Effects of pulmonary stretch reflex on lung injury in rabbits with acute respiratory distress syndrome

doi:10.5847/wjem.j.1920-8642.2011.04.010

Abstract

Abstract:

BACKGROUND: Pulmonary stretch reflex plays an important role in regulation of respiratory movement. This study aimed to evaluate the effect of pulmonary stretch reflex on lung injury in rabbits with acute respiratory distress syndrome (ARDS).
METHODS: ARDS rabbits were given intratracheal infusion of hydrochloric acid and ventilated with neurally adjusted ventilatory assistance (NAVA) with a tidal volume (V_T) of 6 mL/kg and the electrical activity of diaphragm (EAdi)-determined positive end expiratory pressure. After isolation of the bilateral vagus nerve trunk, the rabbits were randomized into two groups: sham operation (SHAM) group (n=5) and bilateral vagotomy (VAG) group (n=5). Gas exchange and respiratory mechanics were detected at baseline, after lung injury and 1, 2, and 3 hours after ventilation respectively. Pulmonary permeability index, pathological changes and inflammatory response were also measured.
RESULTS: Compared with the SHAM group, PaO₂/FiO₂ in the VAG group decreased significantly 2 and 3 hours after ventilation (P<0.05). There was no significant difference in PaCO₂ between the SHAM and VAG groups (P>0.05), and the VAG group had a high V_T, peak pressure (Ppeak), and mean pressure (Pm) compared with the SHAM group 1, 2, 3 hours after ventilation (P<0.05). Compared to the SHAM group, dead space fraction (V_D/V_T) and respiratory system elastance (Ers) in the VAG group increased (P<0.05) and static pulmonary compliance (Cst) decreased markedly (P<0.05) after ventilation for 3 hours. Lung wet/dry weight ratio (W/D) (8.4±1.2 vs. 6.6±1.0), lung injury score (6.3±1.8 vs. 3.8±1.3), tumor necrosis factor-α (TNF-α) (779±372 pg/mL vs. 355±130 pg/mL) and interleukin-8 (IL-8) (169±21 pg/mL vs. 118±17 pg/mL) increased significantly in the VAG group compared with the SHAM group (P<0.05).
CONCLUSION: Lung injury is aggravated after bilateral vagotomy, demonstrating that pulmonary stretch reflex may have protective effect on the lung.

Key words: Pulmonary stretch reflex, Vagus nerve, Lung injury, Acute respiratory distress syndrome, Electrical activity of diaphragm, Mechanical ventilation

Xiao-yan Wu, Ying-zi Huang, Huo-gen Liu, Dong-ya Huang, Rui Tang, Hai-bo Qiu. Effects of pulmonary stretch reflex on lung injury in rabbits with acute respiratory distress syndrome[J]. World Journal of Emergency Medicine, 2011, 2(4): 296-301.

Figures/Tables 4

Table 1

Table 2

Table 3

Figure 1.

