Invest Clin 65(2): 155 - 168, 2024 https://doi.org/10.54817/IC.v65n2a03

Corresponding author: Yansong Xu, Department of Hepatobiliary Surgery, Affiliated Hospital of Beihua University,

Jilin, 132012, Jilin, China. E-mail: tonggubu9822@163.com

Benefits of a modified local precision liver

resection using intraoperative laparoscopic

ultrasound in the treatment and prognosis

of patients with liver cancer.

Yansong Xu

and Lin Shen

Department of Hepatobiliary Surgery, Affiliated Hospital of Beihua University, Jilin,

China.

Department of Anesthesiology, Affiliated Hospital of Beihua University, Jilin, China.

Keywords: precision hepatectomy; liver function; hepatic venous injury; immune

factors; immune response; cytokines; Karnofsky performance scale.

Abstract. The incidence and mortality rate of liver cancer has increased

significantly. Recently, intraoperative laparoscopic ultrasound (LUS) has been

used in hepatectomy, in addition to open liver resection, as the most common

treatment method. The current research aims to address this issue. Seventy-six

patients with liver cancer who were admitted to the Hospital of Beihua Univer-

sity from February 2018 to September 2021 were randomly divided into two

groups of 38 patients, one group undergoing conventional laparoscopic sur-

gery (control group) and the other group undergoing a precise laparoscopic

liver resection after placing an intraoperative LUS instrument (study group).

Blood loss and hepatic vein damage during surgery were less in the study group

(p<0.05). Seven days after surgery, liver function indices (albumin, total bil-

irubin, and alanine and aspartate aminotransferases) and indices related to

immune function interleukin 6, tumor necrosis factor α, CD3+ and CD4+ T

lymphocytes and NK cells level in the study group improved compared to the

control group. The postoperative complications were less in the study group,

and the nine-month follow-up showed that the recurrence rate was lower and

the survival rate was higher in this group. This study shows that precise laparo-

scopic hepatectomy modified with the use of intraoperative laparoscopic ultra-

sound results in better intraoperative and postoperative outcomes for the prog-

nosis and survival rate of patients with liver cancer, which makes this surgical

technique worth generalizing in clinical practice.

156 Xu and Shen

Investigación Clínica 65(2): 2024

Beneficios de la resección hepática de precisión local

modificada, utilizando ecografía intraoperatoria

laparoscópica en el tratamiento y pronóstico de pacientes

con cáncer de hígado.

Invest Clin 2024; 65 (2): 155 – 168

Palabras clave: hepatectomía de precisión; función hepática; lesión venosa hepática;

factores inmunológicos; respuesta inmune; citocinas; escala de

desempeño de Karnofsky.

Resumen. La tasa de incidencia y mortalidad del cáncer de hígado ha au-

mentado drásticamente. Además de la resección hepática abierta como método

de tratamiento más común, la ecografía laparoscópica intraoperatoria (LUS) se

ha utilizado recientemente en la hepatectomía. El objetivo de la investigación

actual es responder a esta pregunta. 76 pacientes con cáncer de hígado ingresa-

dos en el Hospital de la Universidad de Beihua entre febrero de 2018 y septiem-

bre de 2021 fueron asignados aleatoriamente a dos grupos de 38 pacientes, un

grupo sometido a cirugía laparoscópica convencional (grupo control) y el otro

grupo sometido a resección hepática laparoscópica precisa, después de colocar

un instrumento LUS intraoperatorio (grupo de estudio). La pérdida de sangre

y el daño a las venas hepáticas durante la cirugía fueron menores en el grupo

de estudio (p < 0,05). Siete días después de la cirugía, los índices de función

hepática (albúmina, bilirrubina total y alanina y aspartato aminotransferasas) e

índices relacionados con la función inmune, interleucina 6, factor de necrosis

tumoral α, linfocitos T CD3+ y CD4+ y nivel de células NK en el grupo de estu-

dio mejoraron en comparación con el grupo control. Las complicaciones posto-

peratorias fueron menores en el grupo de estudio, y el seguimiento a los 9 me-

ses mostró que la tasa de recurrencia fue menor y la tasa de supervivencia fue

mayor en este grupo. Este estudio demuestra que la hepatectomía laparoscópi-

ca precisa modificada con el uso de la ecografía laparoscópica intraoperatoria

da como resultado mejores resultados intraoperatorios y postoperatorios para

el pronóstico y la tasa de supervivencia de los pacientes con cáncer de hígado, y

hace que valga la pena generalizar esta técnica quirúrgica en la práctica clínica.

