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research-article2014
SRIXXX10.1177/1553350614552733Surgical InnovationChen et al
Procedural Innovations
Transumbilical Thoracoscopy Versus Conventional Thoracoscopy for Lung Wedge Resection: Safety and Efficacy in a Live Canine Model
Surgical Innovation 2015, Vol. 22(6) 568–576 © The Author(s) 2014 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/1553350614552733 sri.sagepub.com
Tzu-Ping Chen, MD1, Yen-Chu, PhD2, Yi-Cheng Wu, MD2, Chi-Ju Yeh, MD2, Chien-Ying Liu, MD2, Ming-Ju Hsieh, MD2, Hsu-Chia Yuan, MD2, Po-Jen Ko, MD2, and Yun-Hen Liu, MD2
Abstract Purpose. Transumbilical single-port surgery has been associated with less postoperative pain and offers better cosmetic outcomes than conventional 3-port laparoscopic surgery. This study compares the safety and efficacy of transumbilical thoracoscopy and conventional thoracoscopy for lung wedge resection. Methods. The animals (n = 16) were randomly assigned to the transumbilical thoracoscopic approach group (n = 8) or conventional thoracoscopic approach group (n = 8). Transumbilical lung resection was performed via an umbilical incision and a diaphragmatic incision. In the conventional thoracoscopic group, lung resection was completed through a thoracic incision. For both procedures, we compared the surgical outcomes, for example, operating time and operative complications; physiologic parameters, for example, respiratory rate and body temperature; inflammatory parameters, for example, white blood cell count; and pulmonary parameters, for example, arterial blood gas levels. The animals were euthanized 2 weeks after the surgery for gross and histologic evaluations. Results. The lung wedge resection was successfully performed in all animals. There was no significant difference in the mean operating times or complications between the transumbilical and the conventional thoracoscopic approach groups. With regard to the physiologic impact of the surgeries, the transumbilical approach was associated with significant elevations in body temperature on postoperative day 1, when compared with the standard thoracoscopic approach. Conclusions. This study suggests that both approaches for performing lung wedge resection were comparable in efficacy and postoperative complications. Keywords NOTES, SILS, single-site surgery, evidence-based medicine/surgery
Introduction Three-port video-assisted transthoracic endoscopic surgery is a safe and effective procedure used in the diagnosis or treatment of pulmonary, pleural, or mediastinal disease. However, chronic chest discomfort after transthoracic surgery is relatively common and occurs in approximately 30% of patients.1-3 Transumbilical single-port laparoscopy has been used to perform various types of surgeries, including appendectomy, cholecystectomy, colectomy, hysterectomy, and nephrectomy. The benefit of transumbilical single-port laparoscopy, compared to 3-port laparoscopic surgery, is less postoperative pain, faster recovery time, and better cosmetic results.4-6 However, limited data have been reported regarding the utility of transumbilical singleport endoscopic approach to the thoracic cavity.
We have previously reported the feasibility of transumbilical pericardial window creation, surgical lung biopsy in dogs.7 In this study, we aimed to compare the safety and efficacy of transumbilical lung wedge resection in comparison to conventional thoracoscopic surgery in a canine model. The main purpose of the study was to collect important information in the development of 1
Department of Surgery, Chang Gung Memorial Hospital at Keelung, Chang Gung University, Taiwan, ROC 2 Chang Gung Memorial Hospital at Linko, Chang Gung University, Taiwan, ROC Corresponding Author: Yun-Hen Liu, Department of Surgery, Chang Gung Memorial Hospital, Chang Gung University, 5, Fushing Street, Gueishan Shiang, Taoyuan 333, Taiwan, ROC. Email:[email protected]
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Figure 1. (A) The umbilical incision for lung wedge resection. (B) Good cosmetic results of umbilical wound at 14 days after surgery.
single-port transumbilical surgery for the diagnosis and treatment of thoracic diseases in humans. 3.
Method The study was approved by the Ethics Committee on Animal Research of the Chang Gung Memorial Hospital (Taiwan, ROC). Sixteen dogs (weight = 6.1-9.0 kg) were used to evaluate the efficacy and safety of transumbilical lung wedge resection (n = 8) and transthoracic lung wedge resection (n = 8). General anesthesia was intramuscularly (i.m.) induced with ketamine (5 mg/kg) and xylazine HCl (10 mg/kg, i.m.). After the onset of anesthesia, the animals were placed in the supine position and were intubated with an endotracheal tube. To facilitate surgical access, the lung on the operated side was collapsed by placing the endotracheal cuff in the main bronchus opposite to the surgical lung. General anesthesia was maintained with isoflurane (2% to 5%) inhalation by one-lung ventilation. The regions of lung resection were predetermined before performing the surgery, as follows: right upper lobe (2 animals in the transumbilical group and 2 animals in the transthoracic group); left upper lobe (2 animals in the transumbilical group and 2 animals in the transthoracic group); right middle lobe (2 animals in the transumbilical group and 2 animals in the transthoracic group); right lower lobe (1 animal in the transumbilical group and 1 animal in the transthoracic group); and left lower lobe (1 animal in the transumbilical group and 1 animal in the transthoracic group). Single-dose intravenous cefazolin (20 mg/kg; Standard Chem & Pharm, Tainan, Taiwan) was administered before surgery to prevent postoperative infection. The transumbilical lung resection consisted of the following steps (Figures 1-3): 1. A short longitudinal incision (2-3 cm) was created on the umbilicus. 2. A self-retaining wound protector (Alexis Wound Retractor, Applied Medical, Rancho Santa
4.
5.
6.
7. 8.
