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Year : 2020  |  Volume : 3  |  Issue : 4  |  Page : 148-154

Evaluation of oxidative stress response in endoscopic and Lichtenstein hernia repair: A randomized control study

Department of Surgery, Maulana Azad Medical College and Lok Nayak Hospital, New Delhi, India

Date of Submission27-Jul-2020
Date of Decision07-Aug-2020
Date of Acceptance09-Sep-2020
Date of Web Publication30-Nov-2020

Correspondence Address:
Dr. Lovenish Bains
Department of Surgery, Maulana Azad Medical College and Lok Nayak Hospital, New Delhi - 110 002
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ijawhs.ijawhs_33_20

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BACKGROUND: The extent of inflammatory and oxidative stress response varies with different surgical procedures. The aim of the study was to compare the same between total extraperitoneal repair and Lichtenstein repair for inguinal hernia.
MATERIALS AND METHODS: Men, aged 18–60 years with an ASA score of 1, presenting with primary unilateral indirect inguinal hernia were randomized to total extraperitoneal repair (TEP) and Lichtenstein repair. Blood samples were collected an evening before surgery and postoperatively at 2, 24, and 48 h to compare the levels of highly sensitive C-reactive protein (hs-CRP), malondialdehyde (MDA), and neutrophil: lymphocyte ratio between the two modes of repair.
RESULTS: Both modalities of repair cause a significant inflammatory response in the body (P < 0.05). The rise in the level of serum hs-CRP and neutrophil: lymphocyte ratio was significantly more in the open surgery group as compared to the TEP group at 2, 24, and 48 h postoperatively (P < 0.05). The levels of serum MDA were distinctively higher (P = 0.042) only at 2 h after surgery in the former group.
CONCLUSION: Endoscopic repair is associated with a significantly lesser oxidative response than Lichtenstein repair based on this study (P < 0.05). Although this might be one of the bases for lesser postoperative pain and earlier return to activity in TEP repair, more randomized studies are required to draw a definitive conclusion.

Keywords: Highly sensitive C-reactive protein, inguinal hernia, Lichtenstein, malondialdehyde, neutrophil: lymphocyte ratio, oxidative stress, total extraperitoneal repair

How to cite this article:
Saini R, Bains L, Hadke NS, Koner BC, Singh R, Lal P. Evaluation of oxidative stress response in endoscopic and Lichtenstein hernia repair: A randomized control study. Int J Abdom Wall Hernia Surg 2020;3:148-54

How to cite this URL:
Saini R, Bains L, Hadke NS, Koner BC, Singh R, Lal P. Evaluation of oxidative stress response in endoscopic and Lichtenstein hernia repair: A randomized control study. Int J Abdom Wall Hernia Surg [serial online] 2020 [cited 2021 May 14];3:148-54. Available from: http://www.herniasurgeryjournal.org/text.asp?2020/3/4/148/302027

  Introduction Top

Postoperative recovery may be associated with the degree of operative injury sustained. Acute-phase response, produced in response to surgery, is directly proportional to tissue trauma.[1],[2] In addition, the level of oxidative stress response predicts the recovery of patients after surgery.[3],[4] Endoscopic procedures may reduce inflammatory response by avoidance of a long skin incision, which is frequently the site of maximum tissue trauma.[5] Although it is claimed through various studies that endoscopic procedures have the advantage of providing higher postoperative patient comfort and lesser pain than open techniques,[6] the actual superiority can only be proved by demonstrating the pathophysiological and/or biochemical mechanisms, which is a more objective method.[7]

  Materials and Methods Top

It was a prospective double-blinded randomized controlled study conducted within the Department of General Surgery for a period of 1 year, which involved patients presenting with inguinal hernia to the outpatient clinics. Institutional ethics committee approval was taken for an equivalent. Male patients, aged 18–60 years, with primary unilateral indirect inguinal hernia, having an ASA score of 1, were included in the study. Those with any systemic or local infection, complicated, direct, or bilateral inguinal hernias, and with medical comorbidities were excluded [Figure 1].
Figure 1: CONSORT flow diagram

