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<article article-type="research-article" dtd-version="1.3" xmlns:mml="http://www.w3.org/1998/Math/MathML" xmlns:xlink="http://www.w3.org/1999/xlink" xmlns:xsi="http://www.w3.org/2001/XMLSchema-instance" xml:lang="ru"><front><journal-meta><journal-id journal-id-type="publisher-id">r-n-j</journal-id><journal-title-group><journal-title xml:lang="ru">Российский неврологический журнал</journal-title><trans-title-group xml:lang="en"><trans-title>Russian neurological journal</trans-title></trans-title-group></journal-title-group><issn pub-type="ppub">2658-7947</issn><issn pub-type="epub">2686-7192</issn><publisher><publisher-name>МИА</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="doi">10.30629/2658-7947-2022-27-6-32-40</article-id><article-id custom-type="elpub" pub-id-type="custom">r-n-j-369</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="section-heading" xml:lang="ru"><subject>ИССЛЕДОВАНИЯ И КЛИНИЧЕСКИЕ НАБЛЮДЕНИЯ</subject></subj-group><subj-group subj-group-type="section-heading" xml:lang="en"><subject>CLINICAL RESEARCHES AND CASE REPORTS</subject></subj-group></article-categories><title-group><article-title>Комбинированное клинико-нейровизуализационное исследование пациентов с болезнью Паркинсона с помощью транскраниальной сонографии и нейромеланин-чувствительной магнитно-резонансной томографии</article-title><trans-title-group xml:lang="en"><trans-title>Clinical and neuroimaging study of patients with Parkinson’s disease using transcranial sonography and neuromelanin-sensitive magnetic resonance imaging</trans-title></trans-title-group></title-group><contrib-group><contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid">https://orcid.org/0000-0003-3843-6435</contrib-id><name-alternatives><name name-style="eastern" xml:lang="ru"><surname>Москаленко</surname><given-names>А. Н.</given-names></name><name name-style="western" xml:lang="en"><surname>Moskalenko</surname><given-names>A. N.</given-names></name></name-alternatives><bio xml:lang="ru"><p>Москаленко Анна Николаевна</p><p>Москва</p></bio><bio xml:lang="en"><p>Moscow</p></bio><email xlink:type="simple">anna_nik_kern@rambler.ru</email><xref ref-type="aff" rid="aff-1"/></contrib><contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid">https://orcid.org/0000-0002-8726-8928</contrib-id><name-alternatives><name name-style="eastern" xml:lang="ru"><surname>Чечеткин</surname><given-names>А. О.</given-names></name><name name-style="western" xml:lang="en"><surname>Chechetkin</surname><given-names>A. O.</given-names></name></name-alternatives><bio xml:lang="ru"><p>Москва</p></bio><bio xml:lang="en"><p>Moscow</p></bio><email xlink:type="simple">andreychechetkin@gmail.com</email><xref ref-type="aff" rid="aff-1"/></contrib><contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid">https://orcid.org/0000-0002-5706-6997</contrib-id><name-alternatives><name name-style="eastern" xml:lang="ru"><surname>Филатов</surname><given-names>А. С.</given-names></name><name name-style="western" xml:lang="en"><surname>Filatov</surname><given-names>A. S.</given-names></name></name-alternatives><bio xml:lang="ru"><p>Москва</p></bio><bio xml:lang="en"><p>Moscow</p></bio><email xlink:type="simple">fil4tovmd@gmail.com</email><xref ref-type="aff" rid="aff-1"/></contrib><contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid">https://orcid.org/0000-0001-8070-7644</contrib-id><name-alternatives><name name-style="eastern" xml:lang="ru"><surname>Федотова</surname><given-names>Е. Ю.</given-names></name><name name-style="western" xml:lang="en"><surname>Fedotova</surname><given-names>E. Yu.</given-names></name></name-alternatives><bio xml:lang="ru"><p>Москва</p></bio><bio xml:lang="en"><p>Moscow</p></bio><email xlink:type="simple">ekfedotova@gmail.com</email><xref ref-type="aff" rid="aff-1"/></contrib><contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid">https://orcid.org/0000-0001-5539-245X</contrib-id><name-alternatives><name name-style="eastern" xml:lang="ru"><surname>Коновалов</surname><given-names>Р. Н.