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Transabdominal cardiophrenic lymph node dissection (CPLND) via incised diaphragm replace conventional video-assisted thoracic surgery for cytoreductive surgery in advanced ovarian cancer
Gynecologic Oncology 129 (2013) 341–345
Contents lists available at SciVerse ScienceDirect
Gynecologic Oncology journal homepage: www.elsevier.com/locate/ygyno
Transabdominal cardiophrenic lymph node dissection (CPLND) via incised diaphragm replace conventional video-assisted thoracic surgery for cytoreductive surgery in advanced ovarian cancer Heon Jong Yoo a, 1, Myong Cheol Lim a, 1, Yong Jung Song a, 2, Yuh-Seock Jung b, 2, Sun Ho Kim a, 3, Chong Woo Yoo a, 4, Sang-Yoon Park a,⁎ a b
Center for Uterine Cancer, Research Institute and Hospital, National Cancer Center, 323, Ilsan-ro, Ilsandong-gu, Goyang-si, Gyeonggi-do, 410-769, Republic of Korea Research Institute and Hospital, National Cancer Center, 323, Ilsan-ro, Ilsandong-gu, Goyang-si, Gyeonggi-do, 410-769, Republic of Korea
H I G H L I G H T S ► We approach a new procedure for ovarian cancer. ► New procedure is a part of the cytoreductive surgery. ► This can be acquired by gynecology oncologist without significant morbidities.
a r t i c l e
i n f o
Article history: Received 12 October 2012 Accepted 12 December 2012 Available online 3 January 2013 Keywords: Cardiophrenic lymph node Ovarian cancer Surgical management
a b s t r a c t Objective. The objective of this study is to describe the feasibility of the new approach, transabdominal CPLND, via incised diaphragm in patients with ovarian cancer by gynecologic oncologists instead of the conventional video-assisted thoracic surgery. Methods. From November 2008 to December 2011, 11 women (10 primary and 1 recurrent ovarian cancers) underwent CPLND for the extensive cytoreductive surgeries via incised muscle of the right diaphragm by gynecologic oncologists. All ≥5 mm tumors in CPLN, which were the criterion for suspicious malignancy on preoperative axial computed tomogram, were completely resected by gynecologic oncologists. Results. The median tumor size of the CPLN was 10 mm (range, 7–17 mm) and metastasis was identified in 45% (5/11) of ≥5 mm CPLN on preoperative computed tomogram. The median number of harvested CPLND was 3 (range 1–12) and metastatic node was 1 (range, 0–10). There was no significant morbidity related to CPLND and mortality associated with surgery. Ten patients achieved the no gross residual disease and one patient accomplished gross residual-1, indicating residual disease measuring ≤ 1 cm in maximal diameter. Conclusion. Transabdominal CPLND via incised diaphragm is feasible as a part of the cytoreductive surgery without significant morbidities by gynecologic oncologist. This procedure could substitute the conventional video-assisted thoracic surgery. © 2013 Published by Elsevier Inc.
Introduction Incidence of ovarian cancer was 2.1 per one hundred thousand people in South Korea, during 2009 [1] and continues to increase. Ovarian cancer is mainly diagnosed at an advanced stage with peritoneal seeding [2]. Minimizing residual tumor is one of the most ⁎ Corresponding author. Fax: +82 31 920 1238. E-mail addresses: [email protected] (H.J. Yoo), [email protected] (M.C. Lim), [email protected] (Y.J. Song), [email protected] (Y.-S. Jung), [email protected] (S.H. Kim), [email protected] (C.W. Yoo), [email protected] (S.-Y. Park). 1 Fax: +82 31 920 1238. 2 Fax: +82 31 920 1230. 3 Fax: +82 31 920 1715. 4 Fax: +82 31 920 1369. 0090-8258/$ – see front matter © 2013 Published by Elsevier Inc. http://dx.doi.org/10.1016/j.ygyno.2012.12.023
important prognostic factors in the management of advanced ovarian cancer [3,4]. A substantial number of patients with advanced-stage ovarian cancer present with bulky upper abdominal disease, and require diaphragmatic or intestinal procedures, splenectomy with or without a distal pancreatectomy, and peritoneal stripping to achieve an optimal cytoreduction. Several studies reported that such extensive procedures could improve the rate of optimal cytoreduction and overall survival with acceptable morbidities in ovarian cancer [5–7]. Cardiophrenic lymph nodes (CPLN) are located behind the xiphoid process and between the diaphragm and the heart, and are cited as an unusual location for lymph node metastasis [8]. Diagnosis and cytoreduction of intrathoracic metastasis, including CPLN from ovarian cancer, remains challenging. In colorectal cancer, intrathoracic
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H.J. Yoo et al. / Gynecologic Oncology 129 (2013) 341–345
metastatectomy is useful for selected patients in terms of attaining favorable survival outcome [9]. In ovarian cancer, some investigator reported that mediastinal lymphadenectomy or pleurodectomy, using video-assisted thoracic surgery (VATS) or subxiphoid mediastinal approach via a laparotomy incision to minimize intrathoracic metastatic disease, is useful in selected patients who have a moderate to large pleural effusion [10–12]. We previously reported the feasibility of pathologic diagnosis and cytoreduction of CPLN and pleural metastasis in ovarian cancer patients, using video-assisted thoracic surgery [13]. However, previous methods mostly needed to help thoracic surgeon and the equipment for the video-assisted thoracic surgery. We tried a different approach of the CPLN, intraabdominal approach via incised or resected diaphragm without the conventional video-assisted thoracic surgery. Until now, no study describing the feasibility and technique for transabdominal cardiophrenic lymph node dissection (CPLND) via incised/resected diaphragm. We, herein, report the usefulness of transabdominal approach via incised or resected diaphragm for CPLND in patients with primary and recurrent epithelial ovarian cancer.