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A single dose of amoxicillin-clavulanic acid, 1.2 g intravenously, was given at the time of induction in all cases. Endoscopic repairs were performed under general anesthesia, while open repairs were carried out under spinal anesthesia given by a consultant anesthetist. All surgeries were performed by the three consultants with wide experience in both hernia techniques. For estimation of the extent of inflammatory markers in serum, namely highly sensitive C-reactive protein (hs-CRP), malondialdehyde (MDA), and neutrophil: lymphocyte ratio, 4 ml of blood samples was taken under aseptic precautions in the evening before surgery at around 6 pm, postoperatively at 2 h, 24 h, and 48 h. Open hernia repair was performed as described by Lichtenstein with approximately 5 cm skin incision.[8] Endoscopic repair was performed via total extraperitoneal approach using midline three-port technique as given by Ferzli et al.[9] A polypropylene lightweight mesh (BARD, USA) of size 4 inches × 6 inches was utilized in all procedures. Mesh was fixed by one nonabsorbable tack (ProTack, Indonesia) placed on Cooper's ligament in total extraperitoneal repair (TEP). On the other hand, six prolene suture ties were used to fix the mesh in open repair: one to the anterior rectus sheath just above the pubic bone, three inferiorly to the inguinal ligament, one to internal oblique aponeurosis just lateral to internal ring, and two sutures used to fix the superior fringe of mesh with the fascia transversalis. Intravenous diclofenac sodium, 37.5 mg, was given to all patients for the first 6 h. It was followed by oral diclofenac sodium, 75 mg, if pain recurred. All cases had an uneventful recovery and were discharged on the 2nd postoperative day. No follow-up after discharge was required concerning the study.

Estimation of hs-CRP was done by enzyme-linked immunosorbent assay. MDA was evaluated by thiobarbituric acid-reactive substance assay utilizing an ultraviolet-visible spectrophotometer. A fully automated cell counter autoanalyzer was used for measuring neutrophil: lymphocyte ratio.

Statistical analysis

The data were collected and analyzed using the Statistical Package for the Social Sciences (version 21.0; SPSS, Inc., Chicago, IL). Normality of data was tested by the Kolmogorov–Smirnov test. If the normality was rejected, then nonparametric test (Mann–Whitney test) was used. P < 0.05 was considered statistically significant. If there was a statistically significant difference between the preoperative values of the markers of TEP and Lichtenstein hernia repair, their respective postoperative values at specified time intervals cannot be compared between the two groups due to confounding variables that might lead to biasness of results. To control such variables, repeated measures ANCOVA was used. Repeated measures ANCOVA compares means across one or more variables that are based on repeated observations while controlling for a confounding variable. Only when there is no significant difference between the preoperative values of two groups, their respective postoperative values can be compared to each other at specified time intervals.

  Results Top

All patients were adult males, presenting with primary indirect unilateral inguinal hernia, with mean (±standard deviation) age of 38.75 (±14.43) and 37.15 (±8.93) years in the open and endoscopic repair groups, respectively, as shown in [Table 1]. The distinction in the duration of surgery was statistically significant (P < 0.001) between the two strata due to unknown reasons. There was negligible blood loss altogether in the surgeries. No conversions of TEP procedure to open repair or the other procedure were done.
Table 1: Demography and comparison of inflammatory markers between Lichtenstein and total extraperitoneal repairs

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Since there was a statistically significant difference between the preoperative serum values of mean hs-CRP of TEP and Lichtenstein hernia repair (P = 0.0004), repeated measures ANCOVA was used to adjust them. As seen in [Figure 2], the levels were significantly higher in both the groups postoperatively at all of the specified time intervals. Furthermore, when serum hs-CRP levels were compared between the open and endoscopic repair strata at 2, 24, and 48 h postoperatively, they were found to be significantly more at all of the time intervals in the former group (P < 0.0001).
Figure 2: Comparison of serum hs-CRP at different time intervals. HS-CRP: Highly sensitive C-reactive protein, Pre-op: Preoperative, Tep: Total extraperitoneal repair

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Serum MDA levels were higher in both repair strata after surgery at all predefined time intervals and were statistically significant. The levels were significantly more in the Lichtenstein group as compared to the TEP group only at 2 h postoperatively (P = 0.042), as shown in [Figure 3]. Furthermore, neutrophil: lymphocyte ratio was significantly higher in both the groups after the procedure. When the same ratio was compared between the open and TEP repair groups postoperatively [Figure 4], they were found to be significantly higher in the former at 2 h (P = 0.012), 24 h (P = 0.006), and 48 h (P = 0.008). Moreover, it was observed that as the duration of surgery increased, there were an insignificant rise and an insignificant decrease in the serum hs-CRP and MDA values, respectively, in both repairs. On the other hand, neutrophil: lymphocyte ratio more or less remained the same in TEP, while there was an unimportant decrease in the ratio in open repair, as the duration of surgery progressed.
Figure 3: Comparison of serum malondialdehyde at different time intervals. Pre-op: Preoperative, Tep: Total extraperitoneal repair

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Figure 4: Comparison of neutrophil: lymphocyte ratio at different time intervals. N: L ratio: Neutrophil-lymphocyte ratio, Pre-op: Preoperative, Tep: Total extraperitoneal repair

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  Discussion Top

As various surgeries use different modes of gaining access to the operating field, such procedures also interfere with the patient's homeostasis in distinct manners. Surgical trauma induced causes an inflammatory and oxidative stress response in the patient, which might have significant effects postoperatively. There are two types of inflammation caused in hernia repair, be it open or endoscopic. First, there is inflammation caused by the type of surgery, open or endoscopic, and second, mesh placement itself leads to an inflammatory reaction. Determining the importance of these responses may help to quantify the degree of tissue trauma inflicted by surgery and thereby understand and compare the clinical outcome between the open hernia repair and TEP better.

