (two fe-
tumour-carotid interface and allowed dissecting strictly on        males and one male), suffered from familial paragangliomato-
the tumour surface. Once the lower pole had been dissected,        sis, with bilateral or multiple unilateral tumours. One case had
the tumour could be separated on its dorsal side all along the     bilateral carotid paragangliomas (surgically treated on both
thick, vascular fascia, which was sometimes fused with the         sides), and a concomitant vagal one (which was followed-up).
deep cervical fascia.                                              The other case had a carotid paraganglioma, which was
Resecting Shamblin 3 paragangliomas involved similar but           surgically treated, and a concomitant carotid and vagal par-
more extensive steps, except for the technique to free the         aganglioma on the other side, which was observed.
carotids from the preoperatively assessed encasement. Af-          The third case of the family, not enrolled in the present sur-
ter haemostasis on the common fascia and its opening, the          gical series, was a right carotid paraganglioma (PGL) op-
dissection proceeded towards either the cranial or caudal          erated on with artery removal in another institution, and a
pole of the tumour encasement, where the carotid entered           right operated vagal tumour. A right TJ PGL was observed
the tumour. There, the curved dissector was run into the           and treated with radiation therapy at the other institution,
tumour-artery interface and lifted off the tumour by a few         as well as a right vocal cord PGL. Left vagal and carotid
millimeters. The dissected bridge of the tumour was then           paraganglioma were observed and followed.
coagulated and cut. The separation-coagulation-section             Tumours were classified as follows: 9 cases Shamblin 1
manoeuver was performed in several steps until the encase-         (30%), 17 Shamblin 2 (59%), and 3 Shamblin 3 (11%).
ment had been completely opened. The tumour was thus               Three cases were preoperatively over-staged class 3, but
opened in two halves carrying the artery in a groove, from         were intraoperatively assessed as 2, because the carotid ar-
which it could be lifted.                                          tery was only partially encased by the tumour and a thick,
Cleavage between tumour and the carotid was done care-             hyper-vascular fascia connected the two close edges of the
fully across the thin connective layers with respect to the        tumour simulating complete encasement. In one case of
artery adventitia. The bleeding spots encountered at this          multiple unilateral paraganglioma (tympano-jugular, ca-
level belonged to the tumour, rather than to the artery,           rotid and vagal PGLs, that appeared as a single mass pre-
except for the glomic artery that was handled as reported          operatively), a lymph node micrometastasis was evident at
above. The condition of “encasement” occurred both par-            frozen sections and confirmed at definitive pathology. The
tially and totally in different areas of the tumour.               tumours were removed in a single procedure. This patient
The external carotid artery was managed with the same              died without evidence of disease after 20 years of follow-
technique as for the internal. In the case of a tumour im-         up. No genetic test was available at the time.
pacting on the cranial base, the microscopic cervico-parotid
approach allowed control of the upper aspect of the tumour,        Clinical and functional results
as well as the carotid and jugular foramina at the skull base.     No major intra- or peri-operative events were recorded. No
Wide variations on fasciae, connective tissue and vascula-         carotid injury requiring repair and no peri- or postoperative
ture were observed and related both to tumour size and to          stroke occurred in this series. The tumour resection time
individual cases. Cleavage planes, as well as fasciae, were        ranged from 30 minutes in Shamblin 1 to 180 minutes in
thick or thin, tight or loose, strong or weak. However, in         Shamblin III cases.
every condition, reaching a cleavage was crucial for a safe        No surgical injury or postoperative-onset functional damage
resection. The variable tumour impact along the dissection         of the main trunk of VII to XII cranial nerves occurred except
planes and at the carotids interface, especially in Shamblin       for the lateral branch of the superior laryngeal nerve of the
3, required flexibility in the order of operative steps so as to   vagal and the descending branch of the hypoglossal, which
perform the carotid dissection in the most favourable con-         were injured or at risk of undetected injury, in Shamblin 2 and
ditions and with the least injury.                                 3. Complete excision was obtained in 100% of the cases and
                                                                   no recurrence was observed during follow-up in this cohort.
Results
Study population
                                                                   Discussion
A total of 26 consecutive patients (11 males, and 15 females),     Surgery of carotid body paragangliomas involves potential



