Advances in Medical Sciences 63 (2018) 220–223

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Advances in Medical Sciences

journal homepage: www.elsevier.com/locate/advms

Original research article

TGF-b and inflammatory blood markers in prediction of

intraperitoneal adhesions
Kamil Torresa,* , Łukasz Pietrzyka,b , Zbigniew Plewab , Karolina Załuska-Patela ,
_
Mariusz Majewskia , Elzbieta Radzikowskac, Anna Torresd
a
Department of Didactics and Medical Simulation, Chair of Human Anatomy, Medical University of Lublin, Lublin, Poland
b
Department of General, Oncological and Minimally Invasive Surgery, 1st Military Clinical Hospital, Lublin, Poland
c
Department of Plastic Surgery, Central Clinical Hospital of Ministry of Interior, Warsaw, Poland
d
Chair and Department of Human Anatomy, Laboratory of Biostructure, Medical University of Lublin, Lublin, Poland

A R T I C L E I N F O A B S T R A C T

Article history: Purpose: Intraperitoneal adhesions (IA) develop as a consequence of the healing process in peritoneum
Received 7 May 2017 injured during surgeries. IA might be formed after all types of surgical interventions regardless the
Received in revised form 11 August 2017 surgical approach with a higher incidence in obese individuals. Here we determine the diagnostic power
Accepted 21 November 2017
of TGF-b and blood inflammatory parameters in the prediction of IA in obese patients undergoing second
Available online xxx
surgical intervention.
Materials and methods: Eighty patients were divided into groups according to body mass index (BMI)
Keywords:
values and presence of intraperitoneal adhesions (IA). Evaluation of peritoneal adhesion index (PAI),
Intraperitoneal adhesions
Obesity
serum TGF-b and blood inflammatory parameters was performed.
Transforming growth factor-b Results: Level of TGF-b, C-reactive protein (CRP), leukocytes, neutrophil to lymphocyte ratio and platelet
Neutrophil to lymphocyte ratio to lymphocyte ratio were significantly higher in obese patients while TGF-b, CRP, and leukocytes were
Platelet to lymphocyte ratio higher in patients with IA. There was a significant correlation between PAI values and TGF-b
concentration (p < 0.001; r = 0.869) in IA group.
Conclusions: The preoperative TGF-b concentration, BMI, CRP and NLR could be strong predictors of
intraperitoneal adhesions in patients with the history of surgeries.
© 2017 Medical University of Bialystok. Published by Elsevier B.V. All rights reserved.

1. Introduction cytokines transforming growth factor-b (TGF-b) has been

Intraperitoneal adhesions (IA) develop as a consequence of the
healing process in peritoneum injured during surgeries. IA might
be formed after all types of surgical interventions regardless the
surgical approach [1]. The presence of IA might lead to
perioperative as well as postoperative complication including
accidental abdominal viscera injuries, longer duration of surgery,
chronic abdominopelvic pain, intestinal obstruction, and infertility
[2,3].
Peritoneum repair involves a various process e.g. inflammation,
angiogenesis, cell migration and adhesion [4]. These interactions
are controlled by cytokines and growth factors secreted by
mesothelial cells and migrated macrophages [5]. Among many
* Corresponding author at: Department of Didactics and Medical Simulation,
Chair of Anatomy Medical University of Lublin, W.Chodzki street No 19,
Jaczewskiego 4, 20-094 Lublin, Poland.
E-mail address: kamiltorres@wp.pl (K. Torres).
documented to be associated with IA development [6]. Increased
secretion of TGF-b due to tissue injury alters the adhesive
properties of cells, expression of integrins, cytoskeletal proteins
and induces migration of fibroblasts [6,7].
IA development could be altered by excessive mass of adipose
tissue. Low-grade inflammation accompanies obesity. Increased
level of numerous inflammatory chemicals including, e.g. C-
reactive protein (CRP), interleukin-1 (IL-1), interleukin-6 (IL-1),
tumor necrosis factor-a (TNF-a), TGF-b, neutrophil to lymphocyte
ratio (NLR) and platelet to lymphocyte ratio (PLR), might stimulate
the formation IA [8–10].
The aim of the research is an evaluation of the inflammatory
markers: TGF-b, WBC, CRP, neutrophil to lymphocyte ratio and
platelet to lymphocyte ratio between obese and non-obese
patients with the history of abdominopelvic surgical intervention
who underwent elective surgeries. Additionally, we aim to assess
the diagnostic power of the preoperative value of TGF-b and
selected inflammatory blood parameters in the prediction of
intraperitoneal adhesions.

