Minimally Invasive Therapy. 2014;23:157–164

ORIGINAL ARTICLE

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Prolonged capnoperitoneum does not cause postoperative ileus in pigs: Safety of prolonged capnoperitoneum

DIETMAR BORCHERT1, PETER KÖHLER2, TARKAN JÄGER3, MIKE DIEDERICH2, LIANE HÜTHER4, ANDREAS BERK4, WOLFRAM LAMADE5 1

Saarland University Hospitals, Department of Surgery, Homburg/Saar, Germany, 2Bundesforschungsinstitut für Tiergesundheit, Friedrich-Loeffler-Institut (FLI), Institut für Nutztiergenetik, Mariensee, Germany, 3Department of Surgery, Paracelsus Medical University, Salzburg, Austria, 4Bundesforschungsinstitut für Tiergesundheit, Friedrich-Loeffler-Institut (FLI), Institut für Tierernährung, Braunschweig, Germany, and 5Helios Hospital, Department of Surgery, Überlingen, Germany

Abstract Introduction: Operative time is an accepted risk factor for the development of postoperative ileus (POI). Innovative surgical procedures such as robotic surgery and natural orifice transluminal endoscopic surgery (NOTES) will be associated with longer operative times. Although intraabdominal manipulation is a major factor for POI the impact of prolonged capnoperitoneum on postoperative gastrointestinal transit time (GIT-TT) has rarely been studied. Material and methods: IRB approved survival pilot study to assess postoperative GIT-TT using fecal collection and chromium-oxide (Cr2O3) labeling in pigs. Twelve female pigs were randomly assigned to three groups of four animals each. Group A received eight hours anesthesia and pressure-controlled high flow capnoperitoneum (15 mmHg), group B eight hours of anesthesia only and group C no intervention. No intraoperative manipulation. The pilot study was terminated after eight days. Results: None of the animals developed POI. In Group A one animal died after eight hours of general anesthesia. No differences in postoperative fecal output, Cr2O3 excretion rate or weight gain were found. Conclusion: This study is the first to investigate eight hours of capnoperitoneum in a survival model. GIT-TT is not affected by prolonged capnoperitoneum in pigs. No POI occurred with prolonged capnoperitoneum. Prolonged capnoperitoneum is safe regarding postoperative gastrointestinal function in innovative surgical procedures.

Key words: Capnoperitoneum, minimally invasive surgery, NOTES, safety, postoperative ileus

Introduction The development of robotic surgery and NOTES procedures is inadvertently challenged by learning curve and possibly a spectrum of complications different from conventional techniques (1). In recent reviews and case reports prolonged operative times with NOTES procedures have been a matter of concern (2,3). Operative time and intraabdominal manipulation are clinically established risk factors for POI (4). Prolonged operative times may specifically occur with NOTES involving the combined use of laparoscopic and endoscopic techniques. This

combined approach has been used before and prolonged disturbance of postoperative gastro-intestinal motility has been noted (5,6). Major laparoscopic abdominal procedures such as colorectal surgery continue to feature consistently more cut-to-needle time compared to conventional open procedures (7,8). But evidence for decrease in POI favours laparoscopic surgery (9). If laparoscopic surgery decreases POI despite longer operative times and manipulation and if clinical experience on the combined use of laparoscopy and endoscopy yields a higher rate of POI, what role does a prolonged capnoperitoneum play in the development of POI? Data available to date

Correspondence: D. H. Borchert, Department of General-, Visceral-, Vascular- and Paediatric Surgery, University Saarland, Kirrbergerstraße, Geb. 57, D-66421 Homburg/Saar, Germany. E-mail: [email protected] ISSN 1364-5706 print/ISSN 1365-2931 online  2014 Informa Healthcare DOI: 10.3109/13645706.2013.855234

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do not allow for a conclusion as most animal experiments and clinical reports do not exceed operative times of four hours (10). The need for further studies was foreseen by experienced reviewers of surgical research (11) and the ASGE/SAGES NOTES White Paper recommending the evaluation of postoperative gastro-intestinal motility and function after NOTES procedures in animal studies (12). So far no pig survival studies have been reported investigating eight hours of capnoperitoneum.

