Skip to main content
Top
Published in: BMC Complementary Medicine and Therapies 1/2016

Open Access 01-12-2016 | Research article

Sex differences in acupuncture effectiveness in animal models of Parkinson's disease: a systematic review

Authors: Sook-Hyun Lee, Maurits van den Noort, Peggy Bosch, Sabina Lim

Published in: BMC Complementary Medicine and Therapies | Issue 1/2016

Login to get access

Abstract

Background

Many animal experimental studies have been performed to investigate the efficacy of acupuncture in Parkinson’s disease (PD). Sex differences are a major issue in all diseases including PD. However, to our knowledge, there have been no reviews investigating sex differences on the effectiveness of acupuncture treatment for animal PD models. The current study aimed to summarize and analyze past studies in order to evaluate these possible differences.

Method

Each of 7 databases (MEDLINE, EMBASE, the Cochrane Library, 3 Korean medical databases, and the China National Knowledge Infrastructure) was searched from its inception through March 2015 without language restrictions.

Results

We included studies of the use of acupuncture treatment in animal models of PD. A total of 810 potentially relevant articles were identified, 57 of which met our inclusion criteria. C57/BL6 mice were used most frequently (42 %) in animal PD models. Most of the studies were carried out using only male animals (67 %); only 1 study (2 %) was performed using solely females. The further 31 % of the studies used a male/female mix or did not specify the sex.

