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 Table of Contents  
ORIGINAL ARTICLE
Year : 2015  |  Volume : 28  |  Issue : 4  |  Page : 818-826

Short-term outcome after laparoscopic versus open liver resection in liver tumors


1 Department of General Surgery, Faculty of Medicine, Menoufia University, Menoufia, Egypt
2 Department of General and Oncological Surgery, Faculty of Medicine, Menoufia University, Menoufia, Egypt
3 Department of General and Laparoscopic Surgery, Faculty of Medicine, Menoufia University, Menoufia, Egypt
4 Department of General and Pediatric Surgery, Faculty of Medicine, Menoufia University, Menoufia, Egypt
5 Department of Oncological and Laparoscopic Surgery, El-Salam Oncology Center, Cairo, Egypt

Date of Submission09-Feb-2015
Date of Acceptance09-Mar-2015
Date of Web Publication12-Jan-2016

Correspondence Address:
Mohammed N Nassar
Department of General Surgery, Faculty of Medicine, Menoufia University, Yassin Abd El-Ghaffar Street of Gamal Abd El-Nasser Street, Shebin El-Kom, Menoufia
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/1110-2098.173598

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  Abstract 

Objective
To compare between laparoscopic and open liver resection for liver tumors.
Background
Laparoscopic surgery has become a standard in many elective procedures, but it is still gaining popularity in liver surgery. The safety of laparoscopic liver resection is still under study.
Materials and methods
This study was prospectively conducted from October 2012 to December 2014 on 30 patients presenting with hepatic tumors (benign and malignant) to the outpatient clinic of both Menoufia University Hospitals and El-Salam Oncology Center. Patients were divided randomly into two groups: group A, which includes 15 patients operated upon by laparoscopic technique; and group B, which includes 15 patients operated upon by open technique.
Results
Operating time was significantly longer in the laparoscopy group: it was 131.54 ± 15.61 versus 118.04 ± 19.41 min. Blood loss was highly significant in laparoscopic resections. Mean hospital stay was highly significant shortly after laparoscopy 6.20 ± 1.10 versus 8.81 ± 1.50 days. Patients who underwent laparoscopic procedure resumed oral intake earlier than the open group. The overall complication rate was significantly lower in the laparoscopic group than the open group.
Conclusion
Laparoscopic liver resection improved surgical and postsurgical outcome for open liver resection regarding less operative blood loss, postoperative pain, postoperative complications, and hospital stay.

Keywords: hepatectomy, laparoscopic liver resection, liver tumors


How to cite this article:
Nassar MN, El-Shakhs SA, Sultan HM, El-Sisy AA, Sultan TA, Hafez AS. Short-term outcome after laparoscopic versus open liver resection in liver tumors. Menoufia Med J 2015;28:818-26

How to cite this URL:
Nassar MN, El-Shakhs SA, Sultan HM, El-Sisy AA, Sultan TA, Hafez AS. Short-term outcome after laparoscopic versus open liver resection in liver tumors. Menoufia Med J [serial online] 2015 [cited 2020 Feb 28];28:818-26. Available from: http://www.mmj.eg.net/text.asp?2015/28/4/818/173598


  Introduction Top


Throughout history, the liver has been viewed as a mysterious organ, clearly central to human survival. Its complex anatomy, many functions, and rich vascularity have accorded it proper respect from surgeons throughout the world. However, improved understanding of segmental liver anatomy, together with radiological technique and critical care improvements, has allowed liver resection to become an established part of surgical practice over the past 30 years [1] .

There is a wide variety of both benign and malignant tumors that develop in the liver. The most common benign entities are hemangioma, followed by focal nodular hyperplasia and adenoma, which together represent more than 80% of all benign liver tumors [2] .

Malignant tumors in the liver can be classified as primary and secondary tumors. Primary tumors include hepatocellular carcinoma and cholangiocarcinoma [3] .

