Am J Transl Res 2021;13(11):12843-12851

www.ajtr.org /ISSN:1943-8141/AJTR0137596

Original Article
Clinical efficacy of thoracoscopic surgery by
subxiphoid approach for thymoma and its
influence on intraoperative blood loss
and postoperative complications
Peng Shen1, Quan Chen2, Fengwei Zhu3, Shouqi Tang3, Xuxian Zhang1, Feng Li2

Departments of 1Chest Surgery, 2Oncology, 3General Surgery, Dongping Hospital Affiliated to Shandong First Medi-
cal University, Dongping 271500, Shandong, China
Received July 22, 2021; Accepted September 27, 2021; Epub November 15, 2021; Published November 30,
2021

Abstract: Objective: To evaluate the clinical efficacy of thoracoscopic surgery by subxiphoid approach for patients
with thymoma and its influence on intraoperative blood loss and postoperative complications. Methods: From Janu-
ary 2019 to January 2020, 90 patients who underwent thoracoscopic surgery were enrolled and evenly divided into
a control group receiving surgery by lateral thoracic approach and an experimental group adopting the subxiphoid
approach according to different surgical approaches, and their clinical data were retrospectively analyzed. The clini-
cal efficacy, perioperative indexes, postoperative complications, pulmonary function, and inflammatory factors were
compared between the two groups. Generic Quality of Life Inventory-74 (GQOLI-74) was used to assess the quality
of life of the patients before and after surgery, and Mini-Mental State Examination (MMSE) was used to assess their
mental state. The Numerical Rating Scale (NRS) was used to evaluate the postoperative pain of the two groups.
Results: After treatment, the total clinical effectiveness rate of the experimental group was significantly higher than
that of the control group (P<0.05). The experimental group obtained superior results in perioperative index and
fewer postoperative complications compared with the control group (P<0.05). Better performance of FEV1 and FVC
was observed in the experimental group than the control group (P<0.05). The experimental group had significantly
higher postoperative GQOLI-74 scores (P<0.001) and MMSE scores (P<0.05) than the control group. Lower levels of
C-reactive protein (CRP), and tumor necrosis factor-α (TNF-α), and lower NRS scores at 12 h and 24 h after surgery
were witnessed in the experimental group compared to the control group (P<0.05). Conclusion: For patients with
thymoma, the thoracoscopic surgery by subxiphoid approach is safe and effective, and can reduce the intraopera-
tive blood loss and postoperative complications.

Keywords: Subxiphoid approach, thymoma, clinical efficacy, postoperative complications

Introduction In light of these, early diagnosis and treatment

of thymoma are of paramount significance.
Thymoma is a common thoracic disease, to Surgical treatment is the main treatment for
which the middle-aged and elderly population patients with confirmed thymoma, in which tra-
are most susceptible. It stems from pathologi- ditional open chest surgery is the mainstay.
cal changes in thymic lymph nodes or thymic However, it has been criticized for major surgi-
epithelial cells [1, 2], accounting for about cal trauma, massive blood loss, and pain. With
19-42% of mediastinal tumors. Generally, its the advancement of medical technology, thora-
symptoms are nonspecific in the early stage, coscopic surgery by subxiphoid approach has
while symptoms such as cough, swollen arms received increasing attention owing to its fea-
and dull pain in the chest may emerge with the tures of minor trauma, minimal blood loss,
advancement of the stage [3-5]. Delayed treat- shorter hospital stay, and superior clinical effi-
ment may give rise to complications such as cacy [6-8]. In order to investigate the clinical
aplastic anemia and myasthenia gravis (MG), efficacy of thoracoscopic surgery by subxiphoid
which can be life-threatening in severe cases. approach for patients with thymoma, and its
 Thoracoscopic surgery by subxiphoid approach for thymoma

