LIVER RESECTION IN BRAZIL: A NATIONAL SURVEY

ABSTRACT Background: Liver surgery has developed significantly in the past decades. In Brazil, the interest on it has grown significantly, but there is no study regarding its clinical practice. Despite intrinsic limitations, surveys are well suited to descriptive studies and allow understanding the current scenario. Aim: To provide an overview on the current spread of liver surgery in Brazil, focusing on groups´ profile, operative techniques and availability of resources. Method: From May to November 2016, was conducted a national survey about liver surgery profile in Brazil composed by 28 questions concerning surgical team characteristics, technical preferences, surgical volume, results and available institutional resources. The survey was sent by e-mail to 84 liver surgery team leaders from different centers including all regions of the country. Results: Forty-three study participants (51.2%), from all Brazilian regions, responded the survey. Most centers have residency/fellowship programs (86%), perform and do laparoscopic procedures (91%); however, laparoscopy is still responsible for a little amount of surgeries (1-9% of laparoscopic procedures over all liver resections in 39.5% of groups). Only seven centers (16.3%) perform more than 50 liver resections/year. Postoperative mortality rate is between 1-3% in 55% of the centers. Conclusion: This is the first depiction of liver surgery in Brazil. It showed a surgical practice aligned with worldwide excellence centers, concentrated on hospitals dedicated to academic practice.


INTRODUCTION
L iver surgery has developed significantly in the past decades. Comprehension about liver anatomy, development of parenchyma transection techniques, incorporation of new technologies and instruments made liver surgery a complex and effective specialty 5 , requiring structure available in tertiary centers 4 . In the last years, minimally invasive techniques were incorporated to liver surgery, adding a new set of complex operations to be learned and performed by liver surgeons 8 .
In Brazil, the interest in liver surgery has been growing in recent years leading to an increase in performance of hepatic resections throughout the country, although there are challenges to provide access for all patients requiring this kind of procedure 2,3,12 . Knowledge of the profile of liver surgery in a continental developing country can provide valuable information to guide actions toward improvement in training and acquisition of resources.
Despite intrinsic limitations, surveys provide a "snapshot of how things are at a specific time" 22 , well suited to descriptive studies, allowing to understand current scenario and to search for trends in specific subjects.
Since there is no study about the clinical practice of liver surgery in Brazil, it was conducted a survey including the most relevant groups in hepatic surgery.
The aim of this study was to provide an overview on the current spread of liver surgery in Brazil, focusing on groups´ profile, operative techniques including minimally invasive procedures and availability of resources.

METHODS
It was conducted a national survey about liver surgery profile in Brazil, using Redcap electronic data capture tools 8 , from May to November 2016. The survey was sent by e-mail, with a cover letter calling for participation and a hyperlink to the survey, to members of the Brazilian Chapter of the International Hepato-Pancreato-Biliary Association (CB-IHPBA) including all regions of the country. The study was designed to understand the institutional profile, so only one expert surgeon from each center was invited to take part of the study.
The survey was composed by 28 questions concerning surgical team characteristics, technical preferences, surgical volume, results and available institutional resources. This questionnaire was designed to be brief, enabling completion in less than 10 min. A total of four reminders were weekly sent to non-responders. No incentives were offered to the participants that completed the questionnaire.
Laparoscopic resection included totally laparoscopic, handassisted and videoassisted procedures. Major hepatectomies were defined as resection of three or more segments. Highvolume centers were defined as those with more than 50 hepatic resections per year.
All studied variables, except one, were categorical and were presented as frequency (percentage). Continuous variable was presented as the mean±standard deviation and median (range).