Received: 20-07-2023 Accepted: 11-11-2023

INTRODUCTION

Liver cancer is a malignant tumor that

seriously affects Chinese residents’ health,

and its incidence is relatively high

1,2

. The

early stage of hepatocellular carcinoma

courses with insidious characteristics and

rapid growth, but it is often diagnosed in

the middle and late stages. At the same

time, liver cancer has high recurrence and

mortality rates

3,4

. At present, liver cancer

is mainly treated through surgery. In clini-

cal practice, different treatment measures

are adopted according to the different liver

function reserve abilities, the physical condi-

tions of people with liver cancer, and the dif-

Benefits of a modified precision hepatectomy with laparoscopic ultrasound 157

Vol. 65(2): 155 - 168, 2024

ferent stages of cancer the patients present.

Liver resection is preferred for patients with

localized liver cancer without accompanying

cirrhosis

. Hepatectomy is the most com-

mon surgical method for radical liver cancer

treatment, which can notoriously reduce the

recurrence and spread of liver tumors and ef-

fectively prolong the survival time of suffer-

ers

6,7

. Conventional open liver resection is a

standard clinical method. However, the pa-

tient’s postoperative recovery and prognosis

are unsatisfactory due to the extensive surgi-

cal trauma and the risk of acquiring a post-

operative infection

. With the development

of science and technology and the enhance-

ment of medical standards, the application

value of laparoscopy in various surgical oper-

ations has become increasingly apparent. In

the 1990s, Reich performed the world’s first

laparoscopic liver resection. Since then, the

door has been opened to minimally invasive

surgery through laparoscopy

In contrast with conventional open liver

resection, laparoscopic liver resection has the

advantages of less trauma and quick postop-

erative recovery, which surgeons and patients

favor. However, laparoscopic surgery also has

limitations since the laparoscopic surgeon

operates only through a few holes and cannot

directly contact and manipulate the related

visceral structure, and because of the reduced

abdomen’s display, the surgeon may not fully

understand the abdominal situation, leading

to a limited surgical field. At the same time,

the lack of palpation increases the risk in lapa-

roscopic surgery

. In addition, because the

field is not comprehensive, it is easy to ignore

some small lesions, and it can easily result in

the presence of tumor residues, leading to a

high recurrence rate in patients. Enhanced lo-

cal precision resection was developed based on

a conventional laparoscopic resection. Using

laparoscopic ultrasound (laparoscopic ultraso-

nography, LUS) can help the operator detect

complex lesions. It can synchronously guide the

surgeon to operate, reduce damage to related

organs and tissues, and make up for the defi-

ciencies of conventional laparoscopic surgery.

Relevant studies have shown that laparoscopic

surgery with LUS is more effective

11,12

. In re-

cent years, ultrasound examination has been

gradually applied to laparoscopic surgery. The

period of clinical use has not been very long,

and since the related studies are few, the thera-

peutic effect of laparoscopic surgery on liver

cancer still needs further analysis

. Therefore,

this study aimed to evaluate the clinical ben-

efits of modified precision hepatectomy using

intraoperative LUS in patients with liver cancer

so that this new treatment technique can be

tested to find a better way to treat liver cancer.

PATIENTS AND METHODS

General Information

In this study, all eighty-seven patients

with liver cancer admitted to the Hospital

of Beihua University, China, from February

2018 to September 2021 were selected for

this study. The inclusion criteria were as fol-

lows: met the diagnosis and implications of

liver cancer, according to the Guidelines

on the diagnosis and treatment of prima-

ry liver cancer (2011 edition)

. Relevant

criteria in TNM stages I, II, and III; Child-

Pugh grades A or B; no associated surgery

or radiofrequency ablation for six months;

and nine months of telephone follow-up af-

ter laparoscopic surgery. Exclusion criteria

were tumor involvement of adjacent organs

or metastases; severe abdominal adhesion;

patients with cardiac or renal failure; abnor-

mal mental status; diabetes; women during

pregnancy or lactation; and patients with an

allergic condition. All patients signed the in-

formed consent form, and the medical eth-

ics committee of our hospital approved this

study. Of the eighty-seven patients who were

accepted at the beginning of the study, af-

ter checking the study conditions and the

inclusion and exclusion criteria, seventy-six

patients were finally included. Seventy-six

patients were randomly selected as control

variables according to the random number

table method and randomly divided into two

groups of 38 patients.