Material and methods Animals This eight-day survival pilot study involved twelve female german landrace pigs (35–45 kg), each three months old. Pigs were born and raised at FLI ensuring minimal genetic heterogeneity. Animal housing environment was maintained at a temperature of 22 C with a 12-hour light-dark cycle (optimal housing temperature range 18 – 22 C, at 60 – 80% humidity (13)). Pigs were acclimatized to their environment for three to five days upon arrival in the experimental unit of FLI and then fasted overnight prior to intervention. Set-up of the experiment Three groups of animals with four animals each were compared. Group A eight hours of 15 mmHg capnoperitoneum, group B eight hours of anesthesia alone, group C no intervention. In group A we aimed to achieve a total insufflation volume of 2000 ltr CO2 (liter of carbon-dioxide). The volume insufflated was deliberately chosen on a background of own unpublished experience with laparoscopic colorectal surgery. In our experience Hybrid-NOTES and single port colorectal resection may use up to 1000 ltr CO2 in operations of six to eight hours. No preoperative bowel preparation. All procedures were performed under aseptic conditions and the animals were kept warm under cotton drapes. No premedication was used. Group A received preoperative antibiotics using LZ-penicillin and dihydrostreptomycin (4.8 mg kg 1, aniMedica, Senden Bösensell, Germany) and intramuscular analgesia using metacam (20 mg ml-1; 0,6 mg kg-1 KG Meloxicam, Vetmedica Boehringer Ingelheim, Ingelheim/Rhein, Germany). For induction of anesthesia we used intramuscular ketamine (10%, 20 mg kg-1, Bremer Pharma, Warburg, Germany), azaperon (4 mg kg-1 Stresnil, JanssenCilag, Neuss, Germany) and atropine (0.5 ml, Köhler Chemie, Alsbach-Hähnlein, Germany), no muscle relaxation. Induction was followed by endotracheal

intubation and maintenance anesthesia using isoflurane, oxygen and compressed air. For pressurecontrolled ventilation we used a Ventilog 2 (Draegerwerke AG, Lübeck, Germany) with a semi-closed circuit and heat moisture exchange filter. The ventilation protocol included an I:E ratio of 1:2, tidal volume of 300 ml, 20 breaths per minute and PEEP of 0.2 kPa. During general anesthesia animals received intravenous fluids using 0.9% sodium-chloride, bicarbonate (NaHCO3, 8.4%), glucose 5%, and ringer lactate. Dobutamin (1 mg min-1 25 kg-1 KG Dobutamin HEXAL,Salutas Pharma, Hexal AG, Barleben, Germany), Dimazon (50 mg ml-1, 2 mg kg-1 KG Furosemid, MSD Animal Health GmbH, Intervet, Unterschleißheim, Germany) and steroids (2 mg ml-1, 0.02 mg kg-1 KG Dexatad, dexamethasone, aniMedica, Senden Bösensell, Germany) were used for anesthetic management as needed. Operating room temperature was set at 23 C. Monitoring via an anaesthetic monitor and a humidity-temperature probe, intraabdominal pH using pH-indicator paper on ascitic samples (14), intraabdominal humidity, oxygen saturation, heart rate, blood pressure and end tidal CO2 (etCO2) measured by continous capnometry (Schiller Argus LCM plus monitor, Ottobrunn, Germany and Extech RH 101, HygroThermometer, Extech Instruments, Nashua, NH, USA) were recorded. Inspiratory oxygen changes (FiO2) during anaesthesia were not recorded. Animals were extubated after eight hours of anesthesia. Recovery time was three hours and feeding restarted thereafter on the same day.

