Search JIM Advanced Search

Journal of Chinese Integrative Medicine ›› 2013, Vol. 11 ›› Issue (3): 213-219.doi: 10.3736/jintegrmed2013024

Special Issue: Acupuncture & Moxibustion

• Research Article • Previous Articles     Next Articles

Effects of electroacupuncture at Zusanli (ST36) on inflammatory cytokines in a rat model of smoke-induced chronic obstructive pulmonary disease

Wen-ye Genga, Zi-bing Liua,b, Na-na Songa, Gui-hong Zhanga, Wei-zhong Jina, Wang Zhoua, Li Lia, Yin-xiang Caoa, Da-nian Zhua, Lin-lin Shena()    

  1. a. Department of Physiology and Pathophysiology, Shanghai Medical College of Fudan University,Shanghai 200032, China
    b. Department of Physiology, Anhui College of Traditional Chinese Medicine, Hefei 230038, AnhuiProvince, China
  • Received:2012-12-05 Accepted:2013-02-27 Online:2013-05-10 Published:2013-05-15


Improvement in lung function was reported after acupuncture treatment of chronic obstructive pulmonary disease (COPD), but little is known about the underlying mechanisms. Because an immune response imbalance could be seen in COPD, we hypothesize that electroacupuncture (EA) may play a role in regulating inflammatory cytokines and contribute to lung protection in a rat model of smoke-induced COPD.


A COPD model using male Sprague-Dawley rats exposed to cigarette smoke was established. The rats were randomly divided into four groups (control, sham, COPD, and COPD plus EA), and COPD model was evaluated by measuring pulmonary pathological changes and lung function. EA was applied to the acupuncture point Zusanli (ST36) for 30 min/d for 14 d in sham and COPD rats. Bronchoalveolar lavage fluid (BALF) was used to measure levels of tumor necrosis factor-α (TNF-α), interleukin-1β (IL-1β), and malonaldehyde (MDA).


Compared with the control rats, COPD rats had significant changes in lung resistance (RL) and lung compliance (CL) (both P<0.01), bronchi and bronchiole airway obstruction (P<0.01), and levels of MDA, TNF-α, and IL-1β (P<0.01). There were no significant differences between the control and the sham groups. Compared with the COPD rats, the COPD plus EA rats had decreased RL and increased CL (both P<0.05), and reduced bronchi and bronchiole airway obstruction (P<0.05, P<0.01, respectively), while levels of TNF-α, IL-1β, and MDA in BALF were lowered (P<0.05 and P<0.01, respectively). However, TNF-α and IL-1β levels of the EA group rats remained higher than those of the control group (P<0.05).


EA at ST36 can reduce lung injury in a COPD rat model, and beneficial effects may be related to down-regulation of inflammatory cytokines. The anti-inflammatory and antioxidant effects may prolong the clinical benefit of EA.

Key words: Chronic obstructive pulmonary disease, Electroacupuncture, Anti-inflammatory, Antioxidant, Zusanli (ST36), Rats

Figure 1

Lung histopathological sections of rats in different groupsA and B: control; C and D: control plus EA; E and F: COPD; G and H: COPD plus EA. Hematoxylin and eosin (Light microscopy; original magnification: A, C, E and G, ×100 and B, D, F and H, ×400). COPD: chronic obstructive pulmonary disease; EA: electroacupuncture."

Figure 2

Effects of of EA on level of MDA Data are expressed as mean ± standard error of mean, n=7; **P<0.01, vs control group; △△P<0.01, vs COPD group. COPD: chronic obstructive pulmonary disease; EA: electroacupuncture; MDA: malondialdehyde."