https://doi.org/10.1016/j.advms.2017.11.006
1896-1126/© 2017 Medical University of Bialystok. Published by Elsevier B.V. All rights reserved.
 K. Torres et al. / Advances in Medical Sciences 63 (2018) 220–223 221

2. Materials and methods
The study enrolled eighty patients admitted to the General,
Oncological and Minimally Invasive Surgery Department of the 1 st
Military Clinical Hospital in Lublin, Poland for scheduled laparo-
scopic cholecystectomy, laparoscopic sleeve gastrectomy, trans-
abdominal preperitoneal (TAPP) hernia repair or anterior
abdominal wall hernia repair (IPOM). The same team of surgeons
operated on all the patients. No complications were reported
during the surgeries, and no malignancies were reported in the
pathological examination of the removed gallbladders and
stomach. The patients included in the study had the history of
the abdominopelvic surgery: open or laparoscopic cholecystecto-
my (n = 10 and n = 32, respectively), laparoscopic inguinal hernia
repair (n = 9), open or laparoscopic appendectomy (n = 15 and
n = 24, respectively). Patients with symptoms of inflammation
(clinical or biochemical) at the hospital admission were excluded
from the study. Exclusion criteria also included acute cholecystitis
due to gallbladder stones, diabetes, connective tissue disorders,
varicose veins, and cigarette smoking. The presence of intraperi-
toneal adhesions was reported during the surgery and classified
according to Coccolini et al. [11]. Patients were informed about the
aim of the study and signed written consent forms before the
study. The Ethical Committee of the Medical University of Lublin in
Poland approved the study (decision no KE-0254/240/2008).
Blood samples were obtained before the surgery. The blood
serum was collected, and the level of TGF-b was determined using
ELISA kit. Demographics and laboratory values of blood tests were
extracted from the hospital medical database records. The
evaluation of blood parameters was performed within 1 h after
venipuncture. The hematological parameters evaluated in the
study: CRP, WBC, platelets, neutrophil, and lymphocyte were
measured by ABX Pentra XL 80 (Horiba Medical). Normal values for
studied blood parameters (according to our laboratory) ranged as
follows: CRP: 0.0–5.0 mg/l, platelets: 150–400  109/l, WBC: 4.0-
10.0  109/l, neutrophil: 2.0–8.0  109/l, and lymphocyte: 2.0–
4.8  109/l.
Patients were divided into groups according to (i) body mass
index (BMI) values and (ii) presence of intraperitoneal adhesions
(IA). First, BMI classification included two groups: non-obese
group (normal weight patients, BMI values less or equal 25 kg/m2)
consisted of 40 patients (male:female, M:F = 22:18) and obese
group (obese patients, with BMI values, equal or above 30 kg/m2)
consisted of 40 patients (M:F = 23:17). Second patients’ classifica-
tion included two groups: group IA consisted of 38 patients in
whom IA was reported, and group no-IA enrolled 42 patients
without IA.
Statistical analysis was performed using 16.0 SPSS software.
Differences between the study groups were accessed using Mann-
Whitney U test and correlations with Spearman’s test. Receiver-
operating characteristics (ROC) curve analysis was performed to
identify cut-off values of studied parameters. Differences of
p < 0.05 were considered to be significant.
3. Results
Forty obese and forty non-obese patients were enrolled in the
study. The demographics, serum concentration of TGF-b, and
laboratory blood parameters of two BMI groups are shown in
Table 1. The age and gender distribution did not differ significantly
between the studied groups.
The mean value of BMI, TGF-b, CPR, and WBC was significantly
