Energy Sources for Laparoscopic Colorectal Surgery: Is One Better than the Others?

Abstract

Background:

Wide acceptance of the laparoscopic approach in both benign and malignant colorectal diseases has led to the development of several multifunctional tools aiming to overcome the limitations of conventional electrosurgery (ES). The aim of this study was to compare ES, ultrasonic coagulating shears (US), electrothermal bipolar vessel sealers (EBVS), and a relatively new energy device that combines both ultrasonic and bipolar energy (Thunderbeat, TB) in terms of safety, efficacy, and cost-effectiveness in patients undergoing laparoscopic colorectal resection (LCR).

Materials and Methods:

A review of the literature was performed in Medline and the Cochrane Library. Only randomized controlled trials (RCTs) and cohort studies were considered for inclusion.

Results:

Four RCTs, one retrospective, and two prospective cohort studies were eligible for inclusion. Bleeding control was better with US compared with ES and operative time was shorter with both US and EBVS compared with ES. These advantages were more evident in challenging colorectal resections, such as low anterior resections. US and EBVS seemed to be more cost-effective compared with ES, although supporting data are limited. US and EBVS appeared to be equivalent with regard to different outcome parameters. Preliminary data on the efficacy and safety of TB are promising.

Conclusion:

Although US and EBVS have the advantages of less blood loss and/or a shorter operative time compared with ES, the current evidence does not demonstrate which multifunctional instrument is the most effective in LCR. High-quality RCTs are required to confirm the preliminary promising results with the use of TB in LCR.

Introduction

Laparoscopic colorectal resection (LCR), both for benign and malignant diseases, has gained wide acceptance since the first report of laparoscopic-assisted colectomy in 1991.¹ This is mainly induced by the more favorable short-term outcomes of the laparoscopic approach compared with open colorectal surgery,^2–5 Additionally, results from large randomized controlled trials (RCTs) have demonstrated that the long-term oncologic outcome after LCR for colorectal cancer is not inferior to open surgery.^6–11

LCR is a technically demanding procedure and mesenteric tissue dissection and vessel ligation might be challenging, particularly in obese patients and in the presence of inflammation, such as in diverticulitis or inflammatory bowel diseases.¹² Conventional mono- and bipolar electrosurgery (ES) is widely used for dissection and vessel control in LCR. However, it has some limitations, including smoke production and the risk of collateral thermal injuries. Furthermore, it might be time-consuming. The rapid increase in popularity of LCR has led to the development of technologies and surgical tools aiming to overcome these shortcomings of ES. Therefore, ultrasonic coagulating shears (US), electrothermal bipolar vessel sealers (EBVS), and, more recently, an energy device that combines both ultrasonic and bipolar energy (Thunderbeat, TB—Olympus Medical Systems Corp., Tokyo, Japan) have become available. However, these devices are nonreusable and are considerably more expensive compared with ES. Therefore, it is essential to prove the advantages compared with ES, justifying their introduction in LCR.

The aim of this study was to review the clinical outcomes of the different energy sources used in LCR.

Materials and Methods

Literature search

A search strategy was performed in Medline by using the Pubmed search engine and the Cochrane Library. The following medical subject headings (MeSHs) and free-text words alone or in combination were used: “laparoscopy,” “minimally invasive,” “colorectal,” “colectomy,” “dissection,” “conventional electrosurgery,” “electrothermal bipolar vessel sealer,” “ultrasonic shears,” “vessel ligation,” “Ligasure,” “Ultracision,” “harmonic scalpel,” and “Thunderbeat.” The publication period was restricted from January 1999 until January 2016 as the more advanced coagulation devices were not available on the market before this period.

Study selection

Two authors (M.E.A. and E.J.B.F.) independently performed the literature search and subsequently the selection of studies. Studies assessing the outcome of ES, US, EBVS, or TB in a group of patients undergoing LCR were eligible for inclusion in this review. Only RCTs and pro- or retrospective cohort studies were accepted as study design in this review. Animal and non-English studies, as well as case reports, were excluded. Reference lists from the included articles were manually checked and additional studies were included when appropriate. The following outcome parameters were extracted from each study included in this review: year of publication, study design, number of patients included, operative time, blood loss, conversion to open surgery, conversion to other laparoscopic instruments, postoperative morbidity and mortality, hospital stay, and costs.