effects on intraoperative blood loss and post- incision was made between the anterior axillary
operative complications, we performed a retro- line and midaxillary line at the 6th or 7th inter-
spective study on 90 patients who underwent costal space, followed by the insertion of a 10
thoracoscopic surgery from January 2019 to mm trocar through the 1 cm incision where a
January 2020 in our hospital. The innovation of 30° thoracoscope was placed. Then another
this research lies in the comparison of the over- incision was made at the anterior axillary line
all curative effect of patients with different at the 3rd or 4th intercostal space as an oper-
approaches of thoracoscopic surgery by com- ating port with a diameter of about 3-4 cm. The
paring their lung function, quality of life, and protective case was placed in the operating
immune factors. hole, the healthy side was ventilated with one
lung, and an ultrasonic knife was used to sepa-
General information rate the adhesions. Simultaneously, the two
ends of the nourishing blood vessel were
From January 2019 to January 2020, 90 clipped with a titanium clip and cut off. The
patients who underwent thoracoscopic surgery thymus, tumor, and fatty tissue at the cardio-
were enrolled and evenly divided into a control phrenic angle were also completely resected
group and an experimental group according to [9, 10]. The incision was then sutured after the
different surgical approaches, and their clinical placement of a drainage tube at the observa-
data were retrospectively studied. Of the 90 tion port.
patients, there were 44 males and 46 fe-
males, aged 61-72 years old, and 27 cases had In the experimental group, thoracoscopic sur-
coexistent MG. In terms of WHO pathology type, gery was performed by subxiphoid approach.
there were 27 cases of Type A, 29 cases of The procedures were as follows. With the
Type AB, and 34 cases of Type B. With regard to patient at a supine position with legs apart,
the clinical stage, 43 cases were in Stage I, and general anesthesia was performed, followed by
47 cases were in Stage II. 46 cases had a his- placement of a single lumen endotracheal
tory of drinking, and 41 cases had a history of tube. Then a 2 cm subxiphoid vertical incision
smoking. This study was approved by the hospi- was made at the midline of rectus abdominis as
tal ethics committee (2018-12-15). an observational port, and 1.5 cm subcostal
incisions were made at the midclavicular line
Inclusion criteria bilaterally as operating ports. Carbon dioxide
was injected uninterruptedly into the thoracic
(1) Patients aged under 80 years old; (2) cavity on the operated side through a pressure
Patients with retrosternal pain, wheezing, dia- of 6~8 cm H2O, and the primary and secondary
phragmatic paralysis, hoarseness, and superi- operating holes were made at the intersection
or vena cava obstruction syndrome; There were of the midclavicular line and the rib arch bilater-
epithelial and immature small T lymphocytes; ally, with the two holes close to the rib arch.
the lobules were unclear, and the fibrous sepa- Based on the direction of the sternal angle pro-
ration was not obvious; Confirmed with thymo- jection, an ultrasonic knife and non-invasive
ma; (3) Patients at Masaoka clinical stage of I forceps were used to separate the thymic tis-
or II [9]. sue in the patient’s mediastinal cavity and to
control the scope of operation. The connective
Exclusion criteria tissue behind the xiphoid was separated, an
artificial pneumothorax was established in
(1) Patients with a history of pleuritis; (2) wake of the building of the sternal tunnel. An
Patients with contraindications to surgery; (3) ultrasonic knife was used to cut through the
Patients with kidney or liver disease. mediastinal pleura, to identify and protect the
phrenic nerve along the pulmonary hilum. After
Methods thymus dissection, the innominate vein was
completely exposed, which was then traced
In the control group, thoracoscopic surgery was and ligated while identifying the thymic artery
performed by lateral thoracic approach. Each and vein. Dissection was performed up to the
patient was given general anesthesia on a lat- superior pole of the thymus gland. After remov-
eral position at 30°-45° angle, with upper al of thymoma and thymic tissue and dissec-
extremities fixed. The operation side was se- tion of mediastinal adipose tissue, the speci-
lected according to preoperative imaging. An men was collected from the subxiphoid inci-

12844 Am J Transl Res 2021;13(11):12843-12851

 Thoracoscopic surgery by subxiphoid approach for thymoma

sion. The incision was then sutured after the Mini-Mental State Examination (MMSE) [13]
placement of a drainage tube at the observa- Scale was used to evaluate the mental state of
tion port [11]. patients during surgery. The total score is 30
points, and a higher score indicates a better
Outcome measures mental state of the patient.

