Feasibility of focused parathyroidectomy in developing countries—a scoping review

Introduction

The ‘gold standard’ operative treatment of primary hyperparathyroidism (HPT) has been bilateral neck exploration (BNE) since the first parathyroidectomy in 1925, with excellent cure rates of greater than 95% demonstrated (1). Cure is defined as re-establishing sustained normocalcaemia that persists for at least 6 months post surgery (2,3). The rationale for BNE at the time was the knowledge of multi-gland disease coupled with the inability to identify specific diseased glands preoperatively. van Heerden et al. [1991] demonstrated a cure rate of 99.5% in 379 patients with primary HPT undergoing BNE (4). Consistently high success rates were further demonstrated, revealing this procedure to be reliable and easily reproducible (5,6).

Focused parathyroidectomy (FP) was conceived due to the realisation that in 80% of cases of primary HPT the aetiology is a single gland adenoma, allowing a more targeted approach to parathyroidectomy (7). However, FP is naturally entirely reliant on adequate preoperative localisation. The greatest advancement being the ^99mTechnetium sestamibi, as described by Coakley et al. [1989] (8). Today, there are numerous preoperative localisation studies available viz; different types of sestamibi radionucleotide scans, computed tomography (CT) scans, magnetic resonance imaging (MRI) scans and ultrasound (US), each with varying degrees of sensitivities.

Initially, certain authors were against the notion of FP, with some advising against the technique as they simply considered it to be a passing trend and misguided (9). They identified two main concerns with this technique. The first was that of inferior cure rates, highlighted by Delbridge et al. [2000] who assessed FP in 50 patients and demonstrated an inferior 84% cure rate with FP, significantly lower compared to the standard of care BNE’s established 95% cure rate (10). These inferior cure rates were mostly due to “double adenomas” which can account for up to 10% of all parathyroid adenomas (11). However, since then, intraoperative adjuncts used during FP evolved significantly, with use of intraoperative nuclear scanning and rapid intraoperative parathyroid hormone (IOPTH) test, FP cure rates equalled that of BNE (12,13). When coupled with intraoperative assays, it also obviates the need of inspection of the remaining parathyroid glands (PGs) thus preventing the complications associated with BNE (14,15).

The second concern with FP was the cost, with some authors demonstrating a higher cost associated with FP compared to BNE, resulting from the requisite preoperative localisation tests and the addition of intraoperative adjuncts (16,17). However, since then, the cost of preoperative localisation studies decreased, and the literature reflected this by subsequently revealing FP to be cost effective comparative to BNE alone, balanced by the added cost of increased operative time and longer hospitalisation associated with the latter (18).

Subsequently, FP has been shown to be superior to BNE. Udelsman et al. in 2000 with 100 cases, in 2002 with 255 cases and in 2011 with 1,037 cases of FP demonstrated a higher cure rate with FP (99.4% vs. 97.1% with BNE) with reduced cost, morbidity and length of hospital stay (19-21). Numerous other authors have demonstrated consistent findings (22-24). The benefits of FP over traditional BNE include equivalent rates of cure (95–98%), with added benefits of: the ability to be performed under a local anaesthetic, outpatient recovery, shorter operative time, desirable cosmesis, reduced nerve injuries and elimination of permanent hypoparathyroidism (25,26). Thus, in the setting of positive preoperative localisation, FP has become the new standard of care.

Importantly however, the mounds of literature we are guided by emanate from the developed, ‘high-income world’, where resources are far more abundant, with remarkable strides made in healthcare resource allocation. Unfortunately, in a developing (middle-income) setting, with marked disparity between the private and public healthcare sector, resources are drastically limited, often to the point of tailoring guideline recommendations to local resource availability (27).

Therefore, despite the described cost-effectiveness of FP with requisite localisation and IOPTH in studies from developed world literature, a developing country may not be able to rationalise this cost. In addition to the cost, availability is a concern, which, when considered, would drastically affect the feasibility of this procedure over a traditional BNE that requires no additional localization or intra-operative adjuncts.

