Surgical Endoscopy

, Volume 27, Issue 9, pp 3465–3473 | Cite as

Carbon dioxide gas pneumoperitoneum induces minimal microcirculatory changes in neonates during laparoscopic pyloromyotomy

  • Stefaan H. A. J. Tytgat
  • David C. van der Zee
  • Can Ince
  • Dan M. J. MilsteinEmail author
Dynamic Manuscript



Little is known about the direct effect of pneumoperitoneum (PP) on microcirculation and its influence on the quality of tissue perfusion. This study aimed to investigate the intraoperative effects of carbon dioxide (CO2) gas PP on microcirculation density and perfusion in neonates receiving laparoscopic surgery for hypertrophic pyloric stenosis.


In a single-center observational study, the oral microcirculation in 12 neonates receiving laparoscopic pyloromyotomy was investigated. Intraoperative hemodynamic parameters, intermittent buccal mucosa capillary density measurements (pre- and postoperative), and continuous intraoperative sublingual microcirculation measurements (i.e., vessels with a diameter <25 μm) of total vessel density, perfused vessel density, proportion of perfused blood vessels, blood vessel diameters (BVd), and microvascular flow index were obtained before (at baseline), during, and after PP insufflation for all patients using sidestream dark-field imaging for the duration of the complete surgical procedure.


With the exception of a significantly elevated end-tidal CO2 (34 ± 4–40 ± 8 mmHg; p < 0.05 vs before [baseline], one-way analysis of variance [ANOVA]) during intraoperative insufflation, no significant differences were found between time points for the intraoperative hemodynamic parameters. Pre- and postoperative buccal capillary density showed no significant changes in mucosal perfusion. Analysis of continuous intraoperative sublingual microcirculation parameters exhibited a statistically significant increase in BVd during insufflation (8.8 ± 2.4–9.3 ± 2.5 μm; p < 0.05, one-way ANOVA) and a significant decrease after exsufflation (8.2 ± 2.3 μm; p < 0.01 vs during insufflation and p < 0.05 vs baseline, one-way ANOVA, respectively). No other significant differences were found between time points for the remaining microcirculatory parameters.


The installation of CO2 gas PP during laparoscopic pyloromyotomy procedures regulates microcirculatory perfusion by inducing changes in microvascular diameters but does not alter microcirculation density in neonates.


Laparoscopy Microcirculation Neonate Pneumoperitoneum SDF imaging 



We acknowledge and thank all the families who kindly consented to participate in this study. We are grateful to the anesthesiologists and operating theater staff for their cooperation and support for this investigation.


Can Ince is the inventor of the SDF imaging technique and as such holds patents on this technology. Stefaan H. A. J. Tytgat, David C. van der Zee, and Dan M. J. Milstein have no conflicts of interest or financial ties to disclose.

Supplementary material

Supplementary material 1 (MOV 14149 kb)

Supplementary material 2 (MOV 109903 kb)