Margarita, CA) was used to maintain an open incision for the lung resection. A diaphragmatic incision (1 cm below the junction of the diaphragm and the subxyphoid process) was created with a needle knife (Olympus Optical Co, Ltd, Tokyo, Japan) via the working channel of a flexible bronchoscope, which was inserted through the umbilical incision. The diaphragmatic incision was sequentially dilated to 25 mm by using a homemade metal tube. The incision served as the entrance to the thoracic cavity. A flexible bronchoscope was introduced into the thoracic cavity through the diaphragmatic incision for selecting the predetermined wedge resection lung lobe. An endostapler was inserted through the diaphragmatic incision via the umbilical wound to perform lung wedge resection with the aid of an endoscopic forceps (node grasping clamps, Scanlan, St Paul, MN). The resected lung margin was evaluated for the complication of air leaks. The diaphragmatic incision was closed with a V-Loc suturing device (Covidien, Mansfield, MA). The umbilical incision was closed with a 3-0 nylon suture.
For the conventional transthoracic approach, the lung resection was performed via a 2 to 3 cm thoracic incision over the seventh intercostal space at the midclavicular line. The predetermined lung lobe was resected with an endostapler and with the aid of endoscopic forceps, as previously described. The animals were extubated immediately after surgery. The animals resumed a normal diet 8 hours after surgery. Oral acetaminophen (30 mg/kg daily) was administered during the first 3 days after surgery to reduce postoperative
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Figure 2. (A) Diaphragmatic wound created with a needle knife. (B) The diaphragmatic wound was sequentially dilated with metallic tube. (C) The thoracic cavity was exposed after entering the thoracic cavity. (D) Lung resection using an endostapler via the diaphragmatic wound. (E) The resected lung margin. (F) Lung specimen.
Figure 3. (A) Diaphragmatic wound after transumbilical lung resection. (B) Complete diaphragmatic wound closure with V-Loc suturing device. (C, D) Complete diaphragmatic wound (superior surface and lower surface) healing at 14 days after surgery.
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Chen et al Table 1. Characteristics of the Experimental Animals. Thoracic Surgery Characteristics Dogs, n Body weight (kg), mean (95% CI) Surgical time (minutes), mean (95% CI) Successful procedure Postoperative complications, n Mortality, n Infection Pain Autopsy after 14 days, n Infection Organ injury Hemorrhage Correct lung surgery Surgical wound healed well Local adhesion Weight gain after 14 days (kg), mean (95% CI)
Total
Transumbilical
Transthoracic
P
16 7.519 (7.047-7.991) 56.31 (45.43-67.19) 16 2 2 0 1 14 0 0 0 14 14 13 0.1500 (−0.1842 to 0.4842) (n = 14)
8 7.188 (6.430-7.945) 60.75 (46.47-75.03) 8 1 1 (on surgical day) 0 0 7 0 0 0 7 7 7 −0.0286 (−0.3896 to 0.3325) (n = 7)
8 7.850 (7.198-8.502) 51.88 (32.15-71.60) 8 1 1 (5th day) 0 1 7 0 0 0 7 7 6 0.3286 (−0.3248 to 0.9819) (n = 7)
.1541 .2463 1.0 1.0 1.0 1.0 .4413
Abbreviation: CI, confidence interval.
discomfort. The animals were closely monitored daily for clinical signs of postoperative discomfort, infection, and complications. Rectal body temperature and the respiratory rate were measured preoperatively and daily until 14 days after surgery. Blood was drawn for the measurement of the white blood cell (WBC) count (normal = 4.0-15.5 × 103 cells/L) before the lung wedge resection and on days 1 to 3, 7, and 14 postprocedure. Arterial blood was also collected from a femoral artery presurgery, postsurgery, and 14 days after the surgery for the analysis of pH, pCO2, and pO2. At 2 weeks after the surgery, the animals were anesthetized with ketamine and xylazine hydrochloric acid. The animals were then euthanized by a lethal dose of xylocaine (200 mg). A necropsy was performed via midline sternotomy and laparotomy incision. The success of the lung wedge resection, evidence of injury to vital organs, postoperative infection, presence of intraperitoneal or intrathoracic adhesions, and healing of diaphragmatic incision were evaluated. The diaphragmatic incision region was also examined by pathologists for microscopic findings.
Statistical Analysis Data are presented as the mean with 95% conference interval (CI), unless otherwise stated. Because the data did not approximate a Gaussian distribution (ie, the mean value did not approximate the median value), nonparametric statistical analyses were used. For univariate analyses, the Wilcoxon signed-rank test was performed to assess the significance of the differences between the
measurements at different time intervals, and the Mann– Whitney U test was performed to assess the significance of the differences in the values between the transumbilical and transthoracic thoracoscopic groups. Differences in categorical data were analyzed by using the χ2 or Fisher’s exact tests. For all tests, P < .05 was considered to be significant. All analyses were performed by using SPSS software version 10.0 (SPSS Inc, Chicago, IL) and GraphPad Prism 5.0 software (GraphPad Software, San Diego, CA).
Results The lung resections were successfully performed in all 16 animals. The mean procedure times for the transthoracic lung resection and the transumbilical lung resection were 60.75 minutes (95% CI = 46.47-75.03) and 51.88 minutes (95% CI = 32.15-71.60), respectively (P = .2463). The average size of lung specimens was 7.28 cm (95% CI = 5.36-9.21) for the transumbilical group and 6.92 cm (95% CI = 5.96-7.88) for the thoracic group. There was no difference between groups (P = .8280). There was 1 postoperative complication and mortality in each group. Furthermore, all other 14 animals survived for 2 weeks. No clinical signs of postoperative infection were noted during 2 weeks postprocedure. The mean weight gain at 2 weeks after surgery in the transthoracic and the transoral group was −0.0286 kg (95% CI = −0.3896 to 0.3325) and 0.3286 kg (95% CI = −0.3248 to 0.9819), respectively (P = .4413; Table 1).
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Figure 4. Changes in the (A) body temperature, (B) the respiratory rate, and (C) the white blood cell count of the experimental animals (n = 15).
Data are expressed as the mean and the 95% confidence interval (CI). *P < .05, compared to the previous time point. #P < .05, compared to the preoperative level, based on the Wilcoxon signed-ranked test.
