Evaluation of the effectiveness of near-infrared autofluorescence (NIRAF) imaging combined with immunocolloidal gold technique (ICGT) in identifying and protecting parathyroid glands during thyroid cancer surgery

Introduction

Analysis of the recently released National Cancer Center epidemiological report (1) reveals thyroid carcinoma has emerged as the leading neoplasia exhibiting the most rapidly accelerating incidence in China throughout the last decade [2013–2023]. Of the newly diagnosed cases, about 90% are differentiated thyroid cancers, and most patients (>85%) can achieve long-term survival through surgical treatment (2). Therefore, it is crucial to focus on the impact of postoperative complications on patients’ quality of life, including postoperative hypocalcemia and hypoparathyroidism due to parathyroid damage. However, even experienced surgeons often encounter the problem that the parathyroid glands (PTGs; especially the inferior PTGs) are not in a fixed location. Often, after exploring and identifying the PTGs, it is found that their blood supply has already been compromised during early dissection and they have to be resected and transplanted into the surrounding area. The absence of reliable real-time identification technology renders contemporary thyroid surgery heavily operator-dependent, entailing significant interoperator variability. Current meta-analytic data demonstrate substantial intraoperative PTG injury rates, with postoperative transient and persistent (defined as lasting >6 months) hypoparathyroidism reaching 29.05% and 4.08% respectively (3). Notably, total thyroidectomy procedures exhibit even greater incidence based on recent multicenter cohort analysis (4). The past decade has witnessed the evolution of intraoperative parathyroid identification into distinct technical paradigms, predicated on diverse physicochemical mechanisms. Current modalities are broadly classifiable into four categories: (I) vital dye staining techniques (4-8); (II) technetium-99m sestamibi scintigraphy (9); (III) intraoperative parathyroid hormone (iPTH) rapid assay (10); and (IV) optical detection systems (11-15). Given the inherent technical constraints of individual modalities (e.g., dye toxicity, radiation exposure, delayed iPTH results), contemporary scholars have implemented multimodal integration strategies in thyroid carcinoma operations, demonstrating improved intraoperative outcomes (16,17).

This retrospective cohort study conducts a head-to-head comparative analysis of the new modalities—combining near-infrared autofluorescence (NIRAF) imaging with immunocolloidal gold technique (ICGT)—versus conventional visual inspection. Our primary endpoint evaluates the clinical efficacy of this combined approach in parathyroid preservation during total thyroidectomy. We present this article in accordance with the STROBE reporting checklist (available at https://gs.amegroups.com/article/view/10.21037/gs-2025-118/rc).

Methods

General information

This single-center retrospective cohort study analyzed 62 consecutive patients undergoing total thyroidectomy with bilateral central lymph node dissection (CLND) (January–December 2023). They all underwent surgery at The First Affiliated Hospital of Nankai University. The patients were divided into an observation group (34 cases) and a control group (28 cases) according to whether the combined technique was used during the operation. The age, gender, hospitalization time, and tumor-node-metastasis (TNM)-stage of the patients in the two groups were counted, and the preoperative levels of calcium, parathyroid hormone (PTH), and 25-hydroxyvitamin D [25(OH)D] were measured in both groups. All procedures were performed by the same experienced surgeons.

Equipment

The imaging equipment used in this study is a near-infrared fluorescence camera (PDE-NeoII) provided by Hamamatsu Photonics (China) Co., Ltd. (Shanghai, China) The excitation and detection of near-infrared light are integrated in a probe, which is convenient for the doctor to operate by hand. The near-infrared excitation wavelength of PDE-NeoII is 760 nm, and the fluorescence wavelength that can be captured is in the range of 790–830 nm. The PTH rapid detection reagent and colloidal gold immunochromatographic analyzer were provided by Bioda-technology (Wuhan) Co., Ltd. (Wuhan, China) They were used to detect the tissue eluate extracted from the suspected parathyroid tissues, and the detection value of PTH given by the analyzer was used to achieve the purpose of rapid identification.