Surgical procedure In group A one 11 mm trocar, 10.5 cm length (Karl Storz, Tuttlingen, Germany) was inserted at the umbilicus under aseptic conditions for insufflations and measurements. The 10 mm trocar was used for insertion of an intraabdominal temperature probe and for testing of intraabdominal pH. A second 5 mm, 10.5 cm length trocar was inserted in the left lower abdomen and kept open for continous desufflation via a silicon exhaust hose 1.2 m, lumen 0.5 cm (Omnilab, Bremen, Germany) after establishing a 15 mmHg capnoperitoneum. The valve at this 5 mm trocar was used to adjust for an IAP (intraabdominal pressure) of 15 mmHg and closed for change of CO2-shells. No laparoscopy and no intraabdominal manipulation were performed. Continous high flow insufflation was started after trocar insertion. For insufflation an Electronic Endoflater Set, SCB, and high pressure tubing with a sterile filter, 102 cm length, (Karl Storz, Tuttlingen, Germany) were used. Group B received aseptic preparation and

Safety of prolonged capnoperitoneum in pigs anesthesia only. No intervention in group C. No positioning of animals (e.g. steep Trendelenburg position).

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Monitoring and Cr2O3 method Postoperatively animals were kept in a caloric cage to allow for collection of all excrements. After recovery animals received 0.8 kg of animal food labeled with 4gr of chromium-III-oxide powder (Cr2O3, i.e. 2.74 g Cr, waterfree Technipur, Merck, Darmstadt, Germany) to assess GIT-TT. Animals received water ad libitum. Faeces and urine were collected from the day after anesthesia in 12 hour intervals for 48 hours. In faeces Cr2O3 excretion was measured in dissolved one gram portions of dried samples using inductively coupled plasma mass spectrometry (ICP-OES, Quantima, GBC Scientific Equipment Pty Ltd, Victoria, Australia) (15). Animal food habits and weight were assessed in two daily intervals. Diet was restricted to 0.8 kg animal food twice daily. Data analysis No funding for an adequately powered study could be achieved; therefore no sample calculcation and design of a pilot study. Data were collected in a standard spreadsheet and analysed using SPSS, Version 14.0.1 (07.12.2005) and GraphPad Prism, Vers. 3.0 (1999, San Diego, CA, USA). Data reported include animal age and weight, intraoperative treatment, physiology and complications, details of postoperative recovery, weight gain and gastrointestinal transit. Postmortem investigation is reported in detail. Numbers are given in mean (±SD) and 95 % confidence intervals. Significance testing included twosided t-test, chi-square, Mann-Whitney U and linear regression.

Results Preoperative status of animals and results of intraoperative physiology Preoperatively all animals were well and thriving. Mean preoperative weight was significantly higher in group C when compared to group A or B (p < 0.01, Table I). There was no difference in age; all animals were 93 ± 2 days old. There was a significant difference in anesthetic time between groups A and B. Animals in group B had on average one hour less of anesthetic time compared to animals in group A (Table I). Mean insufflation time was eight hours (473 minutes, SD 9.6, Tables I and II) . Average volume insufflated in