After the lung resection, we observed no significant change from the preoperative values in the animals’ postoperative body temperatures. The respiratory rate significantly increased above the preoperative levels 1 day after surgery, and returned to normal 14 days after surgery (Figure 4A and B). The WBC counts significantly increased above the preoperative levels 1 day after surgery. They returned to the preoperative level by 7 days after surgery (Figure 4C). Figure 5 shows the preoperative and postoperative comparison between the transumbilical and the transthoracic groups. On day 1, the body temperature was significantly higher in the transumbilical group (39.40°C; 95% CI = 39.17-39.63) than in the transthoracic group (39.02°C; 95% CI = 38.71-39.33, P = .041, Figure 5A). However, there was no significant intergroup difference in the respiratory rate and the WBC counts at any time point (Figure 5B and C). The pH levels significantly decreased immediately after the lung resection. They returned to the preoperative levels by 14 days after surgery (Figure 6A). The PaO2 and PaCO2 levels immediately after surgery were significantly higher than their preoperative levels; they returned to the
preoperative levels by 14 days after surgery (Figure 6B and C). Figure 6 shows the preoperative and postoperative comparison between the groups. We observed a trend toward better preservation of pulmonary function (ie, higher postoperative PaO2 and lower PaCO2 levels) in the immediate postoperative period after the transumbilical approach, compared to the transthoracic approach. However, there was no significant difference in the values of pH, PaO2, and PaCO2 between the groups at any time point (Figure 6D-F). Based on reduced food intake or decreased activity as a manifestation of postoperative pain, the transumbilical group tended to have reduced postoperative pain (1 animal with mild postoperative pain in the transthoracic group vs no animal with postoperative discomfort in the transumbilical group; Table 1). Two animals died during the procedure. In the transthoracic group, 1 animal had the complication of massive bleeding that required intravenous fluid resuscitation. This complication resulted from a penetrating injury of the lung parenchyma when introducing the stapler through the thoracic wound. This animal had intermittent breathing difficulty, lethargy, and poor oral intake in the
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Figure 5. The changes in (A) the body temperature, (B) respiratory rate, and (C) white blood cell (WBC) count in the transumbilical endoscopic group (N = 7) and in the conventional thoracoscopic group (N = 8).
The data are expressed as the mean and the 95% confidence interval (CI). *P < .05, between groups, based on the Mann–Whitney U test.
postoperative period and died 5 days after the operation because of respiratory failure and sepsis. Another animal in the transumbilical group died because of inadvertent extubation of the endotracheal tube after successful lung resection surgery. This animal died 30 minutes after cardiopulmonary resuscitation. Fourteen dogs that completed the 2-week study received a postmortem examination. The autopsy revealed a successful lung resection in all animals. There was no evidence of thoracic infection, injury to the thoracic organ, or hemorrhage. The diaphragmatic incision and the surgical wounds over the chest and umbilicus were completely healed. None of the animals had visceral herniation. During autopsy, 13 of 14 animals revealed adhesions in the abdominal cavity or the thoracic cavity (n = 7 in the transumbilical group and n = 6 in the transthoracic group; P = 1.0). See Table 1 and Figure 7). Histopathologic evaluation of the diaphragmatic wound was performed in 7 of the animals that survived 2 weeks after transumbilical lung resection. All specimens revealed a normal healing process without evidence of infection or abscess formation. Microscopic examination of the specimens revealed fibrosis and
inflammation in all 7 animals. Liver adhesion was found in 1 animal (Figure 8).
Discussion The feasibility of performing thoracic surgery through a transabdominal approach has been demonstrated in several case series. Our previous studies reported that a single transumbilical incision allows adequate inspection of the thoracic cavity and surgical lung biopsy in all lobes of the left and right lungs.7,8 However, comparative studies of the Golden approach (ie, the transthoracic approach) have been lacking. This experimental study was used to compare the outcomes of a novel transumbilical lung resection with the outcomes of the conventional transthoracic lung resection. In this animal model, both approaches were similar with regard to completeness of thoracoscopy with lung resection. The incidence of major intraoperative complications was similar with both approaches. A major concern of approaching the thoracic cavity by using a transdiaphragmatic incision is visceral herniation and compromised lung function. Our research group has previously reported liver herniation through the
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Figure 6. Changes in the arterial blood gases in (A) the pH, (B) the PaO2 level, and (C) the PaCO2 level in the 15 animals, and a comparison of (D) the pH, (E) the PaO2 level, and (F) the PaCO2 level in the transumbilical endoscopic group (n = 7) and in the conventional thoracoscopic group (n = 8). The data are expressed as the mean and the 95%confidence interval (CI). *P < .05, compared with previous time point, #P < .05, compared with preoperative level, based on the Wilcoxon signed-ranked test; there is no significance between the groups, based on the Mann–Whitney U test.
diaphragmatic incision into the right hemithorax that is not surgically repaired after transdiaphragmatic lung resection.9 To reduce the risk of visceral herniation in the present study, we repaired the diaphragmatic wound by endoscopic suturing. This technique obviated the visceral herniation complication in all animals that underwent transdiaphragmatic thoracoscopy. In postoperative lung function, the transumbilical group showed a trend of higher postoperative PaO2 and lower PaCO2 levels than the transthoracic group. Based on these results, our study suggests that, in the immediate postoperative period, transumbilical lung resection may be associated with less impairment of pulmonary function, compared to the conventional transthoracic thoracoscopy. Another concern in thoracic surgery is postoperative pain after the procedure. Chen et al compared the outcome of transumbilical diaphragmatic thoracic sympathectomy with conventional VATS (video-assisted thoracoscopic surgery) thoracic sympathectomy in 66 patients with palmar hyperhidrosis. They suggest that transumbilical surgery is safe and associated with less
postoperative pain, compared to the transthoracic surgery.10,11 In the current study, the transumbilical approach group and the conventional thoracoscopic group had similar respiratory patterns, and weight gain at 2 weeks after surgery. Based on the fact that the skin of the umbilical area is less innervated than the rest of the abdomen and chest wall, and based on the preliminary finding of this study, we reasonably suggest that transumbilical lung resection exposes the animals to a similar level or a decreased level of postoperative pain as the conventional thoracoscopic approach.12,13 In addition, avoiding the creation of thoracic incisions when using the transumbilical approach prevents chronic thoracotomy discomfort. The transumbilical approach may have the following technical challenges. First, the surgical field is restricted because of using 2 incisions (ie, an umbilical incision and a diaphragmatic incision) through which the instruments must pass before reaching the target. Second, crowding of the instruments and diminished triangulation through a single transumbilical incision can result in a greater workload, compared to using the conventional transthoracic
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Figure 7. (A) Autopsy showing mild mesenteric adhesion over the umbilical incision region. (B) Autopsy showing mild liver adhesion over the diaphragmatic incision region. (C) Autopsy showing pleural cavity without infection. (D) Autopsy showing good healing of resected margin.