Inclusion and exclusion criteria

Inclusion criteria: (I) adults aged 18–80 years old; (II) preoperative examination of PTH and blood calcium levels are within the normal range; (III) patients who have undergone primary surgery for papillary thyroid cancer confirmed by postoperative paraffin pathology; (IV) total thyroidectomy with bilateral CLND; (V) the tumor has not invaded distant tissues. Exclusion criteria: (I) patients with benign thyroid tumors; (II) patients with unilateral thyroid cancer and unilateral lobectomy; (III) patients with hyperparathyroidism or combined with parathyroid tumors; (IV) patients with other diseases combined with abnormal calcium and phosphorus metabolism; (V) patients with a history of neck trauma or surgery; (VI) patients with preoperative radiotherapy to the neck for other tumors. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. This study was approved by the Research Ethics Committee of Tianjin Union Medical Center, The First Affiliated Hospital of Nankai University (No. 2024B78). All enrolled patients signed informed consent.

Surgery

Surgical procedure

Both groups of patients underwent total thyroidectomy with bilateral CLND. In the observation group, NIRAF visualization was performed by removing the surgical shadowless lamp and holding the probe about 5 cm away from the detected tissues. The surgical area was probed with near-infrared light, and the PTGs were observed and located through the difference in fluorescence intensity between the tissues. The resulting fluorescence images were stored (Figure 1). NIRAF was used to image the surgical field at least three times during surgery: (I) during thyroidectomy and before CLND; (II) after CLND was completed; and (III) after the specimen was removed, and the excitation light was used to search for the PTGs in the isolated specimen. For intraoperative parathyroid identification via ICGT, 0.5 mL sterile saline was injected into the target tissue using a 1 mL syringe. Subsequently, 3–4 precise needle punctures were performed with the same syringe to enhance interstitial fluid extraction. The eluate was aspirated through controlled aspiration and precisely applied to a PTH rapid diagnostic strip. Following standardized incubation, initial visual assessment was conducted to verify the presence of two distinct reaction bands. The strip was then inserted into an automated analyzer for quantitative validation, where optical scanning detected PTH concentrations exceeding the predefined threshold (>65 ng/mL). Tissues meeting both qualitative (dual-band visualization) and quantitative (machine-read PTH >65 ng/mL) criteria were confirmed as parathyroid tissue (as illustrated in Figure 2).

Figure 1 Intraoperative images of parathyroid glands identified using NIRAF imaging technology. (A) White light image of the operative field; (B) autofluorescence image of the operative field. The white arrows indicate the parathyroid glands. NIRAF, near-infrared autofluorescence.

Figure 2 Images of intraoperative rapid PTH detection using ICGT technology. (A) PTH detection reagent strip, white arrow shows the number of bands in the reaction zone of the reagent strip; (B) PTH detection analyzer, white arrow shows the value of the detection result. ICGT, immunocolloidal gold technique; PTH, parathyroid hormone.

Intraoperative determination of PTGs

In the control group, intraoperative identification was conducted by two senior surgeons (each with over 5 years of thyroid surgery experience). When both surgeons concurred that the target tissue represented a PTG, it was documented as an intact parathyroid. In the observation group, parathyroid confirmation required both: (I) fluorescence imaging demonstrating round/oval hyperintense signals, and (II) positive ICGT verification. In instances where surgeons questioned the tissue identity or noted discrepancies between imaging results and clinical judgment, excised suspect specimens underwent intraoperative frozen section analysis. Any intraoperatively identified parathyroid tissue subjected to accidental resection was immediately autotransplanted. All surgical specimens received histopathological evaluation through paraffin embedding to detect potential parathyroid excisions.

Observation indexes

Intraoperative documentation included: (I) total PTG identification count; (II) in-situ preservation rate; (III) accidental resection incidents; and (IV) autotransplantation frequency across both cohorts. Postoperative monitoring encompassed serial measurements of serum calcium (reference range, 2.11–2.52 mmol/L) and PTH (reference range, 15–65 pg/mL) at standardized intervals: postoperative days 1 and 3, followed by months 1, 3, and 6.