</given-names></name><name name-style="western" xml:lang="en"><surname>Konovalov</surname><given-names>R. N.</given-names></name></name-alternatives><bio xml:lang="ru"><p>Москва</p></bio><bio xml:lang="en"><p>Moscow</p></bio><email xlink:type="simple">krn_74@mail.ru</email><xref ref-type="aff" rid="aff-1"/></contrib><contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid">https://orcid.org/0000-0002-2704-6282</contrib-id><name-alternatives><name name-style="eastern" xml:lang="ru"><surname>Иллариошкин</surname><given-names>С. Н.</given-names></name><name name-style="western" xml:lang="en"><surname>Illarioshkin</surname><given-names>S. N.</given-names></name></name-alternatives><bio xml:lang="ru"><p>Москва</p></bio><bio xml:lang="en"><p>Moscow</p></bio><email xlink:type="simple">snillario@gmail.com</email><xref ref-type="aff" rid="aff-1"/></contrib></contrib-group><aff-alternatives id="aff-1"><aff xml:lang="ru">ФГБНУ «Научный центр неврологии»<country>Россия</country></aff><aff xml:lang="en">Research Center of Neurology<country>Russian Federation</country></aff></aff-alternatives><pub-date pub-type="collection"><year>2022</year></pub-date><pub-date pub-type="epub"><day>10</day><month>01</month><year>2023</year></pub-date><volume>27</volume><issue>6</issue><fpage>32</fpage><lpage>40</lpage><permissions><copyright-statement>Copyright &amp;#x00A9; Москаленко А.Н., Чечеткин А.О., Филатов А.С., Федотова Е.Ю., Коновалов Р.Н., Иллариошкин С.Н., 2023</copyright-statement><copyright-year>2023</copyright-year><copyright-holder xml:lang="ru">Москаленко А.Н., Чечеткин А.О., Филатов А.С., Федотова Е.Ю., Коновалов Р.Н., Иллариошкин С.Н.</copyright-holder><copyright-holder xml:lang="en">Moskalenko A.N., Chechetkin A.O., Filatov A.S., Fedotova E.Y., Konovalov R.N., Illarioshkin S.N.</copyright-holder><license license-type="creative-commons-attribution" xlink:href="https://creativecommons.org/licenses/by/4.0/" xlink:type="simple"><license-p>This work is licensed under a Creative Commons Attribution 4.0 License.</license-p></license></permissions><self-uri xlink:href="https://www.r-n-j.com/jour/article/view/369">https://www.r-n-j.com/jour/article/view/369</self-uri><abstract><sec><title>Введение</title><p>Введение. К ведущим патологическим признакам болезни Паркинсона (БП) относятся дегенерация содержащих нейромеланин (НМ) дофаминергических нейронов и отложение железа в черной субстанции (ЧС) среднего мозга. Показана определенная патогенетическая связь между повышенным отложением железа и снижением уровня НМ в ЧС у пациентов с БП. Логично предположить, что различные методы нейровизуализации, чувствительные к НМ и железу, могут иметь большое клиническое значение для диагностики и мониторинга прогрессирования заболевания. К таким методам нейровизуализации относятся в первую очередь транскраниальная сонография (ТКС) и нейромеланин-чувствительная магнитно-резонансная томография (НМ-МРТ).</p></sec><sec><title>Цель исследования</title><p>Цель исследования. Сравнение диагностической значимости и эффективности ТКС и НМ-МРТ в дифференцировании пациентов с БП от нормы, а также уточнение патофизиологии феномена гиперэхогенности ЧС (ГЧС) посредством косвенного изучения концентрации НМ при НМ-МРТ.</p></sec><sec><title>Материал и методы</title><p>Материал и методы. В основную группу были включены 40 пациентов с БП, в группу контроля — 20 здоровых добровольцев, сопоставимых по полу и возрасту с основной группой. В случае обнаружения ГЧС при проведении ТКС гиперэхогенную область обводили курсором вручную с последующим автоматическим расчетом площади. При НМ-МРТ полученные изображения предварительно обрабатывались с помощью общедоступной программы для обработки изображений Image-J (NIH, США) с последующим автоматическим расчетом площади ЧС. На основании полученных данных рассчитывались клинико-демографические показатели и клинико-нейровизуализационные корреляции.