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Effects of Human Interleukin-10 on Ventilator-Associated Lung Injury in Rats

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Effects of Human Interleukin-10 on Ventilator-Associated Lung Injury in Rats Inflammation, Vol. 42, No. 2, April 2019 (# 2018) DOI: 10.1007/s10753-018-0911-7 ORIGINAL ARTICLE Effects of Human Interleukin-10 on Ventilator-Associated Lung Injury in Rats Jinzhuan Chen,1 Jianqing Lin,1,3 Huiqin Luo,2 and Minjie Li1 Abstract—Ventilator-induced lung injury (VILI) is one of the most serious complications of mechanical ventilation (MV) and can increase the mortality of patients with acute respiratory distress syndrome (ARDS). This work aimed to test the hypothesis that the anti-inflammatory properties of human interleukin-10 (hIL-10) can reduce VILI. Thirty-six healthy male Sprague-Dawley rats were randomly assigned into three groups (n = 12) as follows: a control group, a VILI group, and a hIL-10 group. Lung function was evaluated by oxygenation index and pulmonary edema, and morphological changes associated with lung injury were assessed by HE staining and quantitative histological lung injury score. Malondialdehyde (MDA) and Superoxide dismutase (SOD) were measured, and the levels of various inflammatory cyto- kines were assessed in BALF and plasma. The oxygenation index in the VILI group decreased significantly relative to the control group and improved substantially in the hIL- 10 group (P < 0.01). Compared to the control group, MDA production was stimulated (P < 0.01), and SOD activity rapidly declined (P < 0.01) in the VILI group. After hIL-10, MDA content was lower than that seen in the VILI group (P <0.01),andSODactivitywas enhanced (P < 0.01). The VILI group had the highest cytokine levels, compared to either the hIL-10 group or the control group (P < 0.05). High tidal volume MV can induce VILI. hIL-10 may regulate the inflammatory response in the lung tissue, improve lung tissue oxygenation, and inhibit oxidative stress, therefore reducing VILI in rats. These experiments reveal a potential new treatment option for VILI. KEY WORDS: human interleukin-10; ventilator-associated lung injury; mechanical ventilation. INTRODUCTION process of respiration [1]. Clinical studies have shown that patients who received MV were subjected to excessive dila- Mechanical ventilation (MV) is widely used in clinical tion of the alveoli by mechanical traction which induced anesthesia and critical care as an important means of respira- inflammation and caused acute lung injury (ALI), specifically tory support. However, MV is an external force and can defined as ventilator-induced lung injury (VILI) [2, 3]. VILI is induce or aggravate lung injury by interfering with the natural the most serious complication of MV, and the high mortality of patients with acute respiratory distress syndrome (ARDS) 1 Department of Anesthesiology, the First Hospital of Fujian Medical is due in part to this complication [4]. University, Fuzhou, 350005, China Previous studies have indicated that various pathways 2 ’ Department of Anesthesiology, the Affiliated People s Hospital of Fujian are involved in the causal mechanisms and devastating University of Traditional Chinese Medicine, Fuzhou, 350005, China 3 To whom correspondence should be addressed at Department of Anes- processes of VILI, including both the direct mechanical thesiology, the First Hospital of Fujian Medical University, Fu- damage and indirect biological injury [5]. Mechanical zhou, 350005, China. E-mail: [email protected] damage can mediate biological damage through multiple 538 0360-3997/19/0200-0538/0 # 2018 Springer Science+Business Media, LLC, part of Springer Nature IL-10 on Ventilator-Associated Lung Injury 539 pathways. During MV, the lungs are subjected to mechan- Factory. The rat TNF-α ELISA kit and the rat IL-8 ELISA ical stretch and direct damage to cell walls, leading to the kit were purchased from Fuzhou’s Biotech Corp. The rat release of a large number of cytokines in the alveolar and MDA and SOD test kit were obtained from Nanjing Insti- systemic circulatory systems, leading to both local and tute of Bioengineering. systemic inflammation. The main pathophysiological changes included alveolar structural damage, increased Study Design pulmonary vascular permeability, activation of various During developing an animal model of VILI, three inflammatory cells and inflammatory factors, and an im- rats died of respiratory depression and one died of respira- balance between oxidation and antioxidation [6]. tory tract obstruction. The remaining 36 male Sprague- Although a small tidal volume with positive end Dawley rats weighing 220~300 g were randomly divided expiratory pressure (PEEP) has been confirmed to effec- into three groups (n = 12). Tail vein catheterization and tively reduce VILI related to mechanical damage [7, 8], the tracheal intubation were performed after inducing anesthe- extensive application of MV coupled with an in-depth sia with 10% chloral hydrate (0.3 ml/100 g) transperitoneal understanding of the pathogenesis of VILI had led more injection for all rats. Spontaneous breathing was main- researchers to focus on biological injury [9] in the search tained in the control group, while