In general, surgery causes trauma to the tissues, which in turn produces a localized and generalized inflammatory response.[10] It is initiated by the release of endogenous molecules, called alarmins, from the necrotic cells, leukocytes, and epithelial cells. These molecules cause phosphorylation of transcription factors and increased cytokine production.[11] The cytokines produced in higher than normal amount from the surgical wound stimulate the hypothalamus, hypophysis, and adrenal axis.[12] All of these alterations induce a change in white blood cells and acute-phase reactants, namely interleukin-6 (IL-6), CRP, tumor necrosis factor (TNF)-alpha, IL-1, IL-8, and ESR.[13] IL-6 plays a key role in the synthesis of acute-phase proteins in hepatocytes, most commonly being CRP. It is normally present as a trace constituent in blood with concentration <0.3 mg/dl.[14] CRP levels generally rise within 24 h following tissue damage, reach a peak, and decrease within 5–7 days with the resolution of inflammation or trauma.[15] An increase in white blood cell and neutrophil counts, along with a decrease in the number of T-lymphocytes and natural killer cells, is characteristic of the acute-phase response after surgery.[16] An inhibition of neutrophil apoptosis in the circulation lasting several days has been observed following tissue trauma,[17] whereas surgical stress enhances the Fas-mediated apoptosis of circulating lymphocytes.[18] Within the first 24 h postoperatively, leukocyte levels increase from 9.3 to 11.5 × 109/L, which normalize by postoperative days 5 to 7. Neutrophil cell count increases at 24 h after surgery from 6.3 to 9.2 × 109/L.[19]

Cytokines have been studied extensively in various studies of inflammatory markers, but oxidative stress response has not been explored much.[12] Reactive oxygen species, generated by tissue injury, cause lipid peroxidation which is used as an indicator of oxidative stress in cells and tissues. Lipid peroxides, derived from polyunsaturated fatty acids found in the cell membrane, are unstable and decompose to form a complex series of compounds. One of the by-products of polyunsaturated fatty acid peroxidation is MDA.[20] Therefore, measurement of serum MDA is widely used as an indicator of lipid peroxidation and oxidative stress. In serum, its normal value is 0.36–1.24 μmol/L[21] that rises to a peak within 2 h and returns to normal in the next 3–4 days following tissue trauma. The rise is more sustained in open hernia repair than in endoscopic procedure as more cells are damaged in the former, thereby releasing more fatty acids from the cell membrane.[2] The implantation of a prosthetic material also sets up an inflammatory process in which it initially causes a subacute inflammatory reaction accompanied by a moderate seroma formation and an infiltrate of neutrophils and macrophages for about 1–3 weeks. It is followed by chronic inflammation that occurs after 2–3 weeks persisting for few years, sealing the prosthesis and formation of epithelioid granulomas.[22]

Although endoscopic repair has the advantages of smaller skin incision, lesser postoperative pain, earlier recovery, and shorter hospital stay as compared to open hernia repair,[23] the comparison between the two has not been made much at biochemical level based on oxidative stress and inflammatory response.

In the study by Hill et al.,[5] the mean duration of operation was 58 min in the TEP group and 45 min in the open repair group. The difference was statistically significant (P < 0.05) due to unknown reasons. This was comparable to our study. As the type of anesthesia used in both the techniques of hernia repair was different, difference in the inflammatory response might be because of the anesthesia also. In one of the studies conducted by Schwab et al., it was observed that when Shouldice repair was performed in local and general anesthesia, there were no significant effects on the levels of CRP and IL-6 until 3 days after surgery.[24] Similarly, no significant difference in hs-CRP and lymphocyte levels was noted at 24 h postoperatively when abdominal colectomy was performed in epidural and general anesthesia.[25]

Recent studies suggest that the method of entry into the abdomen, mainly the length of skin incision, is the most important determinant of postoperative immune response and surgical trauma.[26] In one of the studies, a comparison of the level of inflammation in laparoscopy, minilaparotomy, and laparotomy was done, where it was found that more oxygen-free radicals and IL-6 were released after laparotomy and minilaparotomy as compared to laparoscopy. They concluded that laparoscopy causes much less inflammation than the other two procedures.[27]