The first case of laparoscopic liver resection (LLR) for benign disease was reported by Gagner and colleagues in 1992, whereas the first case of LLR for malignant disease was reported by Wayand and Woisetschlager in 1994 [1] .

Initially described for peripheral, benign tumors resected by nonanatomic wedge resections, minimally invasive liver resections are now being performed more frequently, even for larger, malignant tumors located in challenging locations [4] .


  Materials and methods Top


This study was prospectively conducted from October 2012 to December 2014 on 30 patients presenting with hepatic tumors (benign and malignant) to the outpatient clinic of both Menoufia University Hospitals and El-Salam Oncology Center. Patients were divided randomly into two groups: group A, which includes 15 patients operated upon by laparoscopic technique; and group B, which includes 15 patients operated upon by open technique.

Inclusion criteria: any patient with hepatic tumors (benign or malignant) less than 6 cm that required resection with intent to cure.

Exclusion criteria:

  1. Patient unfit for surgery,
  2. Patients with malignant liver tumors in advanced stage.


Ethical issue

The procedure followed is in accordance with ethical standards of the responsible institutional committee on human experimentation and with the Helsinki Declaration of 1975, as revised in 1983.

All the patients were assessed through:

  1. Detailed history taking.
  2. Examination:
    1. General examination.
    2. Local examination.
  3. Investigations:
    1. Fundamental laboratory studies: complete blood count, liver functions and kidney functions. Prothrombin time and concentration, random blood sugar, blood group (ABO, Rh states), serum Na, K, total bilirubin and direct bilirubin, alkaline phosphates, and γ-glutamyl transpeptidase.
    2. Viral markers hepatitis C virus antibody, hepatitis B surface antigen, and HIV.
    3. Tumor markers: α-fetoprotien, carbohydrate antigen 19-9, and carcinoembryonic antigen.
    4. Radiological investigations: Abdominal ultrasonography, with duplex on portal vein, triphasic computed tomography (CT) of the abdomen and pelvis to evaluate the lesion and MRI of the abdomen and pelvis in some cases.
    5. Upper gastrointestinal endoscopy to detect the presence of esophageal varices and signs of portal hypertension.
    6. Metastatic work-up: chest radiography and CT chest if needed, MRI of the brain and bone scan.


Surgical technique for laparoscopic procedure

  1. The patient is positioned in French position in which the patient is supine with the legs in stirrups and the surgeon is positioned between the patient's legs.
  2. Central venous catheter, arterial line, and Hugger thermometer (warm blanket on peripheries) are placed by the anesthesia team with continuous monitoring and serial arterial blood gas and hemoglobin % analysis during perioperative time.
  3. The abdomen and lower chest (till nipple line) were prepared and draped.
  4. Pneumoperitonium was established at 13 or 14 mmHg with either by closed verrus needle technique or open Hasson technique through the umbilicus.
  5. Four additional ports are placed under direct visualization. A 12 mm port is placed along the midclavicular line 5 cm below the costal margin. Two 5 mm ports are placed to the left and right of the camera port. In some cases additional port (12 mm) was placed to apply the retractor of the liver.
  6. A complete sonographic examination is then completed with a flexible tip laparoscopic ultrasound probe if needed.
  7. Division of the falciform ligament from the anterior abdominal wall.
  8. In some cases with the left-sided lesions, the left triangular ligament was incised and freed close to the liver (by harmonic scalpel) or ligasure, whereas in the right-sided lesion the anterior leaf of right coronary ligament was incised by harmonic scalpel or ligasure.
  9. After marking the line of dissection by monopolar diathermy (with safety margins 1-2 cm), hepatic dissection was undertaken using ligasure, the harmonic scalpel, or Habib 4X sealer, with the use of articulated endovascular stapler in some cases.
  10. Extraction of the resected part of the liver done after its placement in plastic bag (endobag) either through subcostal incision (about 5 cm) or small Pfannestiel incision in some cases.
  11. Ports and specimen extraction wounds closure were carried out with intra-abdominal drain in the resection bed in some cases applied.
  12. Operative blood loss was estimated (ml) at the end of the operation and recorded along with perioperative blood transfusion (if needed). Operative time (min) (from the start of the procedure to closure of the abdomen) was recorded as well ([Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]).
Figure 1 Division of falciform ligament using harmonic scalpel.