Conclusions

The results of our review suggest that acupuncture is an effective treatment for animal PD models, but there is insufficient evidence to determine whether sex differences exist. Future studies of acupuncture treatment for PD should use female animal models because they reflect the physiological characteristics of both males and females to fully evaluate the effect and the safety of the treatment for each sex.
Appendix
Available only for authorised users
Literature
1.
go back to reference Obeso JA, Rodríguez-Oroz MC, Benitez-Temino B, Blesa FJ, Guridi J, Marin C, Rodriguez M. Functional organization of the basal ganglia: therapeutic implications for Parkinson's disease. Mov Disord. 2008;23 Suppl 3:548–59.CrossRef Obeso JA, Rodríguez-Oroz MC, Benitez-Temino B, Blesa FJ, Guridi J, Marin C, Rodriguez M. Functional organization of the basal ganglia: therapeutic implications for Parkinson's disease. Mov Disord. 2008;23 Suppl 3:548–59.CrossRef
3.
go back to reference Wooten GF, Currie LJ, Bovbjerg VE, Lee JK, Patrie J. Are men at greater risk for Parkinson’s disease than women? J Neurol Neurosurg Psychiatry. 2004;75(4):637–9.CrossRefPubMedPubMedCentral Wooten GF, Currie LJ, Bovbjerg VE, Lee JK, Patrie J. Are men at greater risk for Parkinson’s disease than women? J Neurol Neurosurg Psychiatry. 2004;75(4):637–9.CrossRefPubMedPubMedCentral
4.
go back to reference Pavon JM, Whitson HE, Okun MS. Parkinson's disease in women: a call for improved clinical studies and for comparative effectiveness research. Maturitas. 2010;65(4):352–8.CrossRefPubMedPubMedCentral Pavon JM, Whitson HE, Okun MS. Parkinson's disease in women: a call for improved clinical studies and for comparative effectiveness research. Maturitas. 2010;65(4):352–8.CrossRefPubMedPubMedCentral
5.
go back to reference Wald C, Wu C. Biomedical research. Of mice and women: the bias in animal models. Science. 2010;327(5973):1571–2.CrossRefPubMed Wald C, Wu C. Biomedical research. Of mice and women: the bias in animal models. Science. 2010;327(5973):1571–2.CrossRefPubMed
6.
go back to reference Haack S, Seeringer A, Thürmann PA, Becker T, Kirchheiner J. Sex-specific differences in side effects of psychotropic drugs: genes or gender? Pharmacogenomics. 2009;10(9):1511–26.CrossRefPubMed Haack S, Seeringer A, Thürmann PA, Becker T, Kirchheiner J. Sex-specific differences in side effects of psychotropic drugs: genes or gender? Pharmacogenomics. 2009;10(9):1511–26.CrossRefPubMed
7.
go back to reference Alvarez-Fischer DC, Noelker F, Vulinović A, Grünewald C, et al. Bee venom and its component apamin as neuroprotective agents in a Parkinson disease mouse model. Plos One. 2013;8(4):e61700.CrossRefPubMedPubMedCentral Alvarez-Fischer DC, Noelker F, Vulinović A, Grünewald C, et al. Bee venom and its component apamin as neuroprotective agents in a Parkinson disease mouse model. Plos One. 2013;8(4):e61700.CrossRefPubMedPubMedCentral
8.
go back to reference Yan B, Zhigang L, Hu B, et al. Effects of electro-acupuncture on Baihui and Taiyang points on caspase- 3 expression and apoptosis of substantia nigra dopaminergic neurons of rats with Parkinson disease. Chinese J Tradit Med Sci &Tech. 2014;21(5):534–6. Yan B, Zhigang L, Hu B, et al. Effects of electro-acupuncture on Baihui and Taiyang points on caspase- 3 expression and apoptosis of substantia nigra dopaminergic neurons of rats with Parkinson disease. Chinese J Tradit Med Sci &Tech. 2014;21(5):534–6.
9.
go back to reference Wang YC, Xu YH, Ma J, et al. Effects of electric acupuncture on the oxidative stress in the rat of Parkinson’s disease abductioned by rotenone. Hubei Univ of TCM. 2013;28(8):2417–9. Wang YC, Xu YH, Ma J, et al. Effects of electric acupuncture on the oxidative stress in the rat of Parkinson’s disease abductioned by rotenone. Hubei Univ of TCM. 2013;28(8):2417–9.
10.
go back to reference Feng J, Sun HM, Wang YY, et al. Influences of needling chorea-tremble controlled zone on expressions of dopaminergic neurons and BDNF in mice with Parkinson’s disease. J Beijing Univ TCM. 2014;37(1):53–7. Feng J, Sun HM, Wang YY, et al. Influences of needling chorea-tremble controlled zone on expressions of dopaminergic neurons and BDNF in mice with Parkinson’s disease. J Beijing Univ TCM. 2014;37(1):53–7.