In our study, the difference between the mean serum levels of baseline CRP measured in the Lichtenstein (14.34 mg/L) and TEP (7.69 mg/L) groups was statistically significant (P = 0.0004). It might have been due to sampling error or selection bias. However, after adjusting the preoperative values using repeated measures ANCOVA, it was found that the postoperative values of serum hs-CRP were significantly higher than their preoperative values, with the peak rise at 24 h in both the strata. Furthermore, serum hs-CRP was significantly more (P < 0.001) in the open group (32.45 mg/L) compared to the TEP group (14.02 mg/L) at 24 h. This was comparable to the studies done by Suter et al.,[7] and Kokotovic et al.,[28] in which there was not only a significant increase in the hs-CRP values in both the classes at 24 and 48 h after surgery, but also there was significantly higher at 48 h in the open group than the endoscopic repair group. In 2011, a comparison of the systemic inflammatory response in inguinal hernia patients undergoing TEP or Stoppa's technique observed that the serum CRP levels at 12 h and 24 h postoperatively were lesser in endoscopic repair than Stoppa's technique, which accounted for the reduced postoperative pain and reduction in hospital stay.[29] Similar results were obtained by Akhtar et al.[30] when postoperative CRP levels at 48 h were compared between open and endoscopic inguinal hernia repair patients. A randomized study comparing postoperative CRP levels between the Lichtenstein repair, Bassini repair, Nyhus repair, and TEP repair groups showed that the TEP repair group had the least rise in CRP levels at 48 h postoperatively than other repair strata.[31] Matching results were found when a comparison between open and endoscopic repairs of recurrent inguinal hernia was done through a study in Greece.[32]

Our study observed that serum MDA was raised in both the repair groups at all predefined postoperative time intervals when compared to their respective baseline levels, with a peak rise at 2 h postoperatively. The mean values were significantly higher in the Lichtenstein group (2.84 μm/L) in comparison to the TEP group (1.37 μm/L) only at 2 h after the operation. This was comparable to another study,[12] in which the difference in the serum MDA values between the open and endoscopic inguinal hernia repair groups was statistically significant at both 6 h and 24 h postoperatively, with higher levels in the former.

In 1994, studies were carried out which involvedin vitro stimulation of peripheral blood mononuclear cells (PBMCs), followed by measurement of cytokine levels in the blood. It was observed that open procedures were associated with significantly higher TNF-α and superoxide anion levels, than endoscopic techniques, following PBMC stimulation. Furthermore, it concluded that both neutrophil chemotaxis and superoxide elaboration increased after open surgeries. Thus, increased tissue trauma with enhanced inflammatory response was seen in open procedures as compared to endoscopic surgeries.[33] In our study, neutrophil: lymphocyte ratio was significantly raised at all of the specified time intervals in both strata, when compared to the preoperative values, except in the TEP group at 48 h after the surgery. The ratio was significantly higher in the open strata at 2, 24, and 48 h postoperatively as compared to the TEP group. Neutrophil: lymphocyte ratio was highest in Lichtenstein repair at 2 h after surgery than in endoscopic repair patients. Our study was comparable to a study published in 2002,[7] in which neutrophils increased significantly after 4 h in both the hernia repair groups, though no significant difference was noted between them. On the contrary, lymphocyte counts decreased significantly in the open group at 4 h and 24 h postoperatively.

Furthermore, it was observed in our study that younger age groups had more increase in the levels of acute-phase reactants as compared to the older age groups. This might be due to a decrease in immunocompetence in older patients, thereby causing lesser immune reaction and inflammatory response to tissue trauma.[34]

One of the limitations of this study for not conclusively demonstrating the superiority of endoscopic repair over Lichtenstein repair for unilateral inguinal hernia in the context of inflammatory response is the small sample size used. Second, although the inflammatory responses between open and TEP repairs were studied, it did not include the impact of different modes of anesthesia on inflammatory marker levels as spinal anesthesia was used in the former and general anesthesia in the latter. This might have biased the results. Third, subjective outcomes of pain and functional recovery were not correlated to the inflammatory levels in both hernia repairs. All these limitations need to be overcome by further research to come to a definite conclusion of TEP being advantageous than open repairs.

  Conclusion Top

The postoperative levels of inflammatory markers studied increased to significant levels as compared to their preoperative values in both repair strata. A higher oxidative stress response was triggered in open hernioplasty than in TEP repair for primary unilateral indirect inguinal hernia. The rise was significant for hs-CRP and neutrophil: lymphocyte ratio at 2, 24, and 48 h postoperatively (P < 0.05), whereas for serum MDA, it was significantly higher only at 2 h (P = 0.042), for the Lichtenstein repair group. This observation of significantly less inflammatory and oxidative responses in endoscopic repair could be liable for a favorable outcome and early return to activity than the open repair. However, a more extensive randomized study is required to correlate the same.

Ethics approval

All procedures performed in the study involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Consent for publication

Written informed consent for the publication of this prospective RCT was obtained from the patients. A copy of the written consent is available for review by the Editor-in-Chief of this journal.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

  References Top

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

  [Table 1]


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