This scoping review serves to ascertain the feasibility of FP in developing countries, considering the perceived additional cost and unclear availability of mandatory preoperative localisation studies along with requisite intraoperative adjuncts and the necessary skill and experience needed to facilitate this procedure successfully. We present this article in accordance with the PRISMA-ScR reporting checklist (available at https://gs.amegroups.com/article/view/10.21037/gs-24-57/rc).

Methods

This scoping review evaluated primary, secondary and tertiary literature, drawing from both published peer-reviewed and grey literature. The framework guide by Arksey & O’Malley [2005], including modifications published by Levac et al. [2010], were followed (28,29). The stages traversed include: (I) identifying the research question; (II) identifying the relevant studies; (III) study selection, with specified inclusion and exclusion criteria; (IV) charting the data and lastly; (V) collating, summarising and reporting the results. Primarily, the PRISMA-Scr extension framework and checklist was adhered to, with reporting of eligible studies via the PRISMA flow diagram. The eligibility of the research question was explored via the PCC framework (30).

To assess the eligibility of the research question, the PCC framework—namely: ‘population, concept and context’ framework, as recommended by the Joanna Briggs Institute (JBI), was employed (31). The population was identified as primary hyperparathyroid patients warranting parathyroidectomy. The concept was identified as cost and availability accounting for feasibility of FP comparative to BNE in developing countries. Finally, context was identified as developing countries.

An extensive literature search was conducted, using Boolean logic operators such as ‘AND’ & ‘OR’, with the following key terms: ‘primary hyperparathyroidism’, ‘parathyroidectomy’, ’surgery’, ‘ultrasound’, ‘nuclear medicine’, ‘developing countries’, and ‘cost’. The keywords used complied with Medical Subject Headings (MeSH) terms, adjoined with relevant subheadings & qualifiers, falling within the jurisdictions of the MeSH tree structures. To broaden the exposure to relevant articles, the following non-MeSH conforming keywords were additionally employed: ‘focused parathyroidectomy’, ‘feasibility’, ‘low-income’, ‘economic viability’, ’sestamibi’ and ‘intra-operative PTH’.

The search utilised the following library databases: PubMed/MEDLINE, Google Scholar, World Cat, Academic Search Complete via EBSCO host, Open Dissertations via EBSCO host, SA ePublications via SABINET African journals, SACat via OCLC and ProQuest. These prodigious evidence sources were identified through their phenomenal reputations as leaders in library database provision, enabling access to a large cohort of invaluable research papers.

All articles encountered were entered into an excel spreadsheet, structured under the heading of each source. Articles were further categorised according to search terms employed.

Articles were retrieved upon exploration of the literature via the aforementioned library databases. Screening was initiated firstly by means of confirming relevance based on review of each title of the studies retrieved. Thereafter, abstracts were scanned, followed by introductions and statements of purpose. If the studies fulfilled the purpose of this review, the countries of origin were then scrutinized and cross checked with the United Nations Development Program (UNDP) & World Bank (WB) list of developing/middle income countries to ensure the articles to be perused were relevant (32,33). Finally, the full texts were engaged.

The basis for which these studies were selected includes: (I) studies providing evidence on surgical management of primary hyperthyroidism, specifically discussing focused or minimally invasive parathyroidectomy; (II) studies providing evidence on preoperative localisation; (III) studies providing evidence on a developing world approach to parathyroidectomy; and (IV) studies providing evidence on economic burden of either parathyroidectomy option. The period explored was literature from the past 15 years (from 2007 onward). No restriction on language was employed, allowing for greater acquaintance.

Studies not meeting the inclusion criteria of: providing evidence on surgical management of primary hyperthyroidism; with specific discussion on focused/minimally invasive parathyroidectomy; providing evidence on preoperative localization; providing evidence on a developing world approach to parathyroidectomy and providing evidence on economic burden of either parathyroidectomy option were all excluded, including all studies published prior to 2007. Additionally, all studies exclusively describing endoscopic or minimally invasive video assisted FP were excluded.