11.
go back to reference Ding YX, Zhao J, Hou LQ. Effects of electroacupuncture on the expressions of neuroal nitric oxide synthase and astrocyte in dentate gyrus of rats with Parkinson's disease. Chin acupunct& mox. 2013;33(6):533–7. Ding YX, Zhao J, Hou LQ. Effects of electroacupuncture on the expressions of neuroal nitric oxide synthase and astrocyte in dentate gyrus of rats with Parkinson's disease. Chin acupunct& mox. 2013;33(6):533–7.
12.
go back to reference Wang SJ, Fang JQ, Ma J. Effect of electroacupuncture stimulation of ``Fengfu'' (GV 16) and ``Taichong'' (LR 3) on expression of COX-2 and tyrosine hydroxylase in substantia nigra in rats with Parkinson's disease. Acupuncture Research. 2013;38(3):198–201.PubMed Wang SJ, Fang JQ, Ma J. Effect of electroacupuncture stimulation of ``Fengfu'' (GV 16) and ``Taichong'' (LR 3) on expression of COX-2 and tyrosine hydroxylase in substantia nigra in rats with Parkinson's disease. Acupuncture Research. 2013;38(3):198–201.PubMed
13.
go back to reference Anita H. Gender bias in research: how does it affect evidence based medicine? J R Soc Med. 2007;100(1):2–3.CrossRef Anita H. Gender bias in research: how does it affect evidence based medicine? J R Soc Med. 2007;100(1):2–3.CrossRef
15.
go back to reference Raz L, Miller VM. Considerations of sex and gender differences in preclinical and clinical trials. Handb Exp Pharmacol. 2012;214:127–47.CrossRef Raz L, Miller VM. Considerations of sex and gender differences in preclinical and clinical trials. Handb Exp Pharmacol. 2012;214:127–47.CrossRef
16.
go back to reference Singh N, Pillay V, Choonara YE. Advances in the treatment of Parkinson’s disease. Prog Neurobiol. 2007;81(1):29–44.CrossRefPubMed Singh N, Pillay V, Choonara YE. Advances in the treatment of Parkinson’s disease. Prog Neurobiol. 2007;81(1):29–44.CrossRefPubMed
17.
go back to reference Walton-Hadlock J. Primary Parkinson's disease: the use of Tuina and acupuncture in accord with an evolving hypothesis of its cause from the perspective of Chinese traditional medicine--part 2. Am J Acupunct. 1999;27(1–2):31–49.PubMed Walton-Hadlock J. Primary Parkinson's disease: the use of Tuina and acupuncture in accord with an evolving hypothesis of its cause from the perspective of Chinese traditional medicine--part 2. Am J Acupunct. 1999;27(1–2):31–49.PubMed
18.
go back to reference Choi YG, Yeo S, Hong YM, Lim S. Neuroprotective changes of striatal degeneration-related gene expression by acupuncture in an MPTP mouse model of Parkinsonism: microarray analysis. Cell Mol Neurobiol. 2011;31(3):377–91.CrossRefPubMed Choi YG, Yeo S, Hong YM, Lim S. Neuroprotective changes of striatal degeneration-related gene expression by acupuncture in an MPTP mouse model of Parkinsonism: microarray analysis. Cell Mol Neurobiol. 2011;31(3):377–91.CrossRefPubMed
19.
go back to reference Yeo S, Choi YG, Hong YM, Lim S. Neuroprotective changes of thalamic degeneration-related gene expression by acupuncture in an MPTP mouse model of Parkinsonism: microarray analysis. Gene. 2013;515(2):329–38.CrossRefPubMed Yeo S, Choi YG, Hong YM, Lim S. Neuroprotective changes of thalamic degeneration-related gene expression by acupuncture in an MPTP mouse model of Parkinsonism: microarray analysis. Gene. 2013;515(2):329–38.CrossRefPubMed
20.
go back to reference Yeo S, Lim S, Choe IH, Choi YG, Chung KC, Jahng GH, Kim SH. Acupuncture stimulation on GB34 activates neural responses associated with Parkinson's disease. CNS Neurosci Ther. 2012;18(9):781–90.CrossRefPubMed Yeo S, Lim S, Choe IH, Choi YG, Chung KC, Jahng GH, Kim SH. Acupuncture stimulation on GB34 activates neural responses associated with Parkinson's disease. CNS Neurosci Ther. 2012;18(9):781–90.CrossRefPubMed
21.
go back to reference Choi YG, Park JH, Lim S. Acupuncture inhibits ferric iron deposition and ferritin-heavy chain reduction in an MPTP-induced Parkinsonism model. Neurosci Lett. 2009;450(2):92–6.CrossRefPubMed Choi YG, Park JH, Lim S. Acupuncture inhibits ferric iron deposition and ferritin-heavy chain reduction in an MPTP-induced Parkinsonism model. Neurosci Lett. 2009;450(2):92–6.CrossRefPubMed