</p></sec><sec><title>Результаты</title><p>Результаты. Чувствительность и специфичность ТКС в дифференцировании БП от нормы составили 70 и 100% соответственно, чувствительность и специфичность НМ-МРТ — 90,0 и 92,5% соответственно. Анализ взаимосвязи площади ГЧС с площадью ЧС по данным НМ-МРТ на ипсилатеральной стороне показал заметную обратную корреляционную зависимость (для правой стороны: ρ = –0,606, р &lt; 0,001; для левой стороны: ρ = –0,550; р &lt; 0,001). Таким образом, в случае увеличения площади ГЧС ожидается уменьшение площади ЧС, измеренной с помощью НМ-МРТ.</p></sec><sec><title>Заключение</title><p>Заключение. ТКС и НМ-МРТ являются надежными биомаркерами, позволяющими высокоэффективно дифференцировать БП от нормы. Патофизиологические и нейровизуализационные корреляты изменений ЧС при нейродегенеративном процессе остаются не до конца ясными и требуют дальнейшего уточнения в многоцентровых проспективных исследованиях.</p></sec></abstract><trans-abstract xml:lang="en"><sec><title>Background</title><p>Background. Parkinson’s disease (PD) is one of the most common neurodegenerative diseases and aff ects 1% of the population above 60 years. The leading pathological features of PD include degeneration of neuromelanin (NM) containing dopaminergic neurons and iron deposition in the substantia nigra (SN) of the midbrain. Various neuroimaging methods sensitive to NM and iron can be clinically important for diagnosing and monitoring disease progression. Examples of such neuroimaging methods include transcranial sonography (TCS) and neuromelanin-sensitive magnetic resonance imaging (NM-MRI) fi rst and foremost.</p></sec><sec><title>Aims</title><p>Aims. To compare the diagnostic signifi cance and eff ectiveness of TCS and NM-MRI in diff erentiating patients with PD from the norm and to elucidate the magnetic resonance- (MR-) morphological representation of the hyperechogenicity (HE) on midbrain during TCS by NM-MRI.</p></sec><sec><title>Material and methods</title><p>Material and methods. 40 patients with PD were included in the main group, and 20 healthy volunteers of gender and age comparable with the main group were included in the control group. In the case of HE detection during TCS, this area was manually traced and automatic calculated. NM-MRI images were pre-processed using image processing program Image-J (USA) with subsequent automatic calculation of SN area. Based on the data obtained, clinical, demographic and neuroimaging correlations were estimated.</p></sec><sec><title>Results</title><p>Results. The sensitivity and specifi city of TCS in diff erentiating PD from the norm were 70 and 100% respectively, the sensitivity and specifi city of NM-MRI were 90.0 and 92.5% respectively. An analysis of the relationship between the HE area and the area of the SN according to NM-MRI data on the ipsilateral side showed a noticeable inverse correlation (for the right side: ρ = –0.606, p &lt; 0.001; for the left side: ρ = –0.550; p &lt; 0.001). Thus, in the case of an increase in the HE area, a decrease in the area of SN measured using NM-MRI is expected.</p></sec><sec><title>Conclusion</title><p>Conclusion. TCS and NM-MRI are reliable biomarkers allowing highly eff ective diff erentiation of PD from normal. The pathophysiological and neuroimaging correlates of PD changes in neurodegenerative process remain not completely clear and require further clarifi cation in multicenter prospective studies.</p></sec></trans-abstract><kwd-group xml:lang="ru"><kwd>болезнь Паркинсона</kwd><kwd>транскраниальная сонография</kwd><kwd>нейромеланин-чувствительная магнитно-резонансная томография</kwd><kwd>нейромеланин</kwd><kwd>железо</kwd></kwd-group><kwd-group xml:lang="en"><kwd>Parkinson’s disease</kwd><kwd>transcranial sonography</kwd><kwd>magnetic resonance imaging</kwd><kwd>neuromelanin</kwd><kwd>iron</kwd></kwd-group><funding-group xml:lang="ru"><funding-statement>Работа поддержана грантом РНФ № 19-15-00320</funding-statement></funding-group><funding-group xml:lang="en"><funding-statement>The study was supported by the RSF grant № 19-15-0032</funding-statement></funding-group></article-meta></front><back><ref-list><title>References</title><ref id="cit1"><label>1</label><citation-alternatives><mixed-citation xml:lang="ru">Dorsey E.R., Sherer T., Okun M.S., Bloem B.R. The Emerging Evidence of the Parkinson Pandemic. J Parkinsons Dis. 2018;8(s1):S3–S8. https://doi.org/10.3233/JPD-181474. PMID: 30584159; PMCID: PMC6311367.