Transient hypoparathyroidism was defined by meeting ≥1 criterion:

• PTH <15 pg/mL on postoperative day 1;
• Neuromuscular symptoms (digital/labial paresthesia or tetany);
• Persistent hypocalcemia (serum calcium <2.11 mmol/L at consecutive assessments), with biochemical/clinical normalization within 90 days. Conditions fulfilling these criteria beyond 6 months confirmed permanent hypoparathyroidism.

Follow-up

Patients demonstrating postoperative hypocalcemia and/or biochemically confirmed hypoparathyroidism were monitored through standardized surveillance protocols comprising outpatient evaluations, WeChat-based consultations, and structured telephone interviews. For cases failing to achieve biochemical normalization (serum calcium ≥2.11 mmol/L and PTH ≥15 pg/mL) within 90 postoperative days, extended surveillance protocols were systematically implemented through postoperative month 6 to confirm temporal resolution patterns.

Statistical analysis

Statistical analyses were performed using SPSS 27.0 (IBM Corp., Armonk, NY, USA). Continuous variables underwent normality assessment via the Shapiro-Wilk (S-W) test. Normally distributed data were presented as mean ± standard deviation (SD) and analyzed using independent samples t-test, while non-normally distributed data were expressed as median with interquartile range (IQR) and compared through Mann-Whitney U test. Categorical variables were summarized as frequencies (%) with between-group comparisons conducted by Chi-squared (χ²) test. A threshold of P<0.05 defined statistical significance.

Results

Comparison of preoperative data

No significant intergroup differences were observed in demographic characteristics (gender, age), clinical parameters (hospitalization duration, TNM-stage), or preoperative biochemical profiles [serum calcium/PTH/25(OH)D concentrations] (all P>0.05) (Table 1).

Comparison of intraoperative identification of PTG

The observation group demonstrated superior parathyroid outcomes compared to controls: gland identification (132 glands; 3.9 per patient vs. 97 glands; 3.5 per patient, P=0.004) and preservation rate (128 glands; 3.8 per patient vs. 83 glands; 3.0 per patient, P<0.001). Auto-transplantation procedures were significantly reduced in the observation group (4 patients/4 grafts) versus controls (13 patients/14 graft; P=0.009). Histopathological analysis revealed fewer inadvertent excisions in the observation group (1 vs. 5 cases, P=0.14). Operative duration was shorter in the observation group (120.6±20.5 minutes) compared to controls (145.6±30.1 minutes; P<0.001) (Table 2).

Postoperative comparison of blood calcium, PTH and complications

On postoperative day 1, the observation group maintained higher serum calcium levels (2.11±0.13 vs. 1.94±0.10 mmol/L; P<0.001), representing 9.05% and 14.91% reductions from preoperative baselines, respectively. Concurrently, PTH levels were significantly preserved in the observation group [median 16.88 pg/mL (IQR 4.97) vs. 10.50 pg/mL (IQR 3.70); P<0.001], corresponding to respective declines of 64.0% vs. 81.63% from preoperative values. The observation group demonstrated superior parathyroid functional protection: lower incidence of transient hypoparathyroidism (n=10 vs. n=16; P=0.03) and reduced hypocalcemia rates (n=12 vs. n=18; P=0.02). By postoperative day 3, serum calcium levels remained favorable in the observation group (2.17±0.77 vs. 2.08±0.11 mmol/L; P<0.001) with significantly recovered PTH levels [25.38 pg/mL (IQR 3.38) vs. 14.32 pg/mL (IQR 2.08); P<0.001] (Table 3). All observation group patients achieved normalized PTH levels within 1 month postoperatively. In contrast, one control patient exhibited persistent hormonal insufficiency (>6 months postoperatively), requiring permanent calcium supplementation for symptomatic hypocalcemia management, confirming permanent hypoparathyroidism.