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group A was 2240 ltr (±240 ltr) at a flow rate of 4.83 ltr min-1 (±0.74). There were significant differences in mean flow rates between animals A 1 vs. A 4 (4.4 vs. 5.9 ltr min-1, p < 0.02, Table II), A 2 vs. A 4 (4.6 vs. 5.9 ltr min-1, p < 0.03) and A 3 vs. A 4 (4.4 vs. 5.9 ltrmin-1, p < 0.008). Intraabdominal pH measurements were compared using pH measures up to 700 ltr of CO2 volume insufflated (N = 20) against pH measures relating to volumes 1500 to 2000 ltr (N = 19). Mean pH was 6.48 (±0.38) with up to 700 ltr insufflated vs. pH 6.33 with 1500 to 2000 ltr CO2 insufflated (±0.33, n.s., Table II). Intraabdominal humidity was compared in a similar way (N = 38 vs. N = 32). No differences were found in mean intraabdominal humidity comparing insufflated volume up to 700 ltr vs. insufflated volumes between 1500 and 2000 ltr (71% ± 17 vs. 73%, ±16; n.s.). No tendency towards differences in intrabdominal pH and humidity in group A animals over time were found. During anesthesia physiology measures yielded no difference in oxygen saturation, heart rate, etCO2 or diastolic blood pressure. Cumulative mean systolic blood pressure was significantly elevated in group A (Table I). Comparing heart rate, systolic and diastolic blood pressure after one hour of equilibrium and before extubation no differences were found between groups A and B (data not shown). Animals with capnoperitoneum received more intravenous volume substitution with sodium-chloride and glucose solutions.

Results of postoperative recovery and gastrointestinal function None of the surviving animals suffered any complications until day eight. All animals made a successful recovery within three hours including normal movements, finding the food bowl and starting normal food intake without vomiting. Feeding behaviour in all animals continued to be normal. Average weight gain in 48 h intervals was 1.13 (±0.5) kg in group A and 0.81 (±0.3) in group B (p = 0.24, Table III). Mean weight after eight days was 41.7 kg in group A and 41.0 kg in group B. There was no difference between animals in average urine, faecal and Cr2O3 output per daily food intake (Table III, Figure 1). As expected, macroscopically green faeces and inorganic Cr were found in dried samples in all groups on day two after uptake of labeled food (16).

Results of complications and postmortem investigation Experiments were carried out according to plan. In group A one animal died on withdrawal of anesthesia

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Table I. Status of animals and intraoperative physiology. N A/B

group A mean

95% CI or SD

group B mean

95% CI or SD

group C mean

95% CI or SD

p

4/4

37.3

36 - 39

37.8

35 - 41

43

41 - 45

< 0.01

age/ days

4/4

92.5

90 - 95

93.5

91 – 96

93.8

91 - 96

anesthetic time/ minutes

4/4

536

493 - 579

465

417 – 513

< 0.02 n.s.

preoperative weight/ kg

insufflation time/ minutes

4

473

457 - 488

38/33

97

96 - 98

98

97 – 99

heart rate/ bpm

37/34

106

101 - 110

111

107 – 115

n.s.

endtidal CO2/ kPa

38/34

4.8

4.0 - 5.7

5.7

5.4 - 6.0

n.s.

systolic blood pressure/ mmHg

38/34

114

108 - 120

103

98 – 109

< 0.01

diastolic blood pressure/ mmHg

38/34

38

35 - 40

35

33 – 37

n.s.

Ketamin/ ml

4/4

7.45

0.2

7.65

0.3

n.s.

Stresnil/ ml

4/4

3.1

0.1

4.4

0.9

n.s.

Dexamethasone/ ml

2/2

0.8

0.1

0.7

0.0

n.s.

Dimazan/ ml

2/2

0.8

0.1

0.7

0.1

n.s.

Sodium-chl. 0.9%/ ml

4/4

1200

0.0

950

58

< 0.003

Ringer-Lactate/ ml

4/4

675

50

650

58

n.s.

NaHCO3/ ml

4/4

60

12

53

5

n.s.

glucose 5%/ml

4/4

85

17

45

17

< 0.02

oxygen saturation/ %

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n.s.

Isofluran/ %

4/4

1.5

0.2

1.6

0.2

n.s.

oxygen ltr/ min

4/4

1.1

0.3

1.4

0.1

n.s.

compressed air ltr/ min

4/4

1.0

0.3

1.0

0.0

n.s.