</mixed-citation><mixed-citation xml:lang="en">Dorsey E.R., Sherer T., Okun M.S., Bloem B.R. The Emerging Evidence of the Parkinson Pandemic. J Parkinsons Dis. 2018;8(s1):S3–S8. https://doi.org/10.3233/JPD-181474. PMID: 30584159; PMCID: PMC6311367.</mixed-citation></citation-alternatives></ref><ref id="cit2"><label>2</label><citation-alternatives><mixed-citation xml:lang="ru">Kouli A., Torsney K.M., Kuan W.L. Parkinson’s Disease: Etiology, Neuropathology, and Pathogenesis. In: Stoker TB, Greenland JC, editors. Parkinson’s Disease: Pathogenesis and Clinical Aspects [Internet]. Brisbane (AU): Codon Publications; 2018; Dec 21. Chapter 1. https://doi.org/10.15586/codonpublications.parkinsonsdisease.2018.ch1</mixed-citation><mixed-citation xml:lang="en">Kouli A., Torsney K.M., Kuan W.L. Parkinson’s Disease: Etiology, Neuropathology, and Pathogenesis. In: Stoker TB, Greenland JC, editors. Parkinson’s Disease: Pathogenesis and Clinical Aspects [Internet]. Brisbane (AU): Codon Publications; 2018; Dec 21. Chapter 1. https://doi.org/10.15586/codonpublications.parkinsonsdisease.2018.ch1</mixed-citation></citation-alternatives></ref><ref id="cit3"><label>3</label><citation-alternatives><mixed-citation xml:lang="ru">Levin J., Högen T., Hillmer A.S., Bader B., Schmidt F., Kamp F. et al.Generation of ferric iron links oxidative stress to α-synuclein oligomer formation. J Parkinsons Dis. 2011;1(2):205–16. https://doi.org/10.3233/JPD-2011-11040. PMID: 23934922</mixed-citation><mixed-citation xml:lang="en">Levin J., Högen T., Hillmer A.S., Bader B., Schmidt F., Kamp F. et al.Generation of ferric iron links oxidative stress to α-synuclein oligomer formation. J Parkinsons Dis. 2011;1(2):205–16. https://doi.org/10.3233/JPD-2011-11040. PMID: 23934922</mixed-citation></citation-alternatives></ref><ref id="cit4"><label>4</label><citation-alternatives><mixed-citation xml:lang="ru">Berardelli A., Wenning G.K., Antonini A., Berg D., Bloem B.R., Bonifati V. et al.EFNS/MDS-ES/ENS [corrected] recommendations for the diagnosis of Parkinson’s disease. Eur J Neurol. 2013;20(1):16–34. https://doi.org/10.1111/ene.12022. Erratum in: Eur J Neurol. 2013;20(2):406. PMID: 23279440.</mixed-citation><mixed-citation xml:lang="en">Berardelli A., Wenning G.K., Antonini A., Berg D., Bloem B.R., Bonifati V. et al.EFNS/MDS-ES/ENS [corrected] recommendations for the diagnosis of Parkinson’s disease. Eur J Neurol. 2013;20(1):16–34. https://doi.org/10.1111/ene.12022. Erratum in: Eur J Neurol. 2013;20(2):406. PMID: 23279440.</mixed-citation></citation-alternatives></ref><ref id="cit5"><label>5</label><citation-alternatives><mixed-citation xml:lang="ru">Monaco D., Berg D., Thomas A., Di Stefano V., Barbone F., Vitale M. et al.The predictive power of transcranial sonography in movement disorders: a longitudinal cohort study. Neurol Sci. 2018;39(11):1887–1894. https://doi.org/10.1007/s10072-018-3514-z. Epub 2018 Aug 7. PMID: 30088164.</mixed-citation><mixed-citation xml:lang="en">Monaco D., Berg D., Thomas A., Di Stefano V., Barbone F., Vitale M. et al.The predictive power of transcranial sonography in movement disorders: a longitudinal cohort study. Neurol Sci. 2018;39(11):1887–1894. https://doi.org/10.1007/s10072-018-3514-z. Epub 2018 Aug 7. PMID: 30088164.</mixed-citation></citation-alternatives></ref><ref id="cit6"><label>6</label><citation-alternatives><mixed-citation xml:lang="ru">Berg D., Grote C., Rausch W.D., Mäurer M., Wesemann W., Riederer P., Becker G. Iron accumulation in the substantia nigra in rats visualized by ultrasound. Ultrasound Med Biol. 1999;25(6):901–4. https://doi.org/10.1016/s0301-5629(99)00046-0. PMID: 10461717.