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Increased Systemic Inflammation After Laparotomy Vs Laparoscopy in an Animal Model of Peritonitis

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Increased Systemic Inflammation After Laparotomy Vs Laparoscopy in an Animal Model of Peritonitis ORIGINAL ARTICLE Increased Systemic Inflammation After Laparotomy vs Laparoscopy in an Animal Model of Peritonitis C. A. Jacobi, MD; J. Ordemann, MD; H. U. Zieren, PhD; H. D. Volk, Prof; A. Bauhofer, PhD; E..Halle, PhD; J. M. Mu¨ller, Prof Objective: To study the influence of laparotomy and Main Outcome Measure: The hypothesis of the ex- laparoscopy on local and systemic inflammation in a rat periment was that laparoscopy with carbon dioxide leads model of peritonitis. to an increase of local and systemic inflammation in com- parison with the laparotomy and control groups. Design: Bacteremia, peripheral leukocyte subpopula- tions, tumor necrosis factor a (TNF-a) plasma levels, and Results: One hour after intervention, bacteremia was sig- ex vivo secretion of peripheral blood mononuclear cells nificantly higher in the laparotomy and laparoscopy were investigated after laparotomy and laparoscopy in a groups compared with the control group (P=.01). Fecal prospective randomized experimental study. inoculum caused significant monocytopenia and lym- phocytopenia in all groups within 1 hour after interven- Setting: Surgical department of a university hospital. tion (P<.05), with complete recovery on day 2 only in the laparoscopy and control groups. Laparotomy caused Animals: 60 male inbred Wistar rats. a significant increase in TNF-a plasma levels and de- crease of ex vivo production of TNF-a compared with Interventions: Standardized fecal inoculum was the other 2 groups (P<.05). injected intraperitoneally and rats underwent lapa- rotomy (n=20), laparoscopy (n=20), or no further Conclusions: Laparotomy and laparoscopy increased the manipulation (control group, n=20). Blood samples incidence of bacteremia and systemic inflammation in this were obtained during the perioperative course to deter- peritonitis model. The inflammatory response was sig- mine bacteremia, leukocytic subpopulations, TNF-a nificantly higher in the laparotomy group compared with plasma levels, and ex vivo secretion. The number of the laparoscopy group. intraperitoneal abscesses was determined in each ani- mal after 1 week. Arch Surg. 1998;133:258-262 APAROSCOPIC SURGERY is in- Therefore, the influence of lapa- creasingly used for intra- rotomy and laparoscopy on bacteremia, abdominal diseases compli- peripheral leukocytic subpopulations, cated by inflammatory proinflammatory tumor necrosis factor processes and peritonitis. a (TNF-a) plasma levels, and ex vivo LSuccessful treatment of appendicitis, per- secretion of peripheral blood mono- forated peptic ulcer, and diverticulitis nuclear cells (PBMCs) was studied in a has been reported with low morbidity.1-5 rat model. However, a theoretical concern is that el- evated intra-abdominal pressure may pro- RESULTS From the Department mote bacteremia and systemic inflamma- of Surgery (Drs Jacobi, tory response during laparoscopic surgery. MICROBIOLOGICAL ANALYSIS Ordemann, Zieren, and Data regarding the effects of pneumoperi- Mu¨ller), the Institute of Medical toneum on physiological changes and sys- The number of blood cultures positive for Immunology temic inflammation during sepsis are organisms was increased in the lapa- (Dr Volk), and the Institute scarce and controversial.6,7 Furthermore, rotomy and laparoscopy group as com- of Microbiology (Dr Halle), University of Berlin, Berlin, only early effects of pneumoperitoneum pared with the control group (P=.01) 1 Germany; and the Institute during peritonitis have been evaluated and hour after stool application (Table 1). of Theoretical Surgery the differences between conventional and There was no difference in bacteremia be- (Dr Bauhofer), University of laparoscopic surgery have not been com- tween the groups 1 week after fecal in- Marburg, Marburg, Germany. pared in all studies. oculum and surgical intervention. ARCH SURG/ VOL 133, MAR 1998 258 ©1998 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/24/2021 MATERIALS AND METHODS TNF-a PLASMA LEVELS AND TNF-a EX VIVO SECRETION BY PBMCs EXPERIMENTAL COURSE Plasma was separated from blood samples by centrifuga- tion at 3000g at 4°C for 10 minutes immediately after Sixty male inbred 2-month-old Wistar rats (Charles River, withdrawal. Tumor necrosis factor a serum levels were Sulzfeld, Germany) were acclimated to a climate- and light determined by using commercially available enzyme cycle–controlled environment for at least 7 days prior to immunoassays (Laboserv). Additionally, 50 µL of blood investigations. The animals were allowed standard labora- from each sample was diluted with 200 µL of fetal calf tory food and water ad libitum. All