Oxidative Medicine and Cellular Longevity

Review Article

Update on the Mechanisms of Pulmonary Inflammation and Oxidative Imbalance Induced by Exercise

Table 2

(a) Animal studies on lung oxidative stress and inflammation induced by acute exercise. (b) Animal studies on lung oxidative stress and inflammation induced by chronic exercise.

(a)


Author, year	Aim	Sample characteristics	Exercise protocols	Samples obtained	Oxidative or inflammatory main results

Akil et al. 2015 [105]	Se administration affects lipid peroxidation in liver and lung tissues of rats subjected to acute swimming exercise	Sprague-Dawley adult male rats divide into general control, Se-administered, swimming control, and Se-administered swimming groups	Swimming was performed once for 30 minutes	Lung tissue	PE: ↑ MDA and ↑ GSH in swimming control versus general control

Al-Hashem 2012 [106]	VitE and VitC in protection of pulmonary damage induced by exercise in altitude	Wistar rats with 6 months of altitude adaptation	Forced swimming for 2.5 h in glass tank at 600 and 2270 MASL in accordance with altitude adaptation	Lung tissue	PE: ↑ [TBARs], ↓ SOD, and CAT activity at 600 MASL Supplementation with VitE and VitC reversed these results

Caillaud et al. 1999 [107]	Effect of acute exercise on lipid peroxidation in lung compared with locomotor muscles	Wistar rats exercised (E) and control rats (C)	Race on treadmill at 28 m/min and 15% grade (80–85 VO₂max) until exhaustion (~66 min)	Lung tissue	PE: no changes of pulmonary activity of SOD, CAT, and [MDA] of E in comparison to C

Cathcart et al. 2013 [108]	Effects of exercise during different ambient temperatures and humidity on eNO, eCO, and pH	Thoroughbred racehorses	Exercised under saddle on an all-weather 1.6 km track at half-pace canter, full-pace canter, or gallop according to the current training regimen for each horse	EBC and EB	PE: only ↑ pH in EBC

Hatao et al. 2006 [109]	Acute exercise and antioxidant enzyme activation in aged rats	Young rats (YR) or aged rats (AR) exercised (E) or not exercised control (C)	Race on treadmill at 25 m/min for YRE and 18–20 m/min for ARE for 60 min	Lung tissue	PE: ↑ Mn-SOD activity in YRE and ARE in comparison to their control subjects; ↑ CuZn-SOD and CAT activity in YRE and ↓ reactive carbonyls derivative in ARE, in comparison to their control subjects

Huang et al. 2008 [110]	Supplementation with L-Arg on pulmonary inflammation and oxidative damage induced by exercise in aged rats	Sprague-Dawley rats exercised (E) or sedentary (S) with L-Arg (+L-Arg) or without control rats L-Arg (C)	Race on treadmill for groups E at ~70% VO₂max until exhaustion (time for E+L-Arg and EC ~63 and ~51 min, resp.)	Lung tissue	PE: ↑ [XO], ↑ [MPO], and ↑ [MDA] in EC in comparison to SC; with no changes between EC and SC for [SOD], [CAT], [GSH-Px], [GR], and [GSH]

Kirschvink et al. 2002 [13]	Oxidative state, pulmonary function, and airway inflammation in healthy horses and with arcades	Trained healthy horses, affected by arcades or clinical remission	Race on treadmill with 2 min to 8, 9, and 10 m/s and 4% inclination, stages interrupted by 2 jogs of 8 min to 3.5 m/s (10 min of warming up and 10 min of recovery)	BALF	PE: ↑ [UA] in healthy horses

Lin et al. 2005 [111]	Oxidative stress and antioxidant defenses in animals supplemented or not with L-Arg	Sprague-Dawley rats grouped as exercised (E) or sedentary (S) with L-Arg (+L-Arg) or control rats without L-Arg (C)	Race on treadmill for E groups at 20 m/min for 15 min and 25 m/min for 30 min; then they run at 30 m/min and 10% of inclination (70–75% VO₂max) until exhaustion (EC ~81 min and E+L-Arg ~87 min)	Lung tissue	PE: ↑ activity XO and MPO in EC in comparison to SC; ↑ [UA], ↑ [NO], and ↑ [MDA] in EC in comparison to SC; ↑ activity SOD and GR in EC in comparison to SC

Mills et al. 1996 [112]	eNO and VNO during acute exercise	Healthy horses	Maximal incremental race until 9 m/s	EB	DE: positive correlation of eNO and VNO with the race intensity

Radák et al. 1998 [113]	Acute anaerobic exercise and oxidative modification of pulmonary proteins	Exercised Wistar rats (E) and sedentary control rats (C)	Two races on treadmills at 30 m/min for 5 min; after 5 min of recovery, a 3rd race to exhaustion was performed	Lung tissue	PE: >pulmonary carbonyls and [glutamine synthetase] in E versus C

