Abstract
Introduction
Identifying the parathyroid gland during surgery may be difficult for surgeons. It is critical for them to be able to locate it during thyroidectomy or parathyroidectomy because of the significant function of the parathyroid in the calcium balance. According to recent reports, intrinsic fluorescence of the parathyroid has been found. There is some evidence to suggest that new equipment can detect the fluorescence via imaging technology. In this study, a newly invented intraoperative fluorescence imaging system and indocyanine green (ICG) dye were applied to detect the parathyroid glands and evaluate the vascularization of the parathyroid.
Methods
From 1 May to 8 August 2018, 26 patients underwent total thyroidectomy in Zhuhai People’s Hospital. These 26 subjects were recruited in our research. All identified parathyroid glands were scored visually from grade 0 to grade 2 according to the vascularity of the parathyroid before ICG angiography was performed. After ICG angiography, the parathyroid glands were scored from 0 to 2 according to the fluorescence intensity (FI).
Results
Visual scores were significantly higher than ICG angiography scores. In the 22 patients with at least one parathyroid gland with an ICG score of 2, postoperative parathyroidism (PTH) levels were in the normal range. Of the four patients with no parathyroid gland with an ICG score of 2, two developed transient hypoparathyroidism, with recovery on postoperative day (POD) 7 for the first patient and after 3 months for the second.
Conclusion
This study has shown that a fluorescence imaging system applied with indocyanine green is a safe, easy and effective method to protect the parathyroid and predict postoperative parathyroidism.
Trial Registration
Chinese Clinical Trial Registry no. ChiCTR1800016864.
Similar content being viewed by others
References
Slakter JS, Yannuzzi LA, Guyer DR, et al. Indocyanine-green angiography. Curr Opin Ophthalmol. 1995;6:25–32.
Hayashi K, Hasegawa Y, Tokoro T, Delaey JJ. Valve of indocyanine green angiography in the diagnosis of occult choroidal neovascular membrane. Jpn J Ophthalmol. 1988;32:827–9.
Destro M, Puliafito CA. Indocyanine green videoangiography of choroidal neovascularization. Ophthalmology. 1989;96:846–53.
Reichel E, Puliafito CA, Duker JS, Guyer DR. Indocyanine green dye-enhanced diode laser photocoagulation of poorly defined sub-foveal choroidal neovascularization. Ophthalmic Surg. 1994;25:195–201.
Gioux S, Choi HS, Frangioni JV. Image-guided surgery using invisible near-infrared light: fundamentals of clinical translation. Mol Imaging. 2010;9(5):237–55.
Imboden S, Papadia A, Nauwerk M, et al. A comparison of radiocolloid and indocyanine green fluorescence imaging, sentinel lymph node mapping in patients with cervical cancer undergoing laparoscopic surgery. Ann Surg Oncol. 2015;22(13):4198–203.
Halle BM, Poulsen TD, Pedersen HP. Indocyanine green plasma disappearance rate as dynamic liver function test in critically ill patients. Acta Anaesthesiol Scand. 2014;58(10):1214–9.
Edafe O, Antakia R, Laskar N, Uttley L, Balasubramanian SP. Systematic review and meta-analysis of predictors of post-thyroidectomy hypocalcaemia. Br J Surg. 2014;101(4):307–20.
Shoback D. Hypoparathyroidism. N Engl J Med. 2008;359(4):391–403.
Park I, Rhu J, Woo JW, et al. Preserving parathyroid gland vasculature to reduce post-thyroidectomy hypocalcemia. World J Surg. 2016;40:1382–9.
Vidal Fortuny J, Sadowski SM, Belfontali V, et al. Indocyanine green angiography in subtotal parathyroidectomy: technique for the function of the parathyroid remnant. J Am Coll Surg. 2016;223:43–9.
Desmettre T, Devoisselle JM, Mordon S. Fluorescence properties and metabolic features of indocyanine green (ICG) as related to angiography. Surv Ophthalmol. 2000;45(1):15–27.
Boni L, David G, Mangano A, et al. Clinical applications of indocyanine green (ICG) enhanced fluorescence in laparoscopic surgery. Surg Endosc. 2015;29(7):2046–55.
Lorente-Poch L, Sancho JJ, Muñoz-Nova JL, Sánchez-Velázquez P, Sitges-Serra A. Defining the syndromes of parathyroid failure after total thyroidectomy. Gland Surg. 2015;4(1):82–90.
Perry D, Bharara M, Armstrong DG, Mills J. Intraoperative fluorescence vascular angiography: during tibial bypass. J Diabetes Sci Technol. 2012;6(1):204–8.
Acknowledgements
We thank the patients and their families for participating in this study. Zhuhai People’s Hospital provided the necessary support of this study. Medical writing support in the form of development of the draft outline and manuscript drafts in consultation with the authors, editorial suggestions for draft versions of this paper, assembling tables and figures, collating author comments, copyediting, referencing and graphic services were provided by Chongwei Chi, PhD, of the Chinese Academy of Science, and Adjunct Assistant Prof. Dr. Karen M. von Deneen from the University of Florida for the modification of this paper.
Funding
No funding or sponsorship was received for this study or publication of this article. The article processing charges were funded by the authors.
Authorship
All named authors meet the International Committee of Medical Journal Editors (ICMJE) criteria for authorship for this manuscript, take responsibility for the integrity of the work as a whole and have given final approval for the version to be published.
Authorship Contributions
Hao Jin and Min Cui designed the study and drafted the manuscript. Qichao Dong, Jinrui Fan, Zhuocheng He and Kun Liao collected and analyzed the data and carried out the literature search. All authors interpreted the data, wrote/reviewed the manuscript and gave final approval of the manuscript.
Disclosures
Hao Jin, Qichao Dong, Zhuocheng He, Jinrui Fan, Kun Liao and Min Cui declare no conflict of interest.
Compliance with Ethics Guidelines
The study protocol was reviewed and approved by the relevant investigational center ethics committee or institutional review board, in accordance with the International Council on Harmonisation. The study was conducted in accordance with the Declaration of Helsinki and all participants provided written informed consent.
Data Availability
The data sets during and/or analyzed during the current study are available from the corresponding author on reasonable request.
Author information
Authors and Affiliations
Corresponding author
Additional information
Enhanced Digital Features
To view enhanced digital features go to https://doi.org/10.6084/m9.figshare.7291262.
Rights and permissions
About this article
Cite this article
Jin, H., Dong, Q., He, Z. et al. 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 (2018). https://doi.org/10.1007/s12325-018-0834-6
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12325-018-0834-6