  1. 1.
    te Velde EA, Bax NM, Tytgat SH, de Jong JR, Vieira Travassos D, Kramer WL, van der Zee DC (2008) Minimally invasive pediatric surgery: increasing implementation in daily practice and resident’s training. Surg Endosc 22:163–166CrossRefGoogle Scholar
  2. 2.
    Bishay M, Giacomello L, Retrosi G, Thyoka M, Nah SA, McHoney M, De Coppi P, Brierley J, Scuplak S, Kiely EM, Curry JI, Drake DP, Cross KMK, Eaton S, Pierro A (2011) Decreased cerebral oxygen saturation during thoracoscopic repair of congenital diaphragmatic hernia and esophageal atresia in infants. J Pediatr Surg 46:47–51PubMedCrossRefGoogle Scholar
  3. 3.
    Yürük K, Milstein DM, Bezemer R, Bartels SA, Biemond BJ, Ince C (2012) Transfusion of banked red blood cells and the effects on hemorrheology and microvascular hemodynamics in anemic hematology outpatients. Transfusion. doi: 10.1111/j.1537-2995.2012.03905.x
  4. 4.
    Atasever B, Boer C, Speekenbrink R, Seyffert J, Goedhart P, de Mol B, Ince C (2011) Cardiac displacement during off-pump coronary bypass grafting surgery: effect on sublingual microcirculation and cerebral oxygenation. Interact Cardiovasc Thorac Surg 13:573–577PubMedCrossRefGoogle Scholar
  5. 5.
    Atasever B, Boer C, Goedhart P, Biervliet J, Seyffert J, Speekenbrink R, Schwarte L, de Mol B, Ince C (2011) Distinct alterations in sublingual microcirculatory blood flow and hemoglobin oxygenation in on-pump and off-pump coronary artery bypass graft surgery. J Cardiothorac Vasc Anesth 25:784–790PubMedCrossRefGoogle Scholar
  6. 6.
    De Backer D, Creteur J, Preiser JC, Dubois MJ, Vincent JL (2002) Microvascular blood flow is altered in patients with sepsis. Am J Respir Care Med 166:98–104CrossRefGoogle Scholar
  7. 7.
    Sakr Y, Dubois MJ, De Backer D, Creteur J, Vincent JL (2004) Persistent microcirculatory alterations are associated with organ failure and death in patients with septic shock. Crit Care Med 32:1825–1831PubMedCrossRefGoogle Scholar
  8. 8.
    Ince C (2005) The microcirculation is the motor of sepsis. Crit Care 9:S13–S19PubMedCrossRefGoogle Scholar
  9. 9.
    Milstein DM, Bezemer R, Lindeboom JA, Ince C (2009) The acute effects of CMF-based chemotherapy on maxillary periodontal microcirculation. Cancer Chemother Pharmacol 64:1047–1052PubMedCrossRefGoogle Scholar
  10. 10.
    Milstein DM, te Boome LC, Cheung YW, Lindeboom JA, van den Akker HP, Biemond BJ, Ince C (2010) Use of sidestream dark-field (SDF) imaging for assessing the effects of high-dose melphalan and autologous stem cell transplantation on oral mucosal microcirculation in myeloma patients. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 109:91–97PubMedCrossRefGoogle Scholar
  11. 11.
    Steeghs N, Gelderblom H, Roodt JO, Christensen O, Rajagopalan P, Hovens M, Putter H, Rabelink TJ, de Koning E (2008) Hypertension and rarefaction during treatment with telatinib, a small molecule angiogenesis inhibitor. Clin Cancer Res 14:3470–3476PubMedCrossRefGoogle Scholar
  12. 12.
    Top AP, Ince C, van Dijk M, Tibboel D (2009) Changes in buccal microcirculation following extracorporeal membrane oxygenation in term neonates with severe respiratory failure. Crit Care Med 37:1121–1124PubMedCrossRefGoogle Scholar
  13. 13.
    Top AP, Ince C, Schouwenberg PH, Tibboel D (2011) Inhaled nitric oxide improves systemic microcirculation in infants with hypoxemic respiratory failure. Pediatr Crit Care Med 12:e271–e274PubMedCrossRefGoogle Scholar
  14. 14.
    Top AP, Ince C, de Meij N, van Dijk M, Tibboel D (2011) Persistent low microcirculatory vessel density in nonsurvivors of sepsis in pediatric intensive care. Crit Care Med 39:8–13PubMedCrossRefGoogle Scholar
  15. 15.
    Genzel-Boroviczény O, Christ F, Glas V (2004) Blood transfusion increases functional capillary density in the skin of anemic preterm infants. Pediatr Res 56:751–755PubMedCrossRefGoogle Scholar
  16. 16.
    Weidlich K, Kroth J, Nussbaum C, Hiedl S, Bauer A, Christ F, Genzel-Boroviczeny O (2009) Changes in microcirculation as early markers for infection in preterm infants: an observational prospective study. Pediatr Res 66:461–465PubMedCrossRefGoogle Scholar
