Skip to main content
Log in

Near-infrared autofluorescence-based parathyroid glands identification in the thyroidectomy or parathyroidectomy: a systematic review and meta-analysis

  • Systematic Reviews and Meta-analyses
  • Published:
Langenbeck's Archives of Surgery Aims and scope Submit manuscript

Abstract

Purpose

To evaluate the diagnostic accuracy of near-infrared autofluorescence-based identification in the identification of parathyroid glands during thyroidectomy or parathyroidectomy.

Methods

The clinical studies were retrieved from PubMed, the Cochrane Central Register of Controlled Trials, Embase, Web of Science, SCOPUS, and Google Scholar. The study protocol was registered on Open Science Framework (https://osf.io/um8rj/). The search period ranged from the date of each database’s inception to May 2021. Cohort studies dealing with patients of whom parathyroid glands were detected by near-infrared autofluorescence and confirmed clinically or pathologically during thyroidectomy or parathyroidectomy were included. Editorials, letters, “how-I-do-it” descriptions, other site head and neck tumors, and articles with lack of diagnostic identification data were excluded. True positive, true negative, false positive, and false negative were extracted. The QUDAS ver. 2 was used to evaluate the methodological quality.

Results

Seventeen studies with 1198 participants were evaluated in this analysis. Near-infrared autofluorescence-based identification of parathyroid glands showed a diagnostic odds ratio of 228.8759 (95% confidence interval, 134.1099; 390.6063). The area under the summary receiver operating characteristic curve was 0.967. The sensitivity, specificity, negative predictive value, and positive predictive value were 0.9693 (0.9491; 0.9816), 0.9248 (0.8885; 0.9499), 0.9517 (0.8981; 0.9778), and 0.9488 (0.9167; 0.9689), respectively. Subgroup analyses were performed to compare two autofluorescence detection methods, because there was high heterogeneity in the outcomes. The diagnostic accuracy was higher in probe-based detection than in image-based detection.

Conclusions

Near-infrared autofluorescence-based identification is valuable for identifying the parathyroid glands of patients during thyroidectomy or parathyroidectomy.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Paras C, Keller M, White L, Phay J, Mahadevan-Jansen A (2011) Near-infrared autofluorescence for the detection of parathyroid glands. J Biomed Opt 16:067012. https://doi.org/10.1117/1.3583571

    Article  PubMed  Google Scholar 

  2. Solórzano CC, Thomas G, Berber E, Wang TS, Randolph GW, Duh QY, Triponez F (2020) Current state of intraoperative use of near infrared fluorescence for parathyroid identification and preservation. Surgery. 169:868–878. https://doi.org/10.1016/j.surg.2020.09.014

    Article  PubMed  Google Scholar 

  3. McWade MA, Paras C, White LM, Phay JE, Solórzano CC, Broome JT, Mahadevan-Jansen A (2014) Label-free intraoperative parathyroid localization with near-infrared autofluorescence imaging. J Clin Endocrinol Metab 99:4574–4580. https://doi.org/10.1210/jc.2014-2503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Falco J, Dip F, Quadri P, de la Fuente M, Prunello M, Rosenthal RJ (2017) Increased identification of parathyroid glands using near infrared light during thyroid and parathyroid surgery. Surg Endosc 31:3737–3742. https://doi.org/10.1007/s00464-017-5424-1

    Article  PubMed  Google Scholar 

  5. Falco J, Dip F, Quadri P, de la Fuente M, Rosenthal R (2016) Cutting edge in thyroid surgery: autofluorescence of parathyroid glands. J Am Coll Surg 223:374–380. https://doi.org/10.1016/j.jamcollsurg.2016.04.049

    Article  PubMed  Google Scholar 

  6. Akbulut S, Erten O, Gokceimam M, Kim YS, Krishnamurthy V, Heiden K, Jin J, Siperstein A, Berber E (2021) Intraoperative near-infrared imaging of parathyroid glands: a comparison of first- and second-generation technologies. J Surg Oncol 123:866–871. https://doi.org/10.1002/jso.26336