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Figure 2 Division of left triangular ligament using harmonic scalpel.



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Figure 3 Marking of the resection margin with ligasure.



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Figure 4 Cutting through the liver parenchyma using ligasure.



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Figure 5 Intraparenchymal left hepatic vein ligation by using a clips.



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Surgical technique for open procedure

  1. The patient is positioned supine with both arms extended and pronated at right angles to the body. Tilting of the table could be used to improve the exposure.
  2. Central venous catheter, arterial line, and Hugger thermometer (warm blanket on peripheries) are placed by the anesthesia team with continuous monitoring and serial arterial blood gas and hemoglobin % analysis during perioperative time.
  3. The abdomen and lower chest (till nipple line) were prepared and draped.
  4. A fixed metal sterile abdominal wall retractor (subcostal) placed and attached to the table.
  5. The mostly used incision was the Mercedes (inverted T) incision in 10 cases, an inverted L (or long inverted C) incision in four cases, and Chevron (bilateral subcostal) in one case. Once the abdomen was opened, the falciform ligament was divided using diathermy and separated from the anterior abdominal wall.
  6. A thorough examination was conducted for the peritoneum and regional lymph nodes to exclude extrahepatic dissemination of malignancy.
  7. The liver was carefully palpated and intraoperative ultrasonography was undertaken, if needed, to confirm the position of the tumor and to assess its relationship with adjacent vascular structures.
  8. For the left-sided lesions, the left triangular ligament was incised and freed close to the liver to avoid injury of inferior phrenic vein.
  9. For the right-sided lesions, the right lobe could be mobilized by dividing the anterior leaf of the coronary ligament and the dissection was continued posteriorly to separate the adhesions between the adrenal gland and the bare area of the liver.
  10. After marking the line of dissection by monopolar diathermy (with safety margins 1-2 cm), hepatic dissection was undertaken using the harmonic scalpel, or Habib 4X sealer, with finger or artery fraction (crush-clamp) technique or ligasure, followed by monopolar or bipolar diathermy hemostasis. The minor blood vessels and bile ducts divided after clipping them by hemoclips or sutures. Wound closure was performed with intra-abdominal drains in the resection bed and/or hepatorenal angle in all cases after good hemostasis.
  11. Operative blood loss was estimated (ml) at the end of the operation. Operative time (min) (from the start of the incision to closure of the abdomen) was recorded as well.


Operative and postoperative parameters

During this period all patients were be assessed for time of operation, intraoperative blood loss (calculated by measuring the volume of blood in suction bottles after subtracting wash fluid), postoperative complications (bleeding, bile leakage, wound infection, chest infection, and ascites), duration of hospital stay, parenteral analgesia, earlier resumption of oral intake, the cost, and histological examination of the tumor to detect resection margin.

After discharge from hospital (short-term outcome), the patients were followed up for 3 to 6 months from the time of operation at 2-week intervals in the first 3 months and monthly for the next 3 months.

Statistical analysis

Results were collected, tabulated, and statistically analyzed by an IBM-compatible personal computer with SPSS statistical package, version 20 (IBM Corp, Armonk, NY, USA).

Two types of statistics were done:

  1. Descriptive statistics, for example, number and percentage for qualitative data, mean (x), and SD for quantitative data.
  2. Analytic statistics, for example:
    1. Student's t-test is a test used for comparison between groups having quantitative variables.
    2. Mann-Whitney test (nonparametric test) is a test of significance used for comparison between two groups not normally distributed having quantitative variables.
    3. χ2 was used to study association between two qualitative variables.
    4. Fisher's exact test for 2 × 2 tables when expected cell count of more than 25% of cases was less than 5.x
    5. Z-test is a significance test for testing proportions.
    6. P value:

      Significant difference if P value less than 0.05.