RESULTS
The questionnaire was sent to 84 Brazilian liver surgeons from different centers. Of these, 43 study participants (51.2%) responded the survey (42 complete and one incomplete responses). Table 1 summarizes questions and answers in the survey.
The mean number of surgeons who perform liver resections in each team is 3.37 (1-6) and the majority (86%) has residents and/or fellows training in their groups ( Figure  2A). Almost half of the answering groups (48.8%) are also involved in liver transplantation. Seven centers (16.3%) report a surgical volume larger than 50 liver resections per year, and only one team (2.3%) report more than 100 hepatectomies annually ( Figure 2B).
More than 90% of liver surgery groups perform laparoscopic resections ( Figure 2C); however, procedures by laparoscopy are still responsible for a little amount of surgeries (1-9% of laparoscopic procedures in 39.5% of groups). The main indication for liver resection is liver metastases (83.3%). Major hepatectomies are responsible for 20-49% of liver resections in most groups (66.2%) and the preferred incision in these cases is "J" shaped incision (64.2%), followed by bilateral subcostal incision (23.8%) and "Mercedes" incision (12%).  Pringle maneuver is used selectively by most surgeons (88.1%); however, in major hepatectomies, the selective use drops down to 69%, and the routine clamping application increases from 4.7-26.2%. The preferred approach to hepatic pedicle is done by dissection of all hilar structures (40.5%), followed by extrahepatic Glissonian approach in 21.4% of cases, pedicle clamping (Pringle/Hemi-Pringle) plus intrahepatic approach during parenchyma transection (19%) and intrahepatic Glissonian approach (16.7%) 9 .

Note: Number of centers in each city is between brackets
In open surgeries, the chosen method for parenchyma transection is ultrasonic surgical aspirator (33.3%), followed by Kelly clamp crushing technique (23.8%), energy disposable devices (19%) and bipolar cautery (14.3%). For laparoscopic parenchyma transection, the preferred method is the harmonic scalpel (40.5%), followed by disposable devices using advanced bipolar energy (31%).
Most centers have only conventional intraoperative  Most surgeons do not use haemostatic or sealants on the raw surface after hepatectomy (64.3%). For those who use, the preferred is haemostatic patch (19%), followed by fibrin glues (16.7%).
For major hepatectomies, most surgeons routinely employ drainage (90.5%) being the preferred a tubular closed suction drain (78.6%), like Blake ® or Jackson-Pratt ® . The use of intraoperative test for biliary leakage in major resections is done routinely by 31% of surgeons, while 45.2% applied in selected cases and 23.8% never do it.

