The feasibility of reducing the thresholds for biopsy in ACR TIRADS and AI TIRADS

doi:10.21203/rs.3.rs-2006919/v1

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The feasibility of reducing the thresholds for biopsy in ACR TIRADS and AI TIRADS

https://doi.org/10.21203/rs.3.rs-2006919/v1

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At present, there is still controversy over whether to perform fine needle aspiration (FNA) on sub-centimeter thyroid nodules with high suspicion of malignancy. Our aim was to estimate the feasibility of reducing the original thresholds for biopsy in American College of Radiology Thyroid Imaging Reporting and Data System (ACR TIRADS) and Artificial Intelligence TIRADS (AI TIRADS). A total of 3201 thyroid nodules with definitive histology obtained were included. Ultrasound categories were assigned according to each TIRADS. We lowered the original FNA thresholds of TR3-TR5 in ACR and AI TIRADS and estimated whether the decreased FNA thresholds could be accepted and used to modified ACR and AI TIRADS. Then, we estimated and compared the diagnostic performance between modified TIRADS and original TRADS to determine if the decreased thresholds could be an effective strategy. 1474 (46.0%) thyroid nodules were diagnosed as malignant after thyroidectomy. Modified ACR TIRADS had higher sensitivity and lower specificity, unnecessary biopsy rate, missed malignancy rate compared with original ACR TIRADS (all P< 0.05). Similar trends were seen in modified AI TIRADS versus original AI TIRADS (all P < 0.05). In conclusion, biopsy of all nodules with TR5 in both ACR TIRADS and AI TIRADS might be an effective strategy, regardless of the nodules dimension. This paper contributes to the contradictory concerning whether perform FNA for the nodules smaller than 10 mm.

With the extensive use of ultrasound since the 1990s, there has been a significant increase in the detection of thyroid nodules. Many risk stratification systems (RSSs) based on ultrasound features and size thresholds were developed to determine fine-needle aspiration (FNA)^1–4. Among several RSSs, the Thyroid Imaging Reporting and Data System proposed by American College of Radiology (ACR TIRADS) is currently widely applied in thyroid imaging and management³. Recently, Wildman-Tobriner et al. ⁵ applied an AI algorithm to simply ACR TIRADS (hereafter, AI TIRADS), which had higher specificity than ACR TIRADS (61.8% vs. 51.1%).

At present, a 10 mm size cutoff is widely used on a thyroid nodule with suspicious ultrasound features to indicate biopsy^1,3,4. Both ACR TIRADS and AI TIRADS suggested biopsy of thyroid nodules ≥ 10 mm. However, some professional societies and groups of investigators also suggested that biopsy should be performed in the nodules smaller than 10 mm^6,7. Previous study has demonstrated that the discrepancy in diagnostic performance between different RSSs may be largely derived from the nodule size threshold difference, but the results have been heterogeneous⁸. ACR TIRADS showed superior diagnostic performance compared to other RSSs and its used has reduced a larger number of unnecessary FNAs ^3,9−13 which may be related to its higher size cutoff for biopsy^3,13. On the contrary, a retrospective study in a pediatric sample, they conducted biopsy on all thyroid nodules with the highest category in ACR TIRADS and other RSSs¹⁴. The results showed that the sensitivity and accuracy of the RSSs improved overall, but without a change in the unnecessary FNA rate. As a matter of fact, there is by far, to our knowledge, insufficient relative researches to confirm the feasibility of reducing the current threshold for FNA to smaller than 10 mm.

Thus, we hypothesized that reducing the original threshold for biopsy might be an effective strategy. First, we determined how the original thresholds of ACR TIRADS and AI TIRADS were reduced. Next, to estimate and compare the diagnostic performance of the two TIRADSs with original thresholds and reduced thresholds in large adult samples of surgical series.

Characteristics of patients and nodules. Of 3201 thyroid nodules, 1727 (54.0%) were diagnosed as benign and 1474 (46.0%) as malignant by surgical pathology (Table 1). The benign nodules were larger than the malignant nodules (20.4 mm ± 15.8 vs. 12.6 mm ± 11.7, P < 0.001).