both the VILI group for safe and effective options for MV. and hIL-10 group were mechanically ventilated for 4 h Interleukin-10 (IL-10) is an anti-inflammatory immu- with the following parameters: tidal volume (VT) = nosuppressive cytokine, known to play an important role in 30 ml/kg, respiratory rate (RR) = 40/min, respiratory ratio immune regulation and relevant to both inflammatory and (I:E) = 1:3, PEEP = 0, fraction of inspired oxygen (FiO )= infectious diseases [10]. An important feature of ALI is the 2 21%. Thirty minutes before ventilation, the hIL-10 group excessive expression of inflammatory mediators such as received 8000 U/kg hIL-10 by intravenous administration, tumor necrosis factor (TNF-α) and interleukin-8 (IL-8) while the control and VILI groups received saline solution [11]. A recent endotoxin study of ALI in a rat model found by intravenous administration. Anesthesia was maintained that exogenous IL-10 reduced pro-inflammatory cytokines with 10% chloral hydrate (0.2 ml/100 g) transperitoneal in pulmonary tissue and minimized lung injury [12]. injection for a 1-h interval in the control group. Anesthesia MV initiates systemic inflammation as well as aggra- was maintained with 10% chloral hydrate (0.2 ml/100 g) vated pulmonary inflammation [13, 14]. The injury is not transperitoneal injection and rocuronium (0.6 mg/kg) in- confined to the lungs, but also enhances the systemic travenous administration for a 1-h interval in the VILI inflammation reaction, increases the incidence of second- group and hIL-10 group. During anesthesia and ventila- ary beat, and facilitates multiple organ dysfunction syn- tion, laboratory temperature was kept at 22 ± 2 °C. Rectal dromes (MODS). temperature was maintained at 37 °C with the aid of servo- The effect of IL-10 on ALI has not been investigated controlled warming blanket (TCAT-2LV,Physitemp instru- sufficiently given the common application of MV for pa- ments Inc., Clifton, NJ). Heart rate and SpO were mea- tients with critical illness or under general anesthesia. Here, 2 sured continuously during anesthesia with a MouseOx™ we designed a VILI model using high tidal volume MVand Pulse Oximeter (Harvard Apparatus, Holliston, MA). After intravenously injected hIL-10 before MV application in experiments were completed, all animals were killed by order to investigate the protective role of hIL-10 and probe overdose of chloral hydrate followed by transection of the its potential mechanisms for the prevention of VILI. abdominal aorta and vena cava. Lungs were then extracted for histology and molecular biology analysis (Fig. 1). MATERIALS AND METHODS Collection and Processing of Blood Samples We used high VT MV to develop an animal model of All rats were euthanized after 4 h of ventilation and VILI in 40 healthy male Sprague-Dawley rats. The rats laparotomy. Blood samples were drawn from the abdomi- were purchased from Shanghai Slack Laboratory Animal nal aorta into a sterile syringe containing heparin. Some Co., LTD, and the administration of the experimental ani- were used for blood gas analysis and the calculation of mals was guided by the principles of the Fujian Medical arterial oxygenation index (PaO2/FiO2), and the others University Ethics Committee. hIL-10 was obtained from were transferred to procoagulant tubes and immediately the American PeproTech Corporation, and the DHX-150 placed in a pre-cooled 4 °C low temperature centrifuge rodent ventilator was purchased from Chengdu Instrument and spun at 3000 rpm/min for 10 min. After centrifugation, 540 Chen, Lin, Luo, and Li Fig. 1. Experimental technology. the supernatant aliquots were dispensed into 0.6 ml EP immunohistochemistry. The right middle lobe was clipped tubes, marked, and stored at − 80 °C in an ultralow tem- and weighed after excess liquid was gently absorbed with perature refrigerator for subsequent ELISA detection. clean gauze. After removal of the soft connective tissue, the lower lobe of the right lung was arranged in a 1.5-ml Collection and Treatment of Bronchoalveolar Lavage sterile centrifuge tube and frozen at – 80 °C in an ultralow Fluid temperature refrigerator for assays of malondialdehyde (MDA) content and superoxide dismutase (SOD) activity. The rat lung tissue and trachea were isolated, and a MDA is an intermediate product of oxidation after cell silk thread was tied to the right lung. A sterile syringe was damage resulting from inadequate oxygen scavenging ac- used to extract 2 ml of cold saline for bronchoalveolar tivity, which reflects the degree of membrane lipid perox- lavage through an endotracheal tube. The normal saline idation and the extent of the damage. SOD is a scavenger was absorbed after a brief incubation in the left lung, and of oxygen free radicals that plays a protective role in cells the process was repeated three times. The subsequent pro- and tissue. cessing and storage for ELISA of the bronchoalveolar lavage fluid was the same that described above for serum. Detection of each Index Collection and Treatment of the Lung Tissue Plasma and BALF were collected to detect the density The right upper lobe of the lung was quickly and of TNF-α, IL-8, and intercellular cell adhesion molecule-1 gently dissected.
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