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Early and late postoperative inflammatory and collagen deposition responses

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Early and late postoperative inflammatory
and collagen deposition responses in three
different meshes: an experimental study in
rats

C. G. Pereira-lucena, R. Artigiani Neto,

D. T. de Rezende, G. de J. Lopes-Filho,
D. Matos & M. M. Linhares

Hernia
The World Journal of Hernia and
Abdominal Wall Surgery

ISSN 1265-4906

Hernia
DOI 10.1007/s10029-013-1206-4

1 23
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1 23
 Author's personal copy
Hernia
DOI 10.1007/s10029-013-1206-4
ORIGINAL ARTICLE
Early and late postoperative inflammatory and collagen
deposition responses in three different meshes: an experimental
study in rats
C. G. Pereira-lucena • R. Artigiani Neto •
D. T. de Rezende • G. de J. Lopes-Filho •
D. Matos • M. M. Linhares
Received: 12 January 2013 / Accepted: 12 December 2013
 Springer-Verlag France 2013
Abstract
Purpose Although meshes reduce abdominal hernia
recurrence, they increase the risk of inflammatory com-
plications. This study aimed to compare the early and late
postoperative inflammation and collagen deposition
responses induced by three meshes.
Methods Rats were allocated into three groups. In group
I, a polypropylene (PP) mesh was implanted in the
abdominal wall. In groups II and III, PP ? polyglactin
(PP ? PG) and PP ? titanium (PP ? TI) meshes were
employed, respectively. On the seventh (7th) postoperative
day, collagen deposition and inflammation were evaluated,
and immunohistochemistry was performed on abdominal
wall biopsies. These data were compared with those
obtained on the fortieth (40th) postoperative day in a pre-
vious study.
Results The early inflammatory responses were the same
in all groups. With time, it decreased in group I
(p = 0.047) and increased in group II (p = 0.003). Group I
exhibited early elevated VEGF (p \ 0.001), COX2
(p \ 0.001), and collagen (p = 0.023) levels, and group II
exhibited the most severe inflammatory tissue response. On
the 40th postoperative day, the VEGF (p \ 0.001) and
C. G. Pereira-lucena  R. Artigiani Neto 
D. T. de Rezende  G. de J. Lopes-Filho  D. Matos 
M. M. Linhares
Pós-Graduação em Ciência Cirúrgica Interdisciplinar,
Universidade Federal de São Paulo, Rua Napoleão de Barros,
610-Vila Clementino, São Paulo, SP CEP 04024-002, Brazil
C. G. Pereira-lucena (&)
Rua Volney Loureiro Tavares, No. 27-bairro Inácio Barbosa,
Aracaju, SE CEP 49040-670, Brazil
e-mail: crisgama@bol.com.br
collagen (p \ 0.005) were reduced as compared with the
7th postoperative day in all groups.
Conclusions Belatedly, the inflammatory reaction
decreased in PP mesh group and increased in PP ? PG
mesh group. The PP mesh induced early great elevations in
VEGF, COX2 and collagen levels, whereas the PP ? PG
mesh caused severe tissue inflammation with small eleva-
tion in these levels. PP ? TI mesh induced inflammatory
response levels between the others. In conclusion, the
inflammatory response depends on the mesh density and
also the mesh material with clinical implications.
Keywords Hernia  Mesh  Inflammatory response 
Collagen  VEGF  COX2.INFLAMMATORY
Introduction
Cytokines are synthesized by injured tissue to modulate the
inflammatory cascade during the initial phase of repair in the
abdominal wall [1]. Cytokines are fundamental to cell pro-
liferation, the extracellular matrix, and collagen synthesis [2].
Meshes were developed due to the high rate of recur-
rence after hernia surgery with primary sutures, and mesh
application in abdominal wall repairs has reduced the
recurrence indexes from over 50 % to approximately 10 %,
particularly in ventral hernias [3]. Although meshes are the
most commonly used biomaterials in medical practice,
with approximately 1.5 million implants used per year [4],
numerous questions remain about the host inflammatory
response induced by mesh implants [3–10]. Despite the
frequent use of mesh implants, there remains no consensus
regarding their classification and nomenclature [11].
Polypropylene (PP) is the most commonly material
used to manufacture meshes, but other absorbable and
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non-absorbable materials are also used [11, 12]. Theo-
retically, the increased diameter of the pores and the