22.
go back to reference Bai Y, LI ZG, Wang S, et al. Study on protective effect of different electro- acupuncture on Baihui and Taiyang points on dopaminergic neurons of rats with Parkinson Disease. Chin Med Sci Tech. 2014a;21(5):536–8. Bai Y, LI ZG, Wang S, et al. Study on protective effect of different electro- acupuncture on Baihui and Taiyang points on dopaminergic neurons of rats with Parkinson Disease. Chin Med Sci Tech. 2014a;21(5):536–8.
23.
go back to reference Wang SJ, Fang JQ, Ma J, et al. Influence of electroacupuncture on p38-mitogen activated protein kinase in substantia nigra cells of rats with Parkinson disease model. Chin Acupunct Mox. 2013b;33(4):329–33. Wang SJ, Fang JQ, Ma J, et al. Influence of electroacupuncture on p38-mitogen activated protein kinase in substantia nigra cells of rats with Parkinson disease model. Chin Acupunct Mox. 2013b;33(4):329–33.
24.
go back to reference Wang YC, He F, Ma J, et al. impacts of electroacupuncture on ubiquitin-proteasome system in rats with Parkinson’s disease. Hubei Univ TCM. 2013d;33(8):725–9. Wang YC, He F, Ma J, et al. impacts of electroacupuncture on ubiquitin-proteasome system in rats with Parkinson’s disease. Hubei Univ TCM. 2013d;33(8):725–9.
25.
go back to reference Ding YX, Hou LQ, Xiong KR. Effect of electroacupuncture on expression of proliferating cell nuclear antigen and glial fibrillary acidic protein in subventricular zone of Parkinson's disease rats. Acupunct Res. 2012;37(4):286–90. Ding YX, Hou LQ, Xiong KR. Effect of electroacupuncture on expression of proliferating cell nuclear antigen and glial fibrillary acidic protein in subventricular zone of Parkinson's disease rats. Acupunct Res. 2012;37(4):286–90.
26.
go back to reference Huang Q, Sun Y, Wang L, Zhang Y, et al. Acupuncture improve motor function in a mouse model of Parkinson's disease. Nucl Tech. 2012;35(11):877–80. Huang Q, Sun Y, Wang L, Zhang Y, et al. Acupuncture improve motor function in a mouse model of Parkinson's disease. Nucl Tech. 2012;35(11):877–80.
27.
go back to reference Lu ZY, Zhao H, Wang T. Effects of Acupuncture on Behavior and Striatal Apoptosis in Mice with Parkinson Disease. Acupunct Res. 2012;37(3):186–90. Lu ZY, Zhao H, Wang T. Effects of Acupuncture on Behavior and Striatal Apoptosis in Mice with Parkinson Disease. Acupunct Res. 2012;37(3):186–90.
28.
go back to reference Guo CX, Zhang L, Shao SJ, Hao L, et al. Oxidative stress effects of electro-acupuncture for "Baihui ", "Fengfu", "Yanglingquan " on PD model rat. Yunnan Univ TCM. 2012;35(5):26–9. Guo CX, Zhang L, Shao SJ, Hao L, et al. Oxidative stress effects of electro-acupuncture for "Baihui ", "Fengfu", "Yanglingquan " on PD model rat. Yunnan Univ TCM. 2012;35(5):26–9.
29.
go back to reference Yang JL, Chen JS, Yang YF, et al. Neuroprotection effects of retained acupuncture in neurotoxin-induced Parkinson's disease mice. Brain Behav Immun. 2011;25(7):1452–9.CrossRefPubMed Yang JL, Chen JS, Yang YF, et al. Neuroprotection effects of retained acupuncture in neurotoxin-induced Parkinson's disease mice. Brain Behav Immun. 2011;25(7):1452–9.CrossRefPubMed
30.
go back to reference Kim JI, Yang EJ, Lee MS, et al. Bee venom reduces neuroinflammation in the MPTP-induced model of Parkinson's disease. Int J Neurosci. 2011;121:209–17.CrossRefPubMed Kim JI, Yang EJ, Lee MS, et al. Bee venom reduces neuroinflammation in the MPTP-induced model of Parkinson's disease. Int J Neurosci. 2011;121:209–17.CrossRefPubMed
31.
go back to reference Du J, Sun ZL, Jia J, Wang X, et al. High-frequency electro-acupuncture stimulation modulates intracerebral γ-aminobutyric acid content in rat model of Parkinson’s disease. Acta Physiol Sinica. 2011;63(4):305–10.PubMed Du J, Sun ZL, Jia J, Wang X, et al. High-frequency electro-acupuncture stimulation modulates intracerebral γ-aminobutyric acid content in rat model of Parkinson’s disease. Acta Physiol Sinica. 2011;63(4):305–10.PubMed
32.
33.
