Correlation Between Emotional-Affective Disorders and Gut Microbiota Composition in Patients with Parkinson’s Disease

Cover Page
  • Authors: Alifirova V.M.1, Zhukova N.G.1, Zhukova I.A.1, Mironova Y.S.1, Petrov V.A.2, Izhboldina O.P.1, Titova M.A.1, Latypova A.V.1, Nikitina M.A.1, Dorofeeva Y.B.2, Saltykova I.V.2, Tyakht A.V.3, Kostryukova E.S.3, Sazonov A.E.4
  • Affiliations:
    1. Department of Neurology and Neurosurgery, Siberian State Medical University
    2. Central Research Laboratory, Siberian State Medical University
    3. Scientific Research Institute of Physical-Chemical Medicine
    4. Central Research Laboratory, Siberian State Medical University Lomonosov Moscow State University
  • Issue: Vol 71, No 6 (2016)
  • Section: NEUROLOGY AND NEUROSURGERY: CURRENT ISSUES
  • URL: https://vestnikramn.spr-journal.ru/jour/article/view/734
  • DOI: https://doi.org/10.15690/vramn734

Abstract


Background: Despite the efforts of scientific community the data available on the correlation between emotional-affective symptoms of Parkinson’s disease and changes in microbiome is still scarce. Deeper studies of nonmotor symptoms evident in premotor stages of the disease and the reciprocal influence of microbiota may help to understand the etiology and pathogenesis of PD neurodegeneration better.

The aim of the study was to discover the relations between emotional-affective disorders prevalent in PD population and changes in gut microbiota composition.

Мethods: 51 patient diagnosed with PD participated in the study. Every participant’s emotional-affective state was examined using Beck’s Depression Inventory (BDI) and Hospital Anxiety and Depression Scale (HADS). Taxonomic richness of microbiome was studied using 16S ribosomal RNA gene sequencing, bioinformatics, and statistical analysis.

Results: Anxiety and depression are prevalent affective disorders in patients with PD. In our study, most of the subjects demonstrated certain anxiety and depression. Taxonomic diversity of gut microbiota in BP was increasing with the increase in anxiety levels, reaching the maximum in the group with subclinical anxiety, and decreasing in the group with clinically significant anxiety disorder. At the species level, patients with clinically significant anxiety had higher abundance of Clostridium clariflavum compared to the anxiety-free patients. Patients with moderate depression were characterized by the higher prevalence of Christensenella minuta, Clostridium disporicum, and Oscillibacter valericigenes compared to subjects without depression or with mild depression.

Conclusion: The data we received in our study allow better understanding of PD pathogenesis.


V. M. Alifirova

Department of Neurology and Neurosurgery, Siberian State Medical University

Author for correspondence.
Email: v_alifirova@mail.ru
ORCID iD: 0000-0002-4140-3223

Russian Federation

Tomsk, Russian Federation

N. G. Zhukova

Department of Neurology and Neurosurgery, Siberian State Medical University

Email: znatali@yandex.ru
ORCID iD: 0000-0001-6547-6622

Russian Federation

Tomsk, Russian Federation

I. A. Zhukova

Department of Neurology and Neurosurgery, Siberian State Medical University

Email: irzhukova@inbox.ru
ORCID iD: 0000-0001-5679-1698

Russian Federation

Tomsk, Russian Federation

Yu. S. Mironova

Department of Neurology and Neurosurgery, Siberian State Medical University

Email: mir.yuli@mail.ru
ORCID iD: 0000-0002-3834-5923

Russian Federation

Tomsk, Russian Federation

V. A. Petrov

Central Research Laboratory, Siberian State Medical University

Email: vyacheslav.a.petrov@mail.ru
ORCID iD: 0000-0002-5205-9739

Russian Federation

младший научный сотрудник Центральной научно-исследовательской лаборатории ФГБОУ ВО «Сибирский государственный медицинский университет» Минздрава России Адрес: 634001, Томск, Московский тракт, д. 2 г, стр. 18, тел.: +7 (3822) 90-11-01 доб. 16-35