Figure 8. Histologic examination showed complete healing with fibrosis over the diaphragmatic wound.
The blue arrows indicated the edges of the diaphragmatic incision. M, diaphragm; F, fibrosis healing margin.
approach. Third, although we could perform the wedge lung resection in all lobes of the lung via transumbilical approach by using current endoscopic instruments in a canine model, we believe that lung resection via transumbilical incision in a tall human may require a longer endoscopic instrument. Fourth, management of the complication of bleeding during the lung resection is more challenging when using the transumbilical approach because of the
restricted working space via umbilical and diaphragmatic incisions. The transthoracic approach via a 3-port incision may simplify the operation and bleeding control. Thus, the skin of the chest and abdomen should be prepped and draped with the patient in the supine position for transumbilical thoracic surgery. Major complications following lung surgery include injury to vital organs, massive bleeding, pulmonary infections, and postoperative respiratory failure. In the present study, we observed 2 (12.5%) major complications (one from each group) that directly caused operative mortality. The 2 mortality complications consisted of 1 case of postoperative respiratory failure and 1 case of massive bleeding. The incidence of major complications was higher than the rates in our previous research reports. We believe that optimal management of the delayed recovery from anesthesia and extubation of endotracheal tubes after full recovery of neuromuscular function may have prevented postoperative respiratory failure and avoided surgical mortality in our animal study. With regard to intraoperative bleeding, the distance from the chest wall to the hilum of the canine model is short and increases the difficulty of lung resection with current endostapling devices. However, the complications can be reduced or even prevented in humans. The potential advantages of the transumbilical thoracoscopy include the following: (a) the pulmonary performance in the immediate postoperative period may be better preserved after the transumbilical technique because the creation of a thoracic incision is avoided;
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(b) the pain in the early postoperative period after transumbilical technique may be less intense than with the transthoracic approach because a thoracic incision and chest drainage are avoided; (c) the technique avoids the creation of a chest wall incision and intercostal nerve damage, which can help eliminate problems of chronic intercostal neuralgia and postthoracotomy chest pain; and (d) the technique results in a better cosmetic outcome since the surgery is completed via an umbilical incision that is almost completely hidden inside the umbilicus. This study has several limitations. First, the study was performed on a small number of animals (8 animals in each group); studies with a larger number of subjects are necessary before the transumbilical approach can be used in clinical practice. Second, there are many differences between the dog and human anatomy; long endoscopic instruments and staplers are required to perform the transumbilical thoracoscopic procedure in the upper thoracic region of humans. Third, the present transdiaphragmatic thoracoscopy technique requires surgical repair of the diaphragmatic wound; we believe that the procedure could be simplified by repairing the diaphragmatic wound with Bioglue. Fourth, pulmonary resection in the current animal model may not be applicable for anatomic lung resection, as used in lung cancer surgery (the pulmonary vein, pulmonary artery, and the bronchus of the targeted lung lobe were independently stapled by using the endostapler). However, the results of this study present very good evidence of the feasibility of using stapled lung resection via transumbilical incision. Further research determining the efficacy of endostapler anatomical lobectomy with complete mediastinal lymph node dissection by the transumbilical approach and the transthoracic approach are needed. This information may facilitate the development of minimally invasive transumbilical surgery in thoracic disease. In conclusion, our study indicates that the transumbilical approach for lung wedge resection is comparable to video-assisted transthoracic lung resection. Further experimental studies in the cadaveric model are warranted for evaluating the transumbilical access of the thoracic cavity before translating this procedure to human application. Author Contributions Conceived and designed the experiments: YC CYL YCW YHL Performed the experiments: YC TPC YCW MJH HCY PJK YHL Analyzed the data: CYL MJHCJY Contributed reagents/materials/analysis tools: CYL MJH Wrote the paper: TPC CYL YHL Supervision and coordination of project: YC YHL
Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by the Chang-Gung Memorial Hospital, Taiwan (Contract No. CMRPG 391913).