go back to reference Doo AR, Kim ST, Kim SN, et al. Neuroprotective effects of bee venom pharmaceutical acupuncture in acute 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced mouse model of Parkinson's disease. Neurolog Res. 2010;32 Suppl 1:88–91.CrossRef Doo AR, Kim ST, Kim SN, et al. Neuroprotective effects of bee venom pharmaceutical acupuncture in acute 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced mouse model of Parkinson's disease. Neurolog Res. 2010;32 Suppl 1:88–91.CrossRef
34.
go back to reference Hong MS, Park HK, Yang JS, et al. Gene expression profile of acupuncture treatment in 1-methyl-4-phenyl-1,2, 3,6- tetrahydropyridine-induced Parkinson's disease model. Neurol Res. 2010;32 Suppl 1:S74–8.CrossRef Hong MS, Park HK, Yang JS, et al. Gene expression profile of acupuncture treatment in 1-methyl-4-phenyl-1,2, 3,6- tetrahydropyridine-induced Parkinson's disease model. Neurol Res. 2010;32 Suppl 1:S74–8.CrossRef
35.
go back to reference Jun HJ, Kim YS. Dose-dependent Effects of Bee Venom Acupuncture on MPTP-induced Mouse Model of Parkinson's Disease. J Korean Acupunct Mox Med Sci. 2010;27(5):59–68. Jun HJ, Kim YS. Dose-dependent Effects of Bee Venom Acupuncture on MPTP-induced Mouse Model of Parkinson's Disease. J Korean Acupunct Mox Med Sci. 2010;27(5):59–68.
36.
go back to reference Kim ST, Moon W, Chae Y, et al. The effect of electroaucpuncture for 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced proteomic changes in the mouse striatum. J Physiol Sci. 2010;60:27–34.CrossRefPubMed Kim ST, Moon W, Chae Y, et al. The effect of electroaucpuncture for 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced proteomic changes in the mouse striatum. J Physiol Sci. 2010;60:27–34.CrossRefPubMed
37.
go back to reference Park W, Kim JK, Kim JI, et al. Neuroprotective and Anti-inflammatory Effects of Bee Venom Acupuncture on MPTP-induced Mouse. J Korean Acupunct Mox Med Sci. 2010;27(3):105–16. Park W, Kim JK, Kim JI, et al. Neuroprotective and Anti-inflammatory Effects of Bee Venom Acupuncture on MPTP-induced Mouse. J Korean Acupunct Mox Med Sci. 2010;27(3):105–16.
38.
go back to reference Sun H, Wu H, Xu H, et al. Protective effect of acupuncture in acupoints of Governor Vessel on dopaminergic neurons protection and influence on ultrastructure in mice with Parkinson’s disease. Beijing Univ TCM. 2010;33(4):257–62. Sun H, Wu H, Xu H, et al. Protective effect of acupuncture in acupoints of Governor Vessel on dopaminergic neurons protection and influence on ultrastructure in mice with Parkinson’s disease. Beijing Univ TCM. 2010;33(4):257–62.
39.
go back to reference Wang YC, Cheng YH, Ma J, et al. Effect of electroacupuncture on morphological changes and apoptosis of substantia nigra cells in Parkinson's disease rats. Acupunct Res. 2010a;35(6):415–21. Wang YC, Cheng YH, Ma J, et al. Effect of electroacupuncture on morphological changes and apoptosis of substantia nigra cells in Parkinson's disease rats. Acupunct Res. 2010a;35(6):415–21.
40.
go back to reference Wang YC, Cheng YH, Ma J, et al. Effects of electroacupuncture on the expression of GDNF and Ret in Parkinson’s disease model rats. Hubei Univ TCM. 2010b;30(9):739–43. Wang YC, Cheng YH, Ma J, et al. Effects of electroacupuncture on the expression of GDNF and Ret in Parkinson’s disease model rats. Hubei Univ TCM. 2010b;30(9):739–43.
41.
go back to reference Wang YY, Sun HM, He X, et al. The protection effect of acupuncture of baihui and dazhui points on the dopaminergic neurons in PD mice. Prog Anatomic Sci. 2010c;16(1):16–20. Wang YY, Sun HM, He X, et al. The protection effect of acupuncture of baihui and dazhui points on the dopaminergic neurons in PD mice. Prog Anatomic Sci. 2010c;16(1):16–20.
42.
go back to reference Yu YP, Ju WP, Li ZG, Wang DZ, Wang YC, Xie AM. Acupuncture inhibits oxidative stress and rotational behavior in 6-hydroxydopamine lesioned rat. Brain Res. 2010;1336:58–65.CrossRefPubMed Yu YP, Ju WP, Li ZG, Wang DZ, Wang YC, Xie AM. Acupuncture inhibits oxidative stress and rotational behavior in 6-hydroxydopamine lesioned rat. Brain Res. 2010;1336:58–65.CrossRefPubMed
43.