A
B
Materials and methods A total of 163 patients were diagnosed with ovarian cancer by pathology at the Department of Uterine Cancer at the National Cancer Center Korea, between November 2008 and December 2011. This retrospective study was approved by the institutional review board (NCCNS-12-594). In the current study, the criterion for suspicious malignancy in the thorax was a CPLN with short-axis dimension of greater than 5 mm on axial computed tomogram (CT) [13]. The CT studies were reviewed by the radiologist who had the specific experiences for gynecologic oncology. We reviewed patients' charts retrospectively and collected demographic, clinical, surgical, and pathologic information. Of the 11 women (10 primary and 1 recurrent ovarian cancer) underwent CPLND with extensive cytoreductive surgeries for optimal cytoreduction, such as partial hepatectomy, distal pancreatectomy, splenectomy, diaphragmatic stripping or resection, low anterior resection of rectum, total colectomy, or ileocecectomy. The end result of cytoreductive surgery in thorax and abdomen were defined as (A) no gross residual, reflecting complete cytoreduction to a visibly disease-free state (microscopic residual); (B) gross residual-1, indicating residual disease measuring ≤1 cm in maximal diameter; and (C) gross residual-bulky (GR-B), for residual disease measuring > 1 cm in maximal diameter [14]. Transabdominal CPLND via incised or resected diaphragm. In routine clinical practice, all patients underwent CT or magnetic resonance imaging of the pelvis, abdomen and chest to evaluate the disease extent, and to estimate the likely extent of surgery (Fig. 1), and positron emission tomogram-computed tomogram (PET-CT) to identify metastatic disease, the resectability of intrathoracic metastatic disease were discussed at the tumor board—a multidisciplinary team meeting of a gynecological oncologist, radiation oncologist, diagnostic radiologist, pathologist, and a nuclear medicine physician. For the transabdominal CPLND, a generous incision from the xiphoid to the symphysis pubis, a fixed upper abdominal retractor, and adequate mobilization of the liver were essential components to ensure appropriate access to the cardiophrenic space (Figs. 2, 3A). For entering cardiophrenic space, the liver was pushed down to the inferior region. To approach the CPLN, we either enter after incising the just below sternum or through the hole that was created in the process of removing metastatic tumor of right diaphragm (Figs. 2, 3B). During the incising or resecting muscle of the right diaphragm, there was no concern about the injury of phrenic vessels and nerves. After entering the cardiophrenic space, biopsy and cytoreduction were performed for all suspicious lesions, including CPLN (Figs. 2, 3C, D). Be careful not to go near the heart while performing the left side dissection (Fig. 3D). On
Fig. 1. (A) In the preoperative chest CT image, an enlargement of the right cardiophrenic lymph node was observed (in a circle) in a 51 year-old patient with primary ovarian cancer. (B) In postoperative chest CT image, right cardiophrenic lymph node enlargement was not founded (in a circle).
occasion, incidental entry into the pleural cavity might be unavoidable. Once the pleural cavity had been entered, the anesthesiologist was notified (Fig. 3E). The perforation of parietal pleura had not been repaired and the opened parietal pleura had just been observed. Large defect of the diaphragmatic muscle had been repaired with a simple fullthickness closure, using an interrupted stitch of large caliber nonabsorbable multifilament suture like 1-0 prolene (Fig. 3F). Then, an air leakage test was performed by placing the patient in a Trendelenburg position, filling the upper abdomen with saline solution, and having the anesthesiologist deliver several large mechanical ventilations. The absence of bubbles indicated an airtight closure. The patients who approached CPLN by way of resecting the diaphragmatic muscle were selectively applied by Jackson Pratt drain through the resected diaphragm. Results From November 2008 to December 2011, a total of 163 patients were diagnosed with ovarian cancer, and 11 patients who had ovarian cancer underwent CPLND via transabdominal approach (6.7%). All 11 patients had the suspicious malignancy in the thorax, which was a CPLN with short-axis dimension of greater than 5 mm on axial preoperative chest CT. The median age was 58 years (range, 52–70 years), the median preoperative serum CA 125 was 897 U/ml (range, 25–8200 U/ml) and the median short diameters of CPLN in axial CT were 10.0 mm (range, 7.0–17.0 mm). Histologic findings were serous carcinoma in 9 patients, mixed Mullerian tumor in 1 patient, and undifferentiated tumor in 1 patient (Table 1). The surgical procedure, completeness of optimal cytoreductive surgery, operation time,
H.J. Yoo et al. / Gynecologic Oncology 129 (2013) 341–345
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Fig. 2. Structural illustration around cardiophrenic lymph node. For entering cardiophrenic space, the liver was pushed down to the inferior region and 1) incise the just below the sternum or 2) resect the central tendon of the right diaphragm for removing tumor and exposing the bared area. CW chest wall, C pericardium, D diaphragm, FL falciform ligament, IVC inferior vena cava, L liver, P pleura, and PV portal vein.
