Abstract
Objective:
The current surgical trend in the treatment of pleomorphic adenomas of the parotid gland is to limit the extent of resection. This raises the need to correctly identify the mass within the normal parenchyma so as to avoid dissecting the entire superficial lobe of the gland. We describe ultrasound-guided tattooing as a technique to facilitate identification and excision of parotid pleomorphic adenomas.
Methods:
We reviewed 23 consecutive patients with pleomorphic adenoma of the parotid gland. All patients underwent ultrasound-guided tattooing of the lesions with a charcoal suspension. Baseline tumor and patients’ characteristics, major and minor complications, and subjective tolerance to the procedure were recorded. We assessed the number of intralesionally marked masses and the percentage of intraoperatively detected marked lesions.
Results:
The injection was well tolerated. No major complications were recorded. In 2 cases (9%), a transient increase in lesion size was observed. No other minor complications were encountered. Charcoal was found inside the tumor in 19 cases (83%). In 4 cases (17%), it was found in the tissues above the lesion. Twenty-three lesions were intraoperatively detected (100%) and dissected.
Conclusion:
Charcoal suspension tattooing is safe and well tolerated for the detection of small pleomorphic adenomas during parotid surgery.
Introduction
Tumors of the parotid gland account for 0.6% of all neoplasms and for 3% of all head and neck tumors. 1 Eighty percent of parotid neoplasms are benign, and among them, pleomorphic adenoma (PA) is the histologic entity with the highest incidence (60%-70%) followed by cystoadenolymphoma (15%) and other less frequent histological types.2,3
The diagnosis is based on fine-needle aspiration cytology (FNAC), even though the value of the technique is still controversial. The specificity of FNAC for the diagnosis of neoplasia (0.98) and malignancy (0.96) is high while its sensitivity is lower and more variable (0.96 and 0.76, respectively). 4
The treatment of choice for PA is surgery. The goal of surgical treatment is complete removal of the neoplastic mass to prevent tumor growth and recurrence, with minimal risk of facial nerve injuries. 5
The most appropriate surgery for PA of the parotid has been the subject of controversial discussions for decades. In the past, surgeons were more concerned about facial nerve injury than about recurrences. Therefore, they tended to operate only on or within the tumor capsule. Procedures included intracapsular enucleation, namely, breaching the tumor capsule and removing the tumor from within, or extracapsular enucleation, namely, enucleation at the level of the loose connective tissue between the tumor and the adjacent parotid. Recurrence rates after enucleation were, however, high, ranging from 20% to 45%. 6 Studies demonstrate that a high percentage of PAs shows focal absence of the capsule and the formation of satellite nodules from the tumor growing through capsular breaches and/or from capsular penetration.7,8 During enucleation, these satellite nodules may escape unnoticed and be left behind. 9
More extensive surgery such as total parotidectomy (TP), especially for deep lobe masses, or superficial parotidectomy (SP) therefore became widespread.10,11 Both TP and SP require dissection of the full facial nerve. Whereas TP removes the parotid tissue lateral and medial to the nerve, SP removes the parotid tissue lateral to it. Recurrence rates of PA fell, settling at a current rate of approximately 2%, while the number of complications increased. 12 The main complication is facial nerve dysfunction. Temporary facial nerve paralysis occurs in 38.4% of TP and 25.6% of SP, while permanent facial nerve injuries follow 3.1% of TP and 7% of SP. 13 Another complication is Frey’s syndrome. Clinically manifest Frey’s syndrome is seen in 2% to 40% patients after TP and SP.13,14
Because of the frequency of complications following surgery for a benign condition, surgeons questioned the need to remove the entire parotid gland or superficial lobe, putting the facial nerve at risk. Less extensive surgery was therefore reappraised as an alternative to minimize the morbidity of parotidectomy and reduce operating room time. Partial superficial parotidectomy (PSP) consists of dissecting less than the full facial nerve and removing the tumor along with 2 cm of healthy parotid tissue. 15 In extracapsular dissection (ECD), a 2 to 3 mm cuff of normal parotid tissue is removed with the tumor and the facial nerve is not dissected at all. 16 Many authors state that PSP and ECD have lower rates of complications without oncological compromise. Indeed, recurrence amounts to 1.8% after TP, 2.6% after SP, 3% after PSP, and 2.6% after ECD.17,18 A meta-analysis has confirmed that the incidence of permanent or transient facial nerve dysfunction is 1.2% and 11% with ECD and 0.2% and 18% with PSP, respectively. 19 Furthermore, it has been demonstrated that Frey’s syndrome and sensory impairment due to section of the auricular nerve are strictly correlated to the extent of surgery. 20 Recently, attention has focused on ECD, with many authors considering this procedure to be an effective alternative in the surgical treatment of PA.21,22 On the other hand, ECD is a minimal-margin surgery that in novice or occasional parotid surgeons may result in higher recurrence rates. 9
The trend to reduce the surgical field and limit resection of parotid tissue to a minimum raises the need to correctly locate the mass within the normal parotid parenchyma, so as to avoid dissecting the entire superficial lobe. This could be a challenge for surgeons, especially in the case of small and less consistent tumors.
