Application of carbon nanoparticles in lymph node dissection and parathyroid protection during thyroid cancer surgeries: a systematic review and meta-analysis

Figures & data

Figure 1 Transmission electron microscopic image of CNs.

Notes: The main active component of CNs is nanosized polymeric carbon granules with an average diameter of 150 nm. Republished with permission of SAGE Publications, Inc., from Liu X, Chang S, Jiang X, Huang P, Yuan Z. Identifying parathyroid glands with carbon nanoparticle suspension does not help protect parathyroid function in thyroid surgery: a prospective, randomized control clinical study. Surg Innov. 2016;23(4):381–389. © The Author(s) 2016; permission conveyed through Copyright Clearance Center, Inc.¹⁸
Abbreviation: CN, carbon nanoparticle.

Figure 2 Intraoperative view of the black-stained clusters of lymph nodes by CN injection.

Notes: Reproduced with permission of John Wiley and Sons, from Zhu Y, Chen X, Zhang H, et al. Carbon nanoparticle-guided central lymph node dissection in clinically node-negative patients with papillary thyroid carcinoma. Head Neck. 2016;38(6):840–845. © 2015 Wiley Periodicals, Inc.¹⁹
Abbreviation: CN, carbon nanoparticle.

Figure 3 Flowchart of the literature search.