higher in obese patients compared to the non-obese group.
Nevertheless, NLR and PLR were higher in obese than in the non-
obese patients, the difference was not significant.
IA adhesions were reported in 47.5% of the total patients’
population and were present statistically more often in the obese
than in the non-obese group (72.5% vs. 22,5%, respectively). The
mean peritoneal adhesion index (PAI) in IA group was 4.33  2.10
(min.–max. = 1.00–9.00). No statistically significant differences in
PAI were observed between obese and non-obese groups.
The number of patients with adhesions in nine regions of the
abdominopelvic cavity was presented in Table 2.
Total patients’ population was divided according to the
presence of IA (Table 3). The mean value of BMI, TGF-b, CPR,
and NLP was significantly higher in patients with IA in comparison
to non-IA patients group. The mean value of WBC and PLR did not
differ significantly between the studied groups.
ROC analysis was performed on parameters which show
significant difference when comparing IA and no IA groups. The
ideal cut-off value of BMI was 32.13 kg/m2 (AUC: 0.731, sensitivity:
61.1%, specificity: 84.2%). The cut-off value of CRP and NLR was
4.12 mg/l (AUC: 0.685, sensitivity: 65.9%, specificity: 73.3%) and
2.36 (AUC: 0.597, sensitivity: 54.7%, specificity 75.2%), respectively.
The cut-off value of TGF-b was 37637.15 as the (AUC: 0.769,
sensitivity: 72.2%, specificity: 68.4%).
Therefore, the patients with IA were divided into low and high
groups according to the cut-off values of BMI, TGF-b, CPR, and NLR
(Table 4). The mean value of PAI was significantly higher in high
compared to the low TGF-b group.
There was a significant correlation between PAI values and TGF-
b concentration (p < 0.001; r = 0.869) in IA group. No significant
correlations were observed between PAI value and BMI, WBC, CRP,
NLR, and PLR values.
4. Discussion
Numerous surgical procedures using minimally invasive
techniques are performed each day. Therefore preoperative
knowledge of IA presence would be essential and might limit
the ratio of complication or procedure conversions from laparo-
scopic into open technique [12–14]. Although few studies have
attempted to evaluate the occurrence of potential difficulties
preoperatively using ultrasonography (US) still there is a need to
discover biomarkers for predicting e.g. intraperitoneal adhesions
prior the surgical intervention [15,16].
According to our best knowledge, our study is probably the first
attempting to evaluate diagnostic power of body mass index and
inflammatory blood parameters values as potential biomarkers of
intraperitoneal adhesions in patients undergoing surgeries. We
evaluated the correlation between body mass index, TGF-b, four
routinely measured hematological parameters and the occurrence
of IA.
Table 1
Demographics, values of TGF-b, and blood parameters of the study groups
according to the BMI value.
Obese group (n = 40) Non-obese group (n = 40) P-value
Age (years) 63.57  7.92 61.24  9.34 0.511
Gender (M:F) 22:18 23:17 0.408
BMI (kg/m2) 34.54  3,46 22.70  1.84 <0.001
IA (n) 29 9 0.039
TGF-b 46387.39  17571.59 32888.23  15520.15 0.017
CRP (mg/l) 5.88  1.91 3.23  0.74 0.033
WBC (x 109/l) 7.22  2.30 5.85  1.56 0.013
NLR 2.28  1.01 2.17  0.82 0.096
PLR 145.75  46.93 139.12  38.46 0.109
Age, BMI, TGF-b and laboratory values of blood parameters are expressed as
mean  SD.
BMI: body mass index, IA: intraperitoneal adhesions; TGF-b: transforming growth
factor-b, CRP: C-reactive protein, WBC: white blood cell, NLR: neutrophil to
lymphocyte ratio, PLR: platelet to lymphocyte ratio.
222 K. Torres et al. / Advances in Medical Sciences 63 (2018) 220–223