O. P. Izhboldina

Department of Neurology and Neurosurgery, Siberian State Medical University

Email: olga.izhboldina@inbox.ru
ORCID iD: 0000-0003-3705-9615

Russian Federation Tomsk, Russian Federation

M. A. Titova

Department of Neurology and Neurosurgery, Siberian State Medical University

Email: titovam82@list.ru
ORCID iD: 0000-0002-0080-3765

Russian Federation

Tomsk, Russian Federation

A. V. Latypova

Department of Neurology and Neurosurgery, Siberian State Medical University

Email: lina.lae@gmail.com
ORCID iD: 0000-0003-0676-3968

Russian Federation

Tomsk, Russian Federation

M. A. Nikitina

Department of Neurology and Neurosurgery, Siberian State Medical University

Email: nikitina_ma@mail.ru
ORCID iD: 0000-0002-2614-207X

Russian Federation Tomsk, Russian Federation

Y. B. Dorofeeva

Central Research Laboratory, Siberian State Medical University

Email: julia.dorofeeva25@gmail.com

Russian Federation

Tomsk, Russian Federation

I. V. Saltykova

Central Research Laboratory, Siberian State Medical University

Email: ira.salticova@mail.ru
ORCID iD: 0000-0002-0457-5392

Russian Federation

Tomsk, Russian Federation

A. V. Tyakht

Scientific Research Institute of Physical-Chemical Medicine

Email: at@niifhm.ru
ORCID iD: 0000-0002-7358-2537

Russian Federation

Moscow, Russian Federation

E. S. Kostryukova

Scientific Research Institute of Physical-Chemical Medicine

Email: el-es@yandex.ru
ORCID iD: 0000-0002-0457-6803

Russian Federation

Moscow, Russian Federation

A. E. Sazonov

Central Research Laboratory, Siberian State Medical University

Lomonosov Moscow State University

Email: sazonov_al@mail.ru

Russian Federation

Tomsk, Russian Federation

Moscow, Russian Federation

  1. Cénit MC, Matzaraki V, Tigchelaar EF, Zhernakova A. Rapidly expanding knowledge on the role of the gut microbiome in health and disease. Biochim Biophys Acta. 2014;1842(10):1981–1992. doi: 10.1016/j.bbadis.2014.05.023.
  2. Найт Р. Смотри, что у тебя внутри. Как микробы, живущие в нашем теле, определяют наше здоровье и нашу личность / Пер. с англ. Е. Валкина. — М.: АСТ Corpus; 2015. 160 p. [Knight R. Follow your gut: the enormous impact of tiny microbes. Transl. from English by E. Valkina. Moscow: AST Corpus; 2015. 160 p. (In Russ).]
  3. Spasova DS, Surh C. Blowing on embers: commensal microbiota and our immune system. Front Immunol. 2014;5:318. doi: 10.3389/fimmu.2014.00318.
  4. Dickson RP, Erb-Downward JR, Huffnagle GB. The role of the bacterial microbiome in lung disease. Expert Rev Respir Med. 2013;7(3):245–257. doi: 10.1586/ers.13.24.
  5. Bercik P, Denou E, Collins J, et al. The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology. 2011;141(2):599–609.e3. doi: 10.1053/j.gastro.2011.04.052.
  6. Cryan JF, Dinan TG. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci. 2012;13(10):701–712. doi: 10.1038/nrn3346.
  7. Heijtz RD, Wang S, Anuar F, et al. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci U S A. 2011;108(7):3047–3052. doi: 10.1073/pnas.1010529108.