Charcoal suspension has been used for years for ultrasound (US)-guided tattooing of nonpalpable breast cancer or before induction therapy.23,24 In recent years, its use has expanded to other anatomical regions such as the gastrointestinal tract and the neck.25-27 We describe US-guided tattooing of small parotid tumors with charcoal suspension as a technique to facilitate the localization of parotid masses and guide the surgeon intraoperatively.
Methods
Patient Selection
We retrospectively assessed 23 consecutive patients who underwent US-guided tattooing by injection of a charcoal suspension for PA of the parotid gland from March to November 2014. The study included 15 men and 8 women, ranging in age from 45 to 79 years (mean age, 69 years). All patients underwent US-guided FNAC before surgery, and only patients with PA undergoing the first surgical procedure were evaluated for the study. Preoperative cytology revealed PA in 21 cases, an adenoma NOS (not otherwise specified) in 1 case and a hypercellular pleomorphic adenoma in 1 case. We also registered the body mass index (BMI) and the circumference of the neck of each patient, measured by a tape measure at the superior border of the hyoid bone. Patient demographics and baseline characteristics of patients and tumors are summarized in Table 1. Informed consent to surgery was obtained from all patients, and the study was approved by the local Ethics Committee.
Baseline Characteristics of Patients Undergoing Ultrasound-Guided Charcoal Tattooing.
Ultrasound-Guided Tattoo Procedure
Charcoal was used as the tattooing material. Vials containing 100 mg of sterilized vegetable charcoal were prepared by the Pharmaceutical Services Department of our institution. The charcoal was diluted by a dedicated nurse with 7 ml of sterilized normal saline just before injection and aspirated with a 10 mL-syringe and a 21-gauge needle. Approximately 1 to 2 mL of charcoal suspension was discarded before injection to ensure adequate flow. No local anesthesia was needed. The lesion was identified under US guidance, and the charcoal tattoo was performed by an experienced radiologist. When the tip of the needle was located into the lesion, 1 to 2.5 mL of charcoal suspension (depending on tumor diameter and US appearance) was slowly injected. The tumor’s largest diameter, depth from skin surface, and location within the parotid parenchyma were recorded.
Assessment of Safety and Reliability of US-Guided Tattoo Localization
Patients were directly asked about their subjective tolerance of the procedure. To assess the safety of charcoal tattooing, we defined procedure-related major complications as those that, if untreated, could lead to death, major morbidity, or hospitalization. All other complications such as persistent pain, bleeding, increased lesion size, transient or permanent facial paralysis, charcoal marking of the skin, or inflammatory reaction was considered minor.
Reliability of the technique was evaluated in terms of the technical success rate, defined as successful localization of the charcoal markings inside the tumor mass, and technique success rate, defined as the percentage of marked lesions detected intraoperatively.
Surgeons were asked to register whether the lumps were intraoperatively palpable or not.
Results
The characteristics of the tumors prior to surgery and the types of surgical procedures are summarized in Table 2.
Preoperative Ultrasound-Guided Tattooing Localization and Surgery.
Abbreviations: ECD, extracapsular dissection; PSP, partial superficial parotidectomy; SP, superficial parotidectomy.
The choice of surgical procedure was made on the basis of lesion size and the surgeon’s preference.
Preoperative injection was well tolerated in all cases; all patients complained of the same slight discomfort as felt during FNAC, which they had all undergone previously.
No major procedure-related complications were encountered. There were no instances of bleeding or persistent pain. In 2 cases (9%), a minimal transient increase in lesion size was observed, lasting less than 24 hours and described as unpleasant by patients. No facial nerve deficit, either transient or permanent, was detected. No inflammatory reaction was observed at the site of injection (Table 3).