Reddy et al. 1998 [114]	Pulmonary oxidative damage by acute strenuous exercise in rats deficient in Se and VitE	Female Wistar albino rats deficient in Se and VitE and control rats	Intense swimming to exhaustion	Lung tissue	PE: >[SOD] and <[GSH-Px] and <[GST] in rats deficient in VitE and in comparison to control rats

Prigol et al. 2009 [115]	Supplementation with (PhSe)₂ and pulmonary oxidative damage caused by the exercise	Adult Swiss albino mice supplemented with (PhSe)₂ and not supplemented control mice	Swimming exercise (20 min) for both groups after 7 d of supplementation	Lung tissue	PE: ↑ [MDA] and ↑ of CAT activity in mice not supplemented with (PhSe)₂

Terblanche 1999 [116]	Exhaustive swimming and CAT activity in the lungs of male and female rats	Sprague-Dawley rats	1 h swimming	Lung tissue	PE: ↑ CAT activity in males and females

BALF: bronchoalveolar lavage fluid; CAT: catalase; (PhSe)₂: diphenyl diselenide; GR: glutathione reductase; GSH: glutathione reduced; GSH-Px: glutathione peroxidase; GST: glutathione S-transferase; L-Arg: L-arginine; MASL: meters above sea level; MDA: malondialdehyde; MPO: myeloperoxidase; NO: nitric oxide; Se: selenium; SOD: superoxide dismutase; CuZn-SOD: copper-zinc-superoxide dismutase; Mn-SOD: manganese-superoxide dismutase; TBARs: thiobarbituric acid reactive substances; UA: uric acid; VNO: volume of nitric oxide; XO: xanthine oxidase; VitE: vitamin E; VitC: vitamin C. In “Oxidative or inflammatory main results,” DE: during exercise and PE: postexercise. In “Aim,” the effect of exercise was not the primary aim of study.

(b)


Author, year	Aim	Sample characteristics	Exercise protocols	Samples obtained	Oxidative or inflammatory main results

Altan et al. 2009 [117]	SOD activity and [TBARs] postadaptation by training in altitude	Wistar albino rats divided into trained in hypobaria (THb) and normobaria (TNb) and nontrained in hypobaria (Hb) and normobaria (Nb)	Comparison of baseline samples between groups trained with swimming (T: 5 at 30 min/day/for 4 days/week for 9 weeks) or nontrained and exposed or not to simulated altitude of 3000 MASL (E: 120 min/day for 4 days/week for 9 weeks)	Lung tissue	PT: >SOD activity in TNb in comparison to Nb; no differences in [TBARS] for the same groups

Asami et al. 1998 [118]	DNA oxidative damage by chronic exercise	Sprague-Dawley rats with spontaneous (S), forced (F) exercise and sedentary control rats (C)	Comparison of baseline samples among rats with spontaneous exercise (wheel), trained on treadmill (T: 30–90 min/day for 25 days), and control rats	Lung tissue	PT: >[8-OH-dG] in F in comparison to S; the DNA oxidative damage was related to the exercise intensity

Aydin et al. 2009 [119]	Long period of dietary restriction and stress produced by high intensity swimming	Sprague-Dawley rats with restricted diet (RD) or ad libitum (AL), grouped in trained (+T), exercised (+E), and sedentary control rats (C)	Comparison of baseline samples of RD and AL in +T (T: 8 weeks of swimming with 2% BW as extra load during ~50–80 min), PE in +E (E: swimming until exhaustion), and baseline C	Lung tissue	PT: <GSH activity and >GSH-Px of AL+T compared to ALC; <LPO, >GSH, and GSH-Px in AL+E that AL+T PE: ↑ [MDA], ↓ [GSH], ↓ GR activity, and ↑ GSH-Px of AL+E compared to ALC (acute effects)

Chimenti et al. 2007 [120]	Epithelial remodeling, inflammatory cells, and apoptosis in the AWs after chronic exercise	Trained Swiss mice (T) and sedentary control mice (C)	Comparison of baseline samples among trained mice (T: 5 d/week for 6 wk at moderate to high intensity)	Lung tissue	PT: >apoptosis, >proliferation, >loss of hair cells, and infiltration of leukocytes in the AWs in T versus C

da Cunha et al. 2013 [121]	Chronic exercise on oxidative stress and NF-кβ/p65 pulmonary immunocontent of rats with lung injury	Trained Wistar rats (T) and nontrained control rats (C)	Comparison of baseline samples among rats trained on treadmill (T: 20 min at 60% VO₂max during 24 days in 3 months)	BALF and lung tissue	PT: >pulmonary catalase activity in T versus C; there are no changes in [TBARs], carbonyls, dichlorofluorescein, [], and NF-кβ/p65 in the lung