  8. Шендеров Б.А. Микробная экология человека и ее роль в поддержании здоровья // Метаморфозы. — 2014. — №5 — С. 72–80. [Shenderov BA. Mikrobnaya ekologiya cheloveka i ee rol’ v podderzhanii zdorov’ya. Metamorfozy. 2014;(5);72–80. (In Russ).]
  9. Шендеров Б.А., Голубев В.Л., Данилов А.Б., Прищепа А.В. Кишечная микробиота человека и нейродегенеративные заболевания // Поликлиника. — 2016. — №1–1 — С. 7–13. [Shenderov BA, Golubev VL, Danilov AB, Prishchepa AV. Gut human microbiota and neurodegenerative diseases. Poliklinika. 2016;(1–1):7–13. (In Russ).]
  10. Hill JM, Bhattacharjee S, Pogue AI, Lukiw WJ. The gastrointestinal tract microbiome and potential link to Alzheimer’s disease. Front Neurol. 2014;5:43. doi: 10.3389/fneur.2014.00043.
  11. Иллариошкин С.Н. Ранняя диагностика нейродегенеративных заболеваний // Нервы. — 2008. — №1 — С. 11–13. [Illarioshkin SN. Rannyaya diagnostika neirodegenerativnykh zabolevanii. Nervy. 2008;(1):11–13. (In Russ).]
  12. Dorsey ER, Constantinescu R, Thompson JP, et al. Projected number of people with Parkinson’s disease in the most populous nations, 2005 through 2030. Neurology. 2006;68(5):384–386. doi: 10.1212/01.wnl.0000247740.47667.03.
  13. Маньковский Н.Б., Карабань Н.В. Качество жизни больных болезнью Паркинсона // Журнал психиатрии и медицинской психологии. — 2004. — №2 — С. 9–13. [Man’kovskii NB, Karaban’ NV. Kachestvo zhizni bol’nykh bolezn’yu Parkinsona. Zhurnal psikhiatrii i meditsinskoi psikhologii. 2004;(2):9–13. (In Russ).]
  14. Жукова И.А., Жукова Н.Г., Алифирова В.М. Немоторные проявления болезни Паркинсона // Бюллетень сибирской медицины. — 2009. — T.8. — №1–2 — С. 136–141. [Zhukova IA, Zhukova NG, Alifirova VM. Nemotornye proyavleniya bolezni Parkinsona. Bulletin of Siberian medicine. 2009;8(1–2):136–141. (In Russ).]
  15. Левин О.С., Федорова Н.В. Болезнь Паркинсона как нейропсихиатрическое заболевание. В кн.: Болезнь Паркинсона и расстройства движений. Руководство для врачей по материалам II Национального конгресса по болезни Паркинсона и расстройствам движений. — М.; 2011. — С. 99–104. [Levin OS, Fedorova NV. Bolezn’ Parkinsona kak neiropsikhiatricheskoe zabolevanie. In: Bolezn’ Parkinsona i rasstroistva dvizhenii. Rukovodstvo dlya vrachei po materialam II Natsional’nogo kongressa po bolezni Parkinsona i rasstroistvam dvizhenii. Moscow; 2011. p. 99–104 (In Russ).]
  16. Нодель М.Р. Депрессия при болезни Паркинсона // Неврология, нейропсихиатрия, психосоматика. — 2010. — №4 — С. 11–17. [Nodel MR. Depression in Parkinson’s disease. Neurology, neuropsychiatry, psychosomatics. 2010;(4):11–17. (In Russ).]
  17. Мирецкая А.В., Федорова Н.В., Макаров В.В. Депрессивные расстройства у больных болезнью Паркинсона. В кн.: Болезнь Паркинсона и расстройства движений. Руководство для врачей по материалам I Национального конгресса по болезни Паркинсона и расстройствам движений. — М.; 2008. ― С. 97–99. [Miretskaya AV, Fedorova NV, Makarov VV. Depressivnye rasstroistva u bol’nykh bolezn’yu Parkinsona. In: Bolezn’ Parkinsona i rasstroistva dvizhenii. Rukovodstvo dlya vrachei po materialam I Natsional’nogo kongressa po bolezni Parkinsona i rasstroistvam dvizhenii. Moscow; 2008. p. 97–99. (In Russ).]