go back to reference Huang PP, Ma J, Wang Y, et al. Effect of electroacupuncture on the expression of BDNF and TrKB in mesencephic substantia nigra of the Parkinson 's disease model rats. J Hubei Univ Chin Med. 2010;12(2):3–5. Huang PP, Ma J, Wang Y, et al. Effect of electroacupuncture on the expression of BDNF and TrKB in mesencephic substantia nigra of the Parkinson 's disease model rats. J Hubei Univ Chin Med. 2010;12(2):3–5.
44.
go back to reference Kim CY, Lee JD, Lee SH. Anti-inflammatory Effect of Bee Venom Acupuncture at Sinsu (BL23) in a MPTP Mouse Model of Parkinson Disease. J Korean Acupunct Mox Med Sci. 2009;26(4):49–58. Kim CY, Lee JD, Lee SH. Anti-inflammatory Effect of Bee Venom Acupuncture at Sinsu (BL23) in a MPTP Mouse Model of Parkinson Disease. J Korean Acupunct Mox Med Sci. 2009;26(4):49–58.
45.
go back to reference Wang S, Jiang H, Qu L. Study on the mechanism of electroacupuncture scalp point penetration therapy in action on apoptosis in the Parkinson's disease rat model. Chin Acupunct Mox. 2009a;29(4):309–13. Wang S, Jiang H, Qu L. Study on the mechanism of electroacupuncture scalp point penetration therapy in action on apoptosis in the Parkinson's disease rat model. Chin Acupunct Mox. 2009a;29(4):309–13.
46.
go back to reference Wang S, Qi XJ, Han D. Effect of electroacupuncture scalp point-through-point therapy on the expression of tyrosine hydroxylase and dopamine transporter mRNAs in substantia nigra of Parkinson's disease model rats. Chin Acupunct Mox. 2009b;29(5):391–4. Wang S, Qi XJ, Han D. Effect of electroacupuncture scalp point-through-point therapy on the expression of tyrosine hydroxylase and dopamine transporter mRNAs in substantia nigra of Parkinson's disease model rats. Chin Acupunct Mox. 2009b;29(5):391–4.
47.
go back to reference Kim YJ, Kim BS, Park HJ. Acupuncture at GB34 modulates laminin expression in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) induced PD mouse model. J Acupunct Acupoint. 2008;25(1):155–64. Kim YJ, Kim BS, Park HJ. Acupuncture at GB34 modulates laminin expression in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) induced PD mouse model. J Acupunct Acupoint. 2008;25(1):155–64.
48.
go back to reference Guan T, Sun H, Zhang L, et al. The effects of electroacupuncture for iron protein and stained cells in the substantia nigra in Parkinson 's disease model mice. Chin J Histochem Cytochem. 2008;17(5):427–31. Guan T, Sun H, Zhang L, et al. The effects of electroacupuncture for iron protein and stained cells in the substantia nigra in Parkinson 's disease model mice. Chin J Histochem Cytochem. 2008;17(5):427–31.
49.
go back to reference Wang S, Qi XJ, Han D. Impacts of penetration therapy with head electrical acupuncture on proliferation of neural stem cells in substantia nigra of rat model of Parkinson. World J Acu-Mox. 2008;18:23–30. Wang S, Qi XJ, Han D. Impacts of penetration therapy with head electrical acupuncture on proliferation of neural stem cells in substantia nigra of rat model of Parkinson. World J Acu-Mox. 2008;18:23–30.
50.
go back to reference Jeon S, Kim YJ, Kim ST, et al. Proteomic analysis of the neuroprotective mechanisms of acupuncture treatment in a Parkinson's disease mouse model. Proteomics. 2008;8(22):4822–32.CrossRefPubMed Jeon S, Kim YJ, Kim ST, et al. Proteomic analysis of the neuroprotective mechanisms of acupuncture treatment in a Parkinson's disease mouse model. Proteomics. 2008;8(22):4822–32.CrossRefPubMed
51.
go back to reference Xie XX, Kou ST, Pu ZH, et al. Effects of scalp catgut embedding on SOD, NO, MDA in the rat with Parkinson's disease. Zhongguo Zhen Jiu. 2007;27(10):753–6.PubMed Xie XX, Kou ST, Pu ZH, et al. Effects of scalp catgut embedding on SOD, NO, MDA in the rat with Parkinson's disease. Zhongguo Zhen Jiu. 2007;27(10):753–6.PubMed
52.
go back to reference Kang JM, Park HJ, Choi YG, Choe IH, Park JH, Kim YS, Lim S. Acupuncture inhibits microglial activation and inflammatory events in the MPTP-induced mouse model. Brain Res. 2007;1131(1):211–9.CrossRefPubMed Kang JM, Park HJ, Choi YG, Choe IH, Park JH, Kim YS, Lim S. Acupuncture inhibits microglial activation and inflammatory events in the MPTP-induced mouse model. Brain Res. 2007;1131(1):211–9.CrossRefPubMed
53.