estimated blood loss and intraoperative transfusion are shown in Table 2. In 9 patients who approached at CPLN by way of incising just below the sternum, Jackson Pratt drain was not applied. Two patients who approached CPLN by way of resecting a muscle of the diaphragm, Jackson Pratt drain was applied through the resected diaphragm. In the 11 patients who were harvested one more CPLN in postoperative biopsy, 10 patients had primary ovarian cancer and 1 patient had recurrent ovarian cancer. The median number of harvested CPLNs was three (range, 1–12). Pathological examination revealed CPLNs positive for metastasis in 5 patients (45%; median 1, range 0–10). The median operative time and blood loss were 470 min (range, 415–700 min) and 2000 mL (1000–5700 mL), respectively. The specific operation time of transabdominal CPLND via incised or resected diaphragm was about 30 minutes. The median amount of red blood cell transfused was 3 units (range, 2–9 units) for 8 patients. Ten patients achieved the no gross residual disease and one patient accomplished the ≤1 cm gross residual disease in maximal diameter.
CW
CW D
CW
PP
L
CPLN
Intra-operative complications specific for transabdominal CPLND, such as severe bleeding due to injury of phrenic arteries or injury to the heart, lung and liver were not observed. Overall morbidity rate was 45% (5/11). Wound problem was the most common complication, occurring in 2 patients (18%). Complications other than wound problem were seen in 3 patients (27%): 1 fistula, 1 ileus, and 1 pleural effusion. Only one patient who concurrently performed the diaphragmatic peritonectomy underwent dyspnea by pleural effusion. Pleural effusion was successfully resolved by indwelling the Jackson Pratt drain. The median postoperative stay and days from operation to chemotherapy were 21 days (range, 14–28 days) and 32 days (range, 15–70 days), respectively (Table 2). There were no surgery-related deaths. The median follow-up time was 15 months (range, 9–31 months) and 24-month disease-free survival was 23%. Six patients had multiple peritoneal metastasis and 1 patient had pleural or lung metastasis with paraaortic lymph node metastsis. Only one case was a localized mesenteric nodal recurrence. No one recurred in CPLN. One patient who applied Jackson Pratt drain through the resected diaphragm had pleural metastasis
C
PP
PP VP
C
Fig. 3. Intraoperative photography (A) liver mobilization. (B) Dissecting the parietal pleura. (C) Entering the cardiophrenic space. (D) Dissecting the cardiophrenic lymph node. (E) Completion of the cardiophrenic lymph node dissection. (F) Repairing the parietal pleura. C pericardium, CW chest wall, CPLN cardiophrenic lymph node, D diaphragm, L liver, PP parietal pleura, VP visceral pleura.
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Table 1 Clinical characteristics of patients with cardiophrenic lymph node dissection via transdiaphragmatic route for ovarian cancer. Clinical characteristics
N = 11
Age (year) Disease status Primary Recurrent Histology Serous Undifferentiated Mixed Neoadjuvant chemotherapy Yes No Preoperative CA 125 (U/ml) Pleural effusion Short diameter in axial computed tomogram (cm)
58 (52–70) 10 1 9 1 1 1 11 897 (25–8200) 3 10.0 (7.0–17.0)
and the other patient had multiple peritoneal metastasis without pleural metastasis. Discussion Transabdominal CPLND via incised/resected diaphragm, a new surgical technique, brought the complete resection of CPLN, resulting in optimal cytoreduction in patients with ovarian cancer. Survival determinants are multifactorial for ovarian cancer; however, the strongest clinician-driven predictors of clinical outcome are the administration of platinum-based chemotherapy and the amount of residual tumor following a primary surgery [15]. Resection of the primary tumor mass, including the upper abdomen, is a key component of the initial cytoreductive surgical effort [15]. Few studies reported that pulmonary
Table 2 Surgical outcomes and complications. Variables
No
Operative time (min) Estimated blood loss (ml) Blood transfusion (units) Residual tumor no gross residual gross residual-1⁎ Surgical procedures Hysterectomy and salpingoophorectomy Pelvic and paraaortic lymph node dissection Omentectomy Splenectomy Distal pancreatectomy Liver segmentectomy Diaphragm peritonectomy Diaphragm resection Low anterior resection of rectum Small bowel resection and anastomosis Ileocecectomy Total colectomy Pelvic peritonectomy Pathology in CPLN Metastatic LN Harvested LN Postoperative complication Wound dehiscence Anastomic site leakage Ileus Pleural effusion From operation to chemotherapy (days) Hospital days
