Introduction

During the last decades, the development of minimally invasive surgical procedures has resulted in the introduction of new endoscopic techniques in modern endocrine surgery [1, 2]. Although thyroidectomy and parathyroidectomy through the traditional collar incision are safe and efficient approaches with great short- and long-term outcomes, the cosmesis seems to considerably affect patients’ quality of life lives [3]. To that end, since 1990, several minimally invasive surgical approaches for endocrine cases such as endoscopic thyroid lobectomy, transaxillary endoscopic thyroidectomy and video-assisted parathyroidectomy have been described [4,5,6,7,8,9,10]. Due to significant limitations, in terms of technical difficulties such as inadequate exposure, the effect of CO2 insufflation and the quality of instrumentation, the adoption of these surgical techniques was not widely spread in the committee of Endocrine Surgeons [11, 12].

In the era of the massive development of technology and minimal invasive surgical techniques, robotic systems have been proposed, and as a result, using these new systems, a plethora of Endocrine surgeons try to overcome the technical disadvantages to offer their patients a safe and scarless thyroidectomy and parathyroidectomy [13, 14]. High-definition three-dimensional view and new precise hand-mimicking robotic instruments improved the ability of the surgical team to perform with safety those procedures, whereas they provide an adequate visibility of sensitive and crucial structures during thyroidectomy and parathyroidectomy, such as superior laryngeal nerve, recurrent laryngeal nerve (RLN) and parathyroid glands [15,16,17].

The aim of our study is to systematically review and analyze the short-term outcomes in all patients who underwent robotic-assisted parathyroidectomy (RAP) diagnosed with primary hyperparathyroidism (PHPT) or secondary hyperparathyroidism.

Methods

Study design

All appropriate case reports, case series and observational studies describing patients who were diagnosed with PHPT or another parathyroid disorder and underwent robotic-assisted parathyroidectomy were considered eligible for inclusion in the current systematic review. Reviews and experimental studies in animal were excluded from tabulation. Studies in English language was only included. Patients who underwent robotic-assisted parathyroidectomy for a mediastinal parathyroid adenoma were excluded.

Search strategy and data collection

We systematically searched the literature for articles published from January 2000 to September 2019 using PubMed (1966–2019), Scopus (2004–2019) and Google Scholar (2004–2019) databases along with the references of the articles, which were retrieved in full text. The following keywords were used for the search: ‘robotic’, ‘robotic parathyroidectomy, ‘robotic-assisted’, and ‘parathyroidectomy’, ‘minimal invasive parathyroidectomy’, “transoral parathyroidectomy”. A minimum number of key words were utilized to assess an eligible number that could be easily searched while simultaneously minimizing the potential loss of articles. Articles that fulfilled or were deemed to fulfil the inclusion criteria were retrieved.

Data on patient characteristics included age and sex, while disease characteristics included diagnosis, preoperative imaging studies, type of surgery and location of parathyroid adenoma. Concerning the main findings of the study, intraoperative and postoperative outcomes, such as the length of hospital stay and complications were also assessed. The Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) flow diagram schematically presents the stages of article selection (Fig. 1) [18].

Fig. 1
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Search flow diagram

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Results

Excluded studies

A total of four studies were excluded from the present study [19,20,21,22]. The study of Tolley et al. was excluded as a part of an already study, while the other two studies were excluded due to insufficient data [19,20,21]. In the study of Wu et al., pediatric cases were reported, so this study was not included [22].

Main characteristics of included studies

A total of 15 studies (6 case reports and 9 case series) described outcomes for patients who were diagnosed with PHPT or secondary hyperparathyroidism and underwent a robotic-assisted parathyroidectomy for cervical parathyroid adenomas and were finally analyzed [8, 23,24,25,26,27,28,29,30,31,32,33,34,35,36,37]. Tables 1, 2 illustrate the main characteristics of total 64 patients. The proportion of men was 21.3% in the current review, while the mean age of 64 patients ranged from 37.5 to 62 years. As shown in Tables 1, 2, indications for surgery was available for all patients. Fifty-eight patients (90.6%) were diagnosed with PHPT, whereas only six (9.3%) underwent parathyroidectomy for secondary hyperparathyroidism. Preoperative imaging studies were reported in 71.8% of cases (n = 46 out of 64 patients), included a combination of neck ultrasound (US), Sestamibi scan, computed tomography (CT) and magnetic resonance imaging (MRI) and are presented in Tables 1, 2. More specifically, the percentage of patients who had a preoperative neck ultrasound and Sestamibi scan for parathyroid adenoma localization was 97.8% and 95.6%, respectively. Computed tomography of neck performed preoperatively in 28 out of 46 patients (60.8%), while only 1 case had a magnetic resonance imaging (2.1%).