DISCUSSION
This is the first national survey about liver surgery in a Latin American country, until our best knowledge. It provides a comprehensive insight into the practice of liver surgery in Brazil. We had a reasonable response rate (51.2%) and all country regions were represented, showing that hepatic surgery is diffused around the country. Since liver surgery is a complex procedure, requiring a complex hospital structure, most of the centers are located at state capitals (86%). This can also be a reflex of a regionalization observed recently in other countries, such as United States 13 , with better results in high-volume hospitals. Only 23.3% of groups are exclusively associated to private healthcare, with 76.7% of groups offering state funded public healthcare, showing that hepatic surgery is largely available to the population in most of these cities.
The groups are small, but they are involved with residency or fellowship training programs, which represents an academic involvement in teaching and disseminating knowledge. It is important to emphasize the need of further training after a general surgery program to achieve excellence in HPB surgery; however, in South America, there are only 14 HPB fellowship programs registered in IHPBA 10 mostly in Argentina and Brazil. Teaching hepatobiliary surgery is still a challenge in South American countries.
There is a worldwide trend to concentrate complex liver surgery in high-volume centers, because it is widely accepted that morbidity and mortality for major surgery correlates with the case-load of the hospital and the experience of the team 6,11,13,27 . However the exact number to consider a center as a high-volume institution is controversial, ranging from 10-110 hepatic procedures each year 6,7,11,13,27 . The International Hepato-Pancreato-Biliary Association (IHPBA) recommends at least 25 hepatic operations in the HPB fellowship 19 . Since there is no consensus in this matter, we decided for a cut-off of 50 procedures/year because it represents a mean of one liver resection/week and is close to American cut-offs for quality, which is 45 liver resections per year 7,13 . Pancreaticoduodenectomy, another complex abdominal procedure, has also a cut-off of 50 procedures/ year for high-volume hospitals 14 .
In the last two decades minimally invasive liver surgery has been increasingly accepted. Its initial development was slow, held by 1) technical barriers, since translation of conventional techniques to laparoscopic approach was needed; 2) fear of anticipated intraoperative hazards, such as massive bleeding and the risk of gas embolism secondary to pneumoperitoneum; and 3) doubts on oncological outcomes such as adequate margins, port site seeding and long-term survival 8 . Our findings show that laparoscopic approach is disseminated around the country, being applied by more than 90% of groups, rates comparable to a worldwide survey that found 88% of centers employ laparoscopic approach in liver surgery 26 . However, this approach is responsible for a small portion of liver resections in most of the groups maybe due to the high cost of the equipment for minimally invasive surgery (laparoscopic ultrasound devices are available in only 16.7% of the centers). This is a clear barrier to development of laparoscopic surgery in Brazil.
Laparoscopic approach for liver resection is gaining space worldwide, especially in the treatment of benign tumors as hepatocellular adenoma 8,17 , which is more common in young women, and in the treatment of hepatocellular carcinoma 8,18 , with a likely advantage over conventional open approach. According to Kawaguchi et al. 21 , the relative number of 30% of minimally invasive approach for all liver resections is the average for specialized centers. An effort in training has to be made to achieve this numbers in the near future.
An interesting finding is that 90.5% of groups still use abdominal drains after major hepatectomies, although this contrasts with evidence from the Cochrane systematic review 15 , and the growing tendency toward fast-track and Enhanced Recovery After Surgery (ERAS) programs 31 , which substantially disagreed with the routine use of surgical drains. Despite evidence on this matter, a recent Italian survey in liver surgery also revealed 93% of drainage following hepatic resection 1 .
Intraoperative blood loss is a significant factor affecting the short-as well as long-term outcomes after liver resection and efforts to avoid it should be done 9,25 . The most employed technique to control liver inflow is hepatic pedicle clamping, called Pringle maneuver 28 . In an Italian liver surgery survey, it was performed in 56.4% of centers 1 . Other multi-institutional survey found that most centers applied Pringle's maneuver routinely (50%) or when excessive bleeding occurs (43%) during open hepatectomy 26 . Our study showed a selective use of Pringle maneuver by Brazilian surgeons (88.1%) in overall liver resections, with increased use of routine pedicle clamping in major resections (26.2%).
Hepatic pedicle control is a key point for liver resection. There is a worldwide tendency to dissect the hepatic artery and the portal vein individually, according to data published by Mise et al. 26 (48% for dissection vs. extrahepatic Glissonian approach in 33%); our survey showed a similar pattern (40.5% hilar structures dissection vs. 21.4% extrahepatic Glissonian approach). The advantage of the en-bloc extrafascial pedicle approach is that the liver can be separated into three sections by simply clamping the secondary Glissonian pedicle after an extrahepatic approach without prolonged liver dissection at the hepatic hilum 32 .
Despite introduction of many devices to transect liver parenchyma in the last years, a conservative trend was observed in our study. Clamp-crushing technique and ultrasonic dissectors (CUSA), which were introduced, respectively, in the 1970s 24 and in the 1980s 30 , were the two favorite methods by 23.8% and 33.3% of surgeons, respectively. The Brazilian experience is a reflex of a worldwide inclination, where these two methods are also preferable 26 . Worlds´ preference reinforces the evidence from randomized trials showing absence of superiority regarding new devices over the classical methods 23 .
Our study has some limitations. The first is a moderate response rate (51.2%), hampering access to a more complete view of the national scenario. This rate is below other world liver surgery surveys, which reached 75% of responders 6,20 . It is the nature of any survey that only part of the population is approached and only part of the surveyed surgeons may reply 6 . Other limitation is a potential selection bias, since most of the responders were from Brazil southeast region (48.8%), perhaps reflecting a regional pattern.

CONCLUSION
Despite its limitations, this is the first depiction of liver surgery in Brazil. All authors are continuously involved in academic and societary interaction through CB-IHPBA. Thus, we do know much about regional practices in our country and, importantly, the results left the authors with a pleasant feeling of a faithful portrait. The study covered all regions of the country through its responders and indicates a surgical practice aligned with worldwide excellence centers, concentrated on hospitals dedicated to academic practice. This is probably the best conclusion our paper offers: liver surgery in Brazil has taken the right path.