</mixed-citation><mixed-citation xml:lang="en">Berg D., Grote C., Rausch W.D., Mäurer M., Wesemann W., Riederer P., Becker G. Iron accumulation in the substantia nigra in rats visualized by ultrasound. Ultrasound Med Biol. 1999;25(6):901–4. https://doi.org/10.1016/s0301-5629(99)00046-0. PMID: 10461717.</mixed-citation></citation-alternatives></ref><ref id="cit7"><label>7</label><citation-alternatives><mixed-citation xml:lang="ru">Berg D., Roggendorf W., Schröder U., Klein R., Tatschner T., Benz P. et al. Echogenicity of the substantia nigra: association with increased iron content and marker for susceptibility to nigrostriatal injury. Arch Neurol. 2002;59(6):999–1005. https://doi.org/10.1001/archneur.59.6.999. PMID: 12056937.</mixed-citation><mixed-citation xml:lang="en">Berg D., Roggendorf W., Schröder U., Klein R., Tatschner T., Benz P. et al. Echogenicity of the substantia nigra: association with increased iron content and marker for susceptibility to nigrostriatal injury. Arch Neurol. 2002;59(6):999–1005. https://doi.org/10.1001/archneur.59.6.999. PMID: 12056937.</mixed-citation></citation-alternatives></ref><ref id="cit8"><label>8</label><citation-alternatives><mixed-citation xml:lang="ru">Zecca L., Berg D., Arzberger T., Ruprecht P., Rausch W.D., Musicco M. et al. In vivo detection of iron and neuromelanin by transcranial sonography: a new approach for early detection of substantia nigra damage. Mov Disord. 2005;20(10):1278–85. https://doi.org/10.1002/mds.20550. PMID: 15986424.</mixed-citation><mixed-citation xml:lang="en">Zecca L., Berg D., Arzberger T., Ruprecht P., Rausch W.D., Musicco M. et al. In vivo detection of iron and neuromelanin by transcranial sonography: a new approach for early detection of substantia nigra damage. Mov Disord. 2005;20(10):1278–85. https://doi.org/10.1002/mds.20550. PMID: 15986424.</mixed-citation></citation-alternatives></ref><ref id="cit9"><label>9</label><citation-alternatives><mixed-citation xml:lang="ru">Friedman A., Arosio P., Finazzi D., Koziorowski D., GalazkaFriedman J. Ferritin as an important player in neurodegeneration. Parkinsonism Relat Disord. 2011;17(6):423–30. https://doi.org/10.1016/j.parkreldis.2011.03.016. Epub 2011 May 7. PMID: 21550835.</mixed-citation><mixed-citation xml:lang="en">Friedman A., Arosio P., Finazzi D., Koziorowski D., GalazkaFriedman J. Ferritin as an important player in neurodegeneration. Parkinsonism Relat Disord. 2011;17(6):423–30. https://doi.org/10.1016/j.parkreldis.2011.03.016. Epub 2011 May 7. PMID: 21550835.</mixed-citation></citation-alternatives></ref><ref id="cit10"><label>10</label><citation-alternatives><mixed-citation xml:lang="ru">Berg D., Godau J., Riederer P., Gerlach M., Arzberger T. Microglia activation is related to substantia nigra echogenicity. J Neural Transm (Vienna). 2010;117(11):1287–92. https://doi.org/10.1007/s00702-010-0504-6. Epub 2010 Nov 6. PMID: 21057966.</mixed-citation><mixed-citation xml:lang="en">Berg D., Godau J., Riederer P., Gerlach M., Arzberger T. Microglia activation is related to substantia nigra echogenicity. J Neural Transm (Vienna). 2010;117(11):1287–92. https://doi.org/10.1007/s00702-010-0504-6. Epub 2010 Nov 6. PMID: 21057966.</mixed-citation></citation-alternatives></ref><ref id="cit11"><label>11</label><citation-alternatives><mixed-citation xml:lang="ru">Mei Y.L., Yang J., Wu Z.R., Yang Y., Xu Y.M. Transcranial Sonography of the Substantia Nigra for the Diff erential Diagnosis of Parkinson’s Disease and Other Movement Disorders: A Meta-Analysis. Parkinsons Dis. 2021;2021:8891874. https://doi.org/10.1155/2021/8891874. PMID: 34007439; PMCID: PMC8110416.</mixed-citation><mixed-citation xml:lang="en">Mei Y.L., Yang J., Wu Z.R., Yang Y., Xu Y.M. Transcranial Sonography of the Substantia Nigra for the Diff erential Diagnosis of Parkinson’s Disease and Other Movement Disorders: A Meta-Analysis. Parkinsons Dis. 2021;2021:8891874. https://doi.org/10.1155/2021/8891874. PMID: 34007439; PMCID: PMC8110416.