      Nonsignificant difference if P value less than 0.05.

      Highly significant difference if P value less than 0.001.




  Results Top


Demographic characteristics are listed in [Table 1]. None of these variables differed significantly between the laparoscopic and open-surgery groups.
Table 1 Demographic characteristics of the studied patients for both surgical techniques


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The mean age of the laparoscopic group and the open-surgery group was 53.20 ± 8.92 and 51.71 ± 11.44 years, respectively. The percentage of female participants in the laparoscopic and open groups was 33.3 and 20%, respectively.

Perioperative parameters are listed in [Table 2]. No deaths during surgery, no decision to convert to laparotomy was taken, and no intraoperative bleeding was observed in either group.
Table 2 Perioperative parameters among the studied patients for both surgical techniques


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Hepatectomy was performed for malignant disease in 14 patients (93.3%) in the laparoscopic group and 13 patients (86.7%) in the open-surgery group.

Mean duration of surgery was significantly higher for laparoscopy versus open surgery (131.54 ± 15.61 vs. 118.04 ± 19.41 min, respectively; P = 0.04). Duration of the surgery will tend to decrease with increasing experience for laparoscopy.

Highly significant less blood loss was observed in the laparoscopic group than in the open-surgery group (260.46 ± 96.20 vs. 440.74 ± 120.61 ml; P < 0.001). Blood loss will also decrease with experience.

Postoperative parameters are listed in [Table 3].
Table 3 Postoperative parameters among the studied patients for both surgical techniques


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There was a significantly earlier resumption of oral intake in the laparoscopic group than in the open-surgery group (1.60 ± 1.45 vs. 2.93 ± 1.08 days; P = 0.008).

Highly significant shorter duration of hospital stay was observed in the laparoscopic group than in the open-surgery group (6.20 ± 1.10 vs. 8.81 ± 1.50 days; P < 0.001).

There was a significantly shorter duration of parenteral analgesia in the laparoscopic group than in the open-surgery group (2.85 ± 0.74 vs. 3.85 ± 0.98 days; P = 0.003).

Early postoperative adverse effects as liver resection-related (i.e. cirrhotic decompensation/ascites, hepatic hemorrhage, biliary leakage, and liver failure) and general complications (i.e. chest infection, wound infection, intra-abdominal abscesses, and pleural effusion) are listed in [Table 4].
Table 4 Postoperative complications among the studied patients for both surgical techniques


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There was one case of cirrhotic decompression/ascites in the open-surgery group, one case of biliary leakage in the laparoscopic group, and two cases of bile leakage in the open-surgery group. There was no significant difference between the two groups regarding these liver resection-related complications (P = 0.99 and 0.49 respectively).

There were one case of chest infection and two cases of wound infection in the open-surgery group. There was no significant difference between the two groups regarding these general complications.

The laparoscopic group showed a lower significant overall complication rate as compared with the open-surgery group (P = 0.03)

Cost of each surgical technique is listed in [Table 5]. There was a highly significant less cost in the open-surgery group than the laparoscopic group.
Table 5 Comparison between both surgical techniques regarding cost


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Oncological clearance in the form of pathological resection margin size is listed in [Table 6]. None of our cases were have involved margin.
Table 6 Oncological results among the studied patients for both surgical techniques


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There was a highly significantly larger safety margin in the laparoscopic group than in the open-surgery group.

Short-term outcome (6 months follow-up) such as incisional hernia, mortality rate, and the recurrence rate are listed in [Table 7]. None of these variables differed significantly between the laparoscopic and open-surgery groups.
Table 7 Short-term outcome (6 months follow-up) among the studied patients for both surgical techniques


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There were no mortality and no recurrence in both groups (port-site metastases, wound metastases, or recurrence of the pathology) during 6 months follow-up on patients with malignant tumors either hepatocellular carcinoma or metastases.

There were two cases of incisional hernia in the open-surgery group with no significant difference between both groups.