                                                                                                                                  79
A. Mazzoni et al.




risks of intra-, peri-, and post-operative complications. The     Handling of the hypertrophic, hyper-vascular fascia invest-
most frequently reported are stroke and new cranial nerve         ing the complex tumour-carotid was a crucial step. It in-
losses. In a systematic review on carotid PGL surgery, Su-        volved the preliminary exposure of the full tumour body
arez et al. 9 examined 2175 cases in 67 articles with 26%         from the lateral to the posterior side, coagulation of the ves-
Shamblin 1, 44% Shamblin 2 and 30% Shamblin 3 cases.              sels all along the fascial surface and, after opening of the
In the high classes, the common or internal carotid was re-       fascial envelop with intra-fascial dissection, the bleeders on
sected in 12.5% of cases due to injury or difficult dissec-       the fascia-tumour interface. This allowed both an ischae-
tion and was reconstructed in 9.7%. Peri- or post-operative       mic tumour and a clear view of the transition area between
stroke with permanent sequelae occurred in 3%, and new            tumour and carotid. Separation of the carotid by a semi-
postoperative permanent cranial nerve loss in 22.2%. In           sharp dissector was also safely performed in Shamblin 3
a review with meta-analysis on 4743 cases, Robertson et           cases, but in these larger tumours more evidence is required
al.8 reported 2.3% of 30-day stroke-death for carotid inju-       to assess whether the microsurgical technique is effective
ry, 30-day stroke of 3.5% and death-stroke rate of 4.1%.          and uneventful as shown in smaller tumours. Microsurgery
The rate was lower for Shamblin 1 and increased with the          on large tumours such as Shamblin 2-3 classes reported in
higher classes. New postoperative cranial nerve losses were       the literature 17-19 and in our series amount to a total of 50
associated to increasing Shamblin class, with an overall          cases with favourable results.
rate of 11.1%. By decreasing rate, the hypoglossal, vagal,        The issue of timing of surgery in multiple carotid PGL
sympathetic, glossopharyngeal, accessory, and facial were         is still debated. Factors influencing the choice are patient
the affected nerves. Although the overall trend in risk of        age, comorbidities, life expectancy, genetics, vagal nerve
complication has shown a continuous decrease during the           function, PGL size and Shamblin class, as well as carotid
past decades, a small, but non-negligible, residual risk still    atherosclerosis. Our current strategy prioritises the chance
remains 20,21. Robertson et al. 8 outlined the possibility that   of recovery, preventing neurovascular injuries at the same
the current risk of complication might be underestimated          time. In bilateral carotid tumours, the Shamblin 1 tumour
due to a possible publication bias, in terms of not report-       is removed first, shortly followed by removal of the larger
ing poor outcomes. The postoperative course of our series         tumour.
was uneventful. No carotid artery complications, in terms         In bilateral Shamblin 2-3, the smaller tumour is removed first.
of stroke, arterial injury requiring repair, graft, or bypass,    In equal sized tumours, there is no general criterion. Multiple
were encountered. Separation of the cranial nerves from the       unilateral lesions are removed in the same procedure.
tumour was also uneventful, except for the lateral branch of      Two aspects deserve mention, the handling of the tumour’s
the superior laryngeal nerve of the vagal and the descend-        lower pole and stenting of the carotid artery. The lower pole
ing branch of the hypoglossal in Shamblin 2 and 3 cases. To       impacting on carotid bifurcation involved an exacting dis-
better characterise outcomes and the safety profile of our        section in a large tumour due to a combination of such fac-
microsurgical technique, a larger prospective series with         tors as adhesion, glomic artery and bleeding from arteries
more cases is needed. Nonetheless, it may be reasonable           of the tumour’s posterior aspect. Injury of the carotid artery
to hypothesise that, applying the same microsurgical prin-        was also a risk despite the dissection steps suggested above
ciples to the neck employed in other surgical fields, such as     and implied vascular expertise for repair. Stenting the in-
the skull base, a safer handling of vessels and connective        ternal carotid artery 26,27 never came into question, since the
tissue interfaces might be achieved by using microsurgery.        compensatory mechanism was pre-operatively assessed,
In this sense, our preliminary results seem to be promising,      and the artery’s sacrifice was to be left to intraoperative ad-
outlining good disease control and a very favourable safety       verse circumstances that did not occur. The absence of clin-
profile.                                                          ically evident complications does not exclude the need to
Microsurgery on carotid PGL was initiated by our group            preoperatively assess both the efficacy of the compensatory
years after operating on jugular 22-24 and vagal PGL 25 ap-       intracranial circle with the balloon occlusion test (BOT)
plying in the neck the same principles of dissection on           and the condition of the vessel wall. Stenting is prescribed
tumour, vessels and nerves, haemostasis with bipolar co-          if BOT is positive 26,27. If BOT is negative, our experience
agulation under suction-irrigation, periadventitial carotid       suggests that the carotid is left unstented and to be repaired
dissection (which is different from the frequently reported       or closed in the infrequent, exceptional case of injury. Dis-
sub-adventitial dissection) and development of a tumour-          secting tumour from carotid involves mechanical trauma
carotid interface. Preservation of the adventitia allowed the     to the artery wall with the inherent, potential morbidity of
carotid root of the glomic artery to be coagulated when the       a thrombo-embolic event, especially in the atheromatous
latter was torn off the common carotid.                           vessel. Preoperative assessment of the artery condition is



80
                                                                                                        Carotid paraganglioma microsurgery




mandatory, and the uneventful management of the carotid          All patients signed an informed consent form regarding
remains a prior concern.                                         the processing and publication of their data, which were
                                                                 examined in agreement with the Italian privacy and sensi-
Conclusions                                                      tive data laws, and the internal regulations of the University
                                                                 Hospital of Padua.
Our microsurgical approach to carotid PGL developed
from the experience gained in the PGL of the jugular fora-
men extending to the neck and the vagal PGL. The crucial
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