Surg Endosc DOI 10.1007/s00464-015-4112-2

and Other Interventional Techniques

Intraoperative core needle biopsy under complete video-assisted thoracic surgery for indeterminate tumor of lung Tetsuya Isaka • Ko Takahashi • Takamitsu Maehara Munetaka Masuda



Received: 8 July 2014 / Accepted: 1 February 2015 Ó Springer Science+Business Media New York 2015

Abstract Background The accuracy, feasibility, and safety of intraoperative core needle biopsy under complete video-assisted thoracic surgery (VATS) (V-CNB) for indeterminate tumors are examined retrospectively, as well as the possibility of pleural dissemination. Methods The diagnostic yield and complications of V-CNB were evaluated for a total of 95 patients who underwent V-CNB for indeterminate tumor during the period of April 2002 through March 2012. Moreover, operation time, number of auto-suture instruments used for resection of the lung, and pleural dissemination were compared between the patients who underwent V-CNB (n = 44) and those who did not (n = 87, non-V-CNB) among stage I primary lung cancer patients, for whom lobectomy was performed under complete VATS during the same period. Results Of the 95 patients, eighty three had primary lung cancer, four had metastatic lung cancer, and eight had benign tumor. Sensitivity, specificity, and accuracy were 94.3, 87.5, and 93.7 %, respectively. There were no complications associated with V-CNB. Among stage I primary lung cancer, for which lobectomy and lymph node dissection were performed, there was no significant difference between the V-CNB group and the non-V-CNB group for

T. Isaka  K. Takahashi  T. Maehara Department of Respiratory Surgery, Yokohama Rosai Hospital, 3211 Kodukue, Kohoku, Yokohama, Kanagawa 222-0036, Japan T. Isaka (&)  M. Masuda Department of Surgery, Yokohama City University, 3-9 Fukuura, Kanazawa, Yokohama, Kanagawa 236-0004, Japan e-mail: [email protected]

tumor size (23.5 and 24.7 mm, p = 0.482), distance between pleura and tumor (3.4 and 5.0 mm, p = 0.202), operation time (228 and 217 min, p = 0.186), and number of auto-suture instruments used for resection of the lung (4.77 and 4.61, p = 0.533). There was no pleural dissemination in the V-CNB group, although there were two cases (2.3 %) in the non-V-CNB group. Conclusion V-CNB diagnosed small-sized indeterminate lung tumors accurately during complete VATS operation, without any complications. V-CNB can reduce the use of auto-suture instruments necessary for performing wedge resection on frozen section diagnosis prior to lobectomy without increasing operation time and the risk of pleural dissemination. Keywords Lung cancer  Core needle biopsy  Complete VATS  Frozen section diagnosis  Accuracy  Dissemination Small-sized non-small cell lung cancer (NSCLC) that is difficult to diagnose definitively at the preoperative stage can be identified more frequently as the imaging diagnostic technology advances. In order to perform frozen section diagnosis on those indeterminate lung tumors, wedge resection biopsy is commonly performed to decide on an operation methodology [1, 2]. However, there are some cases where wedge resection biopsy cannot be easily undertaken. Those are when large-sized tumors are located at deep position from pleura or hilar area [3]. In these cases, diagnostic segmentectomy provides definitive diagnosis [4]; otherwise initial lobectomy is considered without evaluating the malignancy of tumor before the lung resection [3], but these strategies may mislead to unnecessary aggressive surgeries. Another methodology for the frozen

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section diagnosis is needle biopsy, including needle aspiration biopsy (NAB) [5, 6] and core needle biopsy (CNB). However, there are limited reports of studies evaluating intraoperative needle biopsy, including CNB under complete video-assisted thoracic surgery (VATS) (V-CNB). The purpose of the present study is to provide a diagnostic yield and incidence of complications and to assess a technical feasibility with respect to V-CNB. Moreover, the study examined the risk of pleural recurrence after V-CNB among pathological stage I primary lung cancer.