  Discussion Top


Hepatic resection is an appropriate treatment for a variety of benign and primary or secondary malignant hepatic lesions [5] .

The aim is to perform hepatic resection with minimal bleeding and leaving adequate functional liver to avoid hepatic insufficiency postoperatively [6] .

In this study, indication for surgery in group A was one (6.7%) case of benign tumor and 14 (93.3%) cases of malignant tumors, whereas group B was two (13.3%) cases of benign tumors and 13 (86.7%) cases of malignant tumors with no significant difference of both groups. As indication for laparoscopic hepatectomy are identical to those for open hepatectomy in terms of preoperative assessment of liver functions. Therefore, in determining whether laparoscopic hepatectomy is indicated, the size, type, and location of the tumors must be evaluated. Nodular tumors smaller than 4 cm or pedunculated tumors smaller than 6 cm are proper indication [7] .

Small number of benign cases who required resection was explained by the recent advances in preoperative imaging studies that enable the surgeon to select more case to conservative treatment. In addition, modern imaging techniques such as triphasic CT and MRI have very high accuracy rate in differentiation between benign and malignant tumors of the liver even without tissue biopsy which enables the surgeon to select the conservative treatment to the patients who had lesions of benign potential [8] .

In this study, intraoperative pringle maneuver was not done in any case in both groups. In a prospective randomized study comparing liver resection with and without hepatic pedicle clamping, it was shown that liver resection can be safely performed without any vascular occlusion [9] .

In this study, there was no intraoperative bleeding in both groups with mean blood loss in group A 260.46 ± 96.20 ml, whereas in group B it was 440.74 ± 12.61 ml, with significant difference between both groups with less blood loss in group A. This agreed with Polignano et al. [10] , Abu Hilal et al. [11] and Ito et al. [12] whose studies show significant difference in LLR versus OLL with decreased blood loss in lap group and disagreed with Endo et al. [13] who stated that blood loss was less in the open-surgery group with no available data.

Topal et al. [14] showed significantly decreased blood loss using laparoscopic compared with open liver resection (OLR). With increasing experience through the learning curve of laparoscopic liver surgery, blood loss was significantly decreased between the first and second halves of the laparoscopic group (200 vs. 50 ml; P = 0.004), and this agreed with our studies.

In this study, the operative time was 131.54 ± 15.61 min in the laparoscopic group, whereas the open-surgery group mean time was 118.04 ± 20.41 min, with statistically significant differences between the two groups, with decreased operative time in the open-surgery group than in the laparoscopic group.

Most studies did not show any significant differences in operative times between the laparoscopic and OLR; however, 4 studies conducted by Ito et al. [12] , Belli et al. [15] , Lesurtel et al. [16] , and Laurent et al. [17] showed significantly longer operative time with the laparoscopic approach compared with open resection, whereas two studies conducted by Buell et al. [18] and Belli et al. [19] showed shorter operative time using a laparoscopic approach [20] .

In this study, the time of the first oral intake in group A was 1.60 ± 1.45 days, whereas it was 2.93 ± 1.08 days in group B, with a significant difference between both groups with earlier oral intake in the laparoscopic group than in the open-surgery group. This is agreed with Kaneko et al. [7] who stated that significant earlier oral intake in the laparoscopic group than in the open-surgery group. In addition, Rowe et al. [21] stated significant earlier oral intake in the laparoscopic group.

In this study, the duration of hospital stay was 6.20 ± 1.10 days in group A ranging from 6 to 9 days, whereas it was 8.81 ± 1.50 days in group B ranging from 5 to 10 days, with significant less hospital stay in the laparoscopic group. This is agreed with Kaneko et al. [7] who stated that there is significant less hospital stay in the laparoscopic group than in the open-surgery group. In addition, Abu Hilal et al. [11] , Ito et al. [12] and Dagher et al. [22] stated significant lower hospital stay in the laparoscopic group.

However, Lesurtel et al. [16] study stated that there were no notable differences between both the groups.

