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The apoptosis of peripheral blood lymphocytes promoted by hyperbaric oxygen treatment contributes to attenuate the severity of early stage acute pancreatitis in rats

Apoptosis volume 19, pages 58–75 (2014)Cite this article

Abstract

The aim of this study was to investigate the immunoregulatory effects of hyperbaric oxygen (HBO) via promoting the apoptosis of peripheral blood lymphocytes (PBLs) to attenuate the severity of early stage acute pancreatitis (AP) in rats. Additionally, the persistence of the HBO treatment effects was evaluated. One hundred and twenty male Wistar rats were randomized into four groups: sham, AP, AP + normobaric oxygen (NBO), and AP + HBO. Each group consisted of 30 rats. Four hours after the induction of AP, the 30 rats in the AP + NBO group were given normobaric oxygen treatment with 100 % oxygen at 1 atm for 90 min. The 30 rats in the AP + HBO group received 100 % oxygen at 2.5 atm for 90 min, with a compression/decompression time of 15 min. The 30 rats in the AP group remained untreated. At 6, 12, and 24 h after the induction of AP, surviving rats from each group were sacrificed, and the blood and tissue samples were collected for the following measurements: the partial pressure of oxygen (PaO2) and oxygen saturation (SaO2) of the arterial blood, the levels of serum amylase, lipase, interleukin-2 (IL-2), interferon-γ (IFN-γ), interleukin-10 (IL-10), hepatocyte growth factor (HGF), and reactive oxygen species (ROS), and the mitochondrial membrane potential (∆Ψm) of the PBLs. The expression levels of procaspase-3, caspase-3, procaspase-9, and caspase-9 were also evaluated in the PBLs. Additionally, the apoptosis of PBLs was assessed, and the pancreatic tissues were subjected to a histopathological analysis by pathological grading and scoring. The histopathology of the lung, liver, kidney, duodenum, and heart was also analyzed at 12 h after the induction of AP. Significant differences were found at 6 and 12 h after AP induction. The HBO treatment significantly elevated the PaO2 and SaO2 levels, and the ROS levels in the PBLs. Additionally, HBO downregulated the levels of amylase and lipase. The HBO treatment also reduced the ∆Ψm levels, upregulated the expression of caspase-3 and caspase-9, and increased the apoptosis rate of the PBLs. Moreover, the HBO treatment decreased the serum concentrations of IL-2, IFN-γ and HGF, and reduced the pathological scores of the pancreatic tissue. The histopathological changes of the lung, liver, kidney, duodenum, and heart were also improved. A significant elevation of IL-10 occurred only at the 12-h time point. However, no obvious differences were found at the 24-h time point. This study demonstrated that the HBO treatment can promote the apoptosis of PBLs via a mitochondrial-dependent pathway and inhibit the inflammatory response. These immunoregulatory effects may play an important therapeutic role in attenuating the severity of early stage AP. The repeated administration of HBO or the use of HBO in combination with other approaches may further improve outcomes.

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Acknowledgments

We acknowledge the technical advice of Liu Meina from the Department of Biostatistics of Public Health of Harbin Medical University in Harbin, China. Also, Dr. Zhu Hong, from the Department of Pathology at the First Affiliated Hospital at Harbin Medical University in Harbin, China assisted us with the evaluation of pathological scores from pancreatic tissues. Finally, we thank Dr. Fu Lu and Dr. Teng Yueqiu of the Department of Medical Laboratory at the First Affiliated Hospital of Harbin Medical University in Harbin, China for their ongoing supports of this research. This paper was supported by grants from the National Natural Scientific Foundation of China (No: 30901437, 81170431, 81100314, 81101799), the Chinese Research Fund for the Doctoral Program of Higher Education (No: 20102307120002), the Chinese Natural Science Foundation of Heilongjiang Province (No: QC08C63), the Chinese Foundation for University Key Teacher of Heilongjiang Province (No: 1155G35), the Chinese Innovative Science and Technology Research Fund of Harbin (No: 2010RFQQS059), the Postdoctoral Science Foundation of the Heilongjiang Province of China and the Doctoral Science Foundation of the First Affiliated Hospital of Harbin Medical University.

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The authors declare no conflict of interest.

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Authors and Affiliations

  1. Department of Pancreatic and Biliary Surgery, First Affiliated Hospital of Harbin Medical University, 23 Youzheng Street, Nangang District, Harbin, 150001, Heilongjiang Province, China

    Xuewei Bai, Zengfu Song, Zuoming Guo, Maitao Jiang, Gang Wang, Rui Kong & Bei Sun

  2. Department of Anesthesiology, First Affiliated Hospital of Harbin Medical University, Harbin, Heilongjiang Province, China

    Yanmei Zhou

  3. Central Laboratory, First Affiliated Hospital of Harbin Medical University, Harbin, Heilongjiang Province, China

    Shangha Pan

  4. Department of Hyperbaric Oxygen, First Affiliated Hospital of Harbin Medical University, Harbin, Heilongjiang Province, China

    Feng Wang

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  1. Xuewei Bai
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  2. Zengfu Song
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  3. Yanmei Zhou
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  4. Shangha Pan
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  5. Feng Wang
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  6. Zuoming Guo
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  7. Maitao Jiang
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  8. Gang Wang
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  9. Rui Kong
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  10. Bei Sun
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Correspondence to Bei Sun.

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Bai, X., Song, Z., Zhou, Y. et al. The apoptosis of peripheral blood lymphocytes promoted by hyperbaric oxygen treatment contributes to attenuate the severity of early stage acute pancreatitis in rats. Apoptosis 19, 58–75 (2014). https://doi.org/10.1007/s10495-013-0911-x

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  • DOI: https://doi.org/10.1007/s10495-013-0911-x

Keywords

  • Acute pancreatitis
  • Inflammation
  • Hyperbaric oxygen
  • Peripheral blood lymphocytes
  • Apoptosis
  • Cytokine