    Article  PubMed  Google Scholar 

  7. Barbieri D, Indelicato P, Vinciguerra A, Di Marco F, Formenti AM, Trimarchi M, Bussi M (2020) Autofluorescence and indocyanine green in thyroid surgery: a systematic review and meta-analysis. Laryngoscope. 131:1683–1692. https://doi.org/10.1002/lary.29297

    Article  PubMed  Google Scholar 

  8. Bonnin-Pascual J, Álvarez-Segurado C, Jiménez-Segovia M, Bianchi A, Bonnin-Pascual F, Molina-Romero FX, González-Argente FX (2018) Contributions of fluorescence to endocrine surgery. Cir Esp (Engl Ed) 96:529–536. https://doi.org/10.1016/j.ciresp.2018.09.005

    Article  Google Scholar 

  9. Abbaci M, De Leeuw F, Breuskin I, Casiraghi O, Lakhdar AB, Ghanem W, Laplace-Builhé C, Hartl D (2018) Parathyroid gland management using optical technologies during thyroidectomy or parathyroidectomy: a systematic review. Oral Oncol 87:186–196. https://doi.org/10.1016/j.oraloncology.2018.11.011

    Article  PubMed  Google Scholar 

  10. Alesina PF, Meier B, Hinrichs J, Mohmand W, Walz MK (2018) Enhanced visualization of parathyroid glands during video-assisted neck surgery. Langenbeck's Arch Surg 403:395–401. https://doi.org/10.1007/s00423-018-1665-2

    Article  CAS  Google Scholar 

  11. Benmiloud F, Godiris-Petit G, Gras R, Gillot JC, Turrin N, Penaranda G, Noullet S, Chéreau N, Gaudart J, Chiche L, Rebaudet S (2020) Association of autofluorescence-based detection of the parathyroid glands during total thyroidectomy with postoperative hypocalcemia risk: results of the PARAFLUO multicenter randomized clinical trial. JAMA Surg 155:106–112. https://doi.org/10.1001/jamasurg.2019.4613

    Article  PubMed  Google Scholar 

  12. Benmiloud F, Rebaudet S, Varoquaux A, Penaranda G, Bannier M, Denizot A (2018) Impact of autofluorescence-based identification of parathyroids during total thyroidectomy on postoperative hypocalcemia: a before and after controlled study. Surgery 163:23–30. https://doi.org/10.1016/j.surg.2017.06.022

    Article  PubMed  Google Scholar 

  13. Cui L, Gao Y, Yu H, Li M, Wang B, Zhou T, Hu Q (2017) Intraoperative parathyroid localization with near-infrared fluorescence imaging using indocyanine green during total parathyroidectomy for secondary hyperparathyroidism. Sci Rep 7:8193. https://doi.org/10.1038/s41598-017-08347-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. De Leeuw F, Breuskin I, Abbaci M, Casiraghi O, Mirghani H, Ben Lakhdar A, Laplace-Builhé C, Hartl D (2016) Intraoperative near-infrared imaging for parathyroid gland identification by auto-fluorescence: a feasibility study. World J Surg 40:2131–2138. https://doi.org/10.1007/s00268-016-3571-5

    Article  PubMed  Google Scholar 

  15. Demarchi MS, Karenovics W, Bédat B, De Vito C, Triponez F (2021) Autofluorescence pattern of parathyroid adenomas. BJS Open 5. https://doi.org/10.1093/bjsopen/zraa047

  16. DiMarco A, Chotalia R, Bloxham R, McIntyre C, Tolley N, Palazzo FF (2019) Autofluorescence in parathyroidectomy: signal intensity correlates with serum calcium and parathyroid hormone but routine clinical use is not justified. World J Surg 43:1532–1537. https://doi.org/10.1007/s00268-019-04929-9