470 (415–700) 2000 (1000–5700) 3 (2–9) 10 (91%) 1 (9%) 10 10 10 5 2 1 6 2 6 1 1 2 6 1 (0–10) 3 (1–12) 5 (45%) 2 (18%) 1 (9%) 1 (9%) 1 (9%) 21 (14–28) 32 (15–70)
CPLN, cardiophrenic lymph node; LN, lymph node *: gross residual-1, indicating residual disease measuring ≤1 cm in maximal diameter
resection for metastatic gynecologic cancer in selected patients has recently been reported to be safe and effective [16,17]. We reported that the accurate pathological diagnosis and intrathoracic resection of pleural and CPLN metastasis in patients with ovarian cancer were acceptable via VATS [13]. The present study utilized new surgical technique from using VATS to direct approach via the incised or resected diaphragm to diagnose and resect intrathoracic metastatic disease from ovarian cancer. As a novel surgical technique like transabdominal CPLND have developed, optimal debulking rate in patients with advanced ovarian cancer could be increased. VATS is a useful tool in the management of ovarian cancer in patients with malignant pleural effusion [18]. There were few reports that VATS in patients with advanced primary ovarian cancer was useful and had acceptable morbidity [13,18]. However, VATS had certain limitations. First, VATS was performed under double-lumen endotracheal anesthesia in the later decubitus position, not in a supine position. Therefore, we need to change the patient's position in an operation. Second, VATS was performed by a specialized thoracic surgeon, not surgeon for gynecologic oncology. Third, following VATS, a 24-Fr chest tube was placed through the port incision and chest pain caused by the chest tube. Although transabdominal approach could not assess the pleural cavity perfectly, the right parietal and visceral pleura could be easily assessed. Surgical evolution from using VATS to the transabdominal approach, via incised or resected diaphragm, brought some benefits. Potential advantages of using the transabdominal CPLND were that there was no need of position change for VATS, feasible procedure for gynecologic oncologist, no need of chest tube insertion and less pain from omitting the chest tube. The previous studies reported the rates of postoperative pleural effusion ranged from 10% to 59% for the ovarian cancer patients who underwent diaphragmatic surgery [19–21]. Transabdominal CPLND via the incised/resected diaphragm with extensive cytoreductive surgery could be increasing the morbidity. In the present study, there was no specific complication for transabdominal CPLND via the incised/resected diaphragm. Only one patient who concurrently performed a diaphragmatic peritonectomy had dyspnea by pleural effusion. However, pleural effusion was successfully resolved by indwelling the Jackson Pratt catheter. Transabdominal CPLND via the incised/ resected diaphragm was a feasible technique for one of the specific intrathoracic cytoreductive surgery, had no risk of specific mortality and had acceptable morbidity. This finding should be confirmed in a larger population. Two patients who approached CPLN by way of resecting a muscle of the diaphragm, Jackson Pratt drain was applied through the resected diaphragm. In this study, 24-month disease-free survival was 23%. Six patients had multiple peritoneal metastasis. One patient had pleural or lung metastasis with paraaortic lymph node metastsis. Only one case was a localized mesenteric nodal recurrence. No one recurred in CPLN. One patient who applied Jackson Pratt drain through the resected diaphragm had pleural metastasis and the other patient had multiple peritoneal metastasis without pleural metastasis. Even though there were only two patients who applied Jackson Pratt drain through the resected diaphragm, inserting the Jackson Pratt drain through the resected diaphragm should be avoided for the possibility of seeding the pleural cavity with tumor from the peritoneal cavity. This finding should be confirmed in a larger population. Although the present study was retrospective, it is not to reveal any conclusions in terms of survival outcome due to the small and heterogenous population, a novel surgical technique enables tumor resection of the CPLN with acceptable morbidities in the surgical management of primary or recurrent ovarian cancer without the support of a specialized thoracic surgeon. In conclusion, transabdominal CPLND via the incised/resected diaphragm is feasible and can be acquired by gynecological oncologist as parts of primary or secondary cytoreductive surgery without significant morbidities. Further studies for survival benefit of CPLND will be needed.
H.J. Yoo et al. / Gynecologic Oncology 129 (2013) 341–345 Conflict of interest statement The authors declare that there are no conflicts of interest.