[1] Moghaddam SJ, Clement CG , De la Garza MM, Zou X, Travis EL, Young HW, Evans CM, Tuvim MJ, Dickey BF.Haemophilus influenzae lysate induces aspects of the chronic obstructive pulmonary disease phenotype[J]. Am J Respir Cell Mol Biol, 2008,38(6):629-638
doi: 10.1165/rcmb.2007-0366OC
[2] Hogg JC, Chu F, Utokaparch S, Woods R, Elliott WM, Buzatu L, Cherniack RM, Rogers RM, Sciurba FC, Coxson HO, Paré PD . The nature of small-airway obstruction in chronic obstructive pulmonary disease[J]. N Engl J Med, 2004,350(26):2645-2653
doi: 10.1056/NEJMoa032158
[3] Sarir H , Henricks PA, van Houwelingen AH, Nijkamp FP, Folkerts G.Cells, mediators and Toll-like receptors in COPD[J]. Eur J Pharmacol, 2008,585(2-3):346-353
doi: 10.1016/j.ejphar.2008.03.009
[4] Rabe KF, Hurd S, Anzueto A, Barnes PJ, Buist SA, Calverley P, Fukuchi Y, Jenkins C , Rodriguez-Roisin R, van Weel C, Zielinski J; Global Initiative for Chronic Obstructive Lung Disease.Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: GOLD executive summary[J]. Am J Respir Crit Care Med, 2007,176(6):532-555
doi: 10.1164/rccm.200703-456SO
[5] Teramoto S . . COPD pathogenesis from the viewpoint of risk factors[J]. Intern Med, 2007,46(2):77-79
doi: 10.2169/internalmedicine.46.1775
[6] Barnes PJ . Small airways in COPD[J]. N Engl J Med, 2004,350(26):2635-2637
doi: 10.1056/NEJMp048102
[7] Jeffery PK . Comparison of the structural and inflammatory features of COPD and asthma. Giles F. Filley Lecture. Chest. 2000; 117(5 Suppl 1):251S-260S.
[8] Chung KF . Cytokines in chronic obstructive pulmonary disease. Eur Respir[J] Suppl. 2001; 34:50s-59s.
[9] Fitzgerald MF, Fox JC . Emerging trends in the therapy of COPD: novel anti-inflammatory agents in clinical development[J]. Drug Discov Today, 2007,12(11-12):479-486
doi: 10.1016/j.drudis.2007.04.005
[10] MacNee W . Oxidants/antioxidants andCOPD. Chest. 2000; 117(5 Suppl 1):303S-317S.
[11] Ciencewicki J, Trivedi S, Kleeberger SR .Oxidants and the pathogenesis of lung diseases[J]. J Allergy Clin Immunol , 2008, 122(3):456-468; quiz 469-470
doi: 10.1016/j.jaci.2008.08.004
[12] Stanojkovic I, Kotur-Stevuljevic J, Milenkovic B, Spasic S, Vujic T, Stefanovic A, Llic A, Ivanisevic J . Pulmonary function, oxidative stress and inflammatory markers in severe COPD exacerbation[J]. Respir Med, 2011,105(Suppl 1):S31-S37
doi: 10.1016/S0954-6111(11)70008-7
[13] Gross NJ . Novel antiinflammatory therapies for COPD[J]. Chest, 2012,142(5):1300-1307
doi: 10.1378/chest.11-2766
[14] Rahman I . Antioxidant therapies in COPD[J]. Int J Chron Obstruct Pulmon Dis, 2006,1(1):15-29
[15] Neumeister W, Kuhlemann H, Bauer T, Krause S, Schultze-Werninghaus G, Rasche K . Effect of acupuncture on quality of life, mouth occlusion pressures and lung function in COPD[J]. Med Klin (Munich), 1999,94(1 Spec No):106-109
[16] Suzuki M, Namura K, Ohno Y, Tanaka H, Egawa M, Yokoyama Y, Akao S, Fujiwara H, Yano T . The effect of acupuncture in the treatment of chronic obstructive pulmonary disease[J]. J Altern Complement Med, 2008,14(9):1097-1105
doi: 10.1089/acm.2007.0786
[17] Liu ZB, Song NN, Geng WY, Jin WZ, Li L, Cao YX, Qian Y, Zhu DN, Shen LL . Orexin-A and respiration in a rat model of smoke-induced chronic obstructive pulmonary disease[J]. Clin Exp Pharmacol Physiol, 2010,37(10):963-968
doi: 10.1111/j.1440-1681.2010.05411.x
[18] Wang J, Wang YQ, Yu J, Cao XD, Wu GC . Electroacupuncture suppresses surgical trauma stress-induced lymphocyte apoptosis in rats[J]. Neurosci Lett, 2005,383(1-2):68-72
doi: 10.1016/j.neulet.2005.03.068
[19] Amdur MO, Mead J . Mechanics of respiration in unanesthetized guinea pigs[J]. Am J Physiol, 1958,192(2):364-368
[20] Jiang HN, Qu JM, He LX, Chen XH, Pan J, Li L, Zhu DN, Cao YX, Shen LL . Effects of N(omega)-nitro-L-arginine methyl ester and aminoguanidine on lipopolysaccharide-induced airway hyperresponsiveness in guinea pigs[J]. Chin Med J (Engl), 2008,121(17):1693-1697