The studies included for this review primarily comprises non-randomized evidence in the form of case series, cohort studies and 1 case report. Consequently, a trio of ‘JBI critical appraisal tools’ were employed to assess the quality of evidence, namely the ‘case series checklist’, ‘cohort study checklist’ and ‘case report checklist’ tools. These tools were completed by two reviewers independently, as recommended by the JBI. The Oxford Centre for Evidence-based Medicine (CEBM) grading was utilized to assess the level of evidence of the included studies. See Appendix 1 for ‘JBI Critical Appraisal Tools’.

Results

A total of 940 relevant articles were encountered upon exploration of the literature from 8 different databases (see Table 1). After duplicates were removed and elimination by screening of article titles, abstracts, full texts and countries of origin, a total of 18 remaining articles fulfilled the purpose of this review and thus were included for study (see Figure 1).

Figure 1 PRISMA flow chart of included studies (30). BNE, bilateral neck exploration; HPT, hyperparathyroidism; FP, focused parathyroidectomy.

In the 18 articles, a total 1,716 patients underwent parathyroidectomy from seven developing countries [five studies from South Africa (upper middle-income); five studies from India (lower middle-income); three studies from Pakistan (lower middle-income); two studies from Turkey (upper middle-income); one study from Egypt (lower middle-income); one study from Algeria (lower middle-income) and one study from Nigeria (lower middle-income)] (see Table 2).

FP was performed in 1,202 patients (70%) with 7 studies (38.9%) reporting on 647 patients having had FP with intraoperative adjuncts (including IOPTH, methylene blue, frozen section or the gamma probe) and 11 studies (61.1%) reporting on 555 patients having had FP without intra-operative adjuncts.

Cure rates from the studies included in this review for FP were reported in 15 (7 with intraoperative adjuncts & 8 without intraoperative adjuncts) of the 18 studies. Of the 15 studies with reported cure rates, only 11 (73%) met the definition of cure following parathyroidectomy, with a minimum of a 6-month follow-up. Consequently, only cure rates from these 11 studies were included in the statistical analysis. Cure rates ranged from 83.3% to 100%, with an overall cure rate of 96.4% (see Tables 3,4).

Preoperative localisation in these developing countries were performed by US and ^99mTc sestamibi, with 1 study describing the use of ¹¹C methionine PET/CT as an additional localisation modality. Accuracy rates of localisation studies in these developing countries ranged from; 44–94% with US, 66.5–100% with ^99mTc sestamibi and 71.4% for the ¹¹C methionine PET/CT (see Table 5).

Discussion

Whilst the operative management of primary HPT has undergone profound evolutionary changes resulting in FP being considered the new standard of care for cases of primary HPT with unequivocally localised single gland disease, as recommended by the American Association of Endocrine Surgeons (AAES) and the Fifth International Workshop on Primary Hyperparathyroidism, the concern for practitioners in developing low and middle-income countries is the relevance of the evolutionary changes and the applicability of its outcome, namely FP, considering the basis for it all emanates from developed high-income countries (53,54).

As demonstrated by Hurst et al. [2005] and Adhikari et al. [2021], evidence-based medicine and the guidelines they produce from high-income countries most often cannot be adhered to in resource constrained low and middle-income countries (55,56). As such, this review was conducted to address the question of feasibility of FP in terms of accessibility to and accuracy of preoperative localisation and adequacy of cure rates with this technique, in developing countries.

The first prerequisite to enable performing FP is adequate preoperative localisation. From this review, it was revealed that preoperative localisation was available in all developing countries from the articles included in this review, with the most common modality used being the ^99mTc sestamibi (used in all studies) followed by US (used in 16 of the 18 studies). The overall accuracy of ^99mTc sestamibi and US for preoperative localisation in these developing countries were 85.7% and 75.7% respectively. The overall accuracy of combined US and ^99mTc sestamibi was 95.2%. These results are in keeping with preoperative localisation rates reported from high-income countries.