158 Xu and Shen

Investigación Clínica 65(2): 2024

METHODS

Surgical method: Our institution’s

chief surgeon has been the same physician

for over eight years. We used a conventional

laparoscopic liver resection for the control

group: a preoperative-related imaging (MRI

or CT) examination in the supine position

was performed to determine the lesion site,

size, and number. This examination was fol-

lowed by the conventional implementation

of an artificial pneumoperitoneum (pres-

sure 12-14 mmHg), the construction of the

conventional “five-port technique” accord-

ing to the location and size of the tumor,

abdominal exploration, to free the perihe-

patic ligament and to fully reveal the tumor

focus, the first portal vascular implication,

the left hepatic artery and portal branch,

according to the liver ischemia line or the

anatomy Cantilie-line mark as a resection

line

9,11,15-17

For the Study group, we used a modi-

fied laparoscopic precision liver resection.

After a preoperative imaging (MRI or CT) ex-

amination to determine the lesion location,

size, and number in the supine position, we

established an arc incision approximately

10 mm below the umbilicus. This incision

was followed by the conventional implemen-

tation of an artificial pneumoperitoneum

(pressure 12-14 mmHg) and placed the LUS

(HITACHI ALOKA Noblus; with an L44LA

soft probe, probe frequency of 7.5 MHz). Dif-

ferent liver parts were scanned successively,

and the tumor location, size, number, and

the relationship between the tumor body

and the peripheral vasculature and tissues

were determined again. The proper liver

blood flow blocking method and liver paren-

chyma disconnection method were selected.

For severe liver parenchyma lesions, it was

not appropriate to block the blood flow into

the liver and use an ultrasonic knife to stop

the liver parenchyma and the bipolar elec-

trocoagulation wound. Selective blood flow

into the liver was blocked for patients with

mild liver parenchymal lesions, and the liver

parenchyma was severed along the ischemic

line with an ultrasound knife. The vascular

structure was fully exposed for the liver re-

section, then treated accordingly to the vas-

cular diameter

17-21

Blood tests: In the early morning, 5 mL

of cubital venous blood was extracted and

centrifuged at 3500 rpm for 10 min, with a

centrifugation radius of 10 cm, and the se-

rum was collected for indicator determina-

tions.

Observation Indicators and Evaluation

Criteria

(1) Perioperative-related indicators:

data and blood samples were collected by the

same nurse working in our hospital for over

three years. The operation time, intraopera-

tive blood loss, hepatic vein injury rate, le-

sion resection edge distance, drainage tube

extubation time, and anal exhaust time were

recorded.

(2) Fasting venous blood was collected

before and seven days after the intervention,

and an analysis was performed using a fully

automatic biochemical analyzer (Beckman

Coulter AU5800). Liver function-related

indicators were measured in both groups

of patients: albumin (ALB), alanine amino-

transferase (ALT), aspartate aminotrans-

ferase, AST), and total bilirubin (TBIL), as

well as the immune factor-related indicators

interleukin 6 (IL-6), tumor necrosis factor

α (TNF-α). T lymphocyte subsets were ana-

lyzed by flow cytometry (Beckman Coulter

EPICS XL) to detect T lymphocytes (CD3

inducible T cells (CD4

), and human natural

killer (NK) cells (NK cell standard). The same

physician performed the specific operations

according to the instructions.

(3) The incidence of related complica-

tions (infection, abdominal hemorrhage,

bile leakage, pleural effusion, etc.) in the

two groups of patients was reported by the

same nurses working for over three years.