[11]
References [12] [1] Ministry of Health and Welfare. Annual report of cancer statistics in Korea in 2009. National Cancer Registry; 2011. [2] Chung HH, Hwang SY, Jung KW, Won YJ, Shin HR, Kim JW, et al. Ovarian cancer incidence and survival in Korea: 1993–2002. Int J Gynecol Cancer 2007;17:595–600. [3] Hoskins WJ, McGuire WP, Brady MF, Homesley HD, Creasman WT, Berman M, et al. The effect of diameter of largest residual disease on survival after primary cytoreductive surgery in patients with suboptimal residual epithelial ovarian carcinoma. Am J Obstet Gynecol 1994;170:974–9 [discussion 979–80]. [4] Bristow RE, Tomacruz RS, Armstrong DK, Trimble EL, Montz FJ. Survival effect of maximal cytoreductive surgery for advanced ovarian carcinoma during the platinum era: a meta-analysis. J Clin Oncol 2002;20:1248–59. [5] Chi DS, Franklin CC, Levine DA, Akselrod F, Sabbatini P, Jarnagin WR, et al. Improved optimal cytoreduction rates for stages IIIC and IV epithelial ovarian, fallopian tube, and primary peritoneal cancer: a change in surgical approach. Gynecol Oncol 2004;94:650–4. [6] Song YJ, Lim MC, Kang S, Seo SS, Park JW, Choi HS, et al. Total colectomy as part of primary cytoreductive surgery in advanced Mullerian cancer. Gynecol Oncol 2009;114:183–7. [7] Song YJ, Lim MC, Kang S, Seo SS, Kim SH, Han SS, et al. Extended cytoreduction of tumor at the porta hepatis by an interdisciplinary team approach in patients with epithelial ovarian cancer. Gynecol Oncol 2011;121:253–7. [8] Moulding FJ, Roach SC, Carrington BM. Unusual sites of lymph node metastases and pitfalls in their detection. Clin Radiol 2004;59:558–72. [9] Pfannschmidt J, Dienemann H, Hoffmann H. Surgical resection of pulmonary metastases from colorectal cancer: a systematic review of published series. Ann Thorac Surg 2007;84:324–38. [10] Juretzka MM, Abu-Rustum NR, Sonoda Y, Downey RJ, Flores RM, Park BJ, et al. The impact of video-assisted thoracic surgery (VATS) in patients with suspected
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Contents lists available at SciVerse ScienceDirect
Gynecologic Oncology journal homepage: www.elsevier.com/locate/ygyno
Transabdominal cardiophrenic lymph node dissection (CPLND) via incised diaphragm replace conventional video-assisted thoracic surgery for cytoreductive surgery in advanced ovarian cancer Heon Jong Yoo a, 1, Myong Cheol Lim a, 1, Yong Jung Song a, 2, Yuh-Seock Jung b, 2, Sun Ho Kim a, 3, Chong Woo Yoo a, 4, Sang-Yoon Park a,⁎ a b
Center for Uterine Cancer, Research Institute and Hospital, National Cancer Center, 323, Ilsan-ro, Ilsandong-gu, Goyang-si, Gyeonggi-do, 410-769, Republic of Korea Research Institute and Hospital, National Cancer Center, 323, Ilsan-ro, Ilsandong-gu, Goyang-si, Gyeonggi-do, 410-769, Republic of Korea
H I G H L I G H T S ► We approach a new procedure for ovarian cancer. ► New procedure is a part of the cytoreductive surgery. ► This can be acquired by gynecology oncologist without significant morbidities.
a r t i c l e
i n f o
Article history: Received 12 October 2012 Accepted 12 December 2012 Available online 3 January 2013 Keywords: Cardiophrenic lymph node Ovarian cancer Surgical management
a b s t r a c t Objective. The objective of this study is to describe the feasibility of the new approach, transabdominal CPLND, via incised diaphragm in patients with ovarian cancer by gynecologic oncologists instead of the conventional video-assisted thoracic surgery. Methods. From November 2008 to December 2011, 11 women (10 primary and 1 recurrent ovarian cancers) underwent CPLND for the extensive cytoreductive surgeries via incised muscle of the right diaphragm by gynecologic oncologists. All ≥5 mm tumors in CPLN, which were the criterion for suspicious malignancy on preoperative axial computed tomogram, were completely resected by gynecologic oncologists. Results. The median tumor size of the CPLN was 10 mm (range, 7–17 mm) and metastasis was identified in 45% (5/11) of ≥5 mm CPLN on preoperative computed tomogram. The median number of harvested CPLND was 3 (range 1–12) and metastatic node was 1 (range, 0–10). There was no significant morbidity related to CPLND and mortality associated with surgery. Ten patients achieved the no gross residual disease and one patient accomplished gross residual-1, indicating residual disease measuring ≤ 1 cm in maximal diameter. Conclusion. Transabdominal CPLND via incised diaphragm is feasible as a part of the cytoreductive surgery without significant morbidities by gynecologic oncologist. This procedure could substitute the conventional video-assisted thoracic surgery. © 2013 Published by Elsevier Inc.