Table 1 Main characteristics of the included case series
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Table 2 Main characteristics of the included case reports
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Operative outcomes

All patients underwent a robotic-assisted parathyroidectomy for neck parathyroid adenomas, but with different approaches. Transaxillary access for RAP was performed in 51 cases (79.6%), transoral RAP in 6 (9.3%), axillo-bilateral-breast approach (BABA) in 6 (9.3%), while 1 patient (1.5%) underwent a retroauricular RAP. In four patients, an en bloc parathyroidectomy and lobectomy of thyroid gland was performed, due to atypical location of parathyroid adenoma or intrathyroidal parathyroid adenoma [32, 34]. In the study which described patients diagnosed with secondary hyperparathyroidism, four glands were removed in five of them, whereas three glands in one patient [29]. The location of parathyroid adenomas was mentioned in 37 cases (57.8%). Among them, right superior parathyroid gland was removed in 6 patients (16.2%), right inferior in 9 (37%), left superior in 2 (5.4%) and left inferior in 12 (32.4%). Six patients (16.2%) underwent RAP for a right-side parathyroid adenoma, while one retropharyngeal (2.7%) and one ectopic parathyroid adenoma in pyriformis (2.7%) were excised. Curative resection was achieved in all patients. The successful excision of the parathyroid adenoma was evaluated with the measurement of levels of intraoperative parathyroid hormone (IOPTH) in 47 cases (73.4%). Conversion to conventional open parathyroidectomy with collar incision was decided in four patients (6.2%). Among them, in three cases, the reason of conversion was the patients’ high BMI (> 30 kg/m2), in two cases, mismatches were observed between preoperative imaging modalities and the intraoperative findings; while one patient was diagnosed intraoperatively with multinodular disease [23, 30, 32]. In 31 patients (48.4%), the mean blood loss ranged from 9.9 to 104 ml, whereas in 59 patients (92.1%), the mean operating time ranged from 119 to 186 min. The rate of drainage tubes that were inserted was 28.8% (n = 15 out of 52 patients). 60.3% of total cases were assessed intraoperatively via nerve monitoring.

Postoperative outcomes

In terms of perioperative and postoperative complications, the majority of cases were uneventful. Five (9.2%) out of 61 cases reported complications. More specifically, among them, two (40%) patients presented with postoperative seroma in neck trauma and three (60%) were observed with a mild wound infection, which was treated with oral antibiotics. All cases had no complications associated with nerve injury. Additionally, 50% of cases were additionally examined postoperatively via flexible laryngoscopy. Postoperative normal levels of calcium were observed in 89% of patients (n = 57 out of 64 patients), while one patient had low levels of calcium postoperatively. Biochemically curative RAP was reported in 60 cases (94%), while only 2 (3.5%) patients underwent reoperation via open bilateral 4-gland exploration due to persistent hyperparathyroidism and 2 (3.5%) cases did not describe any postoperative biochemical result. Furthermore, in 57 cases (89%), the length of hospital stay day was described. More precisely, 2 patients (3.5%) were discharged the same day, while 47 (82.4%), 2 (3.5%) and 6 (10.5%) patients were discharged on postoperative day 1, 3 and 6, respectively. No reoperation or readmission was required due to a severe complication.

Discussion

In our study, we highlighted and evaluated the intraoperative and postoperative outcomes in patients with PHPT and secondary hyperparathyroidism who underwent RAP for a cervical parathyroid adenoma. RLN injury, postoperative hypoparathyroidism and bleeding were not reported in our systematic review. All patients were cured undergoing RAP, while in 6.2% of cases, the procedure was converted to the conventional open one. Postoperatively, the percentage of patients presented complications were 9.2%. All of these complications were managed conservatively. All patients had an excellent postoperative cosmetic result.

The adoption of minimal access procedures in endocrine surgery was significantly delayed, in comparison to other fields of general surgery, due to many critical operative difficulties and technical limitations, including lack of operative space and a great risk of damage of sensitive structures like vessels and nerves in neck [5, 11,12,13,14,15]. During last decade, the new trend in endocrine surgery was robotic approaches, and especially RAP which was first described by Tolley et al. in 2011 [19]. Compared with other endoscopic and minimal invasive techniques, RAP is less complicated in terms of systems and instruments offering a considerably better cosmetic result [19].