Cheung et al. [2012] in their meta-analysis revealed sensitivities for ^99mTc sestamibi and US of 78.9% and 76.1% respectively (57). Combined ^99mTc sestamibi/US use for preoperative localisation has been reported to have a sensitivity of 96%, in keeping with the sensitivity of preoperative localisation from the developing countries in this study (58). In a single lower middle-income country, Nigeria, Olatoke et al. [2013] demonstrated preoperative localisation to be possible, but not feasible, as each ^99mTc sestamibi test required a 250 km journey to access a facility with the necessary equipment (45).

Intraoperative adjuncts were used in 7 of the total 18 studies: IOPTH was used in three studies; frozen section in two studies; methylene blue in one study and the gamma probe in one study. Cure rates of the study were adjusted according to whether the correct definition of cure was achieved in a study, with statistical exclusion of the study if the standard definition was not met (see Table 6). The adjusted cure rate for patients undergoing FP with IOPTH was 98.5%, with an overall cure of 99.2% for patients undergoing FP with intraoperative adjuncts. In the remaining studies of FP without intraoperative adjuncts, the overall cure rate was 95.3%. These figures from the developing countries included are in keeping with reported cure rates from high-income countries as demonstrated by Quinn et al. [2021]. In their meta-analysis the authors compared cure rates of patients undergoing FP with vs. without IOPTH. The authors reported cure rates of 98% for FP with IOPTH and 94.8% for FP without (59).

The lowest cure rate in this review was reported by Zitouni et al. [2021] from the lower middle-income Algeria, who reported a cure rate of 83.3% with FP (42). The limitation with this study was the low sample size of only 18 patients who underwent FP, thus the 83.3% represents 15 of the 18 cured, with 3 patients having had persistence. Additionally, individual preoperative localisation accuracy rates were relatively low in this study, with US accurate in 60.7% of cases and ^99mTc sestamibi accurate in 66.5% of cases.

With the 18 studies from developing countries included in this review, a total of 1,202 patients underwent FP with an overall cure rate of 96.4%. This is in keeping with reported cure rates from high income countries. Ishii et al. [2018] in their meta-analysis of 5,282 patients, from 14 included studies having undergone FP, demonstrated an overall cure rate of 96.9% (60).

From this review, it is evident that not only is preoperative localisation accessible and accurate in these developing countries, but FP is also successfully being performed within these regions. The two lower middle-income countries with difficulties were Nigeria and Algeria, demonstrating that perhaps the upper-middle income developing regions are currently better suited to adapting to this minimally invasive technique.

Limitations

There were only seven developing countries included in this review, thus limiting the relevance of this review to other developing countries. A small number of studies did not report individual preoperative localisation rates or overall cure rates, thus distorting representation. The quality of evidence of studies included in this review mostly (17/18) comprise of case series and cohort studies, however one study, number 11 by Olatoke et al., is a single case report, thus representing low quality evidence. Additionally, this study offered no statistical benefit, however this report of only a single case is due to and demonstrates the challenges of FP in this country, which speaks to the aim of this review (45,61).

Conclusions

Preoperative localisation is available in developing countries, with adequate accuracy rates, in keeping with rates described in literature from high-income countries. FP is performed in developing countries with adequate cure rates in keeping with that of randomised controlled trials (RCTs) published from high-income countries. Although some developing countries lack availability of certain intraoperative adjuncts, this was not prohibitive and cure rates with or without these adjuncts were similar in these countries. With the established availability and impressive accuracy rates of preoperative localisation and the demonstrated success rates of FP, it is evident this technique is safe and feasible in developing countries.

Acknowledgments

The research for this study was done in partial fulfilment of the requirements for KR’s MMed (Surg) degree at the University of KwaZulu-Natal.

Funding: None.

Footnote

Reporting Checklist: The authors have completed the PRISMA-ScR reporting checklist. Available at https://gs.amegroups.com/article/view/10.21037/gs-24-57/rc

Peer Review File: Available at https://gs.amegroups.com/article/view/10.21037/gs-24-57/prf

Conflicts of Interest: Both authors have completed the ICMJE uniform disclosure form (available at https://gs.amegroups.com/article/view/10.21037/gs-24-57/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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