    Article  PubMed  Google Scholar 

  17. DiMarco A, Chotalia R, Bloxham R, McIntyre C, Tolley N, Palazzo FF (2019) Does fluoroscopy prevent inadvertent parathyroidectomy in thyroid surgery? Ann R Coll Surg Engl 101:508–513. https://doi.org/10.1308/rcsann.2019.0065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Dip F, Falco J, Verna S, Prunello M, Loccisano M, Quadri P, White K, Rosenthal R (2019) Randomized controlled trial comparing white light with near-infrared autofluorescence for parathyroid gland identification during total thyroidectomy. J Am Coll Surg 228:744–751. https://doi.org/10.1016/j.jamcollsurg.2018.12.044

    Article  PubMed  Google Scholar 

  19. Idogawa H, Sakashita T, Homma A (2020) A novel study for fluorescence patterns of the parathyroid glands during surgery using a fluorescence spectroscopy system. Eur Arch Otorhinolaryngol 277:1525–1529. https://doi.org/10.1007/s00405-020-05849-4

    Article  PubMed  Google Scholar 

  20. Idogawa H, Sakashita T, Yagi T, Segawa K, Homma A (2020) Pathological evaluation of the accuracy of a fluorescence spectroscopy system for detecting parathyroid glands. Eur Arch Otorhinolaryngol 277:3145–3147. https://doi.org/10.1007/s00405-020-06011-w

    Article  PubMed  Google Scholar 

  21. Jin H, Dong Q, He Z, Fan J, Liao K, Cui M (2018) Application of a fluorescence imaging system with indocyanine green to protect the parathyroid gland intraoperatively and to predict postoperative parathyroidism. Adv Ther 35:2167–2175. https://doi.org/10.1007/s12325-018-0834-6

    Article  CAS  PubMed  Google Scholar 

  22. Kahramangil B, Berber E (2017) Comparison of indocyanine green fluorescence and parathyroid autofluorescence imaging in the identification of parathyroid glands during thyroidectomy. Gland Surg 6:644–648. https://doi.org/10.21037/gs.2017.09.04

    Article  PubMed  PubMed Central  Google Scholar 

  23. Kahramangil B, Dip F, Benmiloud F, Falco J, de La Fuente M, Verna S, Rosenthal R, Berber E (2018) Detection of parathyroid autofluorescence using near-infrared imaging: a multicenter analysis of concordance between different surgeons. Ann Surg Oncol 25:957–962. https://doi.org/10.1245/s10434-018-6364-2

    Article  PubMed  Google Scholar 

  24. Kim SW, Lee HS, Ahn YC, Park CW, Jeon SW, Kim CH, Ko JB, Oak C, Kim Y, Lee KD (2018) Near-infrared autofluorescence image-guided parathyroid gland mapping in thyroidectomy. J Am Coll Surg 226:165–172. https://doi.org/10.1016/j.jamcollsurg.2017.10.015

    Article  PubMed  Google Scholar 

  25. Kim SW, Song SH, Lee HS, Noh WJ, Oak C, Ahn YC, Lee KD (2016) Intraoperative real-time localization of normal parathyroid glands with autofluorescence imaging. J Clin Endocrinol Metab 101:4646–4652. https://doi.org/10.1210/jc.2016-2558

    Article  CAS  PubMed  Google Scholar 

  26. Kim Y, Kim SW, Lee KD, Ahn YC (2019) Video-assisted parathyroid gland mapping with autofocusing. J Biophotonics 12:e201900017. https://doi.org/10.1002/jbio.201900017

  27. Kose E, Kahramangil B, Aydin H, Donmez M, Berber E (2019) Heterogeneous and low-intensity parathyroid autofluorescence: patterns suggesting hyperfunction at parathyroid exploration. Surgery 165:431–437. https://doi.org/10.1016/j.surg.2018.08.006