reduction in the density of meshes could minimize
inflammation and, therefore, the complications related
to this implant [8]. However, several studies have
reported conflicting results, including reports of the
reduction of early complications and reports of a pos-
sible increase in recurrences [13–18]. Unexpected
complications, such as the reduced sperm mobility in
response to lightweight mesh implanted in the inguinal
region [17] and mechanical failure with fracture of a
lightweight mesh in the surgical repair of a recurrent
median ventral hernia [18], have been reported.
Klinge et al. [11] evaluated the indications for explant-
ing mesh implants in 1,000 cases. Infection was the main
reason for removing small pore PP meshes, which were
prevalent in the reviewed data. Hernia recurrence was the
main reason for explanting large-pore meshes [11].
Pascual et al. [19] observed that an intense inflammatory
reaction was related to the presence of absorbable material;
additional characteristics include low expression of growth
factors, worse collagen deposition, and worse mesh inte-
gration in host tissue [19].
Some authors have studied mesh modified with a coat-
ing film or the use of various substances, including those
from hormonal sources, like aldosterone. Although these
authors shared the goals of reducing the formation of
adhesions or modulating the inflammatory process, e.g., the
action of mast cells, foreign body reactions, or fibrosis [12,
20–22], their results are varied.
In a previous study, we assessed the serum, inflam-
matory response, and collagen deposition in rats on the
40th postoperative day after mesh implantation, includ-
ing conventional PP, lightweight PP ? polyglactin
(PG ? PG), and lightweight PP ? titanium (PP ? TI).
Serum cytokines were similar in all groups. The heavy-
weight PP mesh belatedly induced the least inflammation
and improved collagen deposition. The PP ? PG mesh
was correlated with the most intense tissue inflammatory
response and low, irregular, and heterogeneous collagen
deposition. The PP ? TI mesh led to an intermediate
result [23].
The above results prompted further questions. The
results appear contradictory with respect to whether
collagen deposition depends on an inflammatory reac-
tion. PP mesh belatedly induces a subdued inflammatory
reaction but leads to greater collagen deposition, which
is in direct contrast with the results observed for the
PP ? PG mesh. Would it be possible to demonstrate a
more intense early tissue inflammatory response with PP
mesh? Could the kind of inflammatory reaction induced
by the PP ? PG mesh be the key factor for the belated
inhibition of collagen deposition? Could the differences
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be due to pro-inflammatory molecules present in the
host tissue, especially growth factors related to collagen
deposition that were not detected in the blood of
animals?
This study aimed to compare the early (7th postopera-
tive day) and late (40th postoperative day) inflammatory
tissue response (histological changes and immunohisto-
chemistry for inflammatory substances) and collagen
morphology in response to conventional PP, lightweight
PP ? PG, and lightweight PP ? TI meshes.
Methods
This research was an experimental study in which it was
employed an acute wound model, not a hernia model.
Thirty male adult Wistar rats weighing 250–300 g were
randomly allocated into groups I, II and III. Each group
comprised 10 animals. An intraperitoneal injection of 10 %
ketamine hydrochloride and 2 % xylazine solution was
applied for anesthesia.
After a 4-cm longitudinal incision was made along the
animal’s flank, a fragment of the anterior abdominal
musculature measuring 2 cm2 (2.0 9 1.0 cm) was
removed. The mesh was positioned to replace the defect
that had been produced and was fixed by six PP 3-0
switches sutures. In group I, the mesh was made of
heavyweight monofilament PP and had small pores (In-
tracorp, Venkuri, Brazil). In group II, the mesh contained
large pores and was made of lightweight PP and an
absorbable material, PG (VyproII, Ethicon, USA). In
group III, a large-pore lightweight mesh made of PP and a
nonabsorbable material, TI, was used (Timesh, GfE,
Germany).
Group I, the group in which the animals were implanted
with the most commonly used type of mesh [11], was
considered the control group.
On the 7th postoperative day, the rats were killed by