Safety and Reliability of Ultrasound-Guided Charcoal Tattooing Localization in 23 Patients.
Twenty-three marked lesions were detected intraoperatively and dissected (100%). Definitive histology on the surgical specimen was consistent with preoperative cytology in 21 out of 23 cases. In 1 case, an adenoma NOS was better defined as a basal cell adenoma, and in 1 case, atypical cells were found.
The injected charcoal was detected intraoperatively in all cases. In 19 patients, it was inside the lesion (technical success rate, 83%). In 4 cases (17%), the charcoal suspension was found in the tissues above the lesion (Table 3).
In 4 cases, the lesion was defined as intraoperatively nonpalpable by surgeons. Characteristics of patients and tumor in nonpalpable lesions are resumed in Tables 4 and 5.
Number of Intraoperatively Nonpalpable Lesions According to Tumor Dimension and Body Mass Index.
Number of Intraoperatively Nonpalpable Lesions According to Tumor Dimension and Neck Circumference.
Discussion
Surgery remains the gold standard treatment for parotid tumors, both benign and malignant. The 2 primary goals of this type of surgery are complete removal of the tumor and functional preservation of the facial nerve. In particular, surgeons should ensure complete tumor removal to prevent recurrences, which are more difficult to cure and involve a greater risk of facial nerve injuries. 28 A variety of surgical techniques exists and has been the subject of controversial discussion for decades. Proponents of the standardized surgical techniques of SP or TP base their arguments on the supposed increased number of recurrences after less invasive procedures.29,30 Those who are in favor of ECD argue that this approach is associated with lower rates of postoperative complications, in particular a lower risk of facial nerve dysfunction.12-31
Charcoal suspension has been used for more than 15 years in breast cancer. The suspension was initially tested for safety and efficacy in mice 32 and then widely employed to mark nonpalpable breast cancer or cancer undergoing neoadjuvant chemotherapy prior to surgery. Charcoal suspension has limited diffusion capacity, can remain as a tattoo for several days, and the procedure is safe and well tolerated. 23 Studies have reported that charcoal has been found in or near the tumor in 94% of cases after chemotherapy. 24
In recent years, charcoal has also been employed in colorectal cancer to mark small colorectal lesions or the area of a previous polypectomy in order to guide the resection, especially during a laparoscopic approach. It is also used to mark transmurally the distal transection point during anterior colorectal resection. The accuracy of endoscopic tattooing is high and varies from 70% to 100%, with a false positive rate of 1.6% to 7% and an incidence of intraoperatively invisible lesions of 1.6% to 15%. A small number of complications has been reported, most of them related to transmural injection.25,26
In the head and neck compartment, US-guided charcoal tattoo localization has been used to aid the surgeon in locating lesions in recurrences after thyroidectomy, in scar tissue, and in regions that are difficult to redissect. To date, available studies all agree about the safety and effectiveness of this technique.27,33,34 Other studies have tested US-guided injection with other tattooing agents, such as methylene blue dye or indigo carmine. Both proved to be effective, but diffusion in peritumoral tissue was high, and disappearance of the color was much faster than with charcoal. Furthermore, potential toxicity such as skin necrosis or nerve toxicity may be related to methylene blue dye.35,36 Charcoal suspension injection proved to be easy to perform, well tolerated, without toxicity, with long-lasting marking (up to 3 months), and with little migration to lymph nodes. 34 The main advantage of its much longer persistence is that the injection can be performed in the radiology unit several days before surgery and thus not need to be performed in the operating room.
Charcoal suspension tattooing becomes especially useful in parotid surgery when an ECD or a PSP is performed and the PA is small and/or with low consistency. Surgical preparation for ECD and PSP is the same as for conventional parotidectomy. The degree of dissection is usually guided by intraoperative visual and palpatory assessment of the tumor extent. In some cases, the lump is not intraoperatively palpable, and so it is unidentifiable from normal parenchyma. In those cases, the safest surgical option is SP, in order not to leave in place the neoplasm. Charcoal helps to identify the exact position of the mass when this is not clear on palpation (Figure 1), and preoperative echography doesn’t indicate the precise parotid segment where the lump is located. Under direct vision of the charcoal, a less extensive surgery can be performed anyway.
The arrow corresponds to the marked pleomorphic adenoma inside the normal parenchyma.