Discussion

As the predominant endocrine malignancy globally, thyroid cancer necessitates surgical management through total thyroidectomy with CLND as the therapeutic cornerstone. Nevertheless, iatrogenic hypoparathyroidism secondary to intraoperative parathyroid disruption persists as a significant clinical challenge in postoperative care (18). Traditional intraoperative identification methods of PTGs include visual identification, specific gravity method, and cryopathologic examination. However, visual identification is more subjective and has a large error margin. The specific gravity method cannot identify PTGs in situ and needs to be measured ex vivo. When PTGs are wrapped in surrounding fat, they will float on the water surface and are likely to be mistaken as fat globules and cut. Cryopathologic examination is complicated, and the operator has to wait for a longer time (>30 min). Emerging in situ identification technologies for PTGs, including NIRAF and ICGT (10,12), have obtained provisional clinical validation yet remain constrained by modality-specific limitations. This technological impasse has catalyzed the development of multimodal integration protocols, where synergistic use of complementary techniques demonstrates enhanced protection outcomes. Our investigation pioneers the clinical evaluation of dual-modality NIRAF-ICGT integration for precision parathyroid mapping during thyroid cancer resection, with particular emphasis on anatomical preservation optimization.

Principle and clinical application of NIRAF and ICGT

NIRAF leverages the inherent optical properties of PTGs, where endogenous fluorophores under specific wavelength excitation emit characteristic fluorescence signals (peak 820–840 nm). This label-free technique creates 3.8–5.1 times stronger autofluorescence in parathyroids compared to thyroid/lymphatic tissues, enabling real-time intraoperative identification without exogenous contrast agents. As a new non-invasive and non-toxic technique, NIRAF has already played an important role in clinical practice (19,20). Compared to traditional visualization, NIRAF can accurately localize PTGs during surgery and protect their functional integrity, increase the rate of in situ parathyroid preservation, and reduce the incidence of postoperative hypocalcemia or hypoparathyroidism. In addition, NIRAF can visualize isolated specimens, which can be used to find PTGs that have been inadvertently removed during surgery and perform autotransplantation. However, the use of NIRAF requires certain skills to avoid false-negative or false-positive results (21). Because PTH is specifically secreted and expressed in PTGs, measuring PTH levels in samples has been shown to be very reliable for identifying parathyroid tissue, and some have even equated ICGT results with cryopathologic examination. ICGT is quantitative, simple, minimally invasive, and time-saving, which has been shown to help surgeons quickly identify PTGs during surgery to avoid inadvertent resection, thus effectively reducing the probability of postoperative complications in patients compared to traditional visualization (10). However, ICGT technology cannot locate the position of the PTG during surgery. To address the inherent limitations of monomodal approaches, we developed a novel NIRAF-ICGT integration protocol designed for synergistic parathyroid evaluation. While previous efforts have explored NIRAF-indocyanine green (ICG) (22) and ICG-carbon nanoparticles (CNP) (16) combinations in thyroid surgery, our cost-benefit optimized technique surpasses existing models through dual functional assessment: real-time quantitative detection (via ICGT) concurrent with metabolic status quantification (through NIRAF). This bimodal integration enables comprehensive intraoperative evaluation of both anatomical integrity and endocrine functionality of PTGs. As the ICGT test values are positively correlated with parathyroid function. The incremental cost analysis revealed that the principal expenditure for the observation cohort originated from PTH rapid assay reagents (USD 50 per case). Notably, surgical proficiency with this combined modality was attainable following 2–3 procedural simulations, demonstrating an abbreviated learning curve characteristic of the technique’s operational efficiency.