Clinical efficacy: The treatment was defined to Numerical Rating Scale (NRS) [14] was used to
be markedly effective if the clinical symptoms assess the pain after surgery. The scale runs
disappeared and the patient could work nor- between 0 and 10 points, with 0 points for no
mally without receiving drug medication; it was pain, 1-3 for mild pain, 4-6 for moderate pain,
defined to be effective if the dosage was and 7-10 for severe pain. Pain levels at 6 h, 12
reduced and an increase of weight was ob- h, and 24 h after surgery were labeled as T0,
served; it was defined to be ineffective if the T1, and T2, respectively, and compared.
patient’s clinical symptoms were not alleviated
Statistical analyses
or even worsened. Total effective rate = the
rate of patients with markedly effective treat- The data were analyzed using SPSS18.0 statis-
ment + that of patients with effective treat- tical software. The measurement data were
ment. expressed as mean ± standard deviation (SD),
and t-test was used for comparison between
Perioperative indexes: Operating time, intraop- two groups; Paired t test was used for intra-
erative blood loss, postoperative drainage, and group comparison; when multiple time points
hospital stay were compared between the two were compared, the corrected P value was
groups. used (P<0.05/3); the count data were ex-
pressed as [n (%)], and χ2 test was used for
Postoperative complications: Pulmonary infec- comparison between groups. The difference
tions, wound liquefaction, and arrhythmia were was considered significant if P<0.05.
compared between the two groups.
Results
Pulmonary functions: Forced expiratory volume
in one second (FEV1) and forced vital capacity Comparison of clinical information
(FVC) of the two groups before and after sur-
gery were collected and analyzed. The clinical information demonstrated that the
general information of the patients was similar
Fasting venous blood samples in the morning between the two groups in terms of age, gen-
were collected and centrifuged to isolate serum der, body mass index (BMI), clinical stage, maxi-
and then the supernatant was obtained. All mal tumor size, WHO pathology type, smoking
serum samples were placed at -80°C, and the or drinking history (all P>0.05). See Table 1.
levels of C-reactive protein (CRP) (kit lot num-
ber: HY-E3648) and tumor necrosis factor-α Comparison of clinical efficacy between the
(TNF-α) (kit lot number: HY-E3145) were ana- two groups
lyzed with corresponding ELISA kits purchased
To assess the clinical efficacy, we recorded the
from Shanghai Hengyuan Biotech Company.
significantly effective, effective, and ineffective
All procedures were conducted in strict accor-
cases respectively in the two groups. Then, we
dance with protocols.
observed that the total clinical effective rate
Generic Quality of Life Inventory-74 (GQOLI-74) after treatment in the experimental group was
Rating Scale [12] was used to evaluate the significantly higher than that in the control
group (P<0.05). See Table 2.
quality of life of the two groups of patients
before and after surgery. It was scored from Comparison of perioperative indexes
four dimensions including mental function,
physical function, social function, and material To observe the perioperative condition, we
life status, with the total score of 100 points. compared the perioperative indexes between
The score is positively correlated with the qual- the two groups using t-test. Perioperative in-
ity of life of the patient. dexes showed superior results in the experi-