(4) We used the Karnofsky scoring

method (KarnofskyPerformance Status,

KPS) 22 to assess the recovery of quality of

Benefits of a modified precision hepatectomy with laparoscopic ultrasound 159

Vol. 65(2): 155 - 168, 2024

life in the two groups of patients. If the score

increased by more than ten points after the

procedure, the activities of daily living (ADL)

were better; if it lessened by more than ten,

it was worse; if it increased or lessened by

ten, it was stable.

(5) The survival and recurrence rates

of both groups were recorded by telephone

follow-ups at three months (T1), six months

(T2), and nine months (T3) after surgery by

the same nurse.

Statistical analysis

The required data of this study were

sorted and entered into a Microsoft

Excel

table. We used the SPSS26.0 software to ana-

lyze the data. If the data (±SD) were nor-

mally distributed, we compared the groups

with the independent sample t-test for the

group’s data and paired sample t-test; count

data was analyzed by percentages and Chi-

square test (χ

test). The Kaplan-Meier sur-

vival curves were employed to determine

sufferers’ survival and recurrence rates in

the two groups. When p

≤ 0.05, the data’s

differences were considered statistically sig-

nificant.

RESULTS

This study was conducted to investigate

the benefits of modified precise hepatecto-

my using intraoperative LUS in patients with

liver cancer.

The clinical and demographic charac-

teristics of the two groups of patients under

investigation are presented in Table 1. The

sex distribution among the study group pa-

tients showed that 21 (55.3%) were male and

17 (44.7%) were female; whereas, in the con-

trol group, there were 20 (52.6%) male and

18 (47.4%) female patients. The mean age

of the study group was 51.52±6.95 years,

while the mean age of the control group was

52.36±8.32 years. The mean body mass in-

dex (BMI) in the study group patients was

22.36±2.68 kg/m

; whereas, in the control

group, it was 22.63±3.01 kg/m

. The two

groups had no significant differences regard-

ing sex distribution, mean age, and mean

BMI.

The staging of patients based on TNM

revealed that in the study group, 14 (36.8%)

patients were in stage I, 13 (34.2%) patients

were in stage II, and 11 (29%) patients were

in stage III. Similarly, in the control group,

there were 14 (36.8%) patients in stage I, 15

(39.5%) patients in stage II, and 9 (23.7%)

patients in stage III. There were no signifi-

cant differences between the two groups re-

garding cancer staging based on TNM. The

tumor diameter in the study group patients

was 5.16±1.49 cm, while in the control

group, it was 5.09±1.53 cm, and there was

no significant difference in tumor diameter

between the two groups. The results of the

Child Grade in the two groups of examined

patients showed that 29 (76.3%) patients in

the study group and 27 (71%) patients in the

control group were classified as Group A. Ad-

ditionally, 9 (23.7%) patients in the study

group and 11 (29%) patients in the control

group were classified as Group B, with no

significant difference observed between the

two groups.

Comparison of perioperative indicators

between the two groups of patients

The mean duration of surgery in

the study group was 103.59±19.12 min-

utes, while in the control group, it was

98.59±20.16 minutes. There was no signifi-

cant difference in the duration of surgery

between the two groups. Hepatic venous

injury was observed in two (5.26%) patients

in the study group and ten (14.28%) pa-

tients in the control group, showing there

was a significant difference (p=0.013). The

blood loss volume in the study group was

183.38±29.71 mL; whereas in the control

group, it was 233.56±24.28 ml, and the two

groups did not differ significantly in blood

loss volume. Other preoperative indicators

are presented in Table 2.

160 Xu and Shen

Investigación Clínica 65(2): 2024

Table 1

Comparison of the clinical and demographic characteristics between the two groups of liver cancer patients.

Group Sex*

Age**

(years)

BMI**

(kg/m

)

TNM& by stages (n) Tumor

diameter

(cm)

Child Grade (n)

Men Women

designated

time

designated

time

III

designated

time

A B

Study group

(n=38)

(55.3%)

17 (44.7%) 51.52±6.95 22.36±2.68 14 (36.8%) 13 (34.2%) 11 (29%) 5.16±1.49 29 (76.3%) 9 (23.7%)

Control group

(n=38)

(52.6%)

18 (47.4%) 52.36±8.32 22.63±3.01 14 (36.8%) 15 (39.5%) 9 (23.7%) 5.09±1.53 27 (71%) 11 (29%)

t/x

0.818 0.769 0.185 0.267 0.486 1.32

p 0.500 0.436 0.498 0.782 0.512 0.329

*Frequency :n (%) , ** Mean± (SD).