means of a lethal dose of ketamine. A fragment was
removed from the central region of the prosthesis as far as
possible from the mesh stitches. The tissue sample was sent
for a histological inflammatory response analysis, includ-
ing hematoxylin-eosin, Masson trichrome, and picrosirius
(under polarized light to assess collagen deposition), and
the immunohistochemical analysis of Vascular Endothelial
Growth Factor (VEGF-Dbs rabbit polyclonal antibody,
Santa Cruz Biotechnology, Inc.) and Cyclooxygenase 2
(COX2-rabbit polyclonal antibody, Spring Cold Spring
Harbor Laboratory, USA).
To objectively evaluate the tissue reaction and expres-
sion of VEGF and COX2, numeric scales were employed
[23–25], and the scoring scales are presented in Tables 1,
2.
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Table 1 Numeric scales to value tissue inflammatory response in
groups I (PP), II (PP ? PG) and (PP ? TI)
Points Legend
A: Cell layers at the margins of the granulomas
1 1–4 layers
2 5–9 layers
3 10–30 layers
4 [30 layers
B: Inflammatory reaction in the host tissue
1 Non-dense, mature fibrous tissue
2 Immature fibrous tissue with fibroblasts and little collagen
3 Dense granular tissue with fibroblasts and many
inflammatory cells
4 Mass of inflammatory cells with disorganized connective
tissue
C: Inflammatory response on the mesh surface
1 Fibroblasts without macrophages or foreign body cells
2 Isolated foci of macrophages or foreign body cells
3 One layer of macrophages and foreign body cells
4 Multiple layers of macrophages and foreign body cells
D: Tissue maturation
1 Dense, mature interstitial tissue, similar to normal connective
or adipose tissue
2 Interstitial tissue with blood vessels, fibroblasts, and a few
macrophages
3 Interstitial tissue with giant inflammatory cells but with
permeating connective tissue
4 Mass of inflammatory cells without permeating connective
tissue
Pixels corresponding to collagen were counted on a
microcomputer after image capture using Image Tool
software, version 3.0, according to the following steps:
• gray scale conversion;
• automatic threshold;
• image inversion for better viewing;
• automatic collagen pixels count by the computer
program.
These data were compared with previously obtained
data from our group using the same methodology on the
40th postoperative day [23].
For the statistical analyses of the histological and
immunohistochemistry scores, the nonparametric Kruskal–
Wallis test was used. For the morphometric analysis of the
collagen and the inflammatory score, a sum ANOVA was
used. To compare early and late postoperative results, the
Mann–Whitney (tissue response, VEGF, and COX2) and
student’s t (tissue response score sum and collagen) tests
were employed. Statistical calculations were performed
using the Statistical Package for the Social Sciences
(SPSS) 19.0 for Windows, R-Program 2.11.1.
Results
In this research, we studied some aspects of the host
response resulting from the implantation of three different
meshes (PP, PP and PP ? PG ? TI) in the abdominal wall
on early (7th PO) and late postoperative period (40th PO).
The obtained results are described below:
• Tissue inflammatory response: The early sum score of
histologic inflammation was quantitatively similar in all
groups (p = 0.509). But, compared with the 7th post-
operative day, the scores on the 40th postoperative day
were decreased in group I (PP) (p = 0.047) and
increased in group II (PP ? PG) (p = 0.003). In group
III (PP ? TI), the early and late inflammatory responses
were the same (p = 0.341). The results of the analyses
and the inflammatory parameters are shown in Fig. 1.
• Immunohistochemical expression of pro-inflammatory
substances: Group I exhibited early elevated expression
of VEGF (p \ 0.001) and COX2 (p \ 0.001), and group
II exhibited the lowest levels. On the 40th postoperative
day, VEGF decreased (p \ 0.001) in all groups, and
reductions in COX2 were observed only in group I
(p = 0.011). These data are presented in Figs. 2, 3 and 4.
• Collagen deposition: On the 7th postoperative day,
group I exhibited the best collagen deposition
(p = 0.023), while group II exhibited the worst. When
we compared the early and late samples, collagen
deposition decreased over time in all groups, but the
reduction was more intense and organized in group I.
Figures 5, 6 and 7 demonstrate this comparison.