[21] Syrkina O, Jafari B, Hales CA, Quinn DA . Oxidant stress mediates inflammation and apoptosis in ventilator-induced lung injury[J]. Respirology, 2008,13(3):333-340
doi: 10.1111/j.1440-1843.2008.01279.x
[22] Murakami K , McGuire R, Cox RA, Jodoin JM, Schmalstieg FC, Traber LD, Hawkins HK, Herndon DN, Traber DL.Recombinant antithrombin attenuates pulmonary inflammation following smoke inhalation and pneumonia in sheep[J]. Crit Care Med, 2003,31(2):577-583
doi: 10.1097/01.CCM.0000050444.52531.08
[23] Shi HW, Hu JL, Tian YP, Huang HM, Li XH, Su JL . Propofol protecting rats from paraquat-induced lung injury[J]. Zhonghua Lao Dong Wei Sheng Zhi Ye Bing Za Zhi, 2006,24(6):345-347
[24] Ikeuchi H, Sakano T, Sanchez J, Mason AD , Jr., Pruitt BA, Jr. The effects of platelet-activating factor(PAF) and a PAF antagonist(CV-3988) on smoke inhalation injury in an ovine model[J]. J Trauma, 1992,32(3):344-349
doi: 10.1097/00005373-199203000-00012
[25] Ricard JD, Dreyfuss D, Saumon G . Production of inflammatory cytokines in ventilator-induced lung injury: a reappraisal[J]. Am J Respir Crit Care Med, 2001,163(5):1176-1180
doi: 10.1164/ajrccm.163.5.2006053
[26] Wright JL, Churg A . Animal models of COPD: Barriers, successes, and challenges[J]. Pulm Pharmacol Ther, 2008,21(5):696-698
doi: 10.1016/j.pupt.2008.01.007
[27] Zheng H, Liu Y, Huang T, Fang Z, Li G, He S . Development and characterization of a rat model of chronic obstructive pulmonary disease(COPD) induced by sidestream cigarette smoke[J]. Toxicol Lett, 2009,189(3):225-234
doi: 10.1016/j.toxlet.2009.06.850
[28] Singh B, Arora S, Khanna V . Association of severity of COPD with IgE and interleukin-1b[J]. Monaldi Arch Chest Dis, 2010,73(2):86-87
[29] Du LN, Jiang JW, Wu GC, Cao XD . Naloxone and electroacunpunture(EA) improve the immune function of traumatized rats[J]. Sheng Li Xue Bao, 1998,50(6):636-642
[30] Kavoussi B, Ross BE . The neuroimmune basis of anti-inflammatory acupuncture[J]. Integr Cancer Ther, 2007,6(3):251-257
doi: 10.1177/1534735407305892
[31] Tian L, Huang YX, Tian M, Gao W, Chang Q . Downregulation of electroacupuncture at ST36 on TNF-α in rats with ulcerative colitis[J]. World J Gastroenterol, 2003,9(5):1028-1033
doi: 10.3748/wjg.v9.i5.1028
[32] Suzuki M, Ohno Y, Namura K, Asai T, Yuugetu H, Sawada M, Akao S, Gotou K, Fujiwara H . A case of chronic obstructive pulmonary disease(COPD) successfully treated by acupuncture[J]. Nihon Kokyuki Gakkai Zasshi, 2005,43(5):289-295
[33] Baginski TK, Dabbagh K, Satjawatcharaphong C, Swinney DC . Cigarette smoke synergistically enhances respiratory mucin induction by proinflammatory stimuli[J]. Am J Respir Cell Mol Biol, 2006,35(2):165-174
doi: 10.1165/rcmb.2005-0259OC
[34] Pogosyan AS, Venediktova NI, Kosenko EA, Kaminskii YG . Antioxidant status of erythrocytes after acupuncture treatment[J]. Bull Exp Biol Med, 2004,138(1):26-29
doi: 10.1007/BF02694465
[35] Chen CM, Wang LF, Shen EY . Maternal acupuncture effects on surfactant and antioxidant enzymes in preterm rat lungs[J]. Acta Paediatr Taiwan, 2005,46(4):206-211
[1] Talat Albukhari, Bassem Refaat, El-Sayed Bakr, Sameh Baz, Bodour Rajab, Hossam Gadalla, Mohamed El-Boshy. Salvadora persica extract attenuates cyclophosphamide-induced hepatorenal damage by modulating oxidative stress, inflammation and apoptosis in rats. Journal of Integrative Medicine, 2022, 20(4): 348-354.
[2] Xiang-yu Wei, Shi-lei Luo, HuiChen, Shan-shan Liu, Zhi-gang Gong, Song-huaZhan. Functional connectivity changes during migraine treatment with electroacupuncture at Shuaigu (GB8). Journal of Integrative Medicine, 2022, 20(3): 237-243.
[3] Miriam Bazzicalupo, Laura Cornara, Bruno Burlando, Alberta Cascini, Marcella Denaro, Antonella Smeriglio, Domenico Trombetta. Carpobrotus edulis (L.) N.E.Br. extract as a skin preserving agent: from traditional medicine to scientific validation. Journal of Integrative Medicine, 2021, 19(6): 526-536.