12845 Am J Transl Res 2021;13(11):12843-12851

 Thoracoscopic surgery by subxiphoid approach for thymoma

Table 1. Clinical Information [n (%)] Comparison of GQOLI-74 scores

Experimental Control Group between the two groups
x2 or t P
Group (n=45) (n=45)
The postoperative GQOLI-74 score
Age (years) 65.21±1.23 65.23±1.22 0.077 0.938
of the experimental group was
Gender 0.178 0.673
significantly higher than that of
Male 23 (51.11) 21 (46.67) the control group (P<0.05), indi-
Female 22 (48.89) 24 (53.33) cating a more robust quality of
BMI (kg/m2) 25.37±1.59 25.42±1.61 0.148 0.883 life in the experimental group, as
Clinical Stage shown in Figure 2.
Stage I 22 (48.89) 21 (56.67)
Comparison of MMSE scores
Stage II 23 (51.11) 24 (53.33)
between the two groups
Maximal Tumor Size 4.05±1.41 4.11±1.35 0.206 0.837
WHO Pathology Type The postoperative MMSE score of
Type A 9 (20.00) 10 (22.22) 0.067 0.796 the experimental group was sig-
Type AB 10 (22.22) 11 (24.44) 0.062 0.803 nificantly higher than that of the
Type B 13 (28.89) 11 (24.44) 0.227 0.634 control group (P<0.05), demon-
Coexistent MG 14 (31.11) 13 (28.89) 0.053 0.818 strating an excellent mental sta-
Smoking 0.045 0.832
te of the experimental group, as
shown in Figure 3.
Yes 20 (44.44) 21 (46.67)
No 25 (55.56) 24 (53.33) Comparison of NRS score
Drinking 0.178 0.673
Yes 22 (48.89) 24 (53.33) The experimental group showed a
No 23 (51.11) 21 (46.67) markedly lower NRS score at 12 h
and 24 h after operation than the
control group (P<0.05), suggest-
mental group as compared to the control group ing that patients in the experimental group
(P<0.05). See Table 3. experienced less pain. See Figure 4.

Comparison of postoperative complications Discussion

To evaluate the complications, we made a com- Currently, surgery is the mainstay for thymo-
parison between the two groups regarding mas, and the thoroughness of resection re-
postoperative complications. The comparison mains the key factor influencing patients’ sur-
results showed that the experimental group vival [13, 14]. Traditional median sternotomy
had lower complication rates after surgery than with open chest surgery is the gold standard for
the control group (P<0.05). See Table 4. treatment. However, due to its disadvantages
of major surgical trauma, tremendous blood
Comparison of lung function indexes between loss, and high risk for complications, its appli-
the two groups cation has been considerably restricted. With
the advancement in medical technology, thora-
Table 5 shows better postoperative lung func- coscopic surgery has captured increasing at-
tion indexes in the experimental group as com- tention due to its minimally-invasive and less
pared to the control group (P<0.05). traumatic features and significant clinical ben-
efits. Lateral thoracic approach was extensively
Comparison of CRP and TNF-α level used in prior surgical practice, which, however,
has been criticized for its unsatisfying outcome
The level of CRP was significantly lower in the that may give rise to intercostal nerve injury
experimental group in contrast to the control and other postoperative complications [15-17].
group (P<0.05, Figure 1A). The experimental Prior research pointed out that compared wi-
group exhibited a lower level of TNF-α than the th the transthoracic approach, the subxiphoid
control group (P<0.05, Figure 1B). approach can simultaneously expose the rela-

12846 Am J Transl Res 2021;13(11):12843-12851

 Thoracoscopic surgery by subxiphoid approach for thymoma

Table 2. Comparison of clinical efficacy between the two groups [n (%)]

Groups n Markedly effective Effective Ineffective Total effective rate
Experimental Group 45 66.67% (30/45) 31.11% (14/45) 2.22% (1/45) 97.78% (44/45)
Control Group 45 46.67% (21/45) 26.67% (12/45) 26.67% (12/45) 73.33% (33/45)
x2 10.879
P 0.001