Table 2 Numeric scales to value VEGF and COX2 imunohistochemistry expression in groups I (PP), II (PP ? PG) and (PP ? TI)
VEGF COX2
% cells Score Intensity Score % cells Score Intensity Score

0–25 1 Weak 1 0–25 1 Weak 1

26–50 2 Moderate 2 26–50 2 Moderate 2
51–75 3 Strong 3 51–100 3 Strong 3
76–100 4

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Fig. 1 Boxplot graph that demonstrates the sum
(S = A ? B ? C ? D) of the items related to inflammatory tissue
reaction on 7th and 40th postoperative days (PO) in groups I, II and
III, where A is the layer of cells on granulomas, B is the inflammatory
reaction in host tissue, C is the inflammatory response on the surface
of the mesh, D is the tissue maturation
Fig. 2 Boxplot graph that demonstrates VEGF imunohistochemistry
expression on 7th and 40th postoperative days (PO) in groups I (PP),
II (PP ? PG) and III (PP ? TI)
Discussion
The main reason for the subject and the design of this
research was our need to continue investigating the ques-
tions raised in our previous study, in which conventional
PP mesh placement unexpectedly and belatedly resulted in
less tissue inflammation and increased late collagen depo-
sition compared with PP ? PG and PP ? TI meshes.
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Fig. 3 Boxplot graph that demonstrates COX2 imunohistochemistry
expression on 7th and 40th postoperative days (PO) in groups I (PP),
II (PP ? PG) and III (PP ? TI)
The first phase of the healing process of the abdominal
wall (hemostasis ? inflammation) is indispensable for the
deposition of collagen and scar formation [2]. We won-
dered whether an early intense reaction, with the release of
pro-inflammatory cytokines, particularly growth factors,
could result in later collagen deposition resulting from PP
mesh.
We were also interested in exploring the effects of mesh
coated with an absorbable material on maintaining a for-
eign body-type inflammation, with granulomas formation
and reduced growth factors expression, potentially resulted
in less collagen deposition. Thus, we asked whether the
pore size, mesh density, or type of material affected the
intensity and characteristics of the inflammatory response.
Previous research demonstrated that PP can induce a fast
inflammatory reaction, especially in the early phase after
surgery [26]. Some authors have noted that PP mesh causes
an elevated short-term inflammatory reaction, resulting in
more discomfort for patients. However, in the long term,
various kinds of meshes exhibit similar behavior, and
higher rates of hernia recurrence have been reported with
lightweight mesh [6, 9, 11, 13, 14, 27]. Other studies,
however, have reported no differences in the inflammatory
response between various materials and have reported that
the mesh density is the most important factor affecting the
inflammatory response [5–8]. These diverse results could
be explained by the heterogeneity in the study designs and
the parameters studied.
In this research study, the results of the histological
analysis of inflammatory process were similar between the
groups on the 7th postoperative day. However, when we
compared the early and late postoperative periods, we
observed that, although there was no accentuation of the
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Fig. 4 Photomicrography (9100). Immunohistochemical analysis of COX2 (narrows) in groups I (PP), II (PP ? PG) and III (PP ? TI) on the
7th postoperative day. Observe mesh filaments (stars)
Fig. 5 Boxplot graph that demonstrates the score of the collagen
representative pixels on 7th and 40th postoperative days (PO) on
groups I (PP), II (PP ? PG) and III (PP ? TI)
inflammatory response over time in group III (PP ? TI), a
significant increase in the inflammatory response was
observed belatedly in group II (PP ? PG) (p = 0.003), as
shown in Figs. 1, 2, 3. These results suggest that the
absorbable material may be the key determinant in the
intensity of the inflammatory process in meshes made of
PG, similar to the results of Pascual et al. [19]. However,
the late inflammatory response in group I (PP) was smaller
Fig. 6 Photomicrgraphy (940). Picrosirius demonstrates collagen deposition (narrows) on the 7th postoperative day in groups I (PP), II
(PP ? PG) and III (PP ? TI). Observe mesh filaments (stars)
than the early response (p = 0.047), supporting the idea
that this material induced a rapid inflammatory reaction.
VEGF expression has been used previously to evaluate
the healing process after abdominal wall hernia surgery.
Some authors have reported increased expression of this
cytokine in response to PP meshes and lower expression in
response to meshes containing biodegradable material
(e.g., PG) [19]. Our results corroborate the findings
described above. In group I (PP), the average VEGF
immunohistochemistry score was elevated on the 7th
postoperative day with respect to the other groups
(p \ 0.001), and all animals in this group, except one,
exhibited the maximum assessment scores. Group III
(PP ? TI) exhibited intermediate scores, whereas group II
(PP ? PG) exhibited the lowest scores.
With respect to the late inflammatory response, all
groups exhibited reductions in the late VEGF score com-
pared with the earlier score. These results are compatible
with the results obtained by Di Vita et al. [26] in their study
of serum VEGF levels in humans. The authors observed
higher cytokine levels during the early postoperative period
in patients undergoing surgical repair of hernias of the
abdominal wall, which could explain the rapidity of the PP-
receiving host response. We believe that new researches
could clarify this response and other questions, including
the COX2 involvement in the tissue inflammatory response