Introduction Incidence of ovarian cancer was 2.1 per one hundred thousand people in South Korea, during 2009 [1] and continues to increase. Ovarian cancer is mainly diagnosed at an advanced stage with peritoneal seeding [2]. Minimizing residual tumor is one of the most ⁎ Corresponding author. Fax: +82 31 920 1238. E-mail addresses: [email protected] (H.J. Yoo), [email protected] (M.C. Lim), [email protected] (Y.J. Song), [email protected] (Y.-S. Jung), [email protected] (S.H. Kim), [email protected] (C.W. Yoo), [email protected] (S.-Y. Park). 1 Fax: +82 31 920 1238. 2 Fax: +82 31 920 1230. 3 Fax: +82 31 920 1715. 4 Fax: +82 31 920 1369. 0090-8258/$ – see front matter © 2013 Published by Elsevier Inc. http://dx.doi.org/10.1016/j.ygyno.2012.12.023
important prognostic factors in the management of advanced ovarian cancer [3,4]. A substantial number of patients with advanced-stage ovarian cancer present with bulky upper abdominal disease, and require diaphragmatic or intestinal procedures, splenectomy with or without a distal pancreatectomy, and peritoneal stripping to achieve an optimal cytoreduction. Several studies reported that such extensive procedures could improve the rate of optimal cytoreduction and overall survival with acceptable morbidities in ovarian cancer [5–7]. Cardiophrenic lymph nodes (CPLN) are located behind the xiphoid process and between the diaphragm and the heart, and are cited as an unusual location for lymph node metastasis [8]. Diagnosis and cytoreduction of intrathoracic metastasis, including CPLN from ovarian cancer, remains challenging. In colorectal cancer, intrathoracic
342
H.J. Yoo et al. / Gynecologic Oncology 129 (2013) 341–345
metastatectomy is useful for selected patients in terms of attaining favorable survival outcome [9]. In ovarian cancer, some investigator reported that mediastinal lymphadenectomy or pleurodectomy, using video-assisted thoracic surgery (VATS) or subxiphoid mediastinal approach via a laparotomy incision to minimize intrathoracic metastatic disease, is useful in selected patients who have a moderate to large pleural effusion [10–12]. We previously reported the feasibility of pathologic diagnosis and cytoreduction of CPLN and pleural metastasis in ovarian cancer patients, using video-assisted thoracic surgery [13]. However, previous methods mostly needed to help thoracic surgeon and the equipment for the video-assisted thoracic surgery. We tried a different approach of the CPLN, intraabdominal approach via incised or resected diaphragm without the conventional video-assisted thoracic surgery. Until now, no study describing the feasibility and technique for transabdominal cardiophrenic lymph node dissection (CPLND) via incised/resected diaphragm. We, herein, report the usefulness of transabdominal approach via incised or resected diaphragm for CPLND in patients with primary and recurrent epithelial ovarian cancer.
A
B
Materials and methods A total of 163 patients were diagnosed with ovarian cancer by pathology at the Department of Uterine Cancer at the National Cancer Center Korea, between November 2008 and December 2011. This retrospective study was approved by the institutional review board (NCCNS-12-594). In the current study, the criterion for suspicious malignancy in the thorax was a CPLN with short-axis dimension of greater than 5 mm on axial computed tomogram (CT) [13]. The CT studies were reviewed by the radiologist who had the specific experiences for gynecologic oncology. We reviewed patients' charts retrospectively and collected demographic, clinical, surgical, and pathologic information. Of the 11 women (10 primary and 1 recurrent ovarian cancer) underwent CPLND with extensive cytoreductive surgeries for optimal cytoreduction, such as partial hepatectomy, distal pancreatectomy, splenectomy, diaphragmatic stripping or resection, low anterior resection of rectum, total colectomy, or ileocecectomy. The end result of cytoreductive surgery in thorax and abdomen were defined as (A) no gross residual, reflecting complete cytoreduction to a visibly disease-free state (microscopic residual); (B) gross residual-1, indicating residual disease measuring ≤1 cm in maximal diameter; and (C) gross residual-bulky (GR-B), for residual disease measuring > 1 cm in maximal diameter [14]. Transabdominal CPLND via incised or resected diaphragm. In routine clinical practice, all patients underwent CT or magnetic resonance imaging of the pelvis, abdomen and chest to evaluate the disease extent, and to estimate the likely extent of surgery (Fig. 1), and positron emission tomogram-computed tomogram (PET-CT) to identify metastatic disease, the resectability of intrathoracic metastatic disease were discussed at the tumor board—a multidisciplinary team meeting of a gynecological oncologist, radiation oncologist, diagnostic radiologist, pathologist, and a nuclear medicine physician. For the transabdominal CPLND, a generous incision from the xiphoid to the symphysis pubis, a fixed upper abdominal retractor, and adequate mobilization of the liver were essential components to ensure appropriate access to the cardiophrenic space (Figs. 2, 3A). For entering cardiophrenic space, the liver was pushed down to the inferior region. To approach the CPLN, we either enter after incising the just below sternum or through the hole that was created in the process of removing metastatic tumor of right diaphragm (Figs. 2, 3B). During the incising or resecting muscle of the right diaphragm, there was no concern about the injury of phrenic vessels and nerves. After entering the cardiophrenic space, biopsy and cytoreduction were performed for all suspicious lesions, including CPLN (Figs. 2, 3C, D). Be careful not to go near the heart while performing the left side dissection (Fig. 3D). On
Fig. 1. (A) In the preoperative chest CT image, an enlargement of the right cardiophrenic lymph node was observed (in a circle) in a 51 year-old patient with primary ovarian cancer. (B) In postoperative chest CT image, right cardiophrenic lymph node enlargement was not founded (in a circle).