In this study, group A was under parenteral analgesia with mean of 2.85 ± 0.74 days, whereas group B was under parenteral analgesia with mean of 3.85 ± 0.98 days, with significantly lower duration of parenteral analgesia of group A. This study agreed with meta-analysis performed by Rao et al. [23] who stated that many studies showed that the duration of parenteral analgesia was significantly lower at the laparoscopic group because there were small wounds, in comparison with large wounds in the open-surgery group.

In this study, there was no statistically significant difference between both the groups regarding these liver-related complications.

This is agreed with the meta-analysis performed by Rao et al. [23] . Comparing open and laparoscopic hepatectomy with many studies showed that with regard to liver-related complications no significant differences were found in both the groups [11],[19],[24] .

There was no significant difference between both the groups with regard to general complications.

This is agreed with the meta-analysis performed by Rao et al. [23] . Comparing open and laparoscopic hepatectomy with many studies showed that with regard to general complications no significant differences were found in both the groups [14],[21],[25] .

There was no hospital mortality in both groups with no significant difference between the laparoscopic and open-surgery group.

This is agreed with the meta-analysis performed by Rao et al. [23] . Comparing open and laparoscopic hepatectomy with many studies showed that with regard to hospital mortality no significant difference was found in both the groups [12],[22],[26] .

In our study, the overall complication rates were significantly lower in group A than in group B.

Our study agreed with the meta-analysis done by Rao et al. [23] . Comparing open and laparoscopic hepatectomy with many studies showed that the overall complication rate was found to be significantly lower than that in the laparoscopic group [27],[28],[29] .

However, a meta-analysis performed by Simillis et al. [30] showed no significant difference in both groups with regarding overall complication rate (LLR 12% while OLR 17%; P = 0.24).

The mean cost in this study in group A was 12 000.17 ± 2500.09 LE ranging from 8000 to 16 000 LE. Whereas the mean cost in group B was 7000.51 ± 1125.12 LE ranging from 5000 to 9000 LE, with significant lower cost in the open group than in the laparoscopic group.

There are concerns that the minimally invasive approach to liver resection may be associated with increased cost because of laparoscopic equipment/instrumentation; however, this may be offset by a shorter length of hospital stay in patients who undergo the laparoscopic approach [20] .

Rowe et al. [21] showed that the cost of stapler/trocar devices was similar between the laparoscopic versus the open group.

In this study, there was no involved margin in both groups: it was 18.50 ± 2.98 mm in group A, whereas 13.70 ± 1.87 mm in group B, with significantly wider resection margin in laparoscopic group.

Initial concerns of adequate margins and tumor seeding prevented the widespread application of LLR for malignant tumors. However, in a comparison study by Belli et al. [19] it was found that the laparoscopic resection group had a significantly wider resection margin than the open resection group. Whereas many studies show that there were no differences in margin-free resections between laparoscopic versus OLR. In addition, to the best our knowledge, no incidence of port-site recurrence or tumor seeding has been reported [20] .

During the period of the early follow-up for the first 3 to 6 months from the date of operation for all of our patients, there was no recurrence in the pathology or mortality among the 30 cases of both groups. Two cases in the open-surgery group developed an incisional hernia at the Mercedes incision wound.

Kaneko et al. [7] observed no recurrences related to laparoscopy, such as peritoneal dissemination or port-site recurrences; in addition, there were no significant differences between procedures concerning the 5-year survival rate (laparoscopic 61% : open 62%) and 5-year survival rate without recurrences (laparoscopic 31% : open 29%).


  Conclusion Top


LLR improved surgical and postsurgical outcome for OLR regarding less operative blood loss, postoperative pain, postoperative complications, and hospital stay. Operating time was longer in the laparoscopic group and there was no difference regarding 6 months follow-up.


  Acknowledgements Top


The authors acknowledge all participants in the study, patients and their family.

Conflicts of interest

There are no conflicts of interest.

 
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7]



 

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Abstract
Introduction
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