References 20

1	Widdicombe J. Reflexes from the lungs and airways: historical perspective. J Appl Physiol 2006; 101:628-634. pmid: 16601307
2	Cross BA, Jones PW, Guz A. The role of vagal afferent information during inspiration in determining phrenic motoneurone output. Respir Physiol 1980; 39:149-167. doi: 10.1016/0034-5687(80)90042-0 pmid: 6769141
3	Malhotra A. Low-tidal-volume ventilation in the acute respiratory distress syndrome. N Engl J Med 2007; 357:1113-1120. pmid: 17855672
4	Terragni PP, Rosboch G, Tealdi A, Corno E, Menaldo E, Davini O, et al. Tidal hyperinflation during low tidal volume ventilation in acute respiratory distress syndrome. Am J Respir Crit Care Med 2007; 175:160-166. pmid: 17038660
5	Katherine J, Peter C. Mechanical ventilation in ARDS: one size does not fit all. Crit Care Med 2005; 33:1141-1143. doi: 10.1097/01.CCM.0000162384.71993.A3
6	Greenfield LJ, Singleton RP, McCaffree DR, Coalson JJ. Pulmonary effects of experimental graded aspiration of hydrochloric acid. Ann Surg 1969; 170:74-86. pmid: 5789532
7	Imai Y, Parodo J, Kajikawa O, de Perrot M, Fischer S, Edwards V, et al. Injurious mechanical ventilation and end-Organ epithelial cell apoptosis and organ dysfunction in an experimental model of acute respiratory distress syndrome. JAMA 2003; 289:2104-2112. pmid: 12709468
8	Sinderby C, Navalesi P, Beck J, Skrobik Y, Comtois N, Friberg S, et al. Neural control of mechanical ventilation. Nat Med 1999; 5:1433-1436. pmid: 10581089
9	Allo JC, Beck JC, Brander L, Brunet F, Slutsky AS, Sinderby CA. Influence of neurally adjusted ventilatory assist and positive end-expiratory pressure on breathing pattern in rabbits with acute lung injury. Crit Care Med 2006; 34:2997-3004. doi: 10.1097/01.CCM.0000242520.50665.9F pmid: 16957635
10	Brander L, Leong-Poi H, Beck J, Brunet F, Hutchison SJ, Slutsky AS, et al. Titration and implementation of neurally adjusted ventilatory assist in critically ill patients. Chest 2009; 135:695-703. pmid: 19017889
11	Valenza F, Guglielmi M, Maffioletti M, Tedesco C, Maccagni P, Fossali T, et al. Prone position delays the progression of ventilator-induced lung injury in rats: does lung strain distribution play a role? Crit Care Med 2005; 33:361-367. pmid: 15699840
12	Smith KM, Mrozek JD, Simonton SC, Bing DR, Meyers PA, Connett JE, et al. Prolonged partial liquid ventilation using conventional and high-frequency ventilatory techniques: gas exchange and lung pathology in an animal model of respiratory distress syndrome. Crit Care Med 1997; 25:1888-1897. doi: 10.1097/00003246-199711000-00030 pmid: 9366775
13	Lin S, Walker J, Xu L, Gozal D, Yu J. Behaviours of pulmonary sensory receptors during development of acute lung injury in the rabbit. Exp Physiol 2006; 92:749-755.
14	Zhang JW, Walker JF, Guardiola J, Yu J. Pulmonary sensory and reflex responses in the mouse. J Appl Physiol 2006; 101:986-992.
15	Wong KA, Bano A, Rigaux A, Wang B, Bharadwaj B, Schürch S, et al. Pulmonary vagal innervation is required to establish adequate alveolar ventilation in the newborn lamb. J Appl Physiol 1998; 85:849-859. pmid: 9729557
16	Berry D, Ikegami M, Jobe A. Respiratory distress and surfactant inhibition following vagotomy in rabbits. J Appl Physiol 1986; 61:1741-1748. pmid: 3781984
17	Lalani S, Remmers JE, Green FH, Bukhari A, Ford GT, Hasan SU. Effects of vagal denervation on cardiorespiratory and behavioral responses in the newborn lamb. J Appl Physiol 2001; 91:2301-2313. doi: 10.1152/jappl.2001.91.5.2301 pmid: 11641375
18	Thomas R, Bernik MD, Steven G. Cholinergic anti-inflammatory pathway inhibition of tumor necrosis factor during ischemia reperfusion. J Vasc Surg 2002; 36:1231-1236.
19	Bernik TR, Friedman SG, Ochani M, DiRaimo R, Ulloa L, Yang H, et al. Pharmacological stimulation of the cholinergic antiinflammotory pathway. J Exp Med 2002; 195:781-788. doi: 10.1084/jem.20011714 pmid: 11901203
20	Borovikova LV, Ivanova S, Zhang M, Yang H, Botchkina GI, Watkins LR, et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 2000; 405:458-462. pmid: 10839541