caused by mesh use and abdominal wall healing.
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Fig. 7 Photomicrography (9400): Picrosirius demonstrates collagen
deposition (arrows) on 7th and 40th postoperative days (PO) in
groups I (PP), II (PP ? PG) and III (PP ? TI). Note the organized
collagen deposition in group I and irregular collagen deposition in
group II
Conflicting findings about collagen deposition in mesh
implants have been reported. Although some authors state
that there is increased collagen deposition in heavyweight
meshes, others claim the opposite [11, 26]. A recently
published study reports that PP meshes can result in a
higher density of collagen in the host scar tissue [28]. In the
current study, collagen reduction was observed in all
groups when we compared the evolution of the morphology
of collagen between the 7th and the 40th postoperative
days. However, on the 40th postoperative day, the collagen
deposition remained more intense and more organized in
response to PP mesh than for the other meshes (Fig. 6).
This amendment is consistent with some authors’
descriptions [2]. Vaz et al. [29] studied collagen deposition
in Wistar rats after PP mesh implantation. The authors’
results demonstrated that, on the 30th postoperative day,
type III collagen (immature) was replaced by type I col-
lagen (mature) [2, 29]. Thus, in this study, we chose the
40th postoperative day as the endpoint of the late evalua-
tion. Moreover, 40 days in a rat’s life correspond to 3 years
and 3 months in humans, which is sufficient time for the
scar remodeling process [30]. This experimental design
minimizes the differences between the host response after
mesh implantation in rats and humans but cannot avoid
them completely. To evaluate tissue inflammation induced
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by mesh implants over time, serial biopsies of the
abdominal wall would be necessary, which would be eth-
ically unacceptable. After experimental studies in animals,
new studies in humans could use other methods to analyze
abdominal wall healing, including computer tomography or
magnetic resonance.
Group II, which was characterized in the histological
studies by an intense inflammatory process, exhibited poor
expression of VEGF, which is a well-established important
inflammatory marker; this observation reinforces the
hypothesis that each mesh type induces a different reaction.
The observation that the mesh that induced lower VEGF
expression also induced less collagen deposition strength-
ens the probable relationship between this growth factor
and collagen. Our results strengthen the conclusions of
Pascual et al. [6], who reported that a material that stim-
ulates a foreign body-type reaction would, with the mini-
mal release of VEGF, result in a frail and disabled scar in
terms of collagen deposition. Further studies may shed
light on this topic.
To synthesize the basic characteristics exhibited by the
mesh studied in this research, we have observed the
following:
• The conventional mesh, made of heavyweight PP with
small pores, exhibited an intense initial tissue inflam-
matory reaction, strong expression of VEGF and
COX2, and increased collagen deposition. Over time,
there was a reduction in the inflammatory response, the
levels of VEGF and COX2, expression, and collagen
deposition. On the 40th postoperative day, collagen
fibers were grouped into organized bundles, and this
mesh exhibited the greatest collagen deposition among
the meshes studied.
• The lightweight mesh made of large pores consisting of
PP ? PG exhibited an intense initial inflammatory
reaction, predominantly of the foreign body type, with
the presence of abundant granulomas and giant cells.
Characteristically, faint VEGF and COX2 expression
and an erratic deposition of collagen were observed.
This reaction can be perpetuated, becomes even more
pronounced over time, and is likely related to the
presence of an absorbable material in the implant.
• The large pores and lightweight mesh made of PP and
covered with TI resulted in an intermediate histolog-
ically defined inflammatory response, intermediate
VEGF and COX2 expression, and intermediate colla-
gen deposition with respect to the other groups.
Although this mesh contains a an inert material that
is used in orthopedic and endovascular prosthesis, it led
to an early inflammatory reaction similar to other
meshes and long-term inflammation that was more
severe than that induced by the PP mesh.
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Therefore, we conclude the following:
• Although the early inflammatory response was the
same in all groups, the late inflammatory response was
elevated in the PP ? PG mesh group and decreased in
the PP mesh group.
• On the 7th postoperative day, the greatest COX2
expression occurred in PP mesh. However, on the 40th
postoperative day, it decreased in the PP mesh group
but not in the PP ? PG and PP ? TI mesh groups.
• The mesh that resulted in the highest early VEGF
expression (PP) resulted in better collagen deposition,
whereas the mesh that resulted in the lowest VEGF
expression (PP ? PG) resulted in the worse collagen
deposition.
• The mesh density, pore diameter, and material can
influence the host inflammatory response resulting from
its implantation in the abdominal wall, with clinical
implications for wall rigidity, foreign body reaction,
abscesses, and infection.
Acknowledgments This research was funded by Fundação de
Amparo à Pesquisa do Estado de São Paulo (FAPESP) and the Co-
ordenação de Aperfeiçoamento de Pessoal de Nı́vel Superior
(CAPES).
Conflict of interest The authors declare no conflict of interest.
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