go back to reference Hwang JY, Choi IH, Park JH, et al. Acupuncture inhibits microglial activation in the rat model of Parkinson's disease. Korean J Meridian Acupoint. 2007;24(1):131–44. Hwang JY, Choi IH, Park JH, et al. Acupuncture inhibits microglial activation in the rat model of Parkinson's disease. Korean J Meridian Acupoint. 2007;24(1):131–44.
54.
go back to reference Luo EL, Zhao FZ, Li GZ, et al. Effects of acupuncture on NOS of the medial part of the globus pallidus in rat model of Parkinson's disease. J Clinic Acupunct Mox. 2007;23(1):54–5. Luo EL, Zhao FZ, Li GZ, et al. Effects of acupuncture on NOS of the medial part of the globus pallidus in rat model of Parkinson's disease. J Clinic Acupunct Mox. 2007;23(1):54–5.
55.
go back to reference Wang Q, Tang CZ, Chen XH, et al. Effects of acupuncture on dopaminergic neurons in rats with Parkinson Disease. Chin J Basic Med Tradit Chin Med. 2007;13(8):621–2. Wang Q, Tang CZ, Chen XH, et al. Effects of acupuncture on dopaminergic neurons in rats with Parkinson Disease. Chin J Basic Med Tradit Chin Med. 2007;13(8):621–2.
56.
go back to reference Jin Z, Liu TT, Zhou BX. Changes of the anti-oxidation capability of rat model of Parkinson disease after acupuncture at subthalamus. Chin J Clinic Rehabil. 2006a;10(23):188–90. Jin Z, Liu TT, Zhou BX. Changes of the anti-oxidation capability of rat model of Parkinson disease after acupuncture at subthalamus. Chin J Clinic Rehabil. 2006a;10(23):188–90.
57.
go back to reference Jin Z, Liu TT, Jiang XC, et al. Effects of electroacupuncture at subthalamus on dopamine homovanillic acid and dihydroxy-phenyl acetic acid of rats with Parkinson disease. Chin J Clinic Rehabil. 2006b;10:128–9. Jin Z, Liu TT, Jiang XC, et al. Effects of electroacupuncture at subthalamus on dopamine homovanillic acid and dihydroxy-phenyl acetic acid of rats with Parkinson disease. Chin J Clinic Rehabil. 2006b;10:128–9.
58.
go back to reference Ma J, Wang YC, Gan SY. Effects of electroacupuncture on behaviors and dopaminergic neurons in the rat of Parkinson's disease. Chin Acupunct Mox. 2006;26(9):655–7. Ma J, Wang YC, Gan SY. Effects of electroacupuncture on behaviors and dopaminergic neurons in the rat of Parkinson's disease. Chin Acupunct Mox. 2006;26(9):655–7.
59.
go back to reference Tang Y, Yu S, Chen J. Effect of Electroacupuncture on the Expression of BDNF and BDNF mRNA in Parkinson's Disease Mice. Acupunct Res. 2006;31(1):38–42. Tang Y, Yu S, Chen J. Effect of Electroacupuncture on the Expression of BDNF and BDNF mRNA in Parkinson's Disease Mice. Acupunct Res. 2006;31(1):38–42.
60.
go back to reference Wang YC, Ma J, Wang H. Changes of content of glutamic acid in striatum of rats with Parkinson disease after electroacupuncture stimulation at acupoints. Chin J Clinic Rehabil. 2006;10:183–5. Wang YC, Ma J, Wang H. Changes of content of glutamic acid in striatum of rats with Parkinson disease after electroacupuncture stimulation at acupoints. Chin J Clinic Rehabil. 2006;10:183–5.
61.
go back to reference Kim ST, Park HJ, Chae YB, et al. Acupuncture at Liver Meridian Protects the Dopaminergic Neuronal Damage in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced Parkinson’s Disease Mouse Model. Korean J Acupunct. 2006;23(4):169–76. Kim ST, Park HJ, Chae YB, et al. Acupuncture at Liver Meridian Protects the Dopaminergic Neuronal Damage in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced Parkinson’s Disease Mouse Model. Korean J Acupunct. 2006;23(4):169–76.
62.
go back to reference Kim YK, Lim HH, Song YK, et al. Effect of acupuncture on 6-hydroxydopamine-induced nigrostratal dopaminergic neuronal cell death in rats. Neurosci Lett. 2005;384(1-2):133–8.CrossRefPubMed Kim YK, Lim HH, Song YK, et al. Effect of acupuncture on 6-hydroxydopamine-induced nigrostratal dopaminergic neuronal cell death in rats. Neurosci Lett. 2005;384(1-2):133–8.CrossRefPubMed
63.
go back to reference Ma J, Zhu SX. Effect of electroacupuncture on anti-oxidase in mesencephalic substantia nigra in rats with Parkinson disease. Chin J Clin Rehabil. 2005;9:120–1. Ma J, Zhu SX. Effect of electroacupuncture on anti-oxidase in mesencephalic substantia nigra in rats with Parkinson disease. Chin J Clin Rehabil. 2005;9:120–1.
64.