Variables	Baseline	ARDS	Ventilation 1 h	Ventilation 2 h	Ventilation 3 h
MAP (mmHg)
SHAM	75.5±10.8	81.5±12.2	65.3±5.7	65.7±6.3	62.7±2.7
VAG	83.1±11.2	75.0±12.2	75.0±14.0	73.0±14.4	65.0±2.4
PaO₂/FiO₂(mmHg)
SHAM	367.3±67.9	133.9±28.2	399.1±62.0	399.7±85.7	392.2±47.0
VAG	475.9±89.0	134.4±26.1	298.5±148.3	237.5±83.9^*	285.2±33.1^*
PaCO₂(mmHg)
SHAM	56.1±6.2	53.3±9.5	47.2±6.1	46.3±7.0	47.9±10.9
VAG	59.1±8.4	54.3±17.1	58.8±18.4	47.9±9.0	51.2±7.0
V_D/V_T
SHAM	0.118±0.018	0.380±0.146			0.310±0.037
VAG	0.119±0.045	0.402±0.114			0.445±0.037^*

Variables	Baseline	ARDS	Ventilation 1 h	Ventilation 2 h	Ventilation 3 h
V_T (mL/kg)
SHAM	6.1±0.1	6.2±0.2	5.5±0.5	5.2±0.4	4.7±0.8
VAG	6.3±0.2	6.2±0.2	9.9±3.5^*	8.5±1.2^*	8.9±0.4^*
Ppeak (cmH₂O)
SHAM	7.3±1.6	11.8±3.0	18.1±2.3	19.4±1.4	20.0±1.0
VAG	5.9±1.6	12.4±2.2	29.3±8.3^*	25.7±3.2^*	27.0±1.6^*
Pm (cmH₂O)
SHAM	3.4±0.6	5.1±0.8	13.3±1.4	13.7±1.2	14.0±0.6
VAG	3.1±0.7	5.5±1.1	17.4±4.6^*	16.5±3.2^*	16.1±0.7^*
PEEP (cmH₂O)
SHAM	2.0±0.1	2.6±0.5	10.4±0.9	10.3±1.0	10.6±0.6
VAG	2.0±0.1	2.5±0.6	10.7±2.9	10.7±2.9	11.1±1.2
Ers (cmH₂O/mL)
SHAM	0.35±0.06	0.64±0.12			0.72±0.07
VAG	0.34±0.08	0.72±0.10			0.93±0.03
Cst (mL/cmH₂O)
SHAM	2.90±0.50	1.62±0.31			1.41±0.13
VAG	3.07±0.63	1.41±0.20			1.08±0.03^*

Variables	SHAM	VAG
W/D	6.6±1.0	8.4±1.2^*
Lung injury score	3.8±1.3	6.3±1.8^*
TNF-α (pg/mL)	355±130	779±372^*
IL-8 (pg/mL)	118±17	169±21^*