_
Table 3. Comparison of perioperative indexes ( x ±s)
Operation Time Intraoperative Blood Postoperative Drainage Hospital Stay
Groups n
(min) Loss (mL) (mL) (d)
Experimental Group 45 89.24±10.53 46.21±8.98 171.22±43.28 3.25±1.11
Control Group 45 145.25±13.75 59.47±11.12 231.82±44.37 5.29±1.38
t 21.695 6.223 6.559 7.727
P 0.001 0.002 0.001 0.002

Table 4. Comparison of postoperative complications [n (%)]

Groups n Pulmonary Infections Wound Liquefaction Arrhythmia Total Rates
Experimental Group 45 0.00% (0/45) 2.22% (1/45) 0.00% (0/45) 2.22% (1/45)
Control Group 45 6.67% (3/45) 6.67% (3/45) 0.00% (0/45) 13.33% (6/45)
x2 3.873
P 0.049

Table 5. Comparison of lung function indexes between the two groups (x±s)
FEV1 (%) FVC (L)
Groups n
Before surgery After surgery Before surgery After surgery
Experimental Group 45 32.29±2.65 65.95±0.67 3.11±0.32 4.15±0.41
Control Group 45 32.32±157 60.55±0.32 3.12±0.29 3.52±0.31
t 0.233 3.614 0.155 8.222
P 0.817 0.001 0.877 0.001

_
Figure 1. Comparison of CRP and TNF-α levels ( x ±s). Note: A. The abscissa indicates Before and after operation from
left to right, and the ordinate indicates the CRP level, mg/L; In the experimental group, the CRP levels before and
after operation were (5.66±2.81) mg/L and (33.21±8.21) mg/L, respectively; In the control group, the CRP levels
before and after operation were (5.81±2.75) mg/L and (46.78±13.25) mg/L, respectively; There was a significant
difference in the CRP level before and after operation in the experimental group (t=21.298, *P<0.05); There was a
significant difference in the CRP level before and after operation in the control group (t=20.309, **P<0.01); There
was a significant difference in the postoperative CRP level between the two groups (t=5.840, *P=0.001). B. The

12847 Am J Transl Res 2021;13(11):12843-12851

 Thoracoscopic surgery by subxiphoid approach for thymoma

abscissa indicates before and after operation from left to right, and the ordinate indicates the TNF-α level, ng/mL;
In the experimental group, the TNF-α levels before and after operation were (0.65±0.44) ng/mL and (1.12±0.85)
ng/mL, respectively; In the control group, the TNF-α levels before and after operation were (0.68±0.42) ng/mL and
(1.65±0.48) ng/mL, respectively; There was a significant difference in the TNF-α level before and after operation in
the experimental group (t=3.294, *P=0.001); There was a significant difference in the TNF-α level before and after
operation in the control group (t=10.202, **P<0.01); There was a significant difference in the postoperative TNF-α
level between the two groups (t=3.642, *P=0.001).