Dissecting tools

US, EBVS, and TB are all multifunctional instruments that can be used as grasper, dissector, cutter, or coagulator during LCR. The principle of US tools is based on the transformation of electrical energy into high-frequency (55,000 kHz) frictional energy. The denaturation of hydrogen bonds in tissue and blood vessel proteins by the vibrating blades results in a coagulum that seals the lumen of vessels up to 5 mm in diameter.¹³ EBVS instrument applies high current (4 A) and low voltage (<200 V). This energy results in denaturation of collagen and elastin within the blood vessel wall that can seal vessels with a diameter up to 7 mm.^14,15

TB integrates both ultrasonic and advanced bipolar energy in a unique instrument: it allows to cut tissue with ultrasonic energy on the one hand and reliably seal vessels up to 7 mm in diameter with bipolar energy on the other.

Results

The search strategy yielded a total of 1694 studies after duplication of studies from the two electronic databases. After study selection, a total of seven studies were eligible for inclusion in this review: two RCTs,^16,17 comparing ES, US, and EBVS; one RCT,¹⁸ comparing ES and US; one RCT¹⁹ and one prospective²⁰ and one retrospective cohort study,²¹ comparing US and EBVS; and one prospective cohort study,²² reporting the outcome in LCR by using TB. These studies were heterogeneous in terms of the surgical procedures performed and all except two RCTs^18,19 were small and underpowered trials.

Conventional ES versus US

In three RCTs, ES and US were compared (Table 1). Targarona et al.¹⁶ randomized 38 patients with a benign or malignant disease in the left colon, sigmoid, and rectum: 11 in the ES group, 12 in the US group, and 15 patients in the EBVS group. Operative time was significantly longer in patients who underwent laparoscopic colectomy with ES than US. Additionally, there was significantly more intraoperative blood loss in the ES group. Conversion to another laparoscopic instrument was only necessary in ES patients. There were no intraoperative complications related to the use of ES or US; conversion rate, postoperative morbidity, hospital stay, and total costs were not significantly different between both groups.

Table 1.

Conventional Electrosurgery Versus Ultrasonic Coagulating Shears: Outcome of Randomized Controlled Trials

Reference	Number of patients	Operative time (minutes)	Blood loss (mL)	Conversion to open surgery (%)	Conversion to other instruments (%)	Postoperative morbidity (%)	Hospital stay (days)	Costs (€)
Targarona et al.¹⁶	11 ES	180 (90–210)	200 (0–350)	1 (9.1)	3 (27.3)	4 (36.4)	7 (6–32)	2995 (2023–5534)
	12 US	120 (65–220)^a	100 (0–150)^a	0 (0)	0 (0)^b	2 (16.7)	8 (4–18)	2928 (2273–3534)
Hubner et al.¹⁷	20 ES	144.8 ± 43.4	138.5 ± 115.1	0 (0)	6 (30)	10 (50)	9.7 ± 5.8	1476 ± 399.1
	20 US	98.5 ± 33.6^c	92.5 ± 129.3^c	0 (0)	5 (25)	6 (30)	8.1 ± 5.1	1213 ± 259.1^a
Morino et al.¹⁸	72 ES	102.6 ± 27.3	182.6 ± 66.5	8 (11.1)	15 (20.8)	5 (6.9)	8.9 ± 1.4	NR
	74 US	93.0 ± 29.7	140.8 ± 60.6^a	9 (12.2)	0 (0)^a	5 (6.7)	8.5 ± 1.2	NR

Data are shown as mean ± standard deviation or as median (range).

P < .05.

P = .09.

P < .001.

ES, electrosurgery; NR, data not reported; US, ultrasonic coagulating shear.