    Article  PubMed  Google Scholar 

  28. Kose E, Rudin AV, Kahramangil B, Moore E, Aydin H, Donmez M, Krishnamurthy V, Siperstein A, Berber E (2020) Autofluorescence imaging of parathyroid glands: an assessment of potential indications. Surgery 167:173–179. https://doi.org/10.1016/j.surg.2019.04.072

    Article  PubMed  Google Scholar 

  29. Ladurner R, Al Arabi N, Guendogar U, Hallfeldt K, Stepp H, Gallwas J (2018) Near-infrared autofluorescence imaging to detect parathyroid glands in thyroid surgery. Ann R Coll Surg Engl 100:33–36. https://doi.org/10.1308/rcsann.2017.0102

    Article  CAS  PubMed  Google Scholar 

  30. Ladurner R, Lerchenberger M, Al Arabi N, Gallwas JKS, Stepp H, Hallfeldt KKJ (2019) Parathyroid autofluorescence—how does it affect parathyroid and thyroid surgery? A 5 year experience. Molecules 24. https://doi.org/10.3390/molecules24142560

  31. Ladurner R, Sommerey S, Arabi NA, Hallfeldt KKJ, Stepp H, Gallwas JKS (2017) Intraoperative near-infrared autofluorescence imaging of parathyroid glands. Surg Endosc 31:3140–3145. https://doi.org/10.1007/s00464-016-5338-3

    Article  PubMed  Google Scholar 

  32. Lerchenberger M, Al Arabi N, Gallwas JKS, Stepp H, Hallfeldt KKJ, Ladurner R (2019) Intraoperative near-infrared autofluorescence and indocyanine green imaging to identify parathyroid glands: a comparison. Int J Endocrinol 2019:4687951–4687957. https://doi.org/10.1155/2019/4687951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Liu J, Wang X, Wang R, Xu C, Zhao R, Li H, Zhang S, Yao X (2020) Near-infrared auto-fluorescence spectroscopy combining with Fisher’s linear discriminant analysis improves intraoperative real-time identification of normal parathyroid in thyroidectomy. BMC Surg 20:4. https://doi.org/10.1186/s12893-019-0670-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. McWade MA, Paras C, White LM, Phay JE, Mahadevan-Jansen A, Broome JT (2013) A novel optical approach to intraoperative detection of parathyroid glands. Surgery 154:1371–1377; discussion. https://doi.org/10.1016/j.surg.2013.06.046

    Article  PubMed  Google Scholar 

  35. McWade MA, Sanders ME, Broome JT, Solórzano CC, Mahadevan-Jansen A (2016) Establishing the clinical utility of autofluorescence spectroscopy for parathyroid detection. Surgery 159:193–202. https://doi.org/10.1016/j.surg.2015.06.047

    Article  PubMed  Google Scholar 

  36. McWade MA, Thomas G, Nguyen JQ, Sanders ME, Solórzano CC, Mahadevan-Jansen A (2019) Enhancing parathyroid gland visualization using a near infrared fluorescence-based overlay imaging system. J Am Coll Surg 228:730–743. https://doi.org/10.1016/j.jamcollsurg.2019.01.017

    Article  PubMed  PubMed Central  Google Scholar 

  37. Papavramidis TS, Chorti A, Tzikos G, Anagnostis P, Pantelidis P, Pliakos I, Panidis S, Papaioannou M, Bakkar S, Unal E, Michalopoulos A (2021) The effect of intraoperative autofluorescence monitoring on unintentional parathyroid gland excision rates and postoperative PTH concentrations—a single-blind randomized-controlled trial. Endocrine 72:546–552. https://doi.org/10.1007/s12020-020-02599-5

    Article  CAS  PubMed  Google Scholar 

  38. Serra C, Silveira L, Canudo A (2020) Identification of inadvertently removed parathyroid glands during thyroid surgery using autofluorescence. Gland Surg 9:893–898. https://doi.org/10.21037/gs-20-163