animals were initially serum–supplemented (2% vol/vol) RPMI 1640 (Bio- anesthetized by intraperitoneal injection of pentobarbital chrom, Berlin, Germany) and incubated for 4 hours (60 mg/kg) under sterile conditions. A standardized fecal (37°C, 5% carbon dioxide) with 100 ng/mL of endotoxin inoculum (130.5 mL/kg) was applied intraperitoneally un- Escherichia coli 0127:B8 (Sigma, Deisenhofen, Germany) der sterile conditions in all animals. The preparation has to assess the ex vivo TNF-a secretion of PBMCs. Cell-free been previously described and has been shown to pro- supernatants were harvested by centrifugation at 3000g at duce a nonfatal bacterial peritonitis after intraperitoneal in- 4°C for 10 minutes. All samples were stored in 2-mL stillation in rats.8 pyrogen-free polypropylene screw-cap tubes (Sarstedt, The rats were randomized into 3 different groups. In Numbrecht-Rommelsdorf, Germany) at −85°C until final the first group (n=20), laparotomy was performed and analysis. the abdomen was closed after 30 minutes. In the second group (n=20), laparoscopy was performed with insuffla- MICROBIOLOGICAL ANALYSIS tion of carbon dioxide at a pressure of 8 mm Hg over a period of 30 minutes. The control group (n=20) under- The microorganisms were grown on chocolate agar went no further manipulation after stool injection. Blood (tryptic soy agar supplemented with 10% defibrinated samples were obtained from the femoral artery and placed sheep blood, heated for 10 minutes to 80°C), blood agar into sterile heparinized vials (pyrogen-free) 2 days before, (Columbia agar supplemented with 5% defibri- 1 hour after, and 2 and 7 days after fecal inoculation. Leu- nated sheep blood), Endo agar, and Sabouraud agar kocyte subpopulations were determined with a differen- in both an aerobic and anaerobic atmosphere. The phe- tial blood smear and plasma was separated from blood notypical identification of all strains was carried out samples by centrifugation at 3000g at 4°C for 10 minutes by testing the carbohydrate fermentation reactions or by to determine TNF-a plasma levels using commercially using commercially available enzyme activity and available enzyme immunoassays (Laboserv, Gießen, Ger- fermentation tests (API, Bio Me´rieux, Nu¨ rtingen, many). Additionally, 50 µL of blood from each sample Germany). was used to measure the ex vivo TNF-a secretion by PBMCs. Microbiological analysis of the blood was per- STATISTICS formed before, 1 hour after, and 7 days after intervention. All animals underwent laparotomy on day 7 to determine Data are given as mean±SD. Data between groups were com- the number of intraperitoneal abscess formations. All pared using the Kruskal-Wallis test for continuous data and studies were performed under protocols approved by the the Fisher exact test for categorical data, if appropriate. local committees of animal use and care. P,.05 was considered significant. Microbiological analysis of blood cultures detected 12 different bacteria species after laparotomy, 7 species Table 1. Number of Positive Blood Cultures after laparoscopy, and 7 species in the control group After 1 Hour and 7 Days (Table 2). No. (%) LEUKOCYTE SUBPOPULATIONS Time After Laparotomy Laparoscopy Control Intervention Group (n=20) Group (n=20) Group (n=20) Anesthesia and fecal inoculum caused a significant leu- 1 h 20 (100) 17 (85) 7 (35)* kocytopenia 1 hour after intervention in all groups 7 d 13 (65) 13 (65) 12 (60) (Figure 1). Leukocyte counts recovered on day 2 in the laparoscopy and control groups (P=.02), while they did *P,.05, laparotomy and laparoscopy groups vs control group. not recover in the laparotomy group during the entire postoperative course. In contrast to the laparotomy group, locyte counts increased in the postoperative course laparoscopy and control groups showed a decrease of leu- (Figure 4). While rats in the laparoscopic and lapa- kocyte counts in the late postoperative course (P=.01). rotomy groups showed a significant increase 1 hour af- Decrease and recovery of the leukocyte count was mainly ter fecal inoculum and surgery, fecal inoculum alone caused by a change in the number of lymphocytic and caused only a slight increase of neutrophil granulocytes monocytic cells (Figure 2 and Figure 3). Decrease of on day 2, with complete recovery after 1 week. Early monocytes and lymphocytes was significantly higher af- granulocytosis after laparoscopy or laparotomy was fol- ter laparotomy compared with laparoscopy and in the con- lowed by complete recovery on day 2 and a second in- trol group 1 hour after intervention. Neutrophil granu- crease on day 7. ARCH SURG/ VOL 133, MAR 1998 259 ©1998 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/24/2021 Table 2. Bacterial Species in Blood Cultures 1 Hour and 7 Days After Endotoxin Application* 1h 7d Laparotomy Laparoscopy Control Laparotomy Laparoscopy
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