Table 1

Summary of demographic for the patients with thyroid nodules
Characteristics	Histopathology diagnosis		Total	P
Characteristics	Benign (n = 1727)	Malignant (n = 1474)	Total	P
Age, y				0.000
Mean	49.6 ± 12.1	44.7 ± 11.9	47.3 ± 12.2
Range	12–82	7–80	7–82
Gender, n(%)*				0.019
Male (510, 23.8%)	375 (11.7)	372 (11.6)	747 (23.3)
Female (1636, 76.2%)	1352 (42.2)	1102 (34.4)	2454 (76.7)
Size, mm				0.000
Mean	20.5 ± 15.8	12.6 ± 11,7	17.0 ± 14.8
Range	2.0–100.0	2–102.0	2 -102.0
< 10	582 (33.7)	829 (56.2)	1411 (44.1)	0.000
≥ 10	1145 (66.3)	645 (43.8)	1790 (55.9)

Note: Data are reported as mean ± standard deviation for continuous variables.

*Denotes number of patients within each category. Numbers in parentheses represent percentage within a given group (benign, malignant).

Gender was not significantly associated with malignancy risk (P > 0.05). Age under 55 years had significantly higher risk of malignancy compared with ≥ 55 years of age (P < 0.05). There were 1411 (44.1%) nodules < 10 mm in diameter, and 1790 (55.9%) nodules ≥ 10 mm. The malignancy risk of nodules < 10 mm was higher compared with nodules ≥ 10 mm (56.2% vs. 43.8%, P < 0.05).

Malignancy rates according to US categories in ACR TI-RADS and AI TI-RADS. The risks of malignancy of different categories in the two TIRADSs are shown in Table 2. All of the calculated risks of malignancy for the two TIRADSs were higher than their estimated risks of malignancy, except for TR3 (5.0% [25 of 497]) and TR5 (83.0% [1135 of 1367]) in ACR TIRADS and TR5 (84.0% [1230 of 2215]) in AI TIRADS.

Table 2

Malignancy risks according to categories in ACR TIRADS and AI TIRADS
System and categories		Pathological diagnosis		Calculated ROM (%)	Suggested ROM (%)
System and categories		Benign (n = 1727)	Malignant (n = 1474)	Calculated ROM (%)	Suggested ROM (%)
ACR TI-RADS	1	66	7	9.6	≤ 2
	2	461	25	5.1	≤ 2
	3	472	25	5.0	≤ 5
	4	496	282	36.2	5–20
	5	232	1135	83.0	≥ 20
AI TI-RADS	1	583	35	5.7	≤ 2
	2	233	17	6.8	≤ 2
	3	304	29	8.7	≤ 5
	4	373	163	30.4	5–20
	5	234	1230	84.0	≥ 20
ROM: risk of malignancy.
*The ROM was calculated as the percentage of malignant nodules in the total nodules of each category.

Comparison of Diagnostic Performances between original TIRADS and modified TIRADS. In simulation (Table 3), We reduced the thresholds for FNA from ≥ 10 mm to 5/zero in TR5, from ≥ 15 mm to ≥ 10 mm in TR4, and from ≥ 25 mm to ≥ 20 mm in TR3 of ACR TIRADS. The RABM was 1-to-6.46/1-to-5.93 in TR5, 26.5-to-1 in TR4, and 1.67-to-1 in TR3, respectively. The changes of threshold for TR5 were accepted, rather than TR4 and TR3. As a consequence, the new threshold of TR5 was accepted to establish the modified ACR TIRADS. We also applied the same decreased thresholds to AI TIRADS, and the RABM was 1-to-6.26/1-to-6.35 in TR5, 2.4-to-1 in TR4, and 10-to-1 in TR3, respectively. Finally, the new threshold of zero for TR5 was accepted to establish the modified AI TIRADS.

Table 3

The original and simulated threshold for FNA in ACR TIRADS and AI TIRADS
Systems	Thresholds for FNA		Additional nodules for FNA		RABM	The final simulated thresholds for FNA
Systems	Original	Simulated	Benign	Malignant	RABM	The final simulated thresholds for FNA
ACR TIRADS
TR1	-	-	-	-	-	-
TR2	-	-	-	-	-	-
TR3	≥ 25 mm	≥ 20 mm	53	2	26.5-to-1	≥ 25 mm
TR4	≥ 15 mm	≥ 10 mm	77	46	1.67-to-1	≥ 15 mm
TR5	≥ 10 mm	0	112	664	1-to-5.93	0
		≥ 5 mm	28	181	1-to-6.46
AI TIRADS
TR1	-	-	-	-	-	-
TR2	-	-	-	-	-	-
TR3	≥ 25 mm	≥ 20 mm	30	3	10-to-1	≥ 25 mm
TR4	≥ 15 mm	≥ 10 mm	60	25	2.4-to-1	≥ 15 mm
TR5	≥ 10 mm	0	115	730	1-to-6.35	0
		≥ 5 mm	84	526	1-to-6.26