Hubner et al.¹⁷ randomized 61 patients undergoing laparoscopic rectosigmoid or low anterior resection: 20 to ES, 20 to US, and 21 to EBVS. They found a significantly longer operative time and more blood loss in the ES group compared with the US group. Additionally, significantly more clips were needed during LCR with ES than US (median 9 versus 3, P < .001). No patients in both groups were converted to open surgery. Overall, postoperative morbidity and hospital stay were not significantly different between both groups. Cost analysis (operating room, energy device, additional instruments) revealed that dissection by using ES was more expensive than US assuming a center volume of 200 cases per year.

The third RCT conducted by our group¹⁸ compared ES and US in patients who underwent laparoscopic right hemicolectomy, left hemicolectomy/sigmoidectomy, or low anterior resection. There was no significant difference in overall mean operative time between ES and US. However, subgroup analysis revealed that low anterior resection took longer if ES was used. Blood loss was significantly higher in the ES group compared with the US group. Intraoperative complication rates were comparable in both groups (1.3% versus 4%, P = .62), as was the conversion rate to open surgery. Conversion to another energy source device was only needed in ES cases, most frequently during right hemicolectomy or low anterior resection. No differences were observed in 30-day postoperative morbidity and hospital stay.

Conventional ES versus EBVS

Both RCTs performed by Targarona et al. and Hubner et al. also included a group of patients who underwent LCR by using EBVS. The outcome parameters of this group of patients compared with the ES group are shown in Table 2.

Table 2.

Conventional Electrosurgery Versus Electrothermal Bipolar Vessel Sealers: Outcome Randomized Controlled Trials

Reference	Number of patients	Operative time (minutes)	Blood loss (mL)	Conversion to open surgery (%)	Conversion to other instruments (%)	Postoperative morbidity (%)	Hospital stay (days)	Costs (€)
Targarona et al.¹⁶	11 ES	180 (90–120)	200 (0–350)	1 (9.1)	3 (27.3)	4 (36.4)	7 (6–32)	2995 (2023–5534)
	15 EBVS	110 (70–210)^a	100 (0–450)	1 (6.7)	1 (6.7)	2 (13.3)	6 (6–16)	2664 (2320–3635)
Hubner et al.¹⁷	20 ES	144.8 ± 43.4	138.5 ± 115.1	0 (0)	6 (30)	10 (50)	9.7 ± 5.8	1476 ± 399.1
	21 EBVS	104.7 ± 31.8^b	108.6 ± 139.1	0 (0)	3 (14.3)	10 (47.6)	9.2 ± 6.7	1209 ± 265.8^b

Data are shown as mean ± standard deviation or as median (range).

P < .05.

P < .001.

ES, electrosurgery; EBVS, electrothermal bipolar vessel sealer.

In the study by Targarona et al.,¹⁶ operative time was significantly longer in patients who underwent laparoscopic colectomy with ES. Additionally, there was more intraoperative blood loss in the ES group, although this difference did not reach statistical significance. A slightly higher rate of conversion to other laparoscopic instruments occurred in the EBVS group. No intraoperative complications related to the use of ES or EBVS were recorded. Conversion rate, postoperative morbidity, hospital stay, and costs were comparable between ES and EBVS.

Hubner et al.¹⁷ found no significant difference in blood loss between both groups, while operative time was significantly shorter in the EBVS group. An additional instrument was more frequently used in ES patients, although the difference did not reach statistical significance. The EBVS procedures were significantly cheaper compared with the ES procedures.

US versus EBVS

Additional to the RCTs by Targarona et al.¹⁶ and Hubner et al.,¹⁷ another RCT compared US with EBVS.¹⁹ The outcomes of these three RCTs are shown in Table 3. Furthermore, one prospective study²⁰ and one retrospective cohort study²¹ were conducted comparing US or EBVS in patients undergoing LCR.

Table 3.