[1]	Zi-wei Ke, Yue Jiang, Ya-ping Bao, Ye-qin Yang, Xiao-mei Zong, Min Liu, Xiang-yun Guan, Zhong-qiu Lu. Intensivists’ response to hyperoxemia in mechanical ventilation patients: The status quo and related factors [J]. World Journal of Emergency Medicine, 2021, 12(3): 202-206.
[2]	Yu-qing Cui, Xian-fei Ding, Huo-yan Liang, Dong Wang, Xiao-juan Zhang, Li-feng Li, Quan-cheng Kan, Le-xin Wang, Tong-wen Sun. Efficacy and safety of low-dose corticosteroids for acute respiratory distress syndrome: A systematic review and meta-analysis [J]. World Journal of Emergency Medicine, 2021, 12(3): 207-213.
[3]	Hao-tian Chen, Jian-feng Xu, Xiao-xia Huang, Ni-ya Zhou, Yong-kui Wang, Yue Mao. Blood eosinophils and mortality in patients with acute respiratory distress syndrome: A propensity score matching analysis [J]. World Journal of Emergency Medicine, 2021, 12(2): 131-136.
[4]	Yi Han, Su-cheng Mu, Jian-li Wang, Wei Wei, Ming Zhu, Shi-lin Du, Min Min, Yun-jie Xu, Zhen-ju Song, Chao-yang Tong. MicroRNA-145 plays a role in mitochondrial dysfunction in alveolar epithelial cells in lipopolysaccharide-induced acute respiratory distress syndrome [J]. World Journal of Emergency Medicine, 2021, 12(1): 54-60.
[5]	Yu-ming Wang, Yan-jun Zheng, Ying Chen, Yun-chuan Huang, Wei-wei Chen, Ran Ji, Li-li Xu, Zhi-tao Yang, Hui-qiu Sheng, Hong-ping Qu, En-qiang Mao, Er-zhen Chen. Effects of fluid balance on prognosis of acute respiratory distress syndrome patients secondary to sepsis [J]. World Journal of Emergency Medicine, 2020, 11(4): 216-222.
[6]	Yi-wen Fan, Shao-wei Jiang, Jia-meng Chen, Hui-qi Wang, Dan Liu, Shu-ming Pan, Cheng-jin Gao. A pulmonary source of infection in patients with sepsis-associated acute kidney injury leads to a worse outcome and poor recovery of kidney function [J]. World Journal of Emergency Medicine, 2020, 11(1): 18-26.
[7]	Suresh Kumar Arumugam, Insolvisagan Mudali, Gustav Strandvik, Ayman El-Menyar, Ammar Al-Hassani, Hassan Al-Thani. Risk factors for ventilator-associated pneumonia in trauma patients: A descriptive analysis [J]. World Journal of Emergency Medicine, 2018, 9(3): 203-210.
[8]	Hui Xie, Zhi-gang Zhou, Wei Jin, Cheng-bin Yuan, Jiang Du, Jian Lu, Rui-lan Wang. Ventilator management for acute respiratory distress syndrome associated with avian influenza A (H7N9) virus infection: A case series [J]. World Journal of Emergency Medicine, 2018, 9(2): 118-124.
[9]	Ming Wei, Yan-jie Gong, Ling Tu, Jia Li, Ying-hong Liang, Yi-hua Zhang. Expression of phosphatidylinositol-3 kinase and effects of inhibitor Wortmannin on expression of tumor necrosis factor-α in severe acute pancreatitis associated with acute lung injury [J]. World Journal of Emergency Medicine, 2015, 6(4): 299-304.
[10]	Ruo Wu, Shi-yun Lin, Hui-min Zhao. Albuterol in the treatment of acute respiratory distress syndrome: A meta-analysis of randomized controlled trials [J]. World Journal of Emergency Medicine, 2015, 6(3): 165-171.
[11]	Zhi-wei Liu, Hai-ying Wang, Lan Guan, Bin Zhao. Regulatory effects of hydrogen sulfide on alveolar epithelial cell endoplasmic reticulum stress in rats with acute lung injury [J]. World Journal of Emergency Medicine, 2015, 6(1): 67-73.
[12]	Ze-hua Dong, Bang-xu Yu, Yun-bo Sun, Wei Fang, Lei Li. Effects of early rehabilitation therapy on patients with mechanical ventilation [J]. World Journal of Emergency Medicine, 2014, 5(1): 48-52.
[13]	Shou-peng Li, Ji-yuan Han, Peng Sun, Guo-yan Wu, Xiang-yan Bai. Effect of SP-A/B in lipoic acid on acute paraquat poisoning [J]. World Journal of Emergency Medicine, 2014, 5(1): 57-62.
[14]	Rui-lan Wang, Kan Xu, Kang-long Yu, Xue Tang, Hui Xie. Effects of dynamic ventilatory factors on ventilator-induced lung injury in acute respiratory distress syndrome dogs [J]. World Journal of Emergency Medicine, 2012, 3(4): 287-293.
[15]	Rong-rong Song, Yan-ping Qiu, Yong-ju Chen, Yong Ji. Application of fiberoptic bronchscopy in patients with acute exacerbations of chronic obstructive pulmonary disease during sequential weaning of invasive-noninvasive mechanical ventilation [J]. World Journal of Emergency Medicine, 2012, 3(1): 29-34.