Measures in SI values (Système international d’unités), N number of measurements in groups A and B.

receiving anesthesia. All animals were able to move, find food and successfully start food intake. Eleven out of twelve pigs survived until day eight. In group A immediate postmortem investigation of animal A 2 showed significant pathology of both lungs (Table V). Another animal in group A showed mild changes of lung parenchyma after eight days of survival. Two further animals in group A did not show any signs of parenchymal change after eight hours of capnoperitoneum and eight days of survival. In group

due to preexisting pneumonia (Table IV). Two further animals in group A suffered cardiovascular problems but had uneventful survival. In none of the animals in group A desufflation was necessary for anesthetic management. In group B an episode of cardiovascular disturbance in one pig and one episode of ventilation problems in another pig could be successfully managed. All animals in group B had uneventful survival. No complications occurred in group C. Recovery was monitored in all animals Table II. Capnoperitoneum data group A. N Insufflation/ time

A 1 mean

SD

480

Total volume insufflated/ ltr

A 2 mean

SD

470

2130

A 3 mean

SD

480

2107

A 4 mean

SD

460

2124

p n.a.

2600

n.a.

25–32

4.43

2.3

4.45

2.0

4.43

1.5

5.91

2.0

< 0.02

pH start

5

6.6

0.5

6.5

0.3

6.1

0.3

6.7

0.3

n.s.

pH end

5

6.1

0.4

6.6

0.2

6.4

0.2

6.3

0.2

n.s.

Flow rate/ ltr min-1

Humidity % start

8–10

71

21

57

12

82

12

75

6

n.s.

Humidity % end

8

73

8

65

26

84

12

72

3

n.s.

A 1 – A 4 animals 1 to 4, N number of measurements in each animal in group A, n.a. calculation of significance not applicable.

Safety of prolonged capnoperitoneum in pigs

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Table III. Postoperative weight and results of metabolic cage.

postop. weight kg*

N A/B/C

group A mean

95% CI

group B mean

95% CI

12/16

41.7

36.1 - 47.3

41.0

36.3 – 45.7

1.13

0.3 – 1.9

0.81

0.4 – 1.2

126

31 - 221

163

102 -224

95% CI

156

64 - 247

faeces mg

12/16/16

urine output ml

12/16/16

507

354 - 659

520

283 - 758

504

354 - 655

Cr mg/kg

15/20/20

1670

369 - 3708

4132

2225 - 6038

1307

518 - 2096

*postoperative weight on day eight. Mean 48 hour weight gain. Mean daily faeces, urine excretion and inorganic chromium (Cr) in mg/kg dry matter, mean values over 48 hrs.

B all animals showed signs of inflammation or even necrotic lung tissue damage after eight days of uneventful survival. In group A three animals showed signs of mild peritonitis or postoperative peritonitic reaction whereas no such pathology was found in group B. No postmortem investigation was carried out in group C. Complications with technical set up occurred in two animals in group A. In one animal insufflation was insufficient on two occasions and managed by manipulation of trocars and insertion of an additional Verres needle. In a second animal in group A the intraabdominal temperature probe was defunct after four hours of capnoperitoneum. Temperature recordings of this animal were excluded from analysis thereafter.

Discussion Prolonged capnoperitoneum and postoperative ileus Animal studies and specifically porcine models have been used to investigate factors contributing to surgical stress and postoperative complications in NOTES procedures (17,18). The main instrument for laparoscopic, endoscopic and NOTES procedures is CO2 insufflation. CO2 is used to create the capnoperitoneum and for insufflation of the gastrointestinal tract. The influence of capnoperitoneum on physiologic measures and outcome has been assessed in a range of experimental settings in pigs (19,20). But capnoperitoneum time in animal experiments rarely exceeds four hours. An extreme example of prolonged capnoperitoneum was tested in a non-survival porcine model of intraabdominal compartment syndrome with a capnoperitoneum pressure of 15 mmHg for 24 hours. When reporting this study in 2002 the authors stated that a safe duration of increased IAP had yet to be determined (21). No reports exist today investigating capnoperitoneum times in animals more than six hours (22). Eliciting differences in animal experiments to test a safe range of intraabdominal