[4] Sutticha Ruangchuay, Qiang-qiang Wang, Liang-yi Wang, Jing Lin, Yong-chao Wang, Guo-huan Zhong, Katesarin Maneenoon, Ze-bo Huang, Sasitorn Chusri. Antioxidant and antiaging effect of traditional Thai rejuvenation medicines in Caenorhabditis elegans . Journal of Integrative Medicine, 2021, 19(4): 362-373.
[5] Ju-Yeon Park, Young-Won Kwon, Sun-Ah Kim, Sun-Dong Park, Chang-Hyun Kim, Jin-Hee Kim, Ju-Hee Lee. Polyherbal formula SC-E3 inhibits rheumatoid arthritis activity in a mouse model of type-II collagen-induced arthritis. Journal of Integrative Medicine, 2021, 19(3): 265-273.
[6] Bing-rong Li, Shi-yun Shao, Long Yuan, Ru Jia, Jian Sun, Qing Ji, Hua Sui, Li-hong Zhou, Yi Zhang, Hui Liu, Qi Li, Yan Wang, Bi-meng Zhang. Effects of mild moxibustion on intestinal microbiome and NLRP3 inflammasome in rats with 5-fluorouracil-induced intestinal mucositis. Journal of Integrative Medicine, 2021, 19(2): 144-157.
[7] Olarewaju M. Oluba, Oghenerobor B. Akpor, Feyikemi D. Adebiyi, Sunday J. Josiah, Olayinka O. Alabi, Ayoola O. Shoyombo, Augustine O. Olusola. Effects of co-administration of Ganoderma terpenoid extract with chloroquine on inflammatory markers and antioxidant status in Plasmodium berghei-infected mice. Journal of Integrative Medicine, 2020, 18(6): 522-529.
[8] Swatantra Kumar, Vimal K Maurya, Debadatta Nayak, Anil Khurana, Raj K Manchanda, Srinivasulu Gadugu, Madan LB Bhatt, Shailendra K Saxena. Calcarea carbonica treatment rescues lipopolysaccharide-induced inflammatory response in human mononuclear cells via downregulation of inducible cyclooxygenase pathway. Journal of Integrative Medicine, 2020, 18(5): 441-449.
[9] Jian-sheng Li, Xue-fang Liu, Hao-ran Dong, Wan-chun Zheng, Su-xiang Feng, Yan-ge Tian, Peng Zhao, Jin-di Ma, Zhou-xin Ren, Yang Xie. Effective-constituent compatibility-based analysis of Bufei Yishen formula, a traditional herbal compound as an effective treatment for chronic obstructive pulmonary disease. Journal of Integrative Medicine, 2020, 18(4): 351-362.
[10] Sitthichai Iamsaard, Supatcharee Arun, Jaturon Burawat, Supataechasit Yannasithinon, Saranya Tongpan, Sudtida Bunsueb, Natthapol Lapyuneyong, Pannawat Choowong-in, Nareelak Tangsrisakda, Chadaporn Chaimontri, Wannisa Sukhorum. Evaluation of antioxidant capacity and reproductive toxicity of aqueous extract of Thai Mucuna pruriens seeds. Journal of Integrative Medicine, 2020, 18(3): 265-273.
[11] Varuni Colamba Pathiranage, Ira Thabrew, Sameera R. Samarakoon, Kamani H. Tennekoon, Umapriyatharshini Rajagopalan, Meran K. Ediriweera. Evaluation of anticancer effects of a pharmaceutically viable extract of a traditional polyherbal mixture against non-small-cell lung cancer cells. Journal of Integrative Medicine, 2020, 18(3): 242-252.
[12] Masoud Seddighfar, Sayid Mahdi Mirghazanfari, Masoumeh Dadpay. Analgesic and anti-inflammatory properties of hydroalcoholic extracts of Malva sylvestris, Carum carvi or Medicago sativa, and their combination in a rat model. Journal of Integrative Medicine, 2020, 18(2): 181-188.
[13] Syed Fairus, Hwee Ming Cheng, Kalyana Sundram. Antioxidant status following postprandial challenge of two different doses of tocopherols and tocotrienols. Journal of Integrative Medicine, 2020, 18(1): 68-79.
[14] Dona Nirmani Ann Wijewickrama Samarakoon, Deepthi Inoka Uluwaduge, Malith Aravinda Siriwardhene. Mechanisms of action of Sri Lankan herbal medicines used in the treatment of diabetes: A review. Journal of Integrative Medicine, 2020, 18(1): 13-20.
[15] Rabie Kachkoul, Tarik Squalli Housseini, Mohamed Mohim, RadouaneEl Habbani, Youssef Miyah, Anissa Lahrichi. Chemical compounds as well as antioxidant and litholytic activities of Arbutus unedo L. leaves against calcium oxalate stones. Journal of Integrative Medicine, 2019, 17(6): 430-437.
Full text