TNM [classifies cancers by the size and extent of the primary tumor (T), involvement of regional lymph nodes (N), and

the presence or absence of distant metastases (M)].

Table 2

Perioperative indicators of the two groups of liver cancer patients.

Group Sample

number

Time of surgery

(min)**

The rate of hepatic

venous injury

(%)&

Intraoperative blood

loss volume (mL)**

Margin

distance

(cm)**

Drainage tube

extubation time

(d)**

Anal exhaust

time (d)**

Study group 38 103.59±19.12 2(5.26) 183.38±29.71 2.97±1.15 5.93±1.28 3.74±1.03

Control group 38 98.59±20.16 10 (14.28) 233.56±24.28 3.21±0.84 6.13±1.65 4.06±1.38

t/x

1.425 8.725 13.125 0.541 1.683 1.532

p* 0.163 0.013 <0.01 0.423 0.113 0.136

*p t-test, ** Mean± (SD),

Frequency: n(%).

Benefits of a modified precision hepatectomy with laparoscopic ultrasound 161

Vol. 65(2): 155 - 168, 2024

Indexes of liver function

The examination of liver function indi-

cators before and after surgery in the two

groups of liver cancer patients revealed that

the mean blood albumin level in the study

group before surgery was 39.38±2.19 g/L,

while in the control group was 39.44±2.17

g/L, showing no significant difference. How-

ever, the mean blood albumin level in the

study group after surgery was 64.41±2.91

g/L, compared to 52.91±2.69 g/L in the

control group, indicating a significant dif-

ference in albumin levels between the two

groups after surgery (p=0.032). The mean

alanine transaminase level in the study

group before surgery was 39.61±5.42 U/L,

and in the control group, it was 39.64±5.49

U/L, with no significant difference observed.

However, the mean alanine transaminase

level in the study group after surgery was

10.85±2.36 U/L, while in the control group,

it was 15.16±2.42 U/L, demonstrating a

significant difference in the mean alanine

transaminase levels after surgery between

the two groups (p=0.037).

The mean preoperative aspartate ami-

notransferase (AST) levels in the study group

of patients were 42.95±3.51 U/L, while in

the control group, it was 43.13±3.57 U/L,

showing there was no statistically signifi-

cant difference observed in the preopera-

tive AST levels between the two groups. On

the other hand, the postoperative mean AST

levels in the study group were 28.47±2.92

U/L, whereas, in the control group, it was

34.94±2.35 U/L. These results indicated a

significant difference in the postoperative

AST levels between the study and control

groups (p=0.041). No significant differ-

ence was observed in the preoperative total

bilirubin levels between the control group

(20.44±2.66 μmol/L) and the study group

(20.43±2.64 μmol/L). However, the mean

total bilirubin level in the study group after

surgery was 4.38±1.43 μmol/L, while in the

control group, it was 7.34±2.17 μmol/L.

These findings demonstrated a significant

difference in the postoperative total bilirubin

levels between the two groups (p=0.031).

The relevant data are presented in Table 3.

Comparison of immune factor indicators

The investigation of immune factor

indices before and after surgery in the two

groups of patients with liver cancer revealed

that the mean concentration of interleukin-6

(IL-6) in the study group prior to surgery was

92.83±12.59 pg/mL, while in the control

group, it was 92.89±12.68 pg/mL, showing

no statistically significant difference. How-

ever, the mean IL-6 concentration in the

study group after surgery was 101.28±15.28

pg/mL, whereas, in the control group, it was

124.49±14.68 pg/mL, demonstrating a sig-

nificant difference in IL-6 levels between the

two groups after surgery (p=0.023).

Regarding tumor necrosis factor-alpha

(TNFα), the mean concentration in the

study group before surgery was 12.06±1.29

ng/mL, while in the control group was

15.68±2.41 ng/mL, with no significant dif-

ference observed. However, the mean TNFα

concentration in the study group after sur-

gery was 12.09±1.32 ng/mL, whereas, in

the control group, it was 19.82±2.39 ng/

mL, indicating a significant difference in the

mean TNFα levels between the two groups af-

ter surgery (p=0.037).