occasion, incidental entry into the pleural cavity might be unavoidable. Once the pleural cavity had been entered, the anesthesiologist was notified (Fig. 3E). The perforation of parietal pleura had not been repaired and the opened parietal pleura had just been observed. Large defect of the diaphragmatic muscle had been repaired with a simple fullthickness closure, using an interrupted stitch of large caliber nonabsorbable multifilament suture like 1-0 prolene (Fig. 3F). Then, an air leakage test was performed by placing the patient in a Trendelenburg position, filling the upper abdomen with saline solution, and having the anesthesiologist deliver several large mechanical ventilations. The absence of bubbles indicated an airtight closure. The patients who approached CPLN by way of resecting the diaphragmatic muscle were selectively applied by Jackson Pratt drain through the resected diaphragm. Results From November 2008 to December 2011, a total of 163 patients were diagnosed with ovarian cancer, and 11 patients who had ovarian cancer underwent CPLND via transabdominal approach (6.7%). All 11 patients had the suspicious malignancy in the thorax, which was a CPLN with short-axis dimension of greater than 5 mm on axial preoperative chest CT. The median age was 58 years (range, 52–70 years), the median preoperative serum CA 125 was 897 U/ml (range, 25–8200 U/ml) and the median short diameters of CPLN in axial CT were 10.0 mm (range, 7.0–17.0 mm). Histologic findings were serous carcinoma in 9 patients, mixed Mullerian tumor in 1 patient, and undifferentiated tumor in 1 patient (Table 1). The surgical procedure, completeness of optimal cytoreductive surgery, operation time,
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Fig. 2. Structural illustration around cardiophrenic lymph node. For entering cardiophrenic space, the liver was pushed down to the inferior region and 1) incise the just below the sternum or 2) resect the central tendon of the right diaphragm for removing tumor and exposing the bared area. CW chest wall, C pericardium, D diaphragm, FL falciform ligament, IVC inferior vena cava, L liver, P pleura, and PV portal vein.
estimated blood loss and intraoperative transfusion are shown in Table 2. In 9 patients who approached at CPLN by way of incising just below the sternum, Jackson Pratt drain was not applied. Two patients who approached CPLN by way of resecting a muscle of the diaphragm, Jackson Pratt drain was applied through the resected diaphragm. In the 11 patients who were harvested one more CPLN in postoperative biopsy, 10 patients had primary ovarian cancer and 1 patient had recurrent ovarian cancer. The median number of harvested CPLNs was three (range, 1–12). Pathological examination revealed CPLNs positive for metastasis in 5 patients (45%; median 1, range 0–10). The median operative time and blood loss were 470 min (range, 415–700 min) and 2000 mL (1000–5700 mL), respectively. The specific operation time of transabdominal CPLND via incised or resected diaphragm was about 30 minutes. The median amount of red blood cell transfused was 3 units (range, 2–9 units) for 8 patients. Ten patients achieved the no gross residual disease and one patient accomplished the ≤1 cm gross residual disease in maximal diameter.
CW
CW D
CW
PP
L
CPLN
Intra-operative complications specific for transabdominal CPLND, such as severe bleeding due to injury of phrenic arteries or injury to the heart, lung and liver were not observed. Overall morbidity rate was 45% (5/11). Wound problem was the most common complication, occurring in 2 patients (18%). Complications other than wound problem were seen in 3 patients (27%): 1 fistula, 1 ileus, and 1 pleural effusion. Only one patient who concurrently performed the diaphragmatic peritonectomy underwent dyspnea by pleural effusion. Pleural effusion was successfully resolved by indwelling the Jackson Pratt drain. The median postoperative stay and days from operation to chemotherapy were 21 days (range, 14–28 days) and 32 days (range, 15–70 days), respectively (Table 2). There were no surgery-related deaths. The median follow-up time was 15 months (range, 9–31 months) and 24-month disease-free survival was 23%. Six patients had multiple peritoneal metastasis and 1 patient had pleural or lung metastasis with paraaortic lymph node metastsis. Only one case was a localized mesenteric nodal recurrence. No one recurred in CPLN. One patient who applied Jackson Pratt drain through the resected diaphragm had pleural metastasis
C
PP
PP VP
C
Fig. 3. Intraoperative photography (A) liver mobilization. (B) Dissecting the parietal pleura. (C) Entering the cardiophrenic space. (D) Dissecting the cardiophrenic lymph node. (E) Completion of the cardiophrenic lymph node dissection. (F) Repairing the parietal pleura. C pericardium, CW chest wall, CPLN cardiophrenic lymph node, D diaphragm, L liver, PP parietal pleura, VP visceral pleura.