Ultrasonic Coagulating Shears Versus Electrothermal Bipolar Vessel Sealers: Outcome of Randomized Controlled Trials

Reference	Number of patients	Operative time (minutes)	Blood loss (mL)	Conversion to open surgery (%)	Conversion to other instruments (%)	Postoperative morbidity (%)	Hospital stay (days)	Costs (€)
Targarona et al.¹⁶	12 US	120 (65–220)	100 (0–150)	0 (0)	0 (0)	2 (16.7)	8 (4–18)	2928 (2273–3534)
	15 EBVS	110 (70–210)	100 (0–450)	1 (6.7)	1 (6.7)	2 (13.3)	6 (6–16)	2664 (2320–3635)
Hubner et al.¹⁷	20 US	98.5 ± 33.6	92.5 ± 129.3	0 (0)	5 (25)	6 (30)	8.1 ± 5.1	1213 ± 259.1
	21 EBVS	104.7 ± 31.8	108.6 ± 139.1	0 (0)	3 (14.3)	10 (47.6)	9.2 ± 6.7	1209 ± 265.8
Rimonda et al.¹⁹	70 US	114.8 ± 47.6	107.9 ± 42.0	6 (8.6)	1 (1.4)	8 (11.4)	7.4 ± 2.2	NR
	70 EBVS	116.3 ± 44.0	111.2 ± 51.5	5 (7.1)	0 (0)	7 (10.0)	6.9 ± 3.3	NR

Data are shown as mean ± standard deviation or as median (range).

US, ultrasonic coagulating shear; EBVS, electrothermal bipolar vessel sealer; NR, data not reported.

In the study by Targarona et al.,¹⁶ operative time, intraoperative blood loss, conversion to open surgery, and conversion to another laparoscopic instrument were comparable between both groups. There were no differences in postoperative morbidity, hospital stay, and costs.

Hubner et al.¹⁷ found no significant differences in blood loss and operative time between US and EBVS. The use of another laparoscopic instrument was necessary in more US procedures, and the postoperative morbidity rate was higher in EBVS patients; however, these differences were not significantly different.

Rimonda et al.¹⁹ included a total of 140 patients. They found no significant differences in operative time and intraoperative blood loss between both groups. Intraoperative complications related to the electronic device occurred in one US patient (1.4%) and in three of the EBVS patients (4.2%) (P = .62). In 1 patient of the US group (1.4%), the surgeon switched to ES due to failure of the dissecting tool. Conversion rate, postoperative complication rate, and hospital stay were not significantly different between both groups.

Takada et al.²⁰ conducted a prospective study comparing 30 patients undergoing laparoscopic transverse colectomy or sigmoidectomy for cancer with US (n = 15) or EBVS (n = 15). They found a higher number of rebleeds and a longer time for mesocolon dissection in the US patients. There were no postoperative complications and hospital stay was not significantly different between both groups.

Campagnacci et al.²¹ retrospectively reported the outcomes of 200 patients who underwent laparoscopic right or left colectomy or low anterior resection with US (100 patients) or EBVS (100 patients). Intraoperative bowel injuries caused by US occurred in 2 patients (2%). Mean operative time was similar in both groups, while intraoperative blood loss was significantly lower in the EBVS group (115 mL versus 370 mL for right colectomies, 150 mL versus 455 mL for left colectomies, and 185 mL versus 495 mL for low anterior resections). Conversion to open surgery was only required in 1 patient in the US group. No difference was observed in hospital stay between both groups.

Thunderbeat

To date, there are no studies comparing TB to other energy sources for dissection and vessel ligation during LCR. We have recently reviewed our initial experience with 25 consecutive patients who underwent LCR with TB between September 2015 and December 2015. The baseline characteristics and types of colorectal resections are summarized in Table 4. There were no intraoperative complications related to the use of TB and estimated blood loss was negligible in all cases. No malfunction of the tool was recorded.

Table 4.