Materials and methods Patients During the period of April 2002 through March 2012, a total of 95 patients without preoperative diagnosis underwent intraoperative V-CNB and lung resections at Yokohama Rosai Hospital. All patients gave appropriate informed consent. V-CNB was performed to diagnose indeterminate tumor of which primary lung cancer was suspected preoperatively, with the tumor being identifiable during operation through finger palpation or inspection intraoperatively. The diagnostic yield and intraoperative complications of V-CNB were evaluated. The factors associated with the failure of V-CNB were statistically assessed by comparison between correctly diagnosed cases and erroneously diagnosed cases that were diagnosed as primary lung cancer in the permanent section examination. Moreover, the number of auto-suture instruments used for resection of lung, operation time, and site of recurrence including pleural dissemination were compared between the patients who underwent V-CNB (V-CNB group), and those who did not (non-V-CNB group) among stage I primary lung cancer patients for whom lobectomy and lymph node dissection were performed under complete VATS during the period of April 2002 through March 2012. Pathologic staging was classified according to the TNM classification, version 7. Procedures VATS lung resections were performed under complete video monitoring or complete VATS, by three ports. One port was placed at the fourth or fifth intercostal space on the anterior axillary line with an incision of 3–5 cm, and the other two ports with incisions of 1–1.5 cm were placed at the seventh or eighth intercostal space on the middle axillary line and at the auscultatory triangle. All intrathoracic procedures were manipulated under video monitoring without direct vision.

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The biopsy needle used for V-CNB was a 16G thru-cut needle or a Quick-CoreÒ (Cook Medical, Bloomington, IN, USA) with needle stroke of 20 mm. The biopsy needle was inserted into the normal lung about 10 mm away from the tumor to the direction that did not direct to the pulmonary hilum and biopsied 1–3 times (Fig. 1A). The punctured site was pressed promptly and properly with thoraco-cotton after the insertion to prevent the occurrence of a hematoma (Fig. 1B). Segmentectomy or lobectomy with nodal dissection under complete VATS was performed if the tumor was diagnosed as primary lung cancer; otherwise, wedge resection was performed for benign tumor or metastatic lung cancer. The lung was resected so as to include puncture sites. Postoperative follow-up Postoperative recurrence patterns were analyzed. Chest CT was routinely performed at least every year during followup examinations, whereas chest roentgenograms and measurements of tumor markers were performed every 3–6 months to survey for recurrence. Pleural dissemination was defined as pleural nodules that were seen growing on radiographic images or malignant pleural effusion proven by cytologic examination. Local recurrence was defined as disease recurrence in contiguous anatomic sites, including the surgical margin, mediastinum, and ipsilateral hemithorax (excluding pleural dissemination), after surgical resection. Distant metastasis was defined as tumor recurrence in the contralateral lung or outside the hemithorax and mediastinum after surgical resection. Statistical analyses Continuous variables were analyzed using Student’s t test, and categorical variables were analyzed using Fisher’s exact test. Statistical significance was defined as a p value of less than 0.05.

Results V-CNB was performed in 95 indeterminate tumors of 95 patients (Table 1). The average tumor size was 22.1 mm (5–50). Forty-three patients (45.3 %) underwent bronchoscopic examination preoperatively. Of the 95 patients, eighty three had primary lung cancer, four had metastatic lung cancer, and eight had benign tumor. Lobectomy, segmentectomy, and wedge resection under complete VATS were performed in 58, 29, and 7 patients, respectively, after V-CNB. There were no complications associated with the V-CNB (Table 1). Intraoperative bleeding from pulmonary artery and vein was not the cause of

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Fig. 1 A The biopsy needle was inserted into the normal lung about 10 mm away from the tumor to the direction that did not direct to the pulmonary hilum and biopsied for 1–3 times. B Punctured site was pressed promptly and properly with thoraco-cotton after the insertion

to prevent the occurrence of a hematoma. C and D V-CNB has full advantages on tumor located at the hilar area of lung where wedge resection biopsy is difficult