References 1. Sihoe AD, Au SS, Cheung ML, et al. Incidence of chest wall paresthesia after video-assisted thoracic surgery for primary spontaneous pneumothorax. Eur J Cardiothorac Surg. 2004;25:1054-1058. 2. Stammberger U, Steinacher C, Hillinger S, Schmid RA, Kinsbergen T, Weder W. Early and long-term complaints following video-assisted thoracoscopic surgery: evaluation in 173 patients. Eur J Cardiothorac Surg. 2000;18:7-11. 3. Passlick B, Born C, Sienel W, Thetter O. Incidence of chronic pain after minimal-invasive surgery for spontaneous pneumothorax. Eur J Cardiothorac Surg. 2001;19:355-358. 4. Champagne BJ, Papaconstantinou HT, Parmar SS, et al. Single-incision versus standard multiport laparoscopic colectomy: a multicenter, case-controlled comparison. Ann Surg. 2012;255:66-69. 5. Bucher P, Pugin F, Buchs NC, Ostermann S, Morel P. Randomized clinical trial of laparoendoscopic single-site versus conventional laparoscopic cholecystectomy. Br J Surg. 2011;98:1695-1702. 6. Asakuma M, Hayashi M, Komeda K, et al. Impact of single-port cholecystectomy on postoperative pain. Br J Surg. 2011;98:991-995. 7. Wu YC, Chu Y, Yeh CJ, et al. Feasibility of transumbilical surgical lung biopsy and pericardial window creation. Surg Innov. 2014;21:15-21. 8. Wen CT, Chu Y, Yeh CJ, et al. Feasibility and safety of endoscopic transumbilical thoracic surgical lung biopsy: a survival study in a canine model. J Surg Res. 2013;183:47-55. 9. Lin TY, Chu Y, Wu YC, et al. Feasibility of transumbilical lung wedge resection in a canine model. J Laparoendosc Adv Surg Tech A. 2013;23:684-692. 10. Zhu LH, Wang W, Yang S, et al. Transumbilical thoracic sympathectomy with an ultrathin flexible endoscope in a series of 38 patients. Surg Endosc. 2013;27:2149-2155. 11. Chen W, Zhu LH, Yang S, Li D, Wang W, Chen L. Embryonic-NOTES thoracic sympathectomy for palmar hyperhidrosis: results of a novel technique and comparison with the conventional VATS procedure. Paper presented at: SAGES 2013 annual meeting. http://www.sages.org/wpcontent/uploads/2013/07/2013-SAGES-Final-Program. pdf?aabf5d. Accessed September 17, 2014. 12. Chouillard E, Dache A, Torcivia A, Helmy N, Ruseykin I, Gumbs A. Single-incision laparoscopic appendectomy for acute appendicitis: a preliminary experience. Surg Endosc. 2010;24:1861-1865. 13. Rozen WM, Tran TM, Ashton MW, Barrington MJ, Ivanusic JJ, Taylor GI. Refining the course of the thoracolumbar nerves: a new understanding of the innervation of the anterior abdominal wall. Clin Anat. 2008;21: 325-333.
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research-article2014
SRIXXX10.1177/1553350614552733Surgical InnovationChen et al
Procedural Innovations
Transumbilical Thoracoscopy Versus Conventional Thoracoscopy for Lung Wedge Resection: Safety and Efficacy in a Live Canine Model
Surgical Innovation 2015, Vol. 22(6) 568–576 © The Author(s) 2014 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/1553350614552733 sri.sagepub.com
Tzu-Ping Chen, MD1, Yen-Chu, PhD2, Yi-Cheng Wu, MD2, Chi-Ju Yeh, MD2, Chien-Ying Liu, MD2, Ming-Ju Hsieh, MD2, Hsu-Chia Yuan, MD2, Po-Jen Ko, MD2, and Yun-Hen Liu, MD2
Abstract Purpose. Transumbilical single-port surgery has been associated with less postoperative pain and offers better cosmetic outcomes than conventional 3-port laparoscopic surgery. This study compares the safety and efficacy of transumbilical thoracoscopy and conventional thoracoscopy for lung wedge resection. Methods. The animals (n = 16) were randomly assigned to the transumbilical thoracoscopic approach group (n = 8) or conventional thoracoscopic approach group (n = 8). Transumbilical lung resection was performed via an umbilical incision and a diaphragmatic incision. In the conventional thoracoscopic group, lung resection was completed through a thoracic incision. For both procedures, we compared the surgical outcomes, for example, operating time and operative complications; physiologic parameters, for example, respiratory rate and body temperature; inflammatory parameters, for example, white blood cell count; and pulmonary parameters, for example, arterial blood gas levels. The animals were euthanized 2 weeks after the surgery for gross and histologic evaluations. Results. The lung wedge resection was successfully performed in all animals. There was no significant difference in the mean operating times or complications between the transumbilical and the conventional thoracoscopic approach groups. With regard to the physiologic impact of the surgeries, the transumbilical approach was associated with significant elevations in body temperature on postoperative day 1, when compared with the standard thoracoscopic approach. Conclusions. This study suggests that both approaches for performing lung wedge resection were comparable in efficacy and postoperative complications. Keywords NOTES, SILS, single-site surgery, evidence-based medicine/surgery
Introduction Three-port video-assisted transthoracic endoscopic surgery is a safe and effective procedure used in the diagnosis or treatment of pulmonary, pleural, or mediastinal disease. However, chronic chest discomfort after transthoracic surgery is relatively common and occurs in approximately 30% of patients.1-3 Transumbilical single-port laparoscopy has been used to perform various types of surgeries, including appendectomy, cholecystectomy, colectomy, hysterectomy, and nephrectomy. The benefit of transumbilical single-port laparoscopy, compared to 3-port laparoscopic surgery, is less postoperative pain, faster recovery time, and better cosmetic results.4-6 However, limited data have been reported regarding the utility of transumbilical singleport endoscopic approach to the thoracic cavity.
We have previously reported the feasibility of transumbilical pericardial window creation, surgical lung biopsy in dogs.7 In this study, we aimed to compare the safety and efficacy of transumbilical lung wedge resection in comparison to conventional thoracoscopic surgery in a canine model. The main purpose of the study was to collect important information in the development of 1
Department of Surgery, Chang Gung Memorial Hospital at Keelung, Chang Gung University, Taiwan, ROC 2 Chang Gung Memorial Hospital at Linko, Chang Gung University, Taiwan, ROC Corresponding Author: Yun-Hen Liu, Department of Surgery, Chang Gung Memorial Hospital, Chang Gung University, 5, Fushing Street, Gueishan Shiang, Taoyuan 333, Taiwan, ROC. Email:[email protected]
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Figure 1. (A) The umbilical incision for lung wedge resection. (B) Good cosmetic results of umbilical wound at 14 days after surgery.
single-port transumbilical surgery for the diagnosis and treatment of thoracic diseases in humans. 3.