The preoperative levels of CD3

(clus-

ter of differentiation 3), CD4

(cluster of di-

fferentiation 4), and NK (Natural killer cells)

did not show a significant difference between

the study group and the control group. Howe-

ver, the postoperative percentage of CD3

the study group was 56.28±7.79%, whereas,

in the control group, it was 50.22±4.63%.

The postoperative percentage of CD4

in the

study group was 27.13±5.38%, while in the

control group was 20.51±4.29%. Additiona-

lly, the postoperative level of NK in the study

group was 10.33±1.19 pg/mL, and in the

control group was 8.29±1.12 pg/mL. These

differences in CD3

, CD4

, and NK levels af-

ter surgery were statistically significant bet-

ween the two groups (p<0.05). The relevant

data are presented in Table 4.

162 Xu and Shen

Investigación Clínica 65(2): 2024

Table 3

The preoperative and postoperative liver function indicators in the two groups of liver cancer patients.

set

ALB (g/L)** ALT (U/L)** AST (U/L)** TBIL (μmol/L)**

Preoperative Postoperative Preoperative Postoperative Preoperative Postoperative Preoperative Postoperative

Study Group 39.38±2.19 64.41±2.91 39.61±5.42 10.85±2.36 42.95±3.51 28.47±2.92 20.43±2.64 4.38±1.43

Control

Group

39.44±2.17 52.91±2.69 39.64±5.49 15.16±2.42 43.13±3.57 34.94±2.35 20.44±2.66 7.34±2.17

t 0.956 2.239 0.853 2.204 0.933 2.228 0.821 2.245

p* 0.425 0.032 0.328 0.037 0.379 0.041 0.455 0.031

*P-Value t-test, ** Mean±SD.

ALB: albumin, ALT: alanine amino transferase, AST: aspartate amino transferase, TBIL: total bilirrubin.

Table 4

Preoperative and postoperative immune factor indicators in the two groups of liver cancer patients.

Group

IL-6 ( pg/mL)** TNF-α ( ng/mL)** CD3+ (%)** CD4+ (%)** NK (pg/mL)**

Preoperative Postoperative Preoperative Postoperative Preoperative Postoperative Preoperative Postoperative Preoperative Postoperative

Study

Group

92.83±12.59 101.28±15.28 12.06±1.29 12.09±1.32 61.19±5.81 56.28±7.79 35.19±3.32 27.13±5.38 13.31±1.49 10.33±1.19

Control

Group

92.89±12.68 124.49±14.68 15.68±2.41 19.82±2.39 62.39±4.91 50.22±4.63 34.25±3.17 20.51±4.29 13.29±1.61 8.29±1.12

t 0.826 9.265 0.756 7.531 0.930 4.283 1.242 5.58 0.813 4.361

p* 0.425 0.023 0.328 0.046 0.375 <0.01 0.219 <0.01 0.465 0.019

*p-value t-test, ** Mean±SD.

Benefits of a modified precision hepatectomy with laparoscopic ultrasound 163

Vol. 65(2): 155 - 168, 2024

Postoperative complications in both sets

The analysis of surgical complications

among the two groups of patients revealed

notable findings (Table 5). Only one patient

(2.63%) experienced infection in the study

group, while another patient (2.63%) devel-

oped pleural effusion following the opera-

tion. Conversely, within the control group,

complications were comparatively higher.

Specifically, three patients (7.89%) encoun-

tered postoperative infection, two patients

(5.26%) suffered from postoperative hemor-

rhage, three patients (7.89%) experienced

bile leak, and one patient (2.63%) developed

pleural effusion. These contrasting com-

plication rates indicate a statistically sig-

nificant difference between the two groups

(p=0.022).

Quality of life score

There were no significant differences

when comparing the postoperative KPS

standard scores between the two groups, p>

0.05 (Table 6).

Postoperative survival and recurrence

rates

The comparison of survival and recur-

rence rates in the two groups of patients is

shown in Table 7. The analysis of survival

rates among the two patient groups yielded

significant statistical differences (p=0.033).

In the study group, the survival rate was re-

markably high, with 37 patients (97.4%) sur-

viving during the first and second follow-up

periods. Only one patient died in the period.