</mixed-citation></citation-alternatives></ref><ref id="cit12"><label>12</label><citation-alternatives><mixed-citation xml:lang="ru">Pavese N. Is neuromelanin the imaging biomarker for the early diagnosis of Parkinson’s disease that we were looking for? Parkinsonism Relat Disord. 2019;58:1–2. https://doi.org/10.1016/j.parkreldis.2018.12.013. Epub 2018 Dec 13. PMID: 30578009.</mixed-citation><mixed-citation xml:lang="en">Pavese N. Is neuromelanin the imaging biomarker for the early diagnosis of Parkinson’s disease that we were looking for? Parkinsonism Relat Disord. 2019;58:1–2. https://doi.org/10.1016/j.parkreldis.2018.12.013. Epub 2018 Dec 13. PMID: 30578009.</mixed-citation></citation-alternatives></ref><ref id="cit13"><label>13</label><citation-alternatives><mixed-citation xml:lang="ru">Zucca F.A., Vanna R., Cupaioli F.A., Bellei C., De Palma A., Di Silvestre D. et al. Neuromelanin organelles are specialized autolysosomes that accumulate undegraded proteins and lipids in aging human brain and are likely involved in Parkinson’s disease. NPJ Parkinsons Dis. 2018;4:17. https://doi.org/10.1038/s41531-018-0050-8. PMID: 29900402; PMCID: PMC5988730.</mixed-citation><mixed-citation xml:lang="en">Zucca F.A., Vanna R., Cupaioli F.A., Bellei C., De Palma A., Di Silvestre D. et al. Neuromelanin organelles are specialized autolysosomes that accumulate undegraded proteins and lipids in aging human brain and are likely involved in Parkinson’s disease. NPJ Parkinsons Dis. 2018;4:17. https://doi.org/10.1038/s41531-018-0050-8. PMID: 29900402; PMCID: PMC5988730.</mixed-citation></citation-alternatives></ref><ref id="cit14"><label>14</label><citation-alternatives><mixed-citation xml:lang="ru">Zecca L., Fariello R., Riederer P., Sulzer D., Gatti A., Tampellini D. The absolute concentration of nigral neuromelanin, assayed by a new sensitive method, increases throughout the life and is dramatically decreased in Parkinson’s disease. FEBS Lett. 2002;510(3):216–20. https://doi.org/10.1016/s0014-5793(01)03269-0. PMID: 11801257.</mixed-citation><mixed-citation xml:lang="en">Zecca L., Fariello R., Riederer P., Sulzer D., Gatti A., Tampellini D. The absolute concentration of nigral neuromelanin, assayed by a new sensitive method, increases throughout the life and is dramatically decreased in Parkinson’s disease. FEBS Lett. 2002;510(3):216–20. https://doi.org/10.1016/s0014-5793(01)03269-0. PMID: 11801257.</mixed-citation></citation-alternatives></ref><ref id="cit15"><label>15</label><citation-alternatives><mixed-citation xml:lang="ru">Sasaki M., Shibata E., Tohyama K., Takahashi J., Otsuka K., Tsuchiya K. et al. Neuromelanin magnetic resonance imaging of locus ceruleus and substantia nigra in Parkinson’s disease. Neuroreport. 2006;17(11):1215–8. https://doi.org/10.1097/01.wnr.0000227984.84927.a7. PMID: 16837857.</mixed-citation><mixed-citation xml:lang="en">Sasaki M., Shibata E., Tohyama K., Takahashi J., Otsuka K., Tsuchiya K. et al. Neuromelanin magnetic resonance imaging of locus ceruleus and substantia nigra in Parkinson’s disease. Neuroreport. 2006;17(11):1215–8. https://doi.org/10.1097/01.wnr.0000227984.84927.a7. PMID: 16837857.</mixed-citation></citation-alternatives></ref><ref id="cit16"><label>16</label><citation-alternatives><mixed-citation xml:lang="ru">Kitao S., Matsusue E., Fujii S., Miyoshi F., Kaminou T., Kato S. et al. Correlation between pathology and neuromelanin MR imaging in Parkinson’s disease and dementia with Lewy bodies. Neuroradiology. 2013;55(8):947–953. https://doi.org/10.1007/s00234-013-1199-9. Epub 2013 May 15. Erratum in: Neuroradiology. 2017 Jun;59(6):637-638. PMID: 23673875.</mixed-citation><mixed-citation xml:lang="en">Kitao S., Matsusue E., Fujii S., Miyoshi F., Kaminou T., Kato S. et al. Correlation between pathology and neuromelanin MR imaging in Parkinson’s disease and dementia with Lewy bodies. Neuroradiology. 2013;55(8):947–953. https://doi.org/10.1007/s00234-013-1199-9. Epub 2013 May 15. Erratum in: Neuroradiology. 2017 Jun;59(6):637-638. PMID: 23673875.