Table 1 Characteristics of the 47 RCTs included in the meta-analysis

Study	n	Male/female		Age, years, mean (SD)		Injection site	Dose (mL)	Waiting time	Staining rate (%)	Indicesa
		CNs	BL	CNs	BL
Chen et al (2016)^Citation25	173	15/72	13/73	33.46 (4.58)	34.32 (4.36)	Upper, middle, and lower points of the thyroid	0.3	5–10 min	NA	1, 4–6
Zhang et al (2016)^Citation26	37	3/14	3/17	41.1 (8.7)	43 (7.2)	In the bilateral thyroid	0.2–0.4	5–20 min	95.5	1–4
Liu et al (2016)^Citation18	156	16/62	17/61	NA	NA	Upper, middle, and lower parts of the lobes	0.4–0.8	NA	NA	4, 6
Li (2015)^Citation27	40	4/16	8/12	47.9 (11.2)	49.5 (12.4)	Top of the tumor	0.4–0.8	3 min	NA	4
Feng and He (2015)^Citation28	60	0/30	0/30	NA	NA	4 points around the tumor	0.8	NA	NA	4–6
Guo et al (2015)^Citation29	59	9/21	8/21	35 (9.5)	32 (8.2)	Upper, middle, and lower points of the bilateral thyroid	0.6	20 min	NA	6
Duan et al (2015)^Citation30	80	14/26	15/25	40.4 (7.18)	42.5 (7.65)	3–5 points around the thyroid	0.3–0.5	30 min	95.7	1, 2, 4, 5
Chen and Wu (2015)^Citation31	96	11/37	16/32	46.1 (10.9)	45.8 (12.6)	NA	NA	NA	NA	1, 5, 6
Du et al (2015)^Citation32	118	19/41	18/40	42.7 (10.6)	43.5 (10.8)	Upper and middle points of the thyroid	0.4	5 min	NA	4–6
Wang et al (2015)^Citation33	120	NA	NA	NA	NA	Upper and middle points of the thyroid	0.2	15 min	NA	1–6
Liu and Qing (2015)^Citation34	66	12/21	11/22	46.11 (2.09)	45.63 (2.7)	Upper, middle, and lower points of the thyroid	0.3	20 min	NA	4–6
Shao et al (2015)^Citation35	60	NA	NA	NA	NA	Multipoint injection of the tumor	0.4–1.2	10 min	NA	1, 5, 6
Fu (2015)^Citation43	250	NA	NA	NA	NA	4–6 points around the tumor	0.8–1.2	15–20 min	NA	5
Wu et al (2015)^Citation36	245	11/79	33/122	NA	NA	Top and middle points of the tumor	0.2–0.6	5–10 min	NA	4–6
Li et al (2015)^Citation37	52	NA	NA	NA	NA	4 points of the bilateral thyroid	1.0	10 min	NA	4–6
Chu et al (2015)^Citation38	57	10/18	8/21	46.28 (12.635)	40.39 (1.711)	Upper, middle, and lower points of the ipsilateral thyroid	0.3–0.6	10 min	NA	1, 4
Wang et al (2015)^Citation39	88	10/34	9/35	36.6 (11.2)	36.8 (11.4)	Upper, middle, and lower points of the thyroid	0.3–0.8	NA	NA	1
Wu et al (2015)^Citation40	86	NA	NA	NA	NA	Upper, middle, and lower points of the thyroid	0.6–1.2	30 min	82.9	1–3
Yin et al (2015)^Citation41	80	17/23	18/22	NA	NA	Upper, middle, and lower points of the thyroid	0.6	5 min	NA	4–6
Li et al (2015)^Citation42	72	9/27	10/26	NA	NA	2–4 points around the thyroid	NA	15 min	84	1–6
Xu and Gu (2016)^Citation23	114	5/52	4/53	45.37 (10.71)	42.68 (14.43)	Around the tumor	0.5	5–10 min	NA	1, 4–6
Wang et al (2015)^Citation64	55	1/27	2/25	30.25 (6.04)	29.44 (6.27)	In the thyroid gland	0.1–0.2	2–3 min	85	1, 4–6
Zhu et al (2016)^Citation19	162	14/67	16/65	46.75 (12.09)	44.31 (10.73)	1–2 points in the thyroid gland	0.1–0.2	Few minutes	92.75	1–6
Gu et al (2015)^Citation65	100	10/40	6/44	46.98 (9.027)	47.76 (13.912)	Upper and lower points of the thyroid	0.2–0.3	3–5 min	NA	1, 2, 4–6
Liu et al (2014)^Citation44	47	3/20	5/19	37.79 (11.2)	33.94 (7.76)	Upper, middle, and lower points of the thyroid	0.6	1 day	NA	1, 4–6
Chen et al (2014)^Citation45	72	5/31	8/28	38.23 (10.67)	34.64 (8.75)	Upper, middle, and lower points of the thyroid	0.4/0.6	30 min	95.4	1, 2, 4
Gao and Zhao (2014)^Citation46	100	12/38	9/41	42 (1.28)	41 (1.36)	3–4 points around the tumor	0.53–1	30 min	95.56	1–5
Yang et al (2014)^Citation47	379	23/155	27/174	42.3 (8.5)	44.2 (7.3)	Upper and lower points of the tumor or the thyroid gland	0.1–0.3	3–5 min	NA	1, 6
Wang and Rang (2014)^Citation48	70	NA	NA	44.3 (8.8)	45.2 (7.9)	4 points in the contralateral thyroid gland	0.4–0.8	15–20 min	NA	1, 2, 4–6
Liu et al (2014)^Citation49	55	5/21	9/20	36.58 (11.31)	33.58 (7.77)	In the ipsilateral thyroid	14 days	NA	NA	1, 4–6
Du (2014)^Citation50	40	4/16	8/12	47.9 (10.12)	49.5 (12.4)	Top point of the thyroid gland	0.4–0.8	3 min	NA	1, 4–6
Zhao (2014)^Citation51	183	23/79	19/62	NA	NA	Upper and lower points of the thyroid	0.1–0.2	5 min	73.5	1, 2
Chun (2014)^Citation52	67	6/27	11/23	41.06 (12.84)	44.65 (12.84)	Upper, middle, and lower points of the thyroid	0.1–0.3	3–5 min	86.8	1, 5
Liu (2014)^Citation53	184	23/53	30/78	46.5 (12.8)	47.2 (13.5)	Multipoint injection of the tumor	0.8	NA	NA	5, 6
Zhang et al (2014)^Citation54	72	12/24	10/26	NA	NA	Upper and lower points of the thyroid	0.2–0.4	5 min	NA	4–6
Shen et al (2014)^Citation55	109	NA	NA	NA	NA	Around the tumor	0.2	10 min	90.5	1, 2, 4
Shao et al (2014)^Citation57	29	NA	NA	NA	NA	Upper, middle, and lower points of the thyroid	0.3–0.6	15 min	NA	4–6
Long et al (2014)^Citation56	150	15/60	12/63	41.4 (1.62)	42.1 (2.56)	Upper, middle, and lower points of the ipsilateral thyroid	0.3	20 min	NA	1, 2, 6
Tian et al (2014)^Citation66	100	5/45	11/39	36.4 (2.5)	44.5 (5.8)	Upper, middle, and lower points of the thyroid	0.6	10–15 min	NA	1, 2, 4–6
Sun et al (2014)^Citation67	80	NA	NA	NA	NA	2–4 points around the tumor	0.2–0.8	15 min	69.89	1–4
Yang et al (2013)^Citation58	43	1/20	1/21	32.48 (4.69)	32.32 (5.35)	In the ipsilateral thyroid gland	0.1	20 min	NA	1, 2, 4, 5
Yang et al (2013)^Citation59	68	17/19	12/20	34.5 (9.1)	33.9 (10.3)	1–2 points around the tumor	0.1–0.3	10 min	91.7	1, 5
Wu (2013)^Citation60	55	5/21	9/20	36.58 (11.31)	33.58 (7.77)	Upper, middle, and lower points of the ipsilateral thyroid	0.6	NA	NA	1, 2, 4–6
Huang et al (2013)^Citation24	72	12/24	10/26	41.22 (2.53)	40.69 (2.42)	Lower and upper points of the tumor	0.2–0.4	NA	NA	5
Bai et al (2013)^Citation61	88	9/39	7/33	46.28 (9.2)	45.39 (12.03)	Lower and upper points of the tumor	0.2	NA	NA	1–6
Zeng et al (2012)^Citation62	80	0/40	0/40	NA	NA	4–6 points around the tumor	1.0	20 min	NA	5, 6
Wang et al (2009)^Citation63	36	10/8	7/11	NA	NA	4–6 points around the tumor	0.4–0.6	30 min	95.2	2–4