pressure and time of pressure applied still requires pilot studies, as recently shown (23). Moreover animal survival studies using capnoperitoneum are still rare. NOTES survival studies so far have not reported problems with postoperative bowel function or incidence of POI in animals. Our experiment used eight hours capnoperitoneum without intraoperative manipulation and on average 2240 ltr of CO2 per animal. The literature reports an average consumption of 60 – 90 ltr of CO2 per hour of laparoscopy (24). In advanced laparoscopic procedures with five or more trocars e.g. bariatric surgery, CO2 volumes insufflated may largely exceed these numbers. From a clinical point of view in robotic colorectal surgery with operative times exceeding eight hours of capnoperitoneum no increased rate of POI has been reported to date (25). At the 2009 SAGES meeting the results of a prospectively maintained single surgeon database of laparoscopic procedures in 96 cases were reported. Maximum operative times of major laparoscopic 7.5

Group A Group B

5.0 mg/kg DM

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48 h weight gain kg

group C mean

Group C

2.5

0.0 10

20

30

40

50

h Figure 1. Inorganic chromium excretion in mg/kg dry matter (DM) per daily feed after 12, 24, 36 and 48 hours. In groups A and B samples from faeces were taken after 12 h, in group C after 24 h. Data points are mean values of inorganic chromium in mg/kg dry matter with upper 95% CI only for keeping the figure within publishable shape. No significant differences.

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Table IV. Details of complications during eight hours of anesthesia.

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Pig No.

Description of complication and intervention

A1

Suffered cardiopulmonary crisis after seven hours of anesthesia. Successfully managed by giving 0.5 gr dexamethason. Uneventful capnoperitoneum and survival

A2

After eight hours of uneventful capnoperitoneum 3rd degree AV Block on planned withdrawal of anesthesia. 0.8 ml dimazon i.v. given. Exitus letalis due to preexisting pneumonia

A3

Cardiogenic shock one hour after anesthesia. 0.7 ml dimazon, 0.7 ml dexamethason. Uneventful capnoperitoneum, extubation and survival

A4

No complications

B1

No complications

B2

Congestion of abdominal veins, episode of extrasystoles. 0.7 ml dexamethason, 0.6 ml dimazon. Uneventful extubation and survival

B3

Difficult ventilation after seven hours of anesthesia. 0.7 ml dexamethason, 0.7 ml dimazon. Withdrawal of anesthesia after seven hours. Uneventful recovery.

B4

No complications

procedures were more than ten hours. Six patients experienced postoperative ileus (26). This indicates long capnoperitoneum times are used in routine daily practice and POI continues to be a problem. At the same meeting a porcine NOTES two week survival study of transanal (TEM) combined with transgastric (TG) rectosigmoid resection was reported (27). Mean operative times were four hours. No postoperative death or bowel problems occurred in this study. Race and preoperative weights of these animals were comparable to those in our experiment. With food ad libitum animals gained 1.54 kg weight over two weeks compared to 1.13 kg every 48 hours in this study with tightly defined food intake of 1.6 kg per day. The German ministry of agriculture states an average weight gain for pigs at three month of 0.6 – 0.8 kg per day if on hog feeding (28). With restricted feed in this experiment weight gain in our survival study was well within this range. One of the authors of the above NOTES survival study went on to compare another set of NOTES procedures (embryonic E-NOTES through the umbilicus vs. TEM + TG = Pure P-NOTES). Again the preoperative weight of animals was comparable to those in our