go back to reference Wang YD, Ma J, Wang H. Experimental study of the protective effect on dopaminergic neurons in substance nigra of the Parkinsonian rats by the acupuncture therapy of 'Shuanggu Yitong'. J Hubei College TCM. 2005;7(3):25–6. Wang YD, Ma J, Wang H. Experimental study of the protective effect on dopaminergic neurons in substance nigra of the Parkinsonian rats by the acupuncture therapy of 'Shuanggu Yitong'. J Hubei College TCM. 2005;7(3):25–6.
65.
go back to reference Park HJ, Lim S, Joo WS, et al. Acupuncture prevents 6-hydroxydopamine-induced neuronal death in the nigrostriatal dopaminergic system in the rat Parkinson's disease model. Exp Neurol. 2003;180(1):92–7.CrossRef Park HJ, Lim S, Joo WS, et al. Acupuncture prevents 6-hydroxydopamine-induced neuronal death in the nigrostriatal dopaminergic system in the rat Parkinson's disease model. Exp Neurol. 2003;180(1):92–7.CrossRef
66.
go back to reference Liang XB, Liu XY, Li FQ, et al. Long-term high-frequency electro-acupuncture stimulation prevents neuronal degeneration and up-regulates BDNF mRNA in the substantia nigra and ventral tegmental area following medial forebrain bundle axotomy. Brain Res Mol Brain Res. 2002;108:51–9.CrossRefPubMed Liang XB, Liu XY, Li FQ, et al. Long-term high-frequency electro-acupuncture stimulation prevents neuronal degeneration and up-regulates BDNF mRNA in the substantia nigra and ventral tegmental area following medial forebrain bundle axotomy. Brain Res Mol Brain Res. 2002;108:51–9.CrossRefPubMed
67.
go back to reference Lin Y, Lin X. Comparative study of D2 receptors and dopamine content in striatum before and after electro-acupuncture treatment in rats. J Chin Med. 2000;113(5):408–11. Lin Y, Lin X. Comparative study of D2 receptors and dopamine content in striatum before and after electro-acupuncture treatment in rats. J Chin Med. 2000;113(5):408–11.
68.
go back to reference He C, Wang L, Dong H, et al. Effects of Acupuncture - Moxibustion on the Contents of Monoamine Transmitters in the Striatum of Rats in Parkinson's Disease. Acupunct res. 1998;1:44–8. He C, Wang L, Dong H, et al. Effects of Acupuncture - Moxibustion on the Contents of Monoamine Transmitters in the Striatum of Rats in Parkinson's Disease. Acupunct res. 1998;1:44–8.
69.
go back to reference Zhu W, Xi G, Ju J. Effect of acupuncture and Chinese medicine treatment on brain dopamine level of MPTP-lesioned C57BL mice. Acupunct Res. 1996;4:46–9. Zhu W, Xi G, Ju J. Effect of acupuncture and Chinese medicine treatment on brain dopamine level of MPTP-lesioned C57BL mice. Acupunct Res. 1996;4:46–9.
70.
go back to reference Beery AK, Zucker I. Sex bias in neuroscience and biomedical research. Neurosci Biobehav Rev. 2011;35(3):565–72.CrossRefPubMed Beery AK, Zucker I. Sex bias in neuroscience and biomedical research. Neurosci Biobehav Rev. 2011;35(3):565–72.CrossRefPubMed
71.
go back to reference Martin RM, Biswas PN, Freemantle SN, Pearce GL, Mann RD. Age and sex distribution of suspected adverse drug reactions to newly marketed drugs in general practice in England: analysis of 48 cohort studies. Br J Clin Pharmacol. 1998;46(5):505–11.CrossRefPubMedPubMedCentral Martin RM, Biswas PN, Freemantle SN, Pearce GL, Mann RD. Age and sex distribution of suspected adverse drug reactions to newly marketed drugs in general practice in England: analysis of 48 cohort studies. Br J Clin Pharmacol. 1998;46(5):505–11.CrossRefPubMedPubMedCentral
72.
go back to reference Smith KM, Dahodwala N. Sex differences in Parkinson's disease and other movement disorders. Exp Neurol. 2014;259:44–56.CrossRefPubMed Smith KM, Dahodwala N. Sex differences in Parkinson's disease and other movement disorders. Exp Neurol. 2014;259:44–56.CrossRefPubMed
Metadata
Title
Sex differences in acupuncture effectiveness in animal models of Parkinson's disease: a systematic review
Authors
Sook-Hyun Lee
Maurits van den Noort
Peggy Bosch
Sabina Lim
Publication date
01-12-2016
Publisher
BioMed Central
Published in
BMC Complementary Medicine and Therapies / Issue 1/2016
Electronic ISSN: 2662-7671
DOI
https://doi.org/10.1186/s12906-016-1405-5

Other articles of this Issue 1/2016

BMC Complementary Medicine and Therapies 1/2016 Go to the issue