Notes:

a Observation indexes: differences in the following: 1) the number of retrieved lymph nodes, 2) the total metastatic rate of the retrieved lymph nodes, 3) the metastatic rate of stained/unstained lymph nodes, 4) the accidental parathyroid removal rate, 5) the postoperative transient or permanent hypoparathyroidism rate, and 6) the postoperative transient or permanent hypocalcemia rate between the CN and blank control groups.

Abbreviations: RCT, randomized controlled trial; SD, standard deviation; CN, carbon nanoparticle; BL, blank; NA, not available.

Table 2 Quality assessment of the 47 randomized controlled trials included using the Jadad scale system

Study	Randomization	Concealment of allocation	Blinding	Loss to follow-up (%)	Quality assessment
Chen et al (2016)^Citation25	No detailed description	Only mentioned randomized	Unclear	0	2
Zhang et al (2016)^Citation26	No detailed description	Only mentioned randomized	Unclear	0	2
Liu et al (2016)^Citation18	Computer-generated permuted	Only mentioned randomized	Unclear	0	3
Li (2015)^Citation27	No detailed description	Only mentioned randomized	Unclear	0	2
Feng and He (2015)^Citation28	No detailed description	Only mentioned randomized	Unclear	0	2
Guo et al (2015)^Citation29	No detailed description	Only mentioned randomized	Unclear	0	2
Duan et al (2015)^Citation30	No detailed description	Only mentioned randomized	Unclear	0	2
Chen and Wu (2015)^Citation31	No detailed description	Only mentioned randomized	Unclear	0	2
Du et al (2015)^Citation32	No detailed description	Only mentioned randomized	Unclear	0	2
Wang et al (2015)^Citation33	No detailed description	Only mentioned randomized	Unclear	0	2
Liu and Qing (2015)^Citation34	No detailed description	Only mentioned randomized	Unclear	0	2
Shao et al (2015)^Citation35	No detailed description	Only mentioned randomized	Unclear	0	2
Fu (2015)^Citation43	No detailed description	Only mentioned randomized	Unclear	0	2
Wu et al (2015)^Citation36	No detailed description	Only mentioned randomized	Unclear	0	2
Li et al (2015)^Citation37	Random-number table	Only mentioned randomized	Unclear	0	3
Chu et al (2015)^Citation38	No detailed description	Only mentioned randomized	Unclear	0	2
Wang et al (2015)^Citation39	No detailed description	Only mentioned randomized	Unclear	0	2
Wu et al (2015)^Citation40	Random-number table	Only mentioned randomized	Unclear	0	3
Yin et al (2015)^Citation41	Random-number table	Only mentioned randomized	Unclear	0	3
Li et al (2015)^Citation42	Random-number table	Only mentioned randomized	Unclear	0	3
Xu and Gu (2016)^Citation23	No detailed description	Only mentioned randomized	Unclear	0	2
Wang et al (2015)^Citation64	Computer-generated	Only mentioned randomized	Unclear	0	3
Zhu et al (2016)^Citation19	Computer-generated random-number tables	Only mentioned randomized	Unclear	0	3
Gu et al (2015)^Citation65	No detailed description	Only mentioned randomized	Unclear	0	2
Liu et al (2014)^Citation44	No detailed description	Only mentioned randomized	Unclear	0	2
Chen et al (2014)^Citation45	No detailed description	Only mentioned randomized	Unclear	0	2
Gao and Zhao (2014)^Citation46	No detailed description	Only mentioned randomized	Unclear	0	2
Yang et al (2014)^Citation47	No detailed description	Only mentioned randomized	Unclear	0	2
Wang and Rang (2014)^Citation48	Random-number table	Only mentioned randomized	Unclear	0	3
Liu et al (2014)^Citation49	No detailed description	Only mentioned randomized	Unclear	0	2
Du (2014)^Citation50	No detailed description	Only mentioned randomized	Unclear	0	2
Zhao (2014)^Citation51	No detailed description	Only mentioned randomized	Unclear	0	2
Chun (2014)^Citation52	No detailed description	Only mentioned randomized	Unclear	0	2
Liu (2014)^Citation53	No detailed description	Only mentioned randomized	Unclear	0	2
Zhang et al (2014)^Citation54	No detailed description	Only mentioned randomized	Unclear	0	2
Shen et al (2014)^Citation55	No detailed description	Only mentioned randomized	Unclear	0	2
Shao et al (2014)^Citation57	No detailed description	Only mentioned randomized	Unclear	0	2
Long et al (2014)^Citation56	Odd or even number	Only mentioned randomized	Unclear	0	1
Tian et al (2014)^Citation66	Randomization chart	Only mentioned randomized	Unclear	0	3
Sun et al (2014)^Citation67	Computer-generated permuted block sequencing	Only mentioned randomized	Unclear	0	3
Yang et al (2013)^Citation58	No detailed description	Only mentioned randomized	Unclear	0	2
Yang et al (2013)^Citation59	No detailed description	Only mentioned randomized	Unclear	0	2
Wu (2013)^Citation60	No detailed description	Only mentioned randomized	Unclear	15.4	3
Huang et al (2013)^Citation24	Computer-generated permuted	Sealed envelopes	Single blinding	0	3
Bai et al (2013)^Citation61	No detailed description	Only mentioned randomized	Unclear	0	2
Zeng et al (2012)^Citation62	No detailed description	Only mentioned randomized	Unclear	0	2
Wang et al (2009)^Citation63	Random-number table	Only mentioned randomized	Unclear	0	3