[1] Dong Yang, Yong-ping Du, Qing Shen, Wei Chen, Yan Yu, Guang-lei Chen. Expression of alpha-smooth muscle actin in renal tubulointerstitium in patients with kidney collateral stasis. Journal of Chinese Integrative Medicine, 2008, 6(1): 41-44
[2] Hai-feng Wei, Bai-liu Ya, Ling Zhao, Cui-fei Ye, Li Zhang, Lin Li. Evaluation of tongue manifestation of blood stasis syndrome and its relationship with blood rheological disorder in a rat model of transient brain ischemia. Journal of Chinese Integrative Medicine, 2008, 6(1): 73-76
[3] Xi Lin, Jian-ping Liu. Herbal medicines for viral myocarditis. Journal of Chinese Integrative Medicine, 2008, 6(1): 76
[4] Xi Lin, Jian-ping Liu. Tai chi for treating rheumatoid arthritis. Journal of Chinese Integrative Medicine, 2008, 6(1): 82
[5] Liang-ping Hu, Hui Gao. Discrimination of errors in statistical analysis of medical papers published in the first issue of 2006 in Journal of Chinese Integrative Medicine. Journal of Chinese Integrative Medicine, 2008, 6(1): 98-106
[6] Yan-bo Zhu , Qi Wang, Cheng-yu Wu, Guo-ming Pang, Jian-xiong Zhao, Shi-lin Shen, Zhong-yuan Xia , Xue Yan . Logistic regression analysis on relationships between traditional Chinese medicine constitutional types and overweight or obesity. Journal of Chinese Integrative Medicine, 2010, 8(11): 1023-1035
[7] Wei Xu, Meng Shi, Jian-gang Liu, Cheng-long Wang . Collagen protein expressions in ischemic myocardium of rats with acute myocardial infarction and effects of qi-tonifying, yin-tonifying and blood-activating herbs and detoxifying and blood-activating herbs. Journal of Chinese Integrative Medicine, 2010, 8(11): 1041-1047
[8] Tao Wang , Feng Qin. Effects of Chinese herbal medicine Xiaoyao Powder on monoamine neurotransmitters in hippocampus of rats with postpartum depression. Journal of Chinese Integrative Medicine, 2010, 8(11): 1075-1079
[9] Ying Xu , Chang-chun Zeng , Xiu-yu Cai , Rong-ping Guo , Guang Nie , Ying Jin. Chromaticity and optical spectrum colorimetry of the tongue color in different syndromes of primary hepatic carcinoma. Journal of Chinese Integrative Medicine, 2012, 10(11): 1263-1271
[10] Xiang-ying Mao , Qin Bian , Zi-yin Shen. Analysis of the osteogenetic effects exerted on mesenchymal stem cell strain C3H10T1/2 by icariin via MAPK signaling pathway in vitro. Journal of Chinese Integrative Medicine, 2012, 10(11): 1272-1278