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Table 1 Clinical characteristics of patients with cardiophrenic lymph node dissection via transdiaphragmatic route for ovarian cancer. Clinical characteristics
N = 11
Age (year) Disease status Primary Recurrent Histology Serous Undifferentiated Mixed Neoadjuvant chemotherapy Yes No Preoperative CA 125 (U/ml) Pleural effusion Short diameter in axial computed tomogram (cm)
58 (52–70) 10 1 9 1 1 1 11 897 (25–8200) 3 10.0 (7.0–17.0)
and the other patient had multiple peritoneal metastasis without pleural metastasis. Discussion Transabdominal CPLND via incised/resected diaphragm, a new surgical technique, brought the complete resection of CPLN, resulting in optimal cytoreduction in patients with ovarian cancer. Survival determinants are multifactorial for ovarian cancer; however, the strongest clinician-driven predictors of clinical outcome are the administration of platinum-based chemotherapy and the amount of residual tumor following a primary surgery [15]. Resection of the primary tumor mass, including the upper abdomen, is a key component of the initial cytoreductive surgical effort [15]. Few studies reported that pulmonary
Table 2 Surgical outcomes and complications. Variables
No
Operative time (min) Estimated blood loss (ml) Blood transfusion (units) Residual tumor no gross residual gross residual-1⁎ Surgical procedures Hysterectomy and salpingoophorectomy Pelvic and paraaortic lymph node dissection Omentectomy Splenectomy Distal pancreatectomy Liver segmentectomy Diaphragm peritonectomy Diaphragm resection Low anterior resection of rectum Small bowel resection and anastomosis Ileocecectomy Total colectomy Pelvic peritonectomy Pathology in CPLN Metastatic LN Harvested LN Postoperative complication Wound dehiscence Anastomic site leakage Ileus Pleural effusion From operation to chemotherapy (days) Hospital days
470 (415–700) 2000 (1000–5700) 3 (2–9) 10 (91%) 1 (9%) 10 10 10 5 2 1 6 2 6 1 1 2 6 1 (0–10) 3 (1–12) 5 (45%) 2 (18%) 1 (9%) 1 (9%) 1 (9%) 21 (14–28) 32 (15–70)
CPLN, cardiophrenic lymph node; LN, lymph node *: gross residual-1, indicating residual disease measuring ≤1 cm in maximal diameter
resection for metastatic gynecologic cancer in selected patients has recently been reported to be safe and effective [16,17]. We reported that the accurate pathological diagnosis and intrathoracic resection of pleural and CPLN metastasis in patients with ovarian cancer were acceptable via VATS [13]. The present study utilized new surgical technique from using VATS to direct approach via the incised or resected diaphragm to diagnose and resect intrathoracic metastatic disease from ovarian cancer. As a novel surgical technique like transabdominal CPLND have developed, optimal debulking rate in patients with advanced ovarian cancer could be increased. VATS is a useful tool in the management of ovarian cancer in patients with malignant pleural effusion [18]. There were few reports that VATS in patients with advanced primary ovarian cancer was useful and had acceptable morbidity [13,18]. However, VATS had certain limitations. First, VATS was performed under double-lumen endotracheal anesthesia in the later decubitus position, not in a supine position. Therefore, we need to change the patient's position in an operation. Second, VATS was performed by a specialized thoracic surgeon, not surgeon for gynecologic oncology. Third, following VATS, a 24-Fr chest tube was placed through the port incision and chest pain caused by the chest tube. Although transabdominal approach could not assess the pleural cavity perfectly, the right parietal and visceral pleura could be easily assessed. Surgical evolution from using VATS to the transabdominal approach, via incised or resected diaphragm, brought some benefits. Potential advantages of using the transabdominal CPLND were that there was no need of position change for VATS, feasible procedure for gynecologic oncologist, no need of chest tube insertion and less pain from omitting the chest tube. The previous studies reported the rates of postoperative pleural effusion ranged from 10% to 59% for the ovarian cancer patients who underwent diaphragmatic surgery [19–21]. Transabdominal CPLND via the incised/resected diaphragm with extensive cytoreductive surgery could be increasing the morbidity. In the present study, there was no specific complication for transabdominal CPLND via the incised/resected diaphragm. Only one patient who concurrently performed a diaphragmatic peritonectomy had dyspnea by pleural effusion. However, pleural effusion was successfully resolved by indwelling the Jackson Pratt catheter. Transabdominal CPLND via the incised/ resected diaphragm was a feasible technique for one of the specific intrathoracic cytoreductive surgery, had no risk of specific mortality and had acceptable morbidity. This finding should be confirmed in a larger population. Two patients who approached CPLN by way of resecting a muscle of the diaphragm, Jackson Pratt drain was applied through the resected diaphragm. In this study, 24-month disease-free survival was 23%. Six patients had multiple peritoneal metastasis. One patient had pleural or lung metastasis with paraaortic lymph node metastsis. Only one case was a localized mesenteric nodal recurrence. No one recurred in CPLN. One patient who applied Jackson Pratt drain through the resected diaphragm had pleural metastasis and the other patient had multiple peritoneal metastasis without pleural metastasis. Even though there were only two patients who applied Jackson Pratt drain through the resected diaphragm, inserting the Jackson Pratt drain through the resected diaphragm should be avoided for the possibility of seeding the pleural cavity with tumor from the peritoneal cavity. This finding should be confirmed in a larger population. Although the present study was retrospective, it is not to reveal any conclusions in terms of survival outcome due to the small and heterogenous population, a novel surgical technique enables tumor resection of the CPLN with acceptable morbidities in the surgical management of primary or recurrent ovarian cancer without the support of a specialized thoracic surgeon. In conclusion, transabdominal CPLND via the incised/resected diaphragm is feasible and can be acquired by gynecological oncologist as parts of primary or secondary cytoreductive surgery without significant morbidities. Further studies for survival benefit of CPLND will be needed.
H.J. Yoo et al. / Gynecologic Oncology 129 (2013) 341–345 Conflict of interest statement The authors declare that there are no conflicts of interest.
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