Note: RABM, the ratio of additional benign to malignant nodules being biopsied when using the simulated thresholds for FNA

The diagnostic performances were calculated according to the FNA indications and were compared between the original TIRADS and modified TIRADS (Fig. 1). The modified ACR TIRADS had higher sensitivity, PPV, NPV, and accuracy, but lower unnecessary biopsy rate and missed malignancy rate than ACR TIRADS (83.8% vs. 38.7%, 65.5% vs. 51.5%, 81.8% vs. 56.8%, 72.2% vs. 55.0%, 34.5% vs. 48.5%, 18.2% vs. 43.2% respectively, all P < 0.05). However, higher specificity was found in ACR TIRADS (68.8% vs. 62.4%, P < 0.05). Similar trends were seen in AI TIRADS versus modified AI TIRADS. Higher specificity was seen in AI TIRADS, while higher sensitivity, PPV, NPV, and accuracy, along with lower unnecessary biopsy rate and missed malignancy rate were seen in modified AI TIRADS (P < 0.05 for all). The diagnostic performances according to FNA indications with ACR TIRADS and AI TIRADS are shown in Table 4.

Table 4

Diagnostic Performances between ACR TIRADS and AI TIRADS according to FNA indications
Systems	Sensitivity	Specificity	PPV	NPV	Accuracy	UFR	MMR
ACR TIRADS	38.7% (571/1474)	68.8% (1189/1727)	51.5% (571/1109)	56.8% (1189/2092)	55.0% (1760/3201)	48.5% (538/1109)	43.2% (903/2092)
AI TIRADS	39.2% (578/1474)	76.4% (1319/1727)	58.6% (578/986)	59.5% (1319/2215)	59.3% (1897/3201)	41.4% (408/986)	40.5% (896/2215)
P value	0.349	0.000	0.001	0.071	0.000	0.001	0.071

Note: PPV, positive predictive value; NPV, negative predictive value; UFR, unnecessary FNA rate; MMR, missed malignancy rate

Comparison of diagnostic performance between the “<10 mm” and “≥10 mm” groups. We calculated the diagnostic performances in the two groups (< 10 mm and ≥ 10 mm) according to US-based final assessment categories (Table 5).

Table 5

Diagnostic Performance of different sizes between ACR TIRADS and AI TIRADS
Systems	Sensitivity	Specificity	PPV	NPV	Accuracy	AUC
ACR TIRADS
< 10 mm	97.7% (96.6–98.6)	49.5% (45.5–53.3)	73.4% (70.7–76.1)	93.8% (90.9–96.4)	77.8% (75.8–80.0)	0.843 (0.823–0.862)
≥ 10 mm	94.1% (92.1–95.8)	62.1% (59.2–65.0)	58.3% (55.2–61.3)	94.9% (93.3–96.4)	73.6% (71.3–75.6)	0.870 (0.854 − 0.85)
P value	0.000	0.000	0.000	0.446	0.006	< 0.05
AI TIRADS
< 10 mm	97.0% (95.8–98.2)	56.4% (52.2–60.1)	76.0% (73.3–78.5)	92.9% (90.1–95.8)	80.2% (78.0-82.1)	0.862 (0.843–0.880)
≥ 10 mm	91.3% (89.1–93.5)	69.2% (66.6–71.8)	62.5% (59.2–65.7)	93.4% (91.6–95.0)	77.2% (75.3–79.2)	0.880 (0.864–0.895)
P value	0.000	0.000	0.000	0.763	0.035	> 0.05

Note: Numbers in parentheses are 95% confidence intervals; PPV, positive predictive value; NPV, negative predictive value

The AUC of ACR TIRADS in “nodules ≥ 10 mm” was higher than that in “nodules < 10 mm” (0.870 vs. 0.843, P < 0.05). While the AUCs of AI TIRADS were not statistically different between “nodules < 10 mm” and “nodules ≥ 10 mm” (0.862 vs. 0.880, P > 0.05).

The present perspectives were contradictory as to whether perform FNA for the nodules smaller than 10 mm with suspicious US features^1,6. In our study, we determined which thresholds for biopsy in ACR TIRADS and AI TIRADS could be decreased. And then the modified TIRADSs were built. The modified TIRADSs which changed the threshold for biopsy for TR5 from 10 mm to zero showed higher sensitivity as well as lower missed malignancy rate and unnecessary biopsy rate than original TIRADS. Thus, our results suggested that biopsy of all nodules with TR5 in ACR TIRADS and AI TIRADS might be an effective strategy.