study. In this one-week survival study animals gained practically no weight with food ad libitum. Mean operative time for P-NOTES was four hours. No postoperative bowel problems were reported (29). Bergström et al. reported on a randomized controlled four week pig survival study of bacterial wound contamination in open, laparoscopic and NOTES surgery in thirty pigs with a similar type of pigs and preoperative weight. Average daily weight gain was 0.4 kg per day (30). Comparing the weight gain in the cited studies to our experiment the obvious difference in gastro-intestinal function (i.e. weight gain) is at least not a problem of prolonged capnoperitoneum. Excretion rates of faeces and chrome were highly variable between animals as expected in a pilot study with small sample size. But excretion of faeces and chromium within 24 hours, as well as postoperative weight gain in our experiment, indicate that prolonged capnoperitoneum does rather not cause POI. Taken this experience together with the aforementioned clinical and NOTES studies specific surgical procedures and intraabdominal manipulation are more likely to cause POI than prolonged capnoperitoneum itself.

Table V. Details of postmortem investigation on day eight. A1

Abdominal parenchymatous organs normal, mild peritonitis. Normal lung parenchyma.

A2

Immediate postmortem showed necrotic destruction of the whole right lung and of the lower lobe of the left lung. Significant dilation of the left ventricle and pericardial effusions. Moreover adhesions between stomach, colon and urinary bladder. No Verress-needle or trocar injury. Hepatomegalie. Gram negative cocci in bronchial aspirate.

A3

Abdominal parenchymatous organs normal. Adhesion of liver at trocar insertion site. Minimal peritonitis, mild bilateral pulmonitis.

A4

Abdominal parenchymatous organs normal. No signs of trocar injury to the viscera. Minimal peritonitic reaction. Enlarged mesenteric lymphnodes. Normal lung parenchyma.

B1

Abdominal parenchymatous organs normal. Mild pulmonitis in both lungs. Lobus cranialis dexter severe pulmonitis.

B2

Abdominal parenchymatous organs normal. Mild pulmonitis in both lungs.

B3

Necrotic areas in both lungs.

B4

Abdominal parenchymatous organs normal. Mild high grade pulmonitis in left lung. Lobus cranialis dexter mild pulmonitis.

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Prolonged capnoperitoneum and physiology

Acknowledgements

As we expected capnoperitoneum did not affect cardiovascular outcome in a significant way. Systolic blood pressure was elevated in group A compared to group B but this did not influence outcome. Animals in group A developed severe peritoneal acidosis shortly after initiation of capnoperitoneum. This did not change towards the end of CO2 insufflation. These data are in accordance with previous findings investigating capnoperitoneum times up to three hours (31,32). What this study adds is that severe peritoneal acidosis after eight hours of capnoperitoneum had no obvious deleterious effects on survival and macroscopic postmortem findings. Our data specifically corroborate the finding of other studies reporting the effect of intraabdominal acidosis on the visceral peritoneum (32). Numbers on CO2 volume insufflated and gas flow are rarely cited in the literature but may easily use up to several hundred liters of CO2 depending on body habit, leak rate and other factors (33). We used a flow rate (mean 4.83 ltr min-1) well within the range for routine laparoscopic procedures such as cholecystectomy or colectomy, although maintenance flow may be much lower if gas leak is low (34). But rather excessive flow and leak rates may occur in bariatric and other procedures as especially gas leak is dependent on number of trocars used (35). By the mid-nineties standard laparoscopic cholecystectomy required an average operative time of 35 – 180 minutes and capnoperitoneum was established at 10 – 15 mmHg, at flow rates of 1-2 ltr min-1 with a total volume of CO2 of 35 – 360 ltr insufflated (36). These numbers have risen sharply with widening indications for laparoscopic surgery but no good estimates are available in published reports to date. As such testing safe limits of capnoperitoneum pressure, flow rates and total volume used seem to be urgently needed. The safety limits of capnoperitoneum on systemic and gastrointestinal blood circulation in pig studies have been investigated with IAP increased up to 40 mmHg over prolonged times (37). We tested a standard capnoperitoneum of 15 mmHg over eight hours – the longest time published for capnoperitoneum in an animal survival study. In summary with previous investigations it seems reasonable to conclude that together with the results of our study a capnoperitoneum with up to 15 mmHg for eight hours is a safe setup for investigating NOTES procedures in pig models. Moreover gastrointestinal transit is not affected by this prolonged capnoperitoneum in pigs. NOTES procedures combining laparoscopic and endoscopic techniques should be carefully investigated for POI.