As the study progressed to the third follow-

up, 35 patients (92.1%) remained alive,

while three patients succumbed to their con-

dition. In comparison, the control group ex-

hibited slightly lower survival rates, with 36

patients (94.7%) surviving the initial follow-

up and 35 patients (92.1%) in the second

follow-up. However, by the third follow-up,

the number of surviving patients decreased

to 28 (73.68%).

The study group showcased favorable

outcomes regarding disease recurrence, as

no recurrences were observed during the

Table 5

Contrast of the incidence of postoperative complications in the two groups.

Group

Sample

number

Infections

Postoperative

hemorrhage

Bile leak Pleural effusion

Study Group 38 1 (2.63%) 0 0 1 (2.63%)

Control Group 38 3 (7.89%) 2 (5.26%) 3(7.89%) 1(2.63%)

5.208

p* 0.022

*p-value Chi-square (χ² tests).

Table 6

Comparison of the quality of life in the two groups.

Group Sample number

KPS grade

Preoperative** Postoperative**

Study Group 38 60.52 ± 12.88 69.03 ± 14.02

Control Group 38 60.46 ± 12.78 68.92 ± 12.43

t 2.366 1.563

p* 0.652 0.312

*p-value t-test, ** Mean±SD.

164 Xu and Shen

Investigación Clínica 65(2): 2024

first follow-up. However, during the sec-

ond follow-up, a marginal recurrence rate

of one patient (2.6%) was identified, which

increased slightly to two patients (5.3%)

during the third follow-up. In contrast, the

control group exhibited higher recurrence

rates, with one patient (2.6%) experienc-

ing a recurrence during the first follow-up,

followed by two patients (5.3%) during the

second follow-up, and a more significant

number of seven patients (8.16%) during the

third follow-up. These contrasting patterns

in recurrence rates between the study and

control groups were statistically significant

(p=0.025). Over time, the control group ex-

hibited lower survival rates than the study

group. Conversely, the disease recurrence

rate in the control group was higher than

in the study group. These disparities in sur-

vival rates and disease recurrence between

the two groups were statistically significant

(p<0.05).

DISCUSSION

Liver cancer is one of the most common

malignant tumors in China. One of the main

options for liver cancer treatment is sur-

gery

. With the development of technology,

laparoscopic hepatectomy has become wide-

ly used in clinical practice, and many stud-

ies have proved that this surgical technique

proceeds with less significant trauma, short-

er recovery time, and a better prognosis

However, the limited field of laparoscopy and

the complex vascular and bile duct systems

in the liver have brought many difficulties to

laparoscopic liver resection, such as how to

reduce liver vascular damage, avoid tumor

residues, and reduce the postoperative re-

currence rate and mortality, which have al-

ways been significant in liver surgery

. In or-

der to preserve more normal liver tissue, the

pursuit of the concept of an accurate liver

resection has gradually become an objective

to accomplish

. In surgery, the LUS probe

can reach deeper lesions, allowing more

comprehensive liver information to be pre-

sented to the operator. Because of the physi-

cal characteristics of ultrasound, it can ef-

fectively avoid the interference of irrelevant

factors. Furthermore, it can show the tumor

size and depth in the liver, reduce the num-

ber of tumor contacts and extrusion, allow

for complete tumor removal, avoid residual

tumors, and reduce the postoperative recur-

rence rate

14,23,24

Fu et al.

found that under the guid-

ance of LUS, the hepatic vein can be located

accurately, which could avoid damage and

reduce the risk of postoperative bleeding.

Following the results of that study, it was found

that intraoperative blood loss and hepatic vein in-

jury rates during peri-surgery were lower than

those in the conventional surgery group.

However, other perioperative indicators (op-

erative time, drainage tube extubation time,

anal exhaust time, etc.) were not significa-

tively different, indicating that the addition

of ultrasound assistance during the opera-

Table 7

Comparison of survival and recurrence rates in the two groups of patients.

Group

Sample

number

Survival rate n (%) Recurrence rate n (%)

T1 T2 T3 T1 T2 T3

Study Group 38 37 (97.4) 37 (97.4) 35 (92.1) 0 (0.0) 1 (2.6) 2 (5.3)

Control Group 38 36 (94.7%) 35 (92.1) 28 (73.68) 1 (2.6) 2 (5.3) 7 (8.16)

4.57 5.029

p* 0.033 0.025

*p-value Chi-square (χ² tests).