Method The study was approved by the Ethics Committee on Animal Research of the Chang Gung Memorial Hospital (Taiwan, ROC). Sixteen dogs (weight = 6.1-9.0 kg) were used to evaluate the efficacy and safety of transumbilical lung wedge resection (n = 8) and transthoracic lung wedge resection (n = 8). General anesthesia was intramuscularly (i.m.) induced with ketamine (5 mg/kg) and xylazine HCl (10 mg/kg, i.m.). After the onset of anesthesia, the animals were placed in the supine position and were intubated with an endotracheal tube. To facilitate surgical access, the lung on the operated side was collapsed by placing the endotracheal cuff in the main bronchus opposite to the surgical lung. General anesthesia was maintained with isoflurane (2% to 5%) inhalation by one-lung ventilation. The regions of lung resection were predetermined before performing the surgery, as follows: right upper lobe (2 animals in the transumbilical group and 2 animals in the transthoracic group); left upper lobe (2 animals in the transumbilical group and 2 animals in the transthoracic group); right middle lobe (2 animals in the transumbilical group and 2 animals in the transthoracic group); right lower lobe (1 animal in the transumbilical group and 1 animal in the transthoracic group); and left lower lobe (1 animal in the transumbilical group and 1 animal in the transthoracic group). Single-dose intravenous cefazolin (20 mg/kg; Standard Chem & Pharm, Tainan, Taiwan) was administered before surgery to prevent postoperative infection. The transumbilical lung resection consisted of the following steps (Figures 1-3): 1. A short longitudinal incision (2-3 cm) was created on the umbilicus. 2. A self-retaining wound protector (Alexis Wound Retractor, Applied Medical, Rancho Santa
4.
5.
6.
7. 8.
Margarita, CA) was used to maintain an open incision for the lung resection. A diaphragmatic incision (1 cm below the junction of the diaphragm and the subxyphoid process) was created with a needle knife (Olympus Optical Co, Ltd, Tokyo, Japan) via the working channel of a flexible bronchoscope, which was inserted through the umbilical incision. The diaphragmatic incision was sequentially dilated to 25 mm by using a homemade metal tube. The incision served as the entrance to the thoracic cavity. A flexible bronchoscope was introduced into the thoracic cavity through the diaphragmatic incision for selecting the predetermined wedge resection lung lobe. An endostapler was inserted through the diaphragmatic incision via the umbilical wound to perform lung wedge resection with the aid of an endoscopic forceps (node grasping clamps, Scanlan, St Paul, MN). The resected lung margin was evaluated for the complication of air leaks. The diaphragmatic incision was closed with a V-Loc suturing device (Covidien, Mansfield, MA). The umbilical incision was closed with a 3-0 nylon suture.
For the conventional transthoracic approach, the lung resection was performed via a 2 to 3 cm thoracic incision over the seventh intercostal space at the midclavicular line. The predetermined lung lobe was resected with an endostapler and with the aid of endoscopic forceps, as previously described. The animals were extubated immediately after surgery. The animals resumed a normal diet 8 hours after surgery. Oral acetaminophen (30 mg/kg daily) was administered during the first 3 days after surgery to reduce postoperative
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Figure 2. (A) Diaphragmatic wound created with a needle knife. (B) The diaphragmatic wound was sequentially dilated with metallic tube. (C) The thoracic cavity was exposed after entering the thoracic cavity. (D) Lung resection using an endostapler via the diaphragmatic wound. (E) The resected lung margin. (F) Lung specimen.
Figure 3. (A) Diaphragmatic wound after transumbilical lung resection. (B) Complete diaphragmatic wound closure with V-Loc suturing device. (C, D) Complete diaphragmatic wound (superior surface and lower surface) healing at 14 days after surgery.
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Total
Transumbilical
Transthoracic
P
16 7.519 (7.047-7.991) 56.31 (45.43-67.19) 16 2 2 0 1 14 0 0 0 14 14 13 0.1500 (−0.1842 to 0.4842) (n = 14)
8 7.188 (6.430-7.945) 60.75 (46.47-75.03) 8 1 1 (on surgical day) 0 0 7 0 0 0 7 7 7 −0.0286 (−0.3896 to 0.3325) (n = 7)
8 7.850 (7.198-8.502) 51.88 (32.15-71.60) 8 1 1 (5th day) 0 1 7 0 0 0 7 7 6 0.3286 (−0.3248 to 0.9819) (n = 7)
.1541 .2463 1.0 1.0 1.0 1.0 .4413
Abbreviation: CI, confidence interval.
discomfort. The animals were closely monitored daily for clinical signs of postoperative discomfort, infection, and complications. Rectal body temperature and the respiratory rate were measured preoperatively and daily until 14 days after surgery. Blood was drawn for the measurement of the white blood cell (WBC) count (normal = 4.0-15.5 × 103 cells/L) before the lung wedge resection and on days 1 to 3, 7, and 14 postprocedure. Arterial blood was also collected from a femoral artery presurgery, postsurgery, and 14 days after the surgery for the analysis of pH, pCO2, and pO2. At 2 weeks after the surgery, the animals were anesthetized with ketamine and xylazine hydrochloric acid. The animals were then euthanized by a lethal dose of xylocaine (200 mg). A necropsy was performed via midline sternotomy and laparotomy incision. The success of the lung wedge resection, evidence of injury to vital organs, postoperative infection, presence of intraperitoneal or intrathoracic adhesions, and healing of diaphragmatic incision were evaluated. The diaphragmatic incision region was also examined by pathologists for microscopic findings.
Statistical Analysis Data are presented as the mean with 95% conference interval (CI), unless otherwise stated. Because the data did not approximate a Gaussian distribution (ie, the mean value did not approximate the median value), nonparametric statistical analyses were used. For univariate analyses, the Wilcoxon signed-rank test was performed to assess the significance of the differences between the
measurements at different time intervals, and the Mann– Whitney U test was performed to assess the significance of the differences in the values between the transumbilical and transthoracic thoracoscopic groups. Differences in categorical data were analyzed by using the χ2 or Fisher’s exact tests. For all tests, P < .05 was considered to be significant. All analyses were performed by using SPSS software version 10.0 (SPSS Inc, Chicago, IL) and GraphPad Prism 5.0 software (GraphPad Software, San Diego, CA).