Animal protection and ethics approval: Lower Saxony Ministry for consumer protection and food safety, Oldenburg, Germany. File reference 33.9-4250204-06/1151, 16.09.2010. Funding Dr. Borchert none, Funding Dr. Köhler none, Funding Dr. Jäger none, Funding Dr. Diederich none, Funding Dr. Hüther none, Funding Dr. Berk none, Funding Prof. Lamade none. Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper. References 1. Hochberger J, Menke D, Matthes K, Lamade W, Kohler P. Transluminal interventions ("NOTES")–status quo. Dtsch Med Wochenschr. 2009;134:467–72. 2. Auyang ED, Santos BF, Enter DH, Hungness ES, Soper NJ. Natural orifice translumenal endoscopic surgery (NOTES((R))): a technical review. Surg Endosc. 2011;25: 3135–48. 3. Lamade W, Schymik K, Rieber F, Friedrich C, Etzrodt J, Ulmer C, et al. Snake charmer NOTES-proctocolectomy in a male patient. Chirurg. 2011;82:719–22. 4. Kalff JC, Schraut WH, Simmons RL, Bauer AJ. Surgical manipulation of the gut elicits an intestinal muscularis inflammatory response resulting in postsurgical ileus. Ann Surg. 1998;228:652–63. 5. Silva A, Hung SH, Mathiesen KA, Wolfe BM. Gastrointestinal endoscopy combined with laparoscopy or laparotomy. Surg. Endosc. 1997;11:214. 6. Souma Y, Nakajima K, Takahashi T, Nishimura J, Fujiwara Y, Takiguchi S, et al. The role of intraoperative carbon dioxide insufflating upper gastrointestinal endoscopy during laparoscopic surgery. Surg Endosc. 2009;23:2279–85. 7. Artinyan A, Nunoo-Mensah JW, Balasubramaniam S, Gauderman J, Essani R, Gonzalez-Ruiz C, et al. Prolonged postoperative ileus-definition, risk factors, and predictors after surgery. World J Surg. 2008;32:1495–500. 8. Lamade W, Hochberger J, Ulmer C, Matthes K, Thon KP. Triluminal hybrid NOS as a novel approach for colonic resection with colorectal anastomosis. Surg Innov. 2010;17:28–35. 9. Abraham NS, Byrne CM, Young JM, Solomon MJ. Meta-analysis of non-randomized comparative studies of the short-term outcomes of laparoscopic resection for colorectal cancer. ANZ J Surg. 2007;77:508–16. 10. Lamade W, Rieber F, Kohler P, Friedrich C, Diederich M, Basar T, et al. Snake charmer NOTES: a two-luminal access for hybrid NOS operations. Minim Invasive Ther Allied Technol. 2011;20:257–62. 11. Hardacre JM, Talamini MA. Pulmonary and hemodynamic changes during laparoscopy–are they important? Surgery. 2000;127:241–4. 12. ASGE; SAGES. ASGE/SAGES working group on natural orifice translumenal endoscopic surgery white paper october 2005. Gastrointest Endosc. 2006;63:199–203. 13. Kolb E. Die Regulation der Körpertemperatur. In Kolb E, editor. Lehrbuch der physiologie der haustiere. Stuttgart: Gustav Fischer Verlag, 1989. p 640–55.

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Prolonged capnoperitoneum does not cause postoperative ileus in pigs: safety of prolonged capnoperitoneum.

Operative time is an accepted risk factor for the development of postoperative ileus (POI). Innovative surgical procedures such as robotic surgery and...
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