Benefits of a modified precision hepatectomy with laparoscopic ultrasound 165

Vol. 65(2): 155 - 168, 2024

tion would not prolong the operation time,

which was in contrast with Lubner et al.

The Allaire et al.

study found that the

resection of liver tumors retained sufficient

residual liver volume to ensure the suffi-

cient compensatory capacity of postopera-

tive liver function, which is also the key to

enhancing the clinical prognosis. However,

in this study, the liver function standard in

the study group was notoriously higher than

in the control group. The reasons may be at-

tributable to the guidance of ultrasound. The

tumor and tumor liver vein branches were

cut down, achieving the purpose of accurate

resection, effective partition lesions of blood

flow, and reducing the remaining liver affect-

ed by blood flow reperfusion, thus reducing

the damage to liver function and retaining

more liver tissue with normal function.

In evaluating immune function indica-

tors in this study, the immune indicators of

the study group were higher than that of the

control group after seven days, indicating

that the precise resection resulted in less

loss of immune function for sufferers, and

the postoperative recovery was faster. Joliat

et al.

and Tayar et al.

confirmed in their

study that laparoscopic hepatectomy under

LUS caused less tissue damage than conven-

tional laparoscopic hepatectomy, produc-

ing less intraoperative bleeding, less post-

operative stress response and a relatively

mild degree of immunosuppression in post-

operative patients. The mechanism may be

that after the damage to the body, immune

cells will synthesize and secrete IL-6 and

TNF-α factors to regulate the related stress

conditions. Increasing IL-6 and TNF- α lev-

els will aggravate the body’s inflammatory

response and reduce the human body’s im-

mune capacity. CD3+ and CD4+ are indica-

tors of the reactive T cell levels; the lower

the levels, the more severely compromised

immune capacity. NK cells are also essential

cells involved in the immune response, to-

gether with CD3

and CD4

T-lymphocytes,

and similarly, the lower the levels, the worse

the decline in the immune function. By com-

paring the study and the control groups, the

study group’s IL-6 and TNF α concentrations

were lower than in the control. CD3

, CD4

and NK cells were higher than those in the

control group, indicating that laparoscopic

precision liver resection results in less im-

mune damage

28,29

Some studies have shown that the im-

mune function has a particular relation-

ship with postoperative complications, and

the less the postoperative immune function

damage, the lower the incidence of postop-

erative complications

30,31

. In this study, the

rate of postoperative complications in the

study group was lower than that in the con-

trol, and this result also reflects this rela-

tionship, which is consistent with the results

of Shazly’s et al.

studies. Comparing the

postoperative morbidity and survival rate of

both groups, they were higher in the control

group, possibly because the precise liver re-

section accomplished a complete resection

of liver tumors and avoided the occurrence

of tumor residues

. The higher indicators

of postoperative liver function show that the

study group can retain more normal liver tis-

sue, which is more beneficial for the patient’s

postoperative rehabilitation

, consistent

with the above scholars’ research results.

In conclusion, the modified laparo-

scopic precision liver resection can effec-

tively reduce the amount of intraoperative

bleeding, reduce the impairment of liver and

immune functions, reduce the incidence of

complications, and reduce the postopera-

tive recurrence rate of liver cancer, which

shows that it is worth generalizing the use of

this technique in clinical practice. Although

this study has obtained relatively important

results, it still needs to be improved to use

these research conclusions as the gold stan-

dard. For example, only 76 patients with

liver cancer were included in this study, and

the research results will inevitably be biased,

so the sample size should be expanded for

further demonstration.

166 Xu and Shen

Investigación Clínica 65(2): 2024

ACKNOWLEDGMENTS

We appreciate Dr Humberto Martínez’s

editing of this research paper.

Conflict of competence

The authors declare no conflict of interest.

Funding

None.

ORCID of the authors

• Yansong Xu: 0000-0002-1915-8014

• Lin Shen: 0000-0003-4192-2493

Contribution of authors

In the present study, both authors made

equal contributions and collaborated closely

throughout the research process.

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