</mixed-citation></citation-alternatives></ref><ref id="cit17"><label>17</label><citation-alternatives><mixed-citation xml:lang="ru">Cho S.J., Bae Y.J., Kim J.M., Kim D., Baik S.H., Sunwoo L. et al. Diagnostic performance of neuromelanin-sensitive magnetic resonance imaging for patients with Parkinson’s disease and factor analysis for its heterogeneity: a systematic review and meta-analysis. Eur Radiol. 2021;31(3):1268–1280. https://doi.org/10.1007/s00330-020-07240-7. Epub 2020 Sep 4. PMID: 32886201.</mixed-citation><mixed-citation xml:lang="en">Cho S.J., Bae Y.J., Kim J.M., Kim D., Baik S.H., Sunwoo L. et al. Diagnostic performance of neuromelanin-sensitive magnetic resonance imaging for patients with Parkinson’s disease and factor analysis for its heterogeneity: a systematic review and meta-analysis. Eur Radiol. 2021;31(3):1268–1280. https://doi.org/10.1007/s00330-020-07240-7. Epub 2020 Sep 4. PMID: 32886201.</mixed-citation></citation-alternatives></ref><ref id="cit18"><label>18</label><citation-alternatives><mixed-citation xml:lang="ru">Postuma R.B., Berg D., Stern M., Poewe W., Olanow C.W., Oertel W. et al. MDS clinical diagnostic criteria for Parkinson’s disease. Mov Disord. 2015;30(12):1591–601. https://doi.org/10.1002/mds.26424. PMID: 26474316.</mixed-citation><mixed-citation xml:lang="en">Postuma R.B., Berg D., Stern M., Poewe W., Olanow C.W., Oertel W. et al. MDS clinical diagnostic criteria for Parkinson’s disease. Mov Disord. 2015;30(12):1591–601. https://doi.org/10.1002/mds.26424. PMID: 26474316.</mixed-citation></citation-alternatives></ref><ref id="cit19"><label>19</label><citation-alternatives><mixed-citation xml:lang="ru">Федотова Е.Ю., Чечеткин А.О., Шадрина М.И., Сломинский П.А., Иванова-Смоленская И.А., Иллариошкин С.Н. Транскраниальная сонография при болезни Паркинсона. Журнал неврологии и психиатрии им. С.С. Корсакова. 2011;1:49–55.</mixed-citation><mixed-citation xml:lang="en">Fedotova E.Yu., Chechetkin A.O., Shadrina M.I., Slominsky P.A., Ivanova-Smolenskaya I.A., Illarioshkin S.N. Transcranial sonography in Parkinson’s disease. Zh Nevrol Psikhiatr Im SS Korsakova. 2011;1:49–55.(In Russ.).</mixed-citation></citation-alternatives></ref><ref id="cit20"><label>20</label><citation-alternatives><mixed-citation xml:lang="ru">Matsuura K., Maeda M., Tabei K.I., Umino M., Kajikawa H., Satoh M. et al. A longitudinal study of neuromelanin-sensitive magnetic resonance imaging in Parkinson’s disease. Neurosci Lett. 2016;633:112–117. https://doi.org/10.1016/j.neulet.2016.09.011. Epub 2016 Sep 9. PMID: 27619539.</mixed-citation><mixed-citation xml:lang="en">Matsuura K., Maeda M., Tabei K.I., Umino M., Kajikawa H., Satoh M. et al. A longitudinal study of neuromelanin-sensitive magnetic resonance imaging in Parkinson’s disease. Neurosci Lett. 2016;633:112–117. https://doi.org/10.1016/j.neulet.2016.09.011. Epub 2016 Sep 9. PMID: 27619539.</mixed-citation></citation-alternatives></ref><ref id="cit21"><label>21</label><citation-alternatives><mixed-citation xml:lang="ru">Jesus-Ribeiro J., Sargento-Freitas J., Sousa M., Silva F., Freire A., Januário C. Substantia nigra hyperechogenicity does not correlate with motor features in Parkinson’s disease. J Neurol Sci. 2016;364:9–11. https://doi.org/10.1016/j.jns.2016.03.002. Epub 2016 Mar 2. PMID: 27084206.</mixed-citation><mixed-citation xml:lang="en">Jesus-Ribeiro J., Sargento-Freitas J., Sousa M., Silva F., Freire A., Januário C. Substantia nigra hyperechogenicity does not correlate with motor features in Parkinson’s disease. J Neurol Sci. 2016;364:9–11. https://doi.org/10.1016/j.jns.2016.03.002. Epub 2016 Mar 2. PMID: 27084206.</mixed-citation></citation-alternatives></ref><ref id="cit22"><label>22</label><citation-alternatives><mixed-citation xml:lang="ru">Lobsien E., Schreiner S., Plotkin M., Kupsch A., Schreiber S.J., Doepp F. No correlation of substantia nigra echogenicity and nigrostriatal degradation in Parkinson’s disease. Mov Disord. 2012;27(3):450–3. https://doi.org/10.1002/mds.24070. Epub 2012 Jan 11. PMID: 22237792.