Thunderbeat: Our Experience and Literature Data

	Our series	Milsom et al.²²
Number of patients	25	30
Sex, n (%)
Male	17 (68)	15 (50)
Female	8 (32)	15 (50)
Age, years (range)	69.5 (66–72)	68.5 (21–86)
Indications, n (%)
Cancer	22 (88)	30 (100)
Diverticolitis	3 (12)	—
Surgical procedure, n (%)
Left hemicolectomy	5 (20)	18 (60)
Right hemicolectomy	12 (48)	12 (30)
Anterior resection	8 (32)
Operative time, minutes (mean ± SD)	115 ± 22	163 ± 86
Intraoperative complications, n (%)	0 (0)	0 (0)
Postoperative morbidity, N (%)	1 (4)	1 (3.6)
Postoperative mortality, n (%)	0 (0)	0 (0)
Length of hospital stay, days (range)	6 (4–9)	4 (3–10)

Data are shown as mean ± SD or as median (range).

SD, standard deviation.

Milsom et al.²² reported in 2015 the results of a single institution prospective pilot study, including 30 patients undergoing laparoscopic right or left hemicolectomy for cancer by using the TB (Table 4). Mean time ± standard deviation for dissection with TB to remove the specimen was 80.6 ± 35 minutes. Ligation of the major vessels was successful in all cases and no intraoperative bleeding occurred. The median number of TB applications to seal the inferior mesenteric artery was 3 (range 2–8), and 2 (range 1–4) seals were required for the ileocolic vessels. No organ injuries or other complications related to TB were observed. The median number of times the TB device was taken out from the abdomen during the operation to clean up the tip was 2 (range 1–4). Malfunction of the TB occurred in 2 patients (6.7%).

Discussion

The current evidence shows that the time needed for mesenteric dissection and vessel ligation during LCR is lower with US and EBVS compared with ES. Additionally, the use of US results in less blood loss compared with ES, while a significant difference in blood loss between EBVS and ES could not be demonstrated. However, the conversion rate, postoperative morbidity, and hospital stay are not influenced by the type of coagulation device used.

The shorter operative time by using US or EBVS in LCR might be explained by several factors, such as reduced instrumental traffic through the ports, reduced need for additional instruments for vessel control, less intraoperative blood loss avoiding repeatedly introducing a suction device, and limited production of smoke. These advantages are even more important in difficult procedures such as low anterior resections for rectal cancer or colon resection for diverticulitis. In addition, pooling of the data with regard to conversion to other instruments in a previous meta-analysis demonstrated that this was significantly more frequent and necessary in ES compared with US or EBVS patients.²³ Therefore, the use of US or EBVS enables the operating surgeon to complete the operation with one device in most cases, thus avoiding the sequelae of changing instruments, saving time, and reducing the risk of conversion to open surgery. However, the intraoperative benefits of US and EBVS are not reflected into advantages with regard to earlier resumption of gastrointestinal functions, reduced postoperative morbidity, and shorter hospital stay.

Even though two small, heterogeneous nonrandomized studies^20,21 showed some advantages with the use of EBVS over US, an RCT¹⁹ that was powered to detect a 20% difference in blood loss between US and EBVS showed no significant differences. The authors of this RCT concluded that both tools are safe and that the choice between both of them should only depend on the surgeon's preference.

With regard to cost-effectiveness, there was no difference in costs between ES and US as well as between ES and EBVS in one RCT,¹⁶ while the other RCT¹⁷ showed that ES was significantly more expensive compared with both US and EBVS. Even though the EBVS and US devices are more expensive, they might be at least as cost-effective as ES since the material-related costs might be counterbalanced by a shorter operative time and a limited need for using additional instruments, mainly including clips.

Very few data on the subjective evaluation of the different energy devices by the operating surgeons are available. Hubner et al.¹⁷ evaluated the following features of the instruments used: dissection capacity, cutting ability, bleeding control, handling, safety, and overall satisfaction. They found similar high overall satisfaction with EBVS, US, and ES by the operating surgeons. The scores regarding bleeding control and safety items were significantly higher for EBVS and US compared with ES. Handling was considered the main limitation to the use of US.