Table 2
Number of patients with intraperitoneal adhesions in nine regions of the abdominopelvic cavity. Classification according to Coccolini et al. [11].

A – Right upper region B - Epigastrium C – Left upper region

9 0 3 2 0 0

H – Right flank I – Central region D – Left flank

1 2 14 5 0 0

G – Right lower region F - Pelvis E – Left lower region

12 7 2 1 4 5

White area obese group, gray area non-obese group.

Table 3
Values of BMI, TGF-b, and blood parameters of the study groups according to the
presence of intraperitoneal adhesions.
IA group (n = 38) No IA group (n = 42)
BMI (kg/m2) 32.24  5.79 27.73  6.57
TGF-b 49046.97  17350.02 33210.56  14992.54
CRP (mg/l) 5.45  1.89 3.87  1.02
WBC (x 109/l) 6.36  1.90 6.97  2.32
NLR 3.41  1.42 2.21  0.87
PLR 151.46  51.84 142.35  39.98
BMI, TGF-b and laboratory values of blood parameters are expressed as mean  SD.
IA: intraperitoneal adhesions, BMI: body mass index, TGF-b: transforming growth
factor-b, CRP: C-reactive protein, WBC: white blood cell, NLR: neutrophil to
lymphocyte ratio, PLR: platelet to lymphocyte ratio.
In our study, IA adhesions were reported significantly more
often in obese than in normal-weighted patients. This observation
could be explained by the metabolic potential of adipose tissue.
Current reports suggest the obesity-related low-grade inflamma-
tion results from deregulation of the immune activity in both
subcutaneous and visceral adipose tissue deposits [10,17]. Adipose
tissue secretes locally numerous proinflammatory cytokines such
as TNF-a, TGF-b, IL-6 into the peritoneal cavity and is infiltrated by
macrophages, leukocytes, neutrophils, and eosinophils [18,19].
Activated neutrophils and macrophages lead to oxidative stress in
mesothelium and initiate formation of fibrous adhesions [20].
Observed in our study higher levels of inflammatory hematological
parameters: WBC, NLR, PLR, and markers: CPR and TGF-b in obese
in comparison to non-obese patients seemed to support the thesis
of the contribution of inflammatory mechanism in IA develop-
ment.
C-reactive protein (CRP) is an acute-phase systemic inflamma-
tory marker oversecreted in response to tissue injury. CRP is a
player in chemotaxis, proliferation of immune cells and activation
of cytokines production [21]. Ellulu et al. [22] documented higher
concentration of CRP in obese individuals. Moreover, BMI has been
reported to have a positive correlation with CRP levels irrespective
of ethnicity or gender difference [23]. These facts are supported by
our results, which showed higher levels of CRP in obese than non-
obese patients as well as in patients with IA adhesions. Association
between BMI and increased CRP level could be explained by liver
activation of CRP production by higher inflammatory mediators
P-value
secreted by the excessive mass of adipose tissue [24].
0.033 Transforming growth factor-b (TGF-b) is a cytokine involved in
0.004
chemotaxis, mitogenesis, and angiogenesis [25]. TGF-b signalling
0.037
0.675
pathways have been reported to have an association with
0.042 metastatic processes and increased aggressiveness of pancreas,
0.212 colon, stomach, breast, and lung tumors [26,27]. TGF-b induces
production of collagen, fibronectin, and integrins. TGF-b is
considered to participate in wound-healing processes and forma-
tion of adhesions by activation of PAI-1 peritoneal secretion that is
an inhibitor of fibrinolysis and stimulant of IA formation [6,28].
Wang et al. [29] observed two postoperative peak time points at 2
and 72–96 h of TGF-b1 concentrations in the peritoneal drainage
fluid after surgery from patients and rodent models. Moreover,
TGF-b1 neutralization in 72–96 h after surgery observed a
significant reduction of the adhesions’ degree. These data have
proved direct involvement of TGF-b in the development of IA and
are in agreement with our results which showed the significantly
higher preoperative concentration of TGF-b in patients in whom
IAs were reported, compared to patients without IA.
The other inflammatory markers evaluated in our study in
obese patients are neutrophil to lymphocyte ratio (NLR) and
platelet to lymphocyte ratio (PLR). These biomarkers mirror
inflammatory processes and are noticed to be elevated in patients
with myocardial infarction, urogenital and digestive system cancer
[30–32]. However, the nature of NLR and PLR in obesity is
controversial. Furuncuog lu et al. [33] did not observe the
correlation between BMI and NLR and PLR. Our results are in
agreement with the findings of Furuncuog lu et al. [33] and Bahadır
et al. [34] who did not find significant differences in NLR in
different body mass index groups. We also did not observe
significant differences in NLR and PLR levels between obese and
non-obese patients. The lack of this association is because obesity
causes an increase in both neutrophil and lymphocyte counts. We
documented the higher level of NLR in patients with IA compared

Table 4
Peritoneal adhesion index (PAI) grouped by BMI, TGF-b, CRP, and NLR.

BMI TGF-b CRP NLR

<32.13 32.13 <37637.15 37637.15 <4.12 4.12 <2.36 2.36

PAI 4.00  1,77 4.40  2.41 2.60  0.89 4.85  2.11 3.89  1.24 4.14  2.02 3,65  0.91 3.99  1.20
p-value 0.61 0.022 0.51 0.46

Values of PAI, BMI, TGF-b, CPR, and NLR are expressed as mean  SD.
PAI: peritoneal adhesion index; BMI: body mass index; TGF-b: transforming growth factor-b, CRP: C-reactive protein; NLR: neutrophil to lymphocyte ratio.
 K. Torres et al. / Advances in Medical Sciences 63 (2018) 220–223
to patients without IA what could be the result of inflammation
component in IA formation. However, data concerning NLR as a
biomarker of inflammation occurring in obesity are controversial
and suggest NLR should not be considered as a reliable indicator of
inflammation [34].
5. Conclusions
Our results showed that preoperative TGF-b concentration,
BMI, CRP and NLR could be strong predictors of intraperitoneal
adhesions in patients with the history of surgeries. Further studies
should include larger population to confirm the importance and
diagnostic value of blood parameters in the prediction of
intraperitoneal adhesions occurrence.
Conflict of interest
The authors declare no conflict of interests.
Financial disclosure
This work was supported by the grant of Medical University of
Lublin (grant # DS205).
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