V-CNB. There were also three cases of long-term air leakage as a perioperative complication, but these were not due to the insertion of V-CNB. Sensitivity, specificity, and accuracy were 94.3, 87.5, and 93.7 %, respectively (Table 2). In five patients (5.3 %), the tumor tissues could not be obtained, and the frozen section diagnoses were normal lung tissues. In one case (1.1 %), the final diagnosis was benign tumor after performing lobectomy, although the intraoperative diagnosis was primary lung cancer. Table 3 shows a comparison of tumor characteristics between cases correctly and erroneously diagnosed by V-CNB in primary lung cancer. Distance between pleura and tumor, tumor size, and the lobar distribution of the tumor were not significantly different between the two groups. However, small-sized tumors (B20 mm) located at a deep position from the pleura (C11 mm) in the upper lobe tended to be associated with failure of V-CNB. Wedge resection, segmentectomy, and lobectomy were performed in 2, 1, and 1 cases, respectively, for which V-CNB failed.

Table 4 shows the characteristics of 83 primary lung cancer patients who underwent V-CNB. There were 53 and 13 patients diagnosed at p-stages IA and IB, respectively. Although pleural invasions were found in 19 cases (22.9 %), there were no pleural disseminations among all V-CNB cases. Table 5 shows a comparison of patient characteristics between the V-CNB group (n = 44) and the non-V-CNB group (n = 87) among stage I primary lung cancer cases for which lobectomy and lymph node dissection were performed, and the follow-up periods of each group were 47.9 months (11–109) and 51.3 months (1–127), respectively (p = 0.516). The average tumor sizes of the V-CNB group and the non-V-CNB group were 23.5 mm (10–48) and 24.7 mm (6–50) (p = 0.482), and the average distances between pleura and tumor were 3.4 mm (0–25) and 5.0 mm (0–30) (p = 0.202), respectively. Other patient background factors and histopathological findings were not significantly different between the groups. The average operation times were 228 min (125–355) and 217 min

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Surg Endosc Table 1 Patient background and complications occurred in the cases of which V-CNB was performed

Table 2 Diagnostic yield of V-CNB n = 95

Final diagnosis

n = 95 Age

66.9 (39–84)

Male/female

56/39

Right/left

64/31

Tumor size (mm)

Average 22.1 (5–50)

10C

7

11–20

41

21–30 31B

35 12

Preoperative examination (%) TBLB

42 (44.2)

CT guided biopsy and TBLB

1 (1.1)

None

52 (54.7)

Frozen section diagnosis

Malignancy Benign

Sensitivity

94.3 %

Specificity

87.5 %

Accuracy

93.7 %

Malignancy

Benign

82

1b

a

7

5

a

In the 5 cases, malignant tumor tissues were not able to obtain because the core needles could not reach tumors, and the frozen section diagnoses concluded that normal lung tissues were biopsied or the tumors were benign b In the one case, frozen section diagnosis was suspicious of nonsmall-cell lung cancer, revealing benign tumor in final diagnosis

Final diagnosis Primary lung cancer

83

Adenocarcinoma

61

Adenosquamous

2

Squamous

13

LCNEC

5

Others

2

Metastatic lung cancer

4

Colon cancer

2

Gastric cancer Bladder cancer

1 1

Benign

3

Inflammation

2

Tuberculoma

2

Sclerosing hemangioma

1

Operative method after V-CNB 58

Segmentectomy

29

Partial resection

7

Biopsy only

1

Intraoperative complication Bleeding from pulmonary artery

5

Bleeding from pulmonary vein

1

Perioperative complication Long-term air leakage Chylothorax

3 2

Hemothorax

1

Atrial fibrillation

1

Deliria

1

Asthma

1

TBLB transbronchial lung biopsy, CT computed tomography, LCNEC large-cell neuroendocrine carcinoma

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Discussion

8

Granuloma

Lobectomy

(137–318) (p = 0.186) and the average numbers of autosuture instruments used for resection of the lung were 4.77 (2–8) and 4.61 (2–9) (p = 0.533) for the V-CNB group and the non-V-CNB group, respectively, which were both not significantly different. There was no pleural dissemination in the V-CNB group, although there were two cases (2.3 %) of pleural dissemination in the non-V-CNB group.