Since US and EBVS have different features in terms of dissection and hemostatic power, a tool combining both characteristics should be ideal. TB is a novel dissecting tool that combines both ultrasonic and bipolar energy. Some experimental studies on porcine models have shown that TB leads to faster dissection of the mesentery than EBVS. For instance, Milsom et al.²⁴ conducted an experimental study on 10 female Yorkshire pigs aiming to assess the versatility, bursting pressure, thermal spread, and dissection time of TB compared with other commercially available devices, including Harmonic^®ACE (HA) (Ethicon Endo-Surgery), LigaSure™ V (LIG) (Covidien), and EnSeal^® (Ethicon). In this study, 2-cm-long samples of small (2–3 mm), medium (4–5 mm), and large (6–7 mm) diameter vessels were created. Versatility, defined as the performance of the surgical instrument based on hemostasis, histologic sealing, cutting, dissection, and tissue manipulation, was higher and dissection time was shorter with TB compared with the other three tools. No differences were observed in bursting pressure and thermal spread among the four instruments. Similarly, Seehofer et al.²⁵ found in eight German Landrace pigs a significantly higher cut speed of TB compared with HA and LIG. The tools were similar in the rate of seal failures. The safety and efficacy of TB demonstrated in these experimental studies seem to be confirmed in humans by the results of a recently published case series of 30 patients²² and the results of our initial experience. Furthermore, large high-quality RCTs are needed to assess the real benefits of this technology in patients undergoing LCR.

Conclusions

The current evidence shows that US and EBVS significantly reduce the operative time and achieve a better bleeding control than ES in patients undergoing LCR. Large RCTs are required to confirm the promising preliminary results about safety and efficacy of TB.

Footnotes

Disclosure Statement

No competing financial interests exist.

References

Jacobs

, Verdeja

, Goldstein

. Minimally invasive colon resection (laparoscopic colectomy). Surg Laparosc Endosc, 1991; 1:144–150.

Lacy

, García-Valdecasas

, Delgado

, Castells

, Taurá

, Piqué

, Visa

. Laparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: A randomised trial. Lancet, 2002; 359:2224–2229.

Clinical Outcomes of Surgical Therapy Study Group. A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med, 2004; 350:2050–2059.

Guillou

, Quirke

, Thorpe

, Walker

, Jayne

, Smith

, Heath

, Brown

. MRC CLASICC trial group. Short-term endpoints of conventional versus laparoscopic-assisted surgery in patients with colorectal cancer (MRC CLASICC trial): Multicentre, randomised controlled trial. Lancet, 2005; 365:1718–1726.

Veldkamp

, Kuhry

, Hop

, Jeekel

, Kazemier

, Bonjer

, Haglind

, Påhlman

, Cuesta

, Msika

, Morino

, Lacy

. COlon cancer Laparoscopic or Open Resection Study Group (COLOR) Laparoscopic surgery versus open surgery for colon cancer: Short-term outcomes of a randomised trial. Lancet Oncol, 2005; 6:477–484.

Fleshman

, Sargent

, Green

, Anvari

, Stryker

, Beart

Jr. , Hellinger

, Flanagan

Jr. , Peters

, Nelson

. Clinical Outcomes of Surgical Therapy Study Group. Laparoscopic colectomy for cancer is not inferior to open surgery based on 5-year data from the COST Study Group trial. Ann Surg, 2007; 246:655–662; discussion 662–664.

Buunen

, Veldkamp

, Hop

, Kuhry

, Jeekel

, Haglind

, Påhlman

, Cuesta

, Msika

, Morino

, Lacy

, Bonjer

. Survival after laparoscopic surgery versus open surgery for colon cancer: Long-term outcome of a randomized clinical trial. Lancet Oncol, 2009; 10:44–52.

Jayne

, Thorpe

, Copeland

, Quirke

, Brown

, Guillou

. Five-year follow-up of the Medical Research Council CLASICC trial of laparoscopically assisted versus open surgery for colorectal cancer. Br J Surg, 2010; 97:1638–1645.

Lacy

, Delgado

, Castells

, Prins

, Arroyo

, Ibarzabal

, Pique

. The long-term results of a randomized clinical trial of laparoscopy-assisted versus open surgery for colon cancer. Ann Surg, 2008; 248:1–7.

10.

Green

, Marshall

, Collinson

, Quirke

, Guillou

, Jayne

, Brown

. Long-term follow-up of the Medical Research Council CLASICC trial of conventional versus laparoscopically assisted resection in colorectal cancer. Br J Surg, 2013; 100:75–82.