  18. Dooneief G, Mirabello E, Bell K, et al. An estimate of the incidence of depression in idiopathic Parkinson’s disease. Arch Neurol. 1992;49(3):305–307. doi: 10.1001/archneur.1992.00530270125028.
  19. Schrag A, Jahanshahi M, Quinn NP. What contributes to quality of life in patients with Parkinson’s disease? J Neurol Neurosurg Psychiatry. 2000;69:308–312. doi: 10.1136/jnnp.69.3.308.
  20. Вейн А.М., Вознесенская Т.Г., Голубев В.Л., Дюкова Г.М. Депрессия в неврологической практике. — М.: МИА; 2007. — 208 с. [Vein AM, Voznesenskaya TG, Golubev VL, Dyukova GM. Depressiya v nevrologicheskoi praktike. Moscow: MIA; 2007. 208 p. (In Russ).]
  21. Cummings JL. Depression and Parkinson’s disease: a review. Am J Psychiatry. 1992;149:443–454. doi: 10.1176/ajp.149.4.443.
  22. Hubble JP, Cao T, Hassanein RE, et al. Risk factors for Parkinson’s disease. Neurology. 1993;43(9):1693–1697. doi: 10.1212/wnl.43.9.1693.
  23. Иллариошкин С.Н. Течение болезни Паркинсона и подходы к ранней диагностике. В кн.: Болезнь Паркинсона и расстройства движений. Руководство для врачей по материалам II Национального конгресса по болезни Паркинсона и расстройствам движений. — М.; 2011. — С. 41–47. [Illarioshkin SN. Techenie bolezni Parkinsona i podkhody k rannei diagnostike. In: Bolezn’ Parkinsona i rasstroistva dvizhenii. Rukovodstvo dlya vrachei po materialam II Natsional’nogo kongressa po bolezni Parkinsona i rasstroistvam dvizhenii. Moscow; 2011. p. 41–47. (In Russ).]
  24. Fang F, Xu Q, Park Y, Huang X, et al. Depression and the subsequent risk of Parkinson’s disease in the NIN-AARP Diet and Health Study. Mov Disord. 2010;25(9):1157–1162. doi: 10.1002/mds.23092 .
  25. Mosharov E, Larsen K, Kanter E, et al. Interplay between cytosolic dopamine, calcium, and alpha-synuclein causes selective death of substantia nigra neurons. Neuron. 2009;62(2):218–229. doi: 10.1016/j.neuron.2009.01.033.
  26. Braak H, Del Tredici K, Rub U, et al. Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging. 2003;24(2):197–210. doi: 10.1016/s0197-4580(02)00065-9.
  27. Richard IH, Schiffer RB, Kurlan R. Anxiety and Parkinson’s disease. J Neuropsychiatry Clin Neurosci. 1996;8(4):383–392. doi: 10.1176/jnp.8.4.383.
  28. Zigmond AS, Snaith RP. The hospital anxiety and depression scale. Acta Psychiatr Scand. 1983;67(6):361–370. doi: 10.1111/j.1600-0447.1983.tb09716.x.
  29. Gintinga H, Näring G, van der Veld WM, et al. Validating the Beck Depression Inventory-II in Indonesia’s general population and coronary heart disease patients. Int J Clin Health Psychol. 2013;13(3):235–242. doi: 10.1016/s1697-2600(13)70028-0.
  30. Beck AT, Steer RA, Brown GK, et al. BDI-II-NL Handleiding [BDI-II-Dutch Manual]. Lisse: Psychological Corporation; 2002.
  31. Egshatyan LV, Kashtanova DA, Popenko AS, et al. Gut microbiota and diet in patients with different glucose tolerance. Endocr Connect. 2015;5(1):1–9. doi: 10.1530/ec-15-0094.
  32. 16S Metagenomic Sequencing Library Preparation: Preparing 16S Ribosomal RNA Gene Amplicons for the Illumina MiSeq System [cited 2016 Sep 09]. Available from: http://web.uri.edu/gsc/files/16s-metagenomic-library-prep-guide-15044223-b.pdf.