Diagnostic yield and the advantage of V-CNB Currently, there are several options for the preoperative and intraoperative diagnosis of lung cancer. TBLB and CTGNB are typical for pathological diagnosis preoperatively. As for TBLB, it is very difficult to identify smallsized and peripheral lung tumor tissues and the diagnostic yield ranges from 18 to 62 %; the diagnostic yield decreases to 14 % for lesions with a diameter of less than 2 cm located in the periphery of the lung [7]. Electromagnetic navigation bronchoscopy has recently emerged as a technology that improves the sensitivity of conventional bronchoscopy. In small-sized peripheral lung lesions, diagnostic yields are from 62.5 to 74 % [8, 9]. Although it is a safe procedure associated with a high diagnostic rate, this technique requires not only new instruments and software, but also training for appropriate use. Further examinations on the current prevalence of navigation bronchoscopy are necessary. The sensitivity of CTGNB varied widely among studies, but it has been consistently reported that the diagnostic yield is higher than that of conventional bronchoscopy (the

Surg Endosc Table 3 Comparison of tumor characteristics between correctly and erroneously diagnosed primary lung cancer by V-CNB Primary lung cancer (n = 83) Correctly diagnosed erroneously diagnosed Distance between pleura and tumor 5C

Location

Case (n = 78)

Case (n = 5)

p value*

2.6 (0–15)

9.0 (0–25)

0.256

64 (95.5 %)

3(4.5 %)

6–10

9 (100 %)

0 (0 %)

11B

5 (71.4 %)

2 (28.6 %)

upper lobe

47(90.4 %)

5 (9.6 %)

middle lobe

2 (100 %)

0 (0 %)

0.249

lower lobe

29 (100 %)

0 (0 %)

tumor size (mm)

22.2 (5 -50)

17.0 (12–25)

10[

6 (100 %)

0 (0 %)

11–20

34 (89.5 %)

4 (10.5 %)

21–30

28 (96.6 %)

1 (3.4 %)

31B

10 (100 %)

0 (0 %)

0.200

Operation procedure after V-CNB (partial resection/segmentectomy/lobectomy) * Two-tailed p value; p \ 0.05 was considered statistically significant

Table 4 Characteristics of primary lung cancer patients of which performed V-CNB

Number of patients

n = 83

Average age

67.2 (39–84)

Male/female

51/32

Average tumor size (mm) Right lung/left lung

21.9 (5–50) 58/25

Operative method Lobectomy

56

Segmentectomy

25

Partial resection

1

Biopsy

1

Pathological Stage (7th TNM classification) IA/IB

53/13

IIA/IIB

6/2

IIIA/IIIB

7/0

IV

2

Pleural invasion Pl 0/Pl 1 or more

64/19

Recurrence (n = 17, excluding two cases of stage IV) Pleural dissemination Distant

0

Lung

2

Bone

3

Lymph node

1

Skin

1

Local TBLB transbronchial lung biopsy

Lung

3

Lymph node

7

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Surg Endosc Table 5 Comparison of patient characteristics between V-CNB and non-V-CNB among stage I primary lung cancer of which lobectomy was performed

Age

V-CNB (n = 44)

Non-V-CNB (n = 87)

p value*

65.9 (33–84)

66.2 (35–83)

0.873

Male/female

26/18

47/40

0.581

Tumor size (mm)

23.5 (10–48)

24.7 (6–50)

0.482

Right/left

35/9

61/26

0.249

Distant local distance between pleura and tumor (mm)

3.4 (0–25)

5.0 (0–30)

0.202

TBLB CT guided biopsy

42 1

68 1

CT guided biopsy and TBLB

1

0

Sputum cytology

0

1

None

23

17

Preoperative diagnosis

0.240

Histopathology Adenocarcinoma

33

67

Adenosquamous

0

2

Squamous

6

10

LCNEC

2

3

Others

0

5

0.280

28/14

61/23

0.489

33/11

66/21

0.914

15/29

26/61

0.624

Differentiation Well differentiated/others Pathological stage (7th TNM classification) IA/IB Vascular invasion ± Pleural invasion 7/37