11.

Kuhry

, Schwenk

, Gaupset

, Romild

, Bonjer

. Longterm outcome of laparoscopic surgery for colorectal cancer: A cochrane systematic review of randomised controlled trials. Cancer Treat Rev, 2008; 34:498–504.

12.

Sardinha

, Wexner

. Laparoscopy for inflammatory bowel disease: Pros and cons. World J Surg, 1998; 22:370–374.

13.

Person

, Vivas

, Ruiz

, Talcott

, Coad

, Wexner

. Comparison of four energy-based vascular sealing and cutting instruments: A porcine model. Surg Endosc, 2008; 22:534–538.

14.

Harold

, Pollinger

, Matthews

, Kercher

, Sing

, Heniford

. Comparison of ultrasonic energy, bipolar thermal energy, and vascular clips for the hemostasis of small-, medium-, and large-sized arteries. Surg Endosc, 2003; 17:1228–1230.

15.

Campbell

, Cresswell

, Frank

, Cuschieri

. Real time thermography during energized vessel sealing and dissection. Surg Endosc, 2003; 17:1640–1645.

16.

Targarona

, Balague

, Marin

, Neto

, Martinez

, Garriga

, Trias

. Energy sources for laparoscopic colectomy: A prospective randomized comparison of conventional electrosurgery, bipolar computer-controlled electrosurgery, and ultrasonic dissection: Operative outcomes and costs analysis. Surg Innov, 2005; 12:339–344.

17.

Hubner

, Demartines

, Muller

, Dindo

, Clavien

, Hahnloser

. Prospective randomized study of monopolar scissors, bipolar vessel sealer and ultrasonic shears in laparoscopic colorectal surgery. Br J Surg, 2008; 95:1098–1104.

18.

Morino

, Rimonda

, Allaix

, Giraudo

, Garrone

. Ultrasonic versus standard dissection in laparoscopic colorectal surgery: A prospective randomized clinical trial. Ann Surg, 2005; 242:897–901.

19.

Rimonda

, Arezzo

, Garrone

, Allaix

, Giraudo

, Morino

. Electrothermal bipolar vessel sealing system vs harmonic scalpel in colorectal laparoscopic surgery: A prospective, randomized study. Dis Colon Rectum, 2009; 52:657–661.

20.

Takada

, Ichihara

, Kuroda

. Comparative study of electrothermal bipolar vessel sealer and ultrasonic coagulating shears in laparoscopic colectomy. Surg Endosc, 2005; 19:226–228.

21.

Campagnacci

, de Sanctis

, Balderelli

, Rimini

, Lezoche

, Guerrieri

. Electrothermal bipolar vessel sealing device vs ultrasonic coagulating shears in laparoscopic colectomies: A comparative study. Surg Endosc, 2007; 21:1526–1531.

22.

Milsom

, Trencheva

, Sonoda

, Nandakumar

, Shukla

, Lee

. A prospective trial evaluating the clinical performance of a novel surgical energy device in laparoscopic colon surgery. Surg Endosc, 2015; 29:1161–1166.

23.

Tou

, Malik

, Wexner

, Nelson

. Energy source instruments for laparoscopic colectomy. Cochrane Database Syst Rev, 2011; CD007886.

24.

Milsom

, Trencheva

, Monette

, Pavoor

, Shukla

, Ma

, Sonoda

. Evaluation of the safety, efficacy, and versatility of a new surgical energy device (THUNDERBEAT) in comparison with Harmonic ACE, LigaSure V, and EnSeal devices in a porcine model. J Laparoendosc Adv Surg Tech A, 2012; 22:378–386.

25.

Seehofer

, Mogl

, Boas-Knoop

, Unger

, Schirmeier

, Chopra

, Eurich

. Safety and efficacy of new integrated bipolar and ultrasonic scissors compared to conventional laparoscopic 5-mm sealing and cutting instruments. Surg Endosc, 2012; 26:2541–2549.