    Article  PubMed  PubMed Central  Google Scholar 

  39. Squires MH, Jarvis R, Shirley LA, Phay JE (2019) Intraoperative parathyroid autofluorescence detection in patients with primary hyperparathyroidism. Ann Surg Oncol 26:1142–1148. https://doi.org/10.1245/s10434-019-07161-w

    Article  PubMed  Google Scholar 

  40. Takahashi T, Yamazaki K, Ota H, Shodo R, Ueki Y, Horii A (2020) Near-infrared fluorescence imaging in the identification of parathyroid glands in thyroidectomy. Laryngoscope. 131:1188–1193. https://doi.org/10.1002/lary.29163

    Article  CAS  PubMed  Google Scholar 

  41. Thomas G, McWade MA, Nguyen JQ, Sanders ME, Broome JT, Baregamian N, Solórzano CC, Mahadevan-Jansen A (2019) Innovative surgical guidance for label-free real-time parathyroid identification. Surgery 165:114–123. https://doi.org/10.1016/j.surg.2018.04.079

    Article  PubMed  Google Scholar 

  42. Thomas G, McWade MA, Paras C, Mannoh EA, Sanders ME, White LM, Broome JT, Phay JE, Baregamian N, Solórzano CC, Mahadevan-Jansen A (2018) Developing a clinical prototype to guide surgeons for intraoperative label-free identification of parathyroid glands in real time. Thyroid 28:1517–1531. https://doi.org/10.1089/thy.2017.0716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Thomas G, Squires MH, Metcalf T, Mahadevan-Jansen A, Phay JE (2019) Imaging or fiber probe-based approach? Assessing different methods to detect near infrared autofluorescence for intraoperative parathyroid identification. J Am Coll Surg 229:596–608.e593. https://doi.org/10.1016/j.jamcollsurg.2019.09.003

    Article  PubMed  PubMed Central  Google Scholar 

  44. Wolf HW, Grumbeck B, Runkel N (2019) Intraoperative verification of parathyroid glands in primary and secondary hyperparathyroidism using near-infrared autofluorescence (IOPA). Updat Surg 71:579–585. https://doi.org/10.1007/s13304-019-00652-1

    Article  Google Scholar 

  45. Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Bmj 339:b2535. https://doi.org/10.1136/bmj.b2535

    Article  PubMed  PubMed Central  Google Scholar 

  46. Goossen K, Tenckhoff S, Probst P, Grummich K, Mihaljevic AL, Büchler MW, Diener MK (2018) Optimal literature search for systematic reviews in surgery. Langenbeck's Arch Surg 403:119–129. https://doi.org/10.1007/s00423-017-1646-x

    Article  Google Scholar 

  47. 8th Biennial Congress of the European Society of Endocrine Surgeons (2018). Langenbecks Arch Surg 403:403-423. https://doi.org/10.1007/s00423-018-1664-3

  48. Gatsonis C, Paliwal P (2006) Meta-analysis of diagnostic and screening test accuracy evaluations: methodologic primer. AJR Am J Roentgenol 187:271–281. https://doi.org/10.2214/ajr.06.0226

    Article  PubMed  Google Scholar 

  49. Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, Leeflang MM, Sterne JA, Bossuyt PM (2011) QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 155:529–536. https://doi.org/10.7326/0003-4819-155-8-201110180-00009

    Article  Google Scholar 

  50. Schünemann HJ, Oxman AD, Brozek J, Glasziou P, Jaeschke R, Vist GE, Williams JW Jr, Kunz R, Craig J, Montori VM, Bossuyt P, Guyatt GH (2008) Grading quality of evidence and strength of recommendations for diagnostic tests and strategies. Bmj 336:1106–1110. https://doi.org/10.1136/bmj.39500.677199.AE