Gündüz et al. 2004 [122]	Oxidant and antioxidant systems in rats organs after a year of training	Wistar albino rats grouped in young control rats (YC), aged control rats (AC), and aged rats-training (AT)	Comparison of baseline samples between AT in swimming (T: 1 h/day for 5 days/week for 1 year) with YC and AC	Lung tissue	PT: >SOD activity and >GSH-Px in AT in comparison to AC; no difference of [TBARs] between the same groups

Lee et al. 2013 [123]	Administration of a ginseng intestinal metabolite (IH901) and exercise-induced oxidative stress in trained rat	Sprague-Dawley rats divided into resting control (RC), training control (EC), resting with IH901 consumption, or exercise with IH901 consumption groups	Training was carried out during 8 weeks on a treadmill; two weeks with 0% inclination and 25 cm/sec; then 2 weeks with 10% and 30 cm/sec; then 4 weeks with 15% and 35 cm/sec	Lung tissue	PT: ↑ TBARs and ↑ protein carbonyls in EC versus RC

Menegali et al. 2009 [124]	Therapeutic effects of physical exercise on histological and oxidative stress markers in animals exposed to cigarette smoke	Old C57BL-6 mice divided into control (C), training (T), cigarette smoke (CS), and cigarette smoke plus training (CS+E) groups	Training groups swam for 10 min/day during one habituation week; then they performed a swimming program 5 days/week for 8 weeks	Lung tissue	PT: ↑ SOD and ↑ CAT activity in E versus C

Olivo et al. 2014 [125]	Moderate aerobic exercise training prior to Streptococcus pneumoniae infection influences pulmonary inflammatory responses	BALB/c mice divided into sedentary untreated (SU), sedentary infected (SI), aerobic trained untreated (ATU), and aerobic trained infected groups (ATI)	Comparison between SU and ATU during 4 weeks after an individual maximal exercise capacity test was performed (0.1 km/h every 2.5 min, 25% inclination); training was for 60 min/day, 5 days/wk for 4 wk at 50% of the maximal speed	BALF and lung tissue	PT: ↑ CuZn-SOD and ↑ Mn-SOD expression in lung parenchyma of ATU versus SU after an individual maximal exercise capacity test

Reis Gonçalves et al. 2012 [15]	Chronic aerobic exercise on pulmonary inflammation, cytokine, and antioxidant enzymes in animal model of acute pulmonary damage	Trained BALB/c mice	Comparison of samples before and after a low intensity training on treadmill (T: 50% of MS for 60 min/d, 3 d/week for 5 weeks)	BALF, EB, and lung tissue	PT: with no changes in leukocytes, [IL-6], [IL-10], nor [TNF-α] in BALF; with no changes in [NO] in EB; ↑ expression of IL-6 and Mn-SOD in the lung, but no changes of activity of GSH-Px and GR in the lung

Toledo et al. 2012 [126]	Regular physical exercise in an experimental mouse model exposed to cigarette smoke	C57BL/6 mice divided into control mice (C), trained (T), exposed to cigarette smoke (Sk), and Sk plus T (Sk+T)	Comparison of baseline samples in T at moderate intensity on treadmill (T: 50% MS for 60 min/d, 5 d/week for 24 weeks)	BALF and lung tissue	PT: <[ROS] in BALF of En compared to C; >GSH-Px activity, but not of Mn-SOD nor CuZn-SOD in lungs of T compared to C; with no changes in the expression of IL-1ra, TNF-α, and IL-10 between T and C

Yang 2011 [127]	Chronic exercise and expression of cytokines related to inflammation in the lung tissue	Old male Sprague-Dawley rats, group with trained rats (T) and sedentary control rats (C)	Comparison of baseline samples between rats trained on treadmill (T: 25 m/min for 120 min/day for 1 week) and control rats	Lung tissue	>expression of mRNA for TNF-α and IL-4 and <expression of mRNA for IFN-γ of group T versus C

BALF: bronchoalveolar lavage fluid; BW: body weight; DEP: diesel exhaust particles; DNA: deoxyribonucleic acid; EB: exhaled breath; 8-OH-dG: 8-hydroxydeoxyguanosine; GR: glutathione reductase; GSH: glutathione reduced; GSH-Px: glutathione peroxidase; IFN-γ: interferon gamma; IL-1ra, IL-4, IL-6, or IL-10: interleukin-1ra, interleukin-4, interleukin-6, or interleukin-10; LPO: lipid peroxidation; MDA: malondialdehyde; MS: maximal speed; mRNA: messenger RNA; MS: maximal speed; NF-кβ/p65: factor nuclear kappa-β/p65; NO: nitric oxide; : nitrite; ROS: reactive oxygen species; SOD: superoxide dismutase; CuZn-SOD: copper-zinc-superoxide dismutase; Mn-SOD: manganese-superoxide dismutase; TBARs: thiobarbituric acid reactive substances; TNF-α: tumor necrosis factor-alpha. In “Oxidative or inflammatory main results,” PE: postexercise and PT: posttraining. In “Aim,” the effect of exercise was not the primary object.