10/77

0.478

Operation time

±

228

217

0.186

Number of auto-suture instruments

4.77 (2–8)

4.61 (2–9)

0.533

Follow-up period (month)

47.9 (11–109)

51.3 (1–127)

0.516

Recurrence (%)

8 (18.2)

18 (20.5)

Pleural dissemination

0

2

0.796

Lung

4

5

0.727

Bone

0

2

0.796

Liver

0

1

0.727

Adrenal Gland

0

2

0.796

Lymph node

3

6

0.727

Chest wall

1

1

0.796

Distant

Local

* Two-tailed p value; p \ 0.05 was considered statistically significant TBLB transbronchial lung biopsy, CT computed tomography, LCNEC large cell neuroendocrine carcinoma

sensitivity ranges from 81 to 97 %) [10–12]. However, there are concerns over the numerous complications that have been observed, such as pneumothorax (23–38 %), pulmonary hemorrhage (4 %), air embolism (0.61 %), and

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even death [13–15]. Risk of such complications may limit the opportunities for subsequent operations. In our study, these were no complications associated with V-CNB (Table 4). Compared with CTGNB, V-CNB was

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considered safe because the tumor biopsy was performed in the collapsed lung under differential pulmonary ventilation, and a surgeon may easily arrest hemorrhage using thoracocotton after V-CNB has been performed. For intraoperative diagnosis, wedge resection biopsy using the auto-suture instrument, intraoperative NAB, and intraoperative CNB are being practiced. Frozen section diagnosis by wedge resection using the auto-suture instrument may be costly [1, 2], especially in large-sized indeterminate tumors which are necessary for the multiple usage of auto-suture instruments for the resection. In order to perform wedge resection, tumor needs to be small and located at the periphery of the lung where the auto-suture instrument can be applied across the tissue; therefore, the large-sized tumors located at deep position from the pleura and at hilar area of the lung are not suitable for the wedge resection [3]. V-CNB has a benefit that the thoracic surgeon can perform frozen section diagnosis on any detectable tumors which are not candidate for wedge resection biopsies (Fig. 1C, D). Thru-cut needle such as Quick-CoreÒ is less expensive than the auto-suture instrument, with a unit price of 52–57 $, whereas the auto-suture instrument itself costs 200–250 $ and each stapler costs 250–300 dollars (according to Japanese medical insurance). In this study, the average numbers of auto-suture instruments for the V-CNB group and the non-V-CNB group were 4.77 and 4.61, respectively, among stage I primary lung cancer cases for which lobectomy was performed (Table 5). V-CNB enables thoracic surgeons to avoid having to use the autosuture instrument that is necessary for wedge resection under complete VATS on frozen section diagnosis, which reduces medical expenses. In our study, the operation times for lobectomy and lymph node dissection on stage I primary lung cancer were not significantly different (228 min for the V-CNB group and 217 min for the non-V-CNB group, Table 5). It is concluded that V-CNB is a convenient means of frozen section diagnosis and does not increase operation time. V-CNB has another advantage compared with wedge resection biopsy in that it does not produce gross distortion of the lung after the biopsy. It is easier to recognize the division of the lung segment during sequential segmentectomy under complete VATS after V-CNB than after wedge resection biopsy. Intraoperative NAB is less costly than wedge resection biopsy and may be an effective approach because of its high sensitivity (94–97 %) and specificity (85–100 %), but the possibility of pleural dissemination remains [5, 6, 16]. Some studies compared the accuracy of CNB with FNA and concluded that cutting needle biopsy increases the diagnostic accuracy for cases of benign pulmonary disease [12, 17].