Results The lung resections were successfully performed in all 16 animals. The mean procedure times for the transthoracic lung resection and the transumbilical lung resection were 60.75 minutes (95% CI = 46.47-75.03) and 51.88 minutes (95% CI = 32.15-71.60), respectively (P = .2463). The average size of lung specimens was 7.28 cm (95% CI = 5.36-9.21) for the transumbilical group and 6.92 cm (95% CI = 5.96-7.88) for the thoracic group. There was no difference between groups (P = .8280). There was 1 postoperative complication and mortality in each group. Furthermore, all other 14 animals survived for 2 weeks. No clinical signs of postoperative infection were noted during 2 weeks postprocedure. The mean weight gain at 2 weeks after surgery in the transthoracic and the transoral group was −0.0286 kg (95% CI = −0.3896 to 0.3325) and 0.3286 kg (95% CI = −0.3248 to 0.9819), respectively (P = .4413; Table 1).
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Figure 4. Changes in the (A) body temperature, (B) the respiratory rate, and (C) the white blood cell count of the experimental animals (n = 15).
Data are expressed as the mean and the 95% confidence interval (CI). *P < .05, compared to the previous time point. #P < .05, compared to the preoperative level, based on the Wilcoxon signed-ranked test.
After the lung resection, we observed no significant change from the preoperative values in the animals’ postoperative body temperatures. The respiratory rate significantly increased above the preoperative levels 1 day after surgery, and returned to normal 14 days after surgery (Figure 4A and B). The WBC counts significantly increased above the preoperative levels 1 day after surgery. They returned to the preoperative level by 7 days after surgery (Figure 4C). Figure 5 shows the preoperative and postoperative comparison between the transumbilical and the transthoracic groups. On day 1, the body temperature was significantly higher in the transumbilical group (39.40°C; 95% CI = 39.17-39.63) than in the transthoracic group (39.02°C; 95% CI = 38.71-39.33, P = .041, Figure 5A). However, there was no significant intergroup difference in the respiratory rate and the WBC counts at any time point (Figure 5B and C). The pH levels significantly decreased immediately after the lung resection. They returned to the preoperative levels by 14 days after surgery (Figure 6A). The PaO2 and PaCO2 levels immediately after surgery were significantly higher than their preoperative levels; they returned to the
preoperative levels by 14 days after surgery (Figure 6B and C). Figure 6 shows the preoperative and postoperative comparison between the groups. We observed a trend toward better preservation of pulmonary function (ie, higher postoperative PaO2 and lower PaCO2 levels) in the immediate postoperative period after the transumbilical approach, compared to the transthoracic approach. However, there was no significant difference in the values of pH, PaO2, and PaCO2 between the groups at any time point (Figure 6D-F). Based on reduced food intake or decreased activity as a manifestation of postoperative pain, the transumbilical group tended to have reduced postoperative pain (1 animal with mild postoperative pain in the transthoracic group vs no animal with postoperative discomfort in the transumbilical group; Table 1). Two animals died during the procedure. In the transthoracic group, 1 animal had the complication of massive bleeding that required intravenous fluid resuscitation. This complication resulted from a penetrating injury of the lung parenchyma when introducing the stapler through the thoracic wound. This animal had intermittent breathing difficulty, lethargy, and poor oral intake in the
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Figure 5. The changes in (A) the body temperature, (B) respiratory rate, and (C) white blood cell (WBC) count in the transumbilical endoscopic group (N = 7) and in the conventional thoracoscopic group (N = 8).
The data are expressed as the mean and the 95% confidence interval (CI). *P < .05, between groups, based on the Mann–Whitney U test.
postoperative period and died 5 days after the operation because of respiratory failure and sepsis. Another animal in the transumbilical group died because of inadvertent extubation of the endotracheal tube after successful lung resection surgery. This animal died 30 minutes after cardiopulmonary resuscitation. Fourteen dogs that completed the 2-week study received a postmortem examination. The autopsy revealed a successful lung resection in all animals. There was no evidence of thoracic infection, injury to the thoracic organ, or hemorrhage. The diaphragmatic incision and the surgical wounds over the chest and umbilicus were completely healed. None of the animals had visceral herniation. During autopsy, 13 of 14 animals revealed adhesions in the abdominal cavity or the thoracic cavity (n = 7 in the transumbilical group and n = 6 in the transthoracic group; P = 1.0). See Table 1 and Figure 7). Histopathologic evaluation of the diaphragmatic wound was performed in 7 of the animals that survived 2 weeks after transumbilical lung resection. All specimens revealed a normal healing process without evidence of infection or abscess formation. Microscopic examination of the specimens revealed fibrosis and
inflammation in all 7 animals. Liver adhesion was found in 1 animal (Figure 8).
Discussion The feasibility of performing thoracic surgery through a transabdominal approach has been demonstrated in several case series. Our previous studies reported that a single transumbilical incision allows adequate inspection of the thoracic cavity and surgical lung biopsy in all lobes of the left and right lungs.7,8 However, comparative studies of the Golden approach (ie, the transthoracic approach) have been lacking. This experimental study was used to compare the outcomes of a novel transumbilical lung resection with the outcomes of the conventional transthoracic lung resection. In this animal model, both approaches were similar with regard to completeness of thoracoscopy with lung resection. The incidence of major intraoperative complications was similar with both approaches. A major concern of approaching the thoracic cavity by using a transdiaphragmatic incision is visceral herniation and compromised lung function. Our research group has previously reported liver herniation through the
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Figure 6. Changes in the arterial blood gases in (A) the pH, (B) the PaO2 level, and (C) the PaCO2 level in the 15 animals, and a comparison of (D) the pH, (E) the PaO2 level, and (F) the PaCO2 level in the transumbilical endoscopic group (n = 7) and in the conventional thoracoscopic group (n = 8). The data are expressed as the mean and the 95%confidence interval (CI). *P < .05, compared with previous time point, #P < .05, compared with preoperative level, based on the Wilcoxon signed-ranked test; there is no significance between the groups, based on the Mann–Whitney U test.