In this study, we reduced the original FNA thresholds with the TR3-TR5 in ACR and AI TIRADS to determine if they could be an effective strategy. Firstly, the ratio of additional benign to malignant nodules being biopsied (RABM) was calculated. The RABM of less than 1 was regarded as a reasonable threshold which would be accepted. Thus, biopsy of all nodules with TR5 in ACR TIRADS and AI TIRADS were accepted and used to their modified TIRADS respectively. Secondly, the modified TIRADS had higher sensitivity and lower unnecessary biopsy rate, missed malignancy rate compared with original TIRADS. A recent study demonstrated similar findings, comparing five US-based risk stratification systems in pediatric populations¹⁴. Middleton et al. also showed that a decrease in the size threshold used for recommending FNA on ACR TR5 nodules would not result in an inverse in the percentage of additional benign nodules being biopsied¹⁷. Lowering the threshold for biopsy could reduce the missed malignancy rate. Furthermore, without the diagnosis of carcinoma, it can be very difficult to persuade patients to undergo a regular checkup. On the contrary, benign nodules with a confirmed cytologic diagnosis were reassuring results for patients, which could reduce their psychological anxiety and economic burden. Finally, in our study sample, both ACR and AI TIRADS seemed to provide a reliable stratification of high suspicion nodules. The calculated ROM of TR4 and TR5 was 36.2% and 83.0% in ACR TIRADS, 30.4% and 84.0% in AI TIRADS. In summary, these results prompted us to consider biopsy of all nodules with TR5 in ACR TIRADS and AI TIRADS, regardless of the nodules dimension. We also recommended that biopsy should be considered first for those suspicious nodules to avoid needless active monitoring and patient concern. After a diagnosis of microcancer (less than 10 mm in size) without any high-risk characteristics (such as pathologic lymph nodes), two management alternatives were available for patients to choose according to their own preferences: active monitoring or surgery. However, due to the positive statistics on active monitoring, we advised using it as the first line of management.

The diagnostic superiority of modified TIRADS may be explained by the fact that ACR and AI TIRADS have efficient diagnostic performances in the thyroid nodules smaller than 10 mm. Although partly significant, AUCs of the two TIRADSs were found similar between the ≥ 10 mm group and < 10 mm group. Moreover, the < 10 mm group had higher sensitivity, accuracy, and PPV than those of the ≥ 10 mm group in both ACR TIRADS and AI TIRADS. Some recent studies verified that ACR TIRADS had good diagnostic efficiency in thyroid nodules smaller than 10 mm, which is in line with our results^18–20. These results suggested that ACR and AI TIRADS were also efficient in the discrimination of malignant in the thyroid nodules smaller than 10 mm, which is essential to RSSs. Although biopsy is not recommended for nodules smaller than 10 mm in adults, it is unclear whether this recommendation is appropriate for pediatric populations¹⁴. Besides, regarding the active surveillance of thyroid nodules smaller than 1 cm, there is no clear agreement on the requirement for biopsy^1,6.

Our study had limitations. Firstly, our institution is a tertiary referral center, patients coming for diagnosis and/or treatment are mostly with malignant diseases. Thus, the proportion of malignant nodules in our study was higher (46.0%) than that in other studies (range, 10.3%-25.8%)^13,21−23. Secondly, the study was a surgical series, which may lead to selection bias and a few of false negative rate and false positive rate. However, surgeon marked surgically removed thyroid specimen, which could minimize false negative rate and false positive rate (one largest or/and highest suspicious thyroid nodule were marked in per thyroid lobe). In addition, at present, only histopathology is the gold standard for diagnosis of thyroid nodules. FNA diagnosis includes a percentage of undetermined lesions during general populations whose final results (benign or malignant) were unknown since surgery was not performed on all of them. Thirdly, the interobserver agreement was not evaluated in this study. However, recent studies showed that interobserver reproducibility for thyroid nodule US reporting and US classification systems in ACR TIRADS and other RSSs appears fairly adequate^24–27. In contrast, an unified lexicon of thyroid US features, a simplified method of classification, and a dedicated training in the description of thyroid US findings may increase the observers' agreement²⁵. Thus, AI TIRADS may have better observers’ agreement than ACR TIRADS, because AI TIRADS is simplified version of ACR TIRADS.

In conclusion, this study suggested that biopsy of all nodules with TR5 in ACR TIRADS and AI TIRADS might be an effective strategy, regardless of the nodules dimension. This paper contributes to the contradictory concerning whether perform FNA for the nodules smaller than 10 mm. Large multi-center prospective research using other risk stratification systems is warranted to further validate the rationality of cytological diagnosis of thyroid nodules smaller than 10 mm.