Figure 3. Comparison
_ of MMSE scores between the
Figure 2. Comparison of GQOLI-74 scores between two groups ( x ±s). Note: The abscissa represents
_ before and after operation from left to right, and the
the two groups ( x ±s). Note: The abscissa represents
before and after operation from left to right, and the ordinate represents MMSE score, points; The MMSE
ordinate represents GQOLI-74 score, points; The scores of the experimental group before and after
GQOLI-74 scores of the experimental group before surgery were (7.92±2.55) points and (21.26±4.32)
and after surgery were (46.52±7.62) points and points, respectively; The MMSE scores of the control
(81.27±5.23) points, respectively; The GQOLI-74 group before and after surgery were (7.85±2.78)
scores of the control group before and after surgery points and (14.22±3.21) points, respectively; There
were (47.11±7.38) points and (63.25±4.26) points, was a significant difference in the MMSE score of
respectively; The GQOLI-74 scores of the experimen- patients in the experimental group before and after
tal group before and after surgery were significantly surgery (t=17.839, *P<0.05); There was a significant
different (t=25.223, *P<0.05); There was a signifi- difference in the MMSE scores of patients in the
cant difference in the GQOLI-74 scores of patients in control group before and after surgery (t=10.063,
the control group before and after surgery (t=12.706,
**
P<0.01); There was a significant difference in the
**
P<0.01); There was a significant difference in the MMSE scores of the two groups of patients after sur-
GQOLI-74 scores between the two groups of patients gery (t=8.775, **P<0.01).
after surgery (t=17.921, **P<0.01).
mus from the posterior sternal space serves to
tionship between the surrounding large veins increase the thymus activity. For dissociating
and the anterior mediastinum, reduce the the upper pole of the thymus, the lower part of
intractable pain to the intercostal nerves, and the thymus can be dissociated first, and then
ensure safer dissection of bilateral adipose tis- distracted downward. Moreover, the tissue
sue and complete tumor removal [18, 19]. In around the upper pole was incised with an
our study, the experimental group outper- ultrasonic knife, and the upper pole of the thy-
formed the control group in terms of both peri- mus was completely stripped by blunt pushing
operative indexes and postoperative complica- and peeling. Reasonable use of an ultrasonic
tions (both P<0.05), suggesting that thoracos- scalpel for sharp separation and hemostasis
copic surgery by subxiphoid approach could during the operation can reduce the amount of
decrease the risk of blood loss and postopera- intraoperative blood loss and achieve “blood-
tive complications. In terms of the subxiphoid free surgical field”. The disadvantages of sub-
approach, the separation of the patient’s thy- xiphoid approach are as follows. First, there

12848 Am J Transl Res 2021;13(11):12843-12851

 Thoracoscopic surgery by subxiphoid approach for thymoma

able recovery in patients with thymoma. In

addition, the FEV1 and FVC also showed more
satisfying results in the experimental group
compared to the control group, which was in
agreement with the results from Yano et al. [25]
who revealed that postoperative FEV1 and FVC
were (2.85±0.42)% and (4.13±0.35) L respec-
tively in the observation group, significantly
higher than those of the control group. Taken
together, the thoracoscopic surgery by subxi-
phoid approach contributes to better pulmo-
nary outcome, less pain, and rapid recovery.
_
Figure 4. Comparison of NRS score ( x ±s). Note: The The limitation of this study was that there was
abscissa indicates time intervals T0, T1, and T2 from no long-term follow-up trial with a large sample
left to right, and the ordinate indicates NRS score, size, and the data obtained are biased. In the
points; In the experimental group, NRS scores at
future, the sample size will be expanded, ran-
T0, T1, and T2 were (8.77±1.12), (4.31±0.48) and
(1.09±0.18) points, respectively; In the control group, domized controlled trials will be conducted,
NRS scores at T0, T1, and T2 were (8.83±1.08), and multi-factor analysis will be performed to
(6.56±0.75) and (4.23±0.54) points, respectively; determine the factors that affect the progno-
There was a significant difference in NRS score at sis.
T1 between the two groups (t=16.950, *P=0.017);
There was a significant difference in NRS score at T2
between the two groups (t=37.005, *P=0.017). In conclusion, the thoracoscopic surgery by
subxiphoid approach can reduce intraoperative
blood loss, shorten hospital stay, and diminish
could be interference during instrumentation postoperative complication rates.
procedures and dissection of fat tissue around
the cardiophrenic angle. Second, the operation Disclosure of conflict of interest
is challenged by limited operating field [20, 21].
Last but not least, surgeons should be alert None.
that 1-3 branches would return back to left
Address correspondence to: Feng Li, Department
innominate vein when dealing with thymic
of Oncology, Dongping Hospital Affiliated to
veins, for which ultrasonic ligation should be
Shandong First Medical University, 18 Dongshan
performed. In this study, patients who received
Road, Dongping 271500, Shandong, China. Tel:
surgery by the subxiphoid approach were in a
+86-13704856214; E-mail: lifeng2021324@163.
supine position, which requires no position
com
change. In addition, single lumen endotracheal
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