diaphragmatic incision into the right hemithorax that is not surgically repaired after transdiaphragmatic lung resection.9 To reduce the risk of visceral herniation in the present study, we repaired the diaphragmatic wound by endoscopic suturing. This technique obviated the visceral herniation complication in all animals that underwent transdiaphragmatic thoracoscopy. In postoperative lung function, the transumbilical group showed a trend of higher postoperative PaO2 and lower PaCO2 levels than the transthoracic group. Based on these results, our study suggests that, in the immediate postoperative period, transumbilical lung resection may be associated with less impairment of pulmonary function, compared to the conventional transthoracic thoracoscopy. Another concern in thoracic surgery is postoperative pain after the procedure. Chen et al compared the outcome of transumbilical diaphragmatic thoracic sympathectomy with conventional VATS (video-assisted thoracoscopic surgery) thoracic sympathectomy in 66 patients with palmar hyperhidrosis. They suggest that transumbilical surgery is safe and associated with less
postoperative pain, compared to the transthoracic surgery.10,11 In the current study, the transumbilical approach group and the conventional thoracoscopic group had similar respiratory patterns, and weight gain at 2 weeks after surgery. Based on the fact that the skin of the umbilical area is less innervated than the rest of the abdomen and chest wall, and based on the preliminary finding of this study, we reasonably suggest that transumbilical lung resection exposes the animals to a similar level or a decreased level of postoperative pain as the conventional thoracoscopic approach.12,13 In addition, avoiding the creation of thoracic incisions when using the transumbilical approach prevents chronic thoracotomy discomfort. The transumbilical approach may have the following technical challenges. First, the surgical field is restricted because of using 2 incisions (ie, an umbilical incision and a diaphragmatic incision) through which the instruments must pass before reaching the target. Second, crowding of the instruments and diminished triangulation through a single transumbilical incision can result in a greater workload, compared to using the conventional transthoracic
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Figure 7. (A) Autopsy showing mild mesenteric adhesion over the umbilical incision region. (B) Autopsy showing mild liver adhesion over the diaphragmatic incision region. (C) Autopsy showing pleural cavity without infection. (D) Autopsy showing good healing of resected margin.
Figure 8. Histologic examination showed complete healing with fibrosis over the diaphragmatic wound.
The blue arrows indicated the edges of the diaphragmatic incision. M, diaphragm; F, fibrosis healing margin.
approach. Third, although we could perform the wedge lung resection in all lobes of the lung via transumbilical approach by using current endoscopic instruments in a canine model, we believe that lung resection via transumbilical incision in a tall human may require a longer endoscopic instrument. Fourth, management of the complication of bleeding during the lung resection is more challenging when using the transumbilical approach because of the
restricted working space via umbilical and diaphragmatic incisions. The transthoracic approach via a 3-port incision may simplify the operation and bleeding control. Thus, the skin of the chest and abdomen should be prepped and draped with the patient in the supine position for transumbilical thoracic surgery. Major complications following lung surgery include injury to vital organs, massive bleeding, pulmonary infections, and postoperative respiratory failure. In the present study, we observed 2 (12.5%) major complications (one from each group) that directly caused operative mortality. The 2 mortality complications consisted of 1 case of postoperative respiratory failure and 1 case of massive bleeding. The incidence of major complications was higher than the rates in our previous research reports. We believe that optimal management of the delayed recovery from anesthesia and extubation of endotracheal tubes after full recovery of neuromuscular function may have prevented postoperative respiratory failure and avoided surgical mortality in our animal study. With regard to intraoperative bleeding, the distance from the chest wall to the hilum of the canine model is short and increases the difficulty of lung resection with current endostapling devices. However, the complications can be reduced or even prevented in humans. The potential advantages of the transumbilical thoracoscopy include the following: (a) the pulmonary performance in the immediate postoperative period may be better preserved after the transumbilical technique because the creation of a thoracic incision is avoided;
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(b) the pain in the early postoperative period after transumbilical technique may be less intense than with the transthoracic approach because a thoracic incision and chest drainage are avoided; (c) the technique avoids the creation of a chest wall incision and intercostal nerve damage, which can help eliminate problems of chronic intercostal neuralgia and postthoracotomy chest pain; and (d) the technique results in a better cosmetic outcome since the surgery is completed via an umbilical incision that is almost completely hidden inside the umbilicus. This study has several limitations. First, the study was performed on a small number of animals (8 animals in each group); studies with a larger number of subjects are necessary before the transumbilical approach can be used in clinical practice. Second, there are many differences between the dog and human anatomy; long endoscopic instruments and staplers are required to perform the transumbilical thoracoscopic procedure in the upper thoracic region of humans. Third, the present transdiaphragmatic thoracoscopy technique requires surgical repair of the diaphragmatic wound; we believe that the procedure could be simplified by repairing the diaphragmatic wound with Bioglue. Fourth, pulmonary resection in the current animal model may not be applicable for anatomic lung resection, as used in lung cancer surgery (the pulmonary vein, pulmonary artery, and the bronchus of the targeted lung lobe were independently stapled by using the endostapler). However, the results of this study present very good evidence of the feasibility of using stapled lung resection via transumbilical incision. Further research determining the efficacy of endostapler anatomical lobectomy with complete mediastinal lymph node dissection by the transumbilical approach and the transthoracic approach are needed. This information may facilitate the development of minimally invasive transumbilical surgery in thoracic disease. In conclusion, our study indicates that the transumbilical approach for lung wedge resection is comparable to video-assisted transthoracic lung resection. Further experimental studies in the cadaveric model are warranted for evaluating the transumbilical access of the thoracic cavity before translating this procedure to human application. Author Contributions Conceived and designed the experiments: YC CYL YCW YHL Performed the experiments: YC TPC YCW MJH HCY PJK YHL Analyzed the data: CYL MJHCJY Contributed reagents/materials/analysis tools: CYL MJH Wrote the paper: TPC CYL YHL Supervision and coordination of project: YC YHL
Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by the Chang-Gung Memorial Hospital, Taiwan (Contract No. CMRPG 391913).
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