Charcoal injection of PA is easy to perform as it uses the same technique as US-guided FNAC. The procedure can be performed on an outpatient basis, irrespective of the scheduled day of surgery, because the patient is not negatively affected and the tattooing material persists for days. At our institution, we perform the injection within 20 days prior to surgery. In selected cases, when patients cannot easily access the hospital, the charcoal injection is done at the same time as FNAC since it is absolutely innocuous. Each tumor was injected with 1 to 2.5 mL of suspension, depending on lesion size. There does not seem to be a limit for lesion size or depth, as we performed this technique in lesions measuring 6 to 42 mm and located 2.5 to 9 mm from the skin surface. The only limit could be the radiologist’s skill in detecting the lesion and reaching it with the needle. In 4 cases in which the charcoal remained in the tissues above the lesion, this was probably due to a greater density of the mass and a consequent higher resistance to the injection. In less consistent masses appearing anechoic at US assessment, injection inside the tumor capsule proved much easier and the amount of charcoal suspension needed was lower. Injection outside the tumor parenchyma was mostly related to the radiologist’s injection technique. In fact, in the first cases, the radiologists continued to inject the suspension while withdrawing the needle, as they are used to doing with breast lumps in order to provide the surgeon with a path to the tumor through the healthy breast parenchyma. The procedure proved nonetheless useful in guiding the dissection because the tattoo was located immediately above the mass. After discussion with the radiologists, we decided that lesions should be marked only within the lesions so that the charcoal spreads under the tumor capsule in order to clearly distinguish between the lesion and the normal parenchyma. After this meeting, all the tumors were marked correctly into the lesion. These 4 cases are illustrative and show the importance of a good communication between surgeon and radiologist.
Alternately to preoperative charcoal marking of the lesion, an intraoperative ultrasound can guide the dissection if difficulty is encountered. At our institution, we have no possibility to keep a radiologist in the operatory room during surgery. Therefore, we opted for charcoal suspension tattoo as procedure of choice, as it doesn’t need to be performed in the operating room. Furthermore, the procedure is fast (only 15 minutes) and doesn’t have significant impact on overall cost of treatment.
As with other applications, charcoal tattooing of parotid masses is harmless, not painful and not demanding for patients. The only unpleasant complication, namely, transient dimensional increase of the mass, can be overcome by reducing the amount of suspension injected, especially in those lesions with lower consistency.
As previously stated, charcoal marking of parotid lesions loses significance when the lump is easily identified intraoperatively by palpation and vision. In our experience, in some cases it is difficult to find the tumor when the incision is made and the cutaneous flap is lifted to expose the glandular capsule. That’s true for little and poorly consistent lesions in particular. For example, some lesions could reduce their volume after FNAC, when the liquid component is aspirated, converting from palpable to nonpalpable.
In our study population, 4 lumps were described as intraoperatively nonpalpable by surgeons. In 2 cases, the surgeon decided to perform a PSP and in 2 cases an ECD, both under visual guidance of the charcoal. In all cases, the anatomopathologist confirmed the correct placement of the charcoal in the lesion, and in all cases, the surgeon found it helpful in locating the lesion. A postoperative echography showed nonresidual tumor in all cases.
After assessing the safety of the procedure, we tried to identify preoperative characteristics of patients and tumors that could guide the choice of which patients can effectively benefit from this technique. We observed that those tumors defined as intraoperatively nonpalpable were all less than 1 cm wide (100%). We then evaluated BMI and neck circumference as indicators of the amount of fat in the neck.37,38 Three of those patients had BMI higher than 30 (75%). Three of them were male patients with neck circumference larger than 42 cm (75%). The procedure seems therefore most useful on tumors 1 cm or less, which should not be easily palpable after flap elevation. These preliminary observations need a largest cohort of patients to be confirmed and to establish indications for a selective use of charcoal suspension tattoo, even if it is a nondemanding and harmful procedure.
All patients had a follow-up visit monthly in the first 3 months after surgery, then every 3 months (mean follow-up 16 months). To date, no recurrences have been recorded.
Conclusions
Ultrasound-guided charcoal tattooing is a new, safe, well-tolerated, and easy-to-perform technique for the intralesional marking of pleomorphic adenoma of the parotid gland. A larger cohort of patients is necessary to establish indications for a selective use of the technique.
Footnotes
Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The author(s) received no financial support for the research, authorship, and/or publication of this article.