As mentioned in the results, sensitivity, specificity, and accuracy were 94.3, 87.5, and 93.7 %, respectively, with no relative complications (Tables 1, 2). These results are favorable compared with those in previous studies, which involved diagnoses by bronchoscopy, CTGNB, and intraoperative NAB, but inferior compared with intraoperative diagnosis by lung wedge resection biopsy under VATS, of which the sensitivity was 100 % [2]. Factor relates to the failure of V-CNB There were five cases of primary lung cancer that could not be diagnosed intraoperatively by V-CNB because the tumor tissues could not be obtained, and the frozen section diagnoses were normal lung tissues (Tables 2, 3). Compared with the correctly diagnosed cases, the tumors associated with V-CNB failure were smaller in size (B20 mm) and at a deeper location from the pleura (C11 mm), although the differences were not statistically significant, as shown in Table 3. Suzuki et al. suggests preoperative marking if the distance to the pleural surface is[5 mm in cases of nodules B10 mm in size because of a low detection rate during VATS [18]. Tumors that were considered difficult to detect were not an indication for V-CNB, and further study is necessary for the prediction of undetectable tumor during complete VATS. In this study, all five cases associated with V-CNB failure were located in the upper lobe, and it was considered that tumor in the upper lobe might be associated with difficulty in V-CNB, although there was no significant difference in the lobar distribution of the tumor between correctly diagnosed and erroneously diagnosed cases (p = 0.249). The largest incision (manipulation port) from which the surgeon manipulates was basically made right above the hilar level of the lung in order to facilitate processing of pulmonary vessels. Thus, surgeons have difficulty with palpation and performing V-CNB on tumors located in the apex of the lung that is far from the manipulation port. Further study on a large number of cases is necessary to improve the accuracy of V-CNB. Possibility of pleural dissemination by V-CNB CNB has been used for definitive diagnosis in several types of cancer and tumor seeding along the needle tract has also been a concern, such as in breast cancers [19], hepatocellular carcinoma [20], and bone sarcoma [21]. There are several reports related to needle tract implantation of lung cancer in percutaneous transthoracic needle biopsy, including CTGNB, and these studies have documented the occurrence of needle tract implantation at a rate of 0–3 % [22]. Moreover, previous studies also documented that the risk of pleural dissemination and implantation increased by CTGNB in primary lung cancer [23–25]. However, the possibility of pleural dissemination after undergoing

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V-CNB has not been studied previously. In this study, there were no pleural disseminations among primary lung cancer cases of stage IA to stage IIIA (Table 4). In addition, there were two cases of pleural dissemination in the non-V-CNB group among stage I primary lung cancer for which lobectomy was performed, while there were no cases of pleural dissemination in the V-CNB group. It is concluded that V-CNB does not increase the risk of pleural dissemination in stage I primary lung cancer compared with non-V-CNB. The follow-up period after the operation for the V-CNB group was 47.9 (11–109) months, which was considered long enough because implantation metastasis occurs within 2–16 months after biopsy [26]. Further examinations are required to validate this conclusion with a sufficient numbers of patients. In our experience, it was suggested that the number of tumor biopsies be limited to three or so, that the punctured site be pressed promptly, and that the site punctured by the biopsy needle be resected completely, to prevent pleural dissemination after V-CNB.

Future and conclusion V-CNB has an advantage in selected indeterminate tumor of which the wedge resection biopsy was considered difficult to perform. It is essential to find out the characteristics of tumors that might gain the greatest benefit from V-CNB. Moreover, V-CNB is not applicable to tumors that are not detectable during operation. A further analysis is necessary to predict whether the tumor can be detected during the operation or not, from the radiological findings before the operation. In conclusion, V-CNB is an effective methodology for diagnosing indeterminate tumor intraoperatively because it is very safe, enables the surgeon to save auto-suture instruments for other procedures, and has high diagnostic yield without increasing the operation time. Moreover, the risk of pleural dissemination is considered to be extremely low. Further examination on a large number of cases is necessary to identify the factors related to increasing accuracy of V-CNB.

Disclosures Tetsuya Isaka, Ko Takahashi, Takamitsu Maehara, and Munetaka Masuda have no conflicts of interest to disclose. Funding information

There is no source of fund.

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Intraoperative core needle biopsy under complete video-assisted thoracic surgery for indeterminate tumor of lung.

The accuracy, feasibility, and safety of intraoperative core needle biopsy under complete video-assisted thoracic surgery (VATS) (V-CNB) for indetermi...
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