  17. 17.
    Hiedl S, Schwepcke A, Weber F, Genzel-Boroviczeny O (2010) Microcirculation in preterm infants: profound effects of patent ducts arteriosis. J Pediatr 156:191–196PubMedCrossRefGoogle Scholar
  18. 18.
    Blumhagen JD, Maclin L, Krauter D, Rosenbaum DM, Weinberger E (1988) Sonographic diagnosis of hypertrophic pyloric stenosis. AJR Am J Roentgenol 150:1367–1370PubMedCrossRefGoogle Scholar
  19. 19.
    Najmaldin A, Tan HL (1995) Early experience with laparoscopic pyloromyotomy for infantile hypertrophic pyloric stenosis. J Pediatr Surg 30:37–38PubMedCrossRefGoogle Scholar
  20. 20.
    Goedhart PT, Khalilzada M, Bezemer R, Merza J, Ince C (2007) Sidestream dark-field (SDF) imaging: a novel stroboscopic LED ring-based imaging modality for clinical assessment of the microcirculation. Opt Express 15:15101–15114PubMedCrossRefGoogle Scholar
  21. 21.
    Milstein DMJ, Bezemer R, Ince C (2012) Sidestream dark-field (SDF) video microscopy for clinical imaging of the microcirculation. In: Leahy MJ (ed) Microcirculation imaging. Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, pp 37–52CrossRefGoogle Scholar
  22. 22.
    De Backer D, Hollenberg S, Boerma C, Goedhart P, Büchele G, Ospina-Tascon G, Dobbe I, Ince C (2007) How to evaluate the microcirculation: report of a round table conference. Crit Care 11:R101PubMedCrossRefGoogle Scholar
  23. 23.
    Spronk PE, Ince C, Gardien MJ, Mathura KR, Oudemans-van Straaten HM, Zandstra DF (2002) Nitroglycerin in septic shock after intravascular volume resuscitation. Lancet 360:1395–1396PubMedCrossRefGoogle Scholar
  24. 24.
    Boerma EC, Mathura KR, van der Voort PH, Spronk PE, Ince C (2005) Quantifying bedside-derived imaging of microcirculatory abnormalities in septic patients: a prospective validation study. Crit Care 9:R601–R606PubMedCrossRefGoogle Scholar
  25. 25.
    Jia WQ, Tian JH, Yang KH, Ma B, Liu YL, Zhang P, Li RJ, Jia RH (2011) Open versus laparoscopic pyloromyotomy for pyloric stenosis: a meta-analysis of randomized controlled trials. Eur J Pediatr Surg 21:77–81PubMedCrossRefGoogle Scholar
  26. 26.
    Hall NJ, Pacilli M, Eaton S, Reblock K, Gaines BA, Pastor A, Langer JC, Koivusalo AI, Pakarinen MP, Stroedter L, Beyerlein S, Haddad M, Clarke S, Ford H, Pierro A (2009) Recovery after open versus laparoscopic pyloromyotomy for pyloric stenosis: a double-blind multicentre randomised controlled trial. Lancet 373:390–398PubMedCrossRefGoogle Scholar
  27. 27.
    Laing S, Walker K, Ungerer J, Badawi N, Spence K (2011) Early development of children with major birth defects requiring newborn surgery. J Paediatr Child Health 47:140–147PubMedCrossRefGoogle Scholar
  28. 28.
    Gutt CN, Oniu T, Mehrabi A, Schemmer P, Kashfi A, Kraus T, Büchler MW (2004) Circulatory and respiratory complications of carbon dioxide insufflation. Dig Surg 21:95–105PubMedCrossRefGoogle Scholar
  29. 29.
    Rasmussen JP, Dauchot PJ, DePalma RG, Sorensen B, Regula G, Anton AH, Gravenstein JS (1978) Cardiac function and hypercarbia. Arch Surg 113:1196–1200PubMedCrossRefGoogle Scholar
  30. 30.
    Simmons GH, Minson CT, Cracowski JL, Halliwill JR (2007) Systemic hypoxia causes cutaneous vasodilation in healthy humans. J Appl Physiol 103:608–615PubMedCrossRefGoogle Scholar
  31. 31.
    Groner W, Winkelman JW, Harris AG, Ince C, Bouma GJ, Messmer K, Nadeau RG (1999) Orthogonal polarization spectral imaging: a new method for study of the microcirculation. Nat Med 5:1209–1212PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Stefaan H. A. J. Tytgat
    • 1
  • David C. van der Zee
    • 1
  • Can Ince
    • 2
  • Dan M. J. Milstein
    • 2
    • 3
    Email author
  1. 1.Department of Pediatric SurgeryWilhelmina Children’s Hospital, University Medical Center UtrechtUtrechtThe Netherlands
  2. 2.Department of Translational PhysiologyAcademic Medical Center, University of AmsterdamAmsterdamThe Netherlands
  3. 3.Department of Oral and Maxillofacial SurgeryAcademic Medical Center, University of AmsterdamAmsterdamThe Netherlands

Personalised recommendations