Analysis of the results of this study

In the study, the observation group employed the combined technique of NIRAF and ICGT. This significantly enhanced the number of PTGs identified during the operation and shortened the operative time. More importantly, it could also identify the PTGs in the isolated tissues, effectively avoiding incorrect excision. It is widely known that the most effective way to avoid postoperative hypoparathyroidism is to identify and protect the PTGs and their surrounding blood supply during surgery (18). Because fluorescence has a certain degree of penetration into tissues, NIRAF can locate the PTGs before the surgical dissection of the thyroid capsule, while visual confirmation of the PTGs needs to be carried out during the dissection of the thyroid capsule. Therefore, the doctors in the observation group were able to carry out the protection of the PTGs’ blood supply in a more targeted manner, which significantly increased the number of in situ retained PTGs during the operation and effectively reduced the risk of postoperative complications (23). In addition, even when autologous transplantation was required, the combined technique in the observation group significantly shortened the time of PTG removal from the body, promoting vascularization and accelerating rapid recovery of parathyroid function. This is similar to Chen’s research findings (24). Nevertheless, the patients in the observation group still showed a certain degree of decrease in blood calcium and PTH levels after surgery, which was attributed to the transient insufficient blood supply to the PTGs due to edema and compression of the surrounding soft tissues caused by surgical pulling, tissue dissection, and the use of energy devices. This suggests that we should monitor the changes of blood calcium and PTH levels in the early postoperative period and provide timely calcium supplementation and other symptomatic treatments to avoid serious complications. For patients with hypocalcemia, intravenous calcium supplementation combined with oral calcium tablets constitutes the primary therapeutic approach. The detection of reduced serum PTH levels necessitates adjunctive administration of oral calcitriol. Continuous biochemical monitoring of calcium and PTH concentrations should be implemented to guide real-time dosage adjustments.

Inadequacies and prospects of this study

This study is a single-center retrospective study with a small number of cases included and a short follow-up period. The surgeons are not blinded to whether it is the control group or the observation group patient. There is a lack of data to identify the location and type of PTGs intraoperatively. In addition, surgical procedures require specialized near-infrared fluorescence imaging equipment, and some hospitals may lack it, limiting their promotion and application. Furthermore, it should be emphasized that during the ICGT surgical procedure, a 1ml syringe is needed to inject saline into the target PTG to obtain puncture eluent, which may cause rupture of the PTG capsule or even damage to the gland. Suzuki et al. reported that immediate hematoma occurred in 5% of parathyroid puncture cases, and delayed complications such as inflammatory response, abscess formation, and hematoma were observed in 10% of cases (25). This requires us to perform as carefully as possible during the operation to ensure the integrity of the gland. We should avoid injecting too much saline (≤0.5 mL) into the gland and pay attention to control the number of punctures (3–4 times). These findings underscore the necessity for future multicenter randomized controlled trials (RCTs) employing triple-blinding protocols with enhanced statistical power. Study designs should incorporate three-dimensional anatomical mapping of intraoperatively identified PTGs, including spatial coordinates and vascular anatomical classification. Technical refinements may focus on developing quantitative perfusion metrics through microvascular hemodynamic analysis, or establishing dynamic imaging-biochemical feedback systems. Long-term endocrine functional outcomes require standardized evaluation via extended surveillance periods (minimum 24-month follow-up). Such methodological advancements will ultimately enable precise validation of the NIRAF-ICGT multimodal platform’s clinical utility in parathyroid preservation during oncologic thyroidectomy.

Conclusions

In summary, the NIRAF-ICGT integration demonstrates superior intraoperative discrimination of PTGs compared to conventional traditional visual inspection in thyroid oncology procedures. This technique optimizes in situ preservation through real-time imaging, significantly mitigating iatrogenic excision risks. Consequently, it achieves a statistically validated reduction in postoperative hypoparathyroidism incidence (P<0.05), establishing its critical role in functional endocrine tissue conservation.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-118/rc

Data Sharing Statement: Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-118/dss

Peer Review File: Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-118/prf

Funding: The study was supported by Tianjin Health Science and Technology Project (No. TJWJ2024MS020) and Tianjin Medical Key Discipline (Specialty) Construction Project (No. TJYXZDXK-058B).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://gs.amegroups.com/article/view/10.21037/gs-2025-118/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. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. This study was approved by the Research Ethics Committee of Tianjin Union Medical Center, The First Affiliated Hospital of Nankai University (No. 2024B78). All enrolled patients signed informed consent.

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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