</mixed-citation><mixed-citation xml:lang="en">Lobsien E., Schreiner S., Plotkin M., Kupsch A., Schreiber S.J., Doepp F. No correlation of substantia nigra echogenicity and nigrostriatal degradation in Parkinson’s disease. Mov Disord. 2012;27(3):450–3. https://doi.org/10.1002/mds.24070. Epub 2012 Jan 11. PMID: 22237792.</mixed-citation></citation-alternatives></ref><ref id="cit23"><label>23</label><citation-alternatives><mixed-citation xml:lang="ru">Berg D., Merz B., Reiners K., Naumann M., Becker G. Five-year follow-up study of hyperechogenicity of the substantia nigra in Parkinson’s disease. Mov Disord. 2005;20(3):383–5. https://doi.org/10.1002/mds.20311. PMID: 15486999.</mixed-citation><mixed-citation xml:lang="en">Berg D., Merz B., Reiners K., Naumann M., Becker G. Five-year follow-up study of hyperechogenicity of the substantia nigra in Parkinson’s disease. Mov Disord. 2005;20(3):383–5. https://doi.org/10.1002/mds.20311. PMID: 15486999.</mixed-citation></citation-alternatives></ref><ref id="cit24"><label>24</label><citation-alternatives><mixed-citation xml:lang="ru">Berg D., Behnke S., Walter U. Application of transcranial sonography in extrapyramidal disorders: updated recommendations. Ultraschall Med. 2006;27(1):12–9. https://doi.org/10.1055/s-2005-858962. PMID: 16470475.</mixed-citation><mixed-citation xml:lang="en">Berg D., Behnke S., Walter U. Application of transcranial sonography in extrapyramidal disorders: updated recommendations. Ultraschall Med. 2006;27(1):12–9. https://doi.org/10.1055/s-2005-858962. PMID: 16470475.</mixed-citation></citation-alternatives></ref><ref id="cit25"><label>25</label><citation-alternatives><mixed-citation xml:lang="ru">Biondetti E., Gaurav R., Yahia-Cherif L., Mangone G., Pyatigorskaya N., Valabrègue R. et al. Spatiotemporal changes in substantia nigra neuromelanin content in Parkinson’s disease. Brain. 2020;143(9):2757–2770. https://doi.org/10.1093/brain/awaa216. Erratum in: Brain. 2021;144(2):e24. PMID: 32856056.</mixed-citation><mixed-citation xml:lang="en">Biondetti E., Gaurav R., Yahia-Cherif L., Mangone G., Pyatigorskaya N., Valabrègue R. et al. Spatiotemporal changes in substantia nigra neuromelanin content in Parkinson’s disease. Brain. 2020;143(9):2757–2770. https://doi.org/10.1093/brain/awaa216. Erratum in: Brain. 2021;144(2):e24. PMID: 32856056.</mixed-citation></citation-alternatives></ref><ref id="cit26"><label>26</label><citation-alternatives><mixed-citation xml:lang="ru">Gaurav R., Yahia-Cherif L., Pyatigorskaya N., Mangone G., Biondetti E., Valabrègue R. et al. Longitudinal Changes in Neuromelanin MRI Signal in Parkinson’s Disease: A Progression Marker. Mov Disord. 2021;36(7):1592–1602. https://doi.org/10.1002/mds.28531. Epub 2021 Mar 10. PMID: 33751655; PMCID: PMC8359265.</mixed-citation><mixed-citation xml:lang="en">Gaurav R., Yahia-Cherif L., Pyatigorskaya N., Mangone G., Biondetti E., Valabrègue R. et al. Longitudinal Changes in Neuromelanin MRI Signal in Parkinson’s Disease: A Progression Marker. Mov Disord. 2021;36(7):1592–1602. https://doi.org/10.1002/mds.28531. Epub 2021 Mar 10. PMID: 33751655; PMCID: PMC8359265.</mixed-citation></citation-alternatives></ref><ref id="cit27"><label>27</label><citation-alternatives><mixed-citation xml:lang="ru">Prasuhn J., Strautz R., Lemmer F., Dreischmeier S., Kasten M., Hanssen H. et al. Neuroimaging Correlates of Substantia Nigra Hyperechogenicity in Parkinson’s Disease. J Parkinsons Dis. 2022;Feb 16. https://doi.org/10.3233/JPD-213000. Epub ahead of print. PMID: 35180131.</mixed-citation><mixed-citation xml:lang="en">Prasuhn J., Strautz R., Lemmer F., Dreischmeier S., Kasten M., Hanssen H. et al. Neuroimaging Correlates of Substantia Nigra Hyperechogenicity in Parkinson’s Disease. J Parkinsons Dis. 2022;Feb 16. https://doi.org/10.3233/JPD-213000. Epub ahead of print. PMID: 35180131.</mixed-citation></citation-alternatives></ref></ref-list><fn-group><fn fn-type="conflict"><p>The authors declare that there are no conflicts of interest present.</p></fn></fn-group></back></article>