  33. Caporaso JG, Kuczynski J, Stombaugh J, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7(5):335–336. doi: 10.1038/nmeth.f.303.
  34. DeSantis TZ, Hugenholtz P, Larsen N, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006;72(7):5069–5072. doi: 10.1128/aem.03006-05.
  35. Ritari J, Salojärvi J, Lahti L, de Vos WM. Improved taxonomic assignment of human intestinal 16S rRNA sequences by a dedicated reference database. BMC Genomics. 2015;16:1056. doi: 10.1186/s12864-015-2265-y.
  36. Paulson JN, Stine OC, Bravo HC, Pop M. Differential abundance analysis for microbial marker-gene surveys. Nat Methods. 2013;10(12):1200–1202. doi: 10.1038/nmeth.2658.
  37. Шток В.Н., Федорова Н.В. Болезнь Паркинсона. В кн.: Руководство по диагностике и лечению / Под ред. Штока В.Н., Ивановой-Смоленской И.А., Левина И.С. — М.: Медпресс-информ; 2002. — С. 87–124. [Shtok VN, Fedorova NV. Bolezn’ Parkinsona. In: Рukovodstvo po diagnostike i lecheniyu. Ed by Shtok V.N., Ivanova-Smolenskaya I.A., Levin I.S. Moscow: Medpress-inform; 2002. p. 87–124. (In Russ).]
  38. Keshavarzian A, Green SJ, Engen PA, et al. Colonic bacterial composition in Parkinson’s disease. Mov Disord. 2015;30(10):1351–1360. doi: 10.1002/mds.26307.
  39. Scheperjans F, Aho V, Pereira PA, et al. Gut microbiota are related to Parkinson’s disease and clinical phenotype. Mov Disord. 2015;30(3):350–358. doi: 10.1002/mds.26069.
  40. Бондаренко В.М, Рябиченко Е.В. Кишечно-мозговая ось. Нейронные и иммуновоспалительные механизмы патологии мозга и кишечника // Журнал микробиологии, эпидемиологии и иммунобиологии. — 2013. — №2 — С. 112–120. [Bondarenko VM, Ryabichenko EV. Intestinal-brain axis. Neuronal and immune-inflammatory mechanisms of brain and intestine pathology. Zh Mikrobiol Epidemiol Immunobiol. 2013;(2):112–120. (In Russ).]
  41. Gill SR, Pop M, Deboy RT, et al. Metagenomic analysis of the human distal gut microbiome. Science. 2006;312(5778):1355–1359. doi: 10.1126/science.1124234.
  42. Mangin I, Bonnet R, Seksik P, et al. Molecular inventory of faecal microflora in patients with Crohn’s disease. FEMS Microbiol Ecol. 2004;50(1):25–36. doi: 10.1016/j.femsec.2004.05.005.
  43. Shenderov BA. Gut indigenous microbiota and epigenetics. Microb Ecol Health Dis. 2012;23:17461. doi: 10.3402/mehd.v23i0.17461.
  44. Asano Y, Hiramoto T, Nishino R, et al. Critical role of gut microbiota in the production of biologically active, free catecholamines in the gut lumen of mice. Am J Physiol Gastrointest Liver Physiol. 2012;303(11):1288–1295. doi: 10.1152/ajpgi.00341.2012.
  45. Naseribafrouei A, Hestad K, Avershina E, et al. Correlation between the human fecal microbiota and depression. Neurogastroenterol Motil. 2014;26(8):1155–1162. doi: 10.1111/nmo.12378.
  46. Starkstein S, Petracca G, Chemerinski E, et al. Depression in classic versus akinetic-rigid Parkinson’s disease. Mov Disord. 1998;13(1):29–33. doi: 10.1002/mds.870130109.0130109.

Views

Abstract - 50

PDF (Russian) - 7

Cited-By


PlumX



Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.