Among advantages of RAP, scar cosmesis seems to be the core reason that patients decide to proceed to this kind of procedure. Tolley et al. highlighted the beneficial long-term outcomes of RAP in terms of quality of life (using VAS score and EuroQOL-5D questionnaire score), including less postoperative pain and higher quality cosmetic result even after 24 months [30]. More specifically, postoperative pain in 2 weeks was significantly less in RAP group compared with FLP group (p = 0.036), and regarding scar cosmesis the mean VAS score was considerably increased at 3 and 6 months in RAP group in comparison to FLP group (p = 0.005 and p = 002, respectively). Additionally, in the study conducted by Noureldine et al. and Foley et al. was described how transaxillary RAP offered a brilliant and hidden scar [32].

The current systematic review depicts the safety and feasibility of RAP in patients diagnosed with PHPT and preoperative localized parathyroid adenoma, but also in patients diagnosed with secondary hyperparathyroidism and multinodular disease. He et al. firstly reported that RAP by axilo-bilateral-breast approach was a viable procedure in patients diagnosed with secondary hyperparathyroidism, where a total or subtotal (excision of three glands) parathyroidectomy with an uneventful postoperative period was performed [29]. In the study of Noureldine et al., a case of multinodular disease and a four-gland exploration was successfully completed by RAP without conversion [32]. However, none of the included studies described parathyroid carcinoma as an indication of RAP or cases of parathyroid adenomas with concurrent thyroid disease, such as thyroiditis or multinodular goiter. Therefore, how RAP deals with these specific indications is questionable and further studies are required. Additionally, there is no evidence if RAP can be performed and successfully completed in patients with history of previous neck operations. More precisely, Tolley et al. excluded from their study cases with potential malignant characteristics, significant thyroiditis and previous neck surgery [30].

Several limitations of this modern and attracting technique should be mentioned. First of all, the most significant disadvantage of RAP is the extremely higher cost compared with the conventional open parathyroidectomy. Total cost of RAP might overcome $1.5 million including either the robotic system and its maintenance and the equipment for each case [30]. Some authors believe that this remarkable financial issue in association with the much longer operative time probably outweigh the high quality of cosmetic result. Prolonged operative time is another disadvantage that characterizes RAP. A plethora of studies illustrated the fact that although RAP is safe and without any significant complications, including RLN injury and bleeding, but it is also a procedure with longer operative time in comparison to traditional cervical parathyroidectomy [30, 37, 38]. Moreover, RAP is not a procedure for every surgical team or hospital, because it demands not only experience in open parathyroidectomy and generally in endocrine surgery, but also surgeons and nursing teams who have been trained and certificated for robotic procedures [30, 35]. Moreover, RAP and especially transaxillary approach demands an incision in the axilla combined with a significant space of dissection in order to reach the neck and complete the parathyroidectomy. Considering this fact, RAP is not as minimal invasive as it has been proposed. In the future, transoral procedures might be more feasible for minimal invasive endocrine procedures, as their results in both cosmetic and perioperative outcomes presented to be more promising and encouraging [39, 40].

To our knowledge, the present study is the first systematic review of patients who underwent RAP with every available access for cervical parathyroid adenoma, which also describes the intraoperative and postoperative outcomes of RAP. Of note, the results of our systematic review should be interpreted in the context of its limitations. There are no randomized trials (RCTs) published in the current literature comparing RAP with FLP, and as a result the evaluation of RAP as a superior surgical approach is impossible. Additionally, total number of patients of our study is small and were meticulously selected by surgical teams, thus, objective results about further advantages or disadvantages of RAP cannot be reported. None of the included studies blinded or randomized the participants and the assessors of the outcomes. Another important limitation of the current study is the fact that these studies conducted at single centers. Therefore, a potential selection bias must influence our results.

In conclusion, our study demonstrates that RAP is a safe and curative surgical approach for patients diagnosed with PHPT or secondary hyperparathyroidism with uncomplicated and beneficial short-term outcomes in selected patients and by experienced surgical and nursing teams. Patients with normal and low BMI with the necessary combination of preoperative studies are proper candidates for RAP. Further randomized and multicenter studies should be published in future, to demonstrate the superiority of RAP, comparing with conventional open parathyroidectomy.