    Article  PubMed  PubMed Central  Google Scholar 

  51. Schünemann HJ, Oxman AD, Brozek J, Glasziou P, Bossuyt P, Chang S, Muti P, Jaeschke R, Guyatt GH (2008) GRADE: assessing the quality of evidence for diagnostic recommendations. ACP J Club 149:2

    PubMed  Google Scholar 

  52. Neagoe RM, Cvasciuc IT, Muresan M, Sala DT (2017) Incidental parathyroidectomy during thyroid surgery-risk, prevention and controversies; an evidence-based review. Acta endocrinologica (Bucharest, Romania : 2005) 13:467–475. https://doi.org/10.4183/aeb.2017.467

    Article  CAS  Google Scholar 

  53. Fleming PS, Koletsi D, Ioannidis JP, Pandis N (2016) High quality of the evidence for medical and other health-related interventions was uncommon in Cochrane systematic reviews. J Clin Epidemiol 78:34–42. https://doi.org/10.1016/j.jclinepi.2016.03.012

    Article  PubMed  Google Scholar 

  54. Nielsen SM, Zobbe K, Kristensen LE, Christensen R (2018) Nutritional recommendations for gout: an update from clinical epidemiology. Autoimmun Rev 17:1090–1096. https://doi.org/10.1016/j.autrev.2018.05.008

    Article  CAS  PubMed  Google Scholar 

  55. Alexander PE, Bero L, Montori VM, Brito JP, Stoltzfus R, Djulbegovic B, Neumann I, Rave S, Guyatt G (2014) World Health Organization recommendations are often strong based on low confidence in effect estimates. J Clin Epidemiol 67:629–634. https://doi.org/10.1016/j.jclinepi.2013.09.020

    Article  PubMed  Google Scholar 

  56. PradeepKumar AR, Shemesh H, Nivedhitha MS, Hashir MMJ, Arockiam S, Uma Maheswari TN, Natanasabapathy V (2021) Diagnosis of vertical root fractures by cone beam computed tomography in root filled teeth with confirmation by direct visualization—a systematic review and meta-analysis. J Endod. https://doi.org/10.1016/j.joen.2021.04.022

Download references

Availability of data and material

The disclosure of raw data of individual articles is not available as this manuscript is a systematic review and meta-analysis.

Funding

This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2018R1D1A1B07045421, 2020R1I1A1A01051844) and the Bio & Medical Technology Development Program of the National Research Foundation (NRF) funded by the Ministry of Science & ICT (2019M3A9H2032424, 2019M3E5D5064110). The sponsors had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author information

Authors and Affiliations

Authors

Contributions

Study conception and design: DHK, SHH. Acquisition of data: SL, JJ, SK, SEK. Analysis and interpretation of data: DHK, SL, JJ, SK, SEK, SHH. Drafting of manuscript: DHK, SHH. Critical revision of manuscript: DHK, SL, JJ, SK, SEK, SHH.

Corresponding author

Correspondence to Se Hwan Hwang.

Ethics declarations

Ethical consideration

This article does not contain any studies with human participants or animals performed by any of the authors. Our institute waived this systematic review and meta-analysis.

Consent to participate/consent for publication

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

ESM 1

(DOCX 18 kb)

ESM 2

(DOCX 18 kb)

ESM 3

(DOCX 14 kb)

ESM 4

(DOCX 14 kb)

ESM 5

(TIF 1129 kb)

High resulotion image (PNG 821 kb)

ESM 6

(TIF 1125 kb)

High resulotion image (PNG 823 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, D.H., Lee, S., Jung, J. et al. Near-infrared autofluorescence-based parathyroid glands identification in the thyroidectomy or parathyroidectomy: a systematic review and meta-analysis. Langenbecks Arch Surg 407, 491–499 (2022). https://doi.org/10.1007/s00423-021-02269-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00423-021-02269-8

Keywords

Navigation