The Scientific Research and Clinical Trials Ethics Committee of the First Affiliated Hospital of Zhengzhou University approved this retrospective study (2022-KY-0974-001) and waived the requirement for informed consent to review images and medical records. All methods were performed in accordance with the Declaration of Helsinki.

Patients. From January 2010 to July 2017, a consecutive of 2582 patients with 3833 thyroid nodules received ultrasound examinations and thyroidectomy at our institution. We excluded 632 nodules in 436 patients because of incomplete ultrasound image data and lack of determined pathological findings. Patients were eligible for inclusion if (1) they had performed US examinations and (2) underwent thyroidectomies within mouth after ultrasound examinations. Consequently, a total of 3201 thyroid nodules in 2146 patients were finally included in this study. Mean age of the patients was 47.3 years ± 12.2 (range, 7–82 years). Mean size of the thyroid nodules was 17.0 mm ± 14.8 (range, 2–102 mm).

US examination and image analysis. Real-time ultrasound examinations were performed using the TOSHIBA Aplio300 device (5–14 MHz linear probe) by a senior radiologist (K.C.) with 33 years of experience in thyroid ultrasonography. All the ultrasound examinations were complied with the AIUM protocol for thyroid scanning. During the US examination, nodule images were generally obtained as at least on gray scale image in each transverse and longitudinal plane. Additional images were obtained to demonstrate important US features of the nodules. The US data were recorded and stored for further analysis.

An overview and discussion session was held by a senior radiologist (K.C.) with 33 years of experience in thyroid imaging to establish consensus regarding the definitions of the US lexicons from the white paper of ACR TIRADS¹⁵, including size (the maximal diameter at US), composition (solid, predominately solid, predominately cystic, cystic, spongiform), echogenicity (hyperechoic, isoechoic, hypoechoic, very hypoechoic), shape (taller-than-wide), margins (smooth, irregular, lobulated, ill-defined, extrathyroidal extension), echogenic foci (punctate echogenic foci, macrocalcification, peripheral calcifications, comet-tail artifacts).

Subsequently, US features were independently reviewed by two radiologists blinded to the biopsy results and the final pathological diagnoses (C.F. and Y.H., with 13 and 12 years, respectively, of clinical experience performing thyroid US scans and evaluating thyroid US images).

Analysis and comparison of the diagnostic performance. Firstly, we conducted biopsy on all thyroid nodules with TR3-TR5 in ACR and AI TIRADS and calculated the ratio of additional benign to malignant nodules being biopsied (RABM). If RABM is less than 1, the decreased FNA thresholds could be accepted and are used to modified TIRADS (modified ACR and AI TIRADS). Secondly, the diagnostic performances were compared between modified TIRADS and original TIRADS to determine if the reduced thresholds could be an effective strategy.

In previous study, the diagnostic performances can be calculated according to indications for FNA and US-based final assessment categories¹⁶. In this study, the diagnostic performances were calculated and compared between the original TIRADS and modified TIRADS according to the indications for FNA. The diagnostic performances of the FNA criteria in the detection of malignant nodules was estimated by calculating the sensitivity, specificity, accuracy, unnecessary biopsy rate (number of benign nodules among those recommended for biopsy), and missed malignancy rate (number of malignant nodules among those not recommended for biopsy).

Finally, thyroid nodules were dichotomized into two groups, < 10 mm and ≥ 10 mm in diameter. The diagnostic performances were calculated and compared between the two groups according to US-based final assessment categories by calculating the sensitivity, specificity and accuracy, and defining the cutoffs for ≥ TR4 as diagnostic positive (suspicious for malignancy).

Statistical Analysis. Quantitative data were presented as the mean ± standard deviation (SD). Qualitative data were presented as frequencies. Differences between groups were compared by using the independent two-sample t test for continuous data and the χ² test or Fisher’s exact test for categorical data. The sensitivity, specificity, PPV, NPV, accuracy, and UFR were calculated and were compared by the McNemar or Pearson tests in ACR TI-RADS and AI TI-RADS, as well as their modified versions. The DeLong or Z-test were used to compare the AUCs. Statistical analysis was performed using SPSS software (Version 26.0, SPSS Chicago, IL, USA) and MedCalc software (Version 18.2.1, MedCalc Software, Ostend, Belgium). A value of P < 0.05 was considered statistically significant.

Data availability

The data presented in the current study are available on reasonable request from the corresponding author.

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No competing interests reported.

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The feasibility of reducing the thresholds for biopsy in ACR TIRADS and AI TIRADS

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