Notes: The Jadad scale was used to assess the quality of these RCTs. Thirteen studies included had a score of 3 points, which reflected the high quality of the study. The majority of studies had 2 points or lower. These studies can be considered to be of relatively low quality.

Abbreviation: RCT, randomized controlled trials.

Figure 4 Forest plot showing the association of CNs with retrieved lymph nodes and metastatic lymph nodes.

Notes: (A) Number of retrieved lymph nodes per patient in the CN and blank control groups. (B) Number of retrieved metastatic lymph nodes per patient.
Abbreviations: CN, carbon nanoparticle; SD, standard deviation; IV, interval variable; CI, confidence interval; random, random effect; df, degrees of freedom.

Figure 5 Forest plot showing the relationship of CNs and different kinds of retrieved lymph nodes.

Notes: (A) Total metastatic rate of the retrieved lymph nodes. Metastatic rates of the (B) stained and (C) unstained lymph nodes in the CN and blank control groups.
Abbreviations: CN, carbon nanoparticle; M–H, Mantel–Haenszel; random, random effect; CI, confidence interval; df, degrees of freedom.

Figure 6 Accidental parathyroid removal rate in the CN and blank control groups.

Abbreviations: CN, carbon nanoparticle; M–H, Mantel–Haenszel; CI, confidence interval; df, degrees of freedom.

Figure 7 (A) Postoperative transient and (B) permanent hypoparathyroidism rates in the CN and blank control groups.

Abbreviations: CN, carbon nanoparticle; M–H, Mantel–Haenszel; CI, confidence interval; df, degrees of freedom.

Figure 8 (A) Postoperative transient and (B) permanent hypocalcemia rates in the CN and blank control groups.

Abbreviations: CN, carbon nanoparticle; M–H, Mantel–Haenszel; CI, confidence interval; df, degrees of freedom.

Figure 9 Funnel plots for publication bias.

Notes: Publication bias for (A) the number of retrieved lymph nodes per patient, (B) number of retrieved metastatic lymph nodes per patient, (C) total metastatic rate of the retrieved lymph nodes, (D) metastatic rate of the stained lymph nodes, (E) metastatic rate of the unstained lymph nodes, (F) accidental parathyroid removal rate, (G) postoperative transient hypoparathyroidism rate, (H) postoperative permanent hypoparathyroidism rate, (I) postoperative transient hypocalcemia rate, and (J) postoperative permanent hypocalcemia rate in the CN and blank control groups. Each point represents a separate study for the indicated association.
Abbreviations: CN, carbon nanoparticle; SE, standard error; MD, mean difference; OR, odds ratio.

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