Skip to main content
Top
Published in: Neurological Sciences 3/2020

Open Access 01-03-2020 | Parkinson's Disease | Original Article

Increased substantia nigra echogenicity correlated with visual hallucinations in Parkinson’s disease: a Chinese population-based study

Authors: Ting Li, Jing Shi, Bin Qin, Dongsheng Fan, Na Liu, Jingnian Ni, Tianqing Zhang, Hufang Zhou, Xiaoqing Xu, Mingqing Wei, Xuekai Zhang, Xiangzhu Wang, Jianping Liu, Yongyan Wang, Jinzhou Tian

Published in: Neurological Sciences | Issue 3/2020

Login to get access

Abstract

As a noninvasive technique, transcranial sonography (TCS) of substantia nigra (SN) has gradually showed its effectiveness not only in diagnosis but also in understanding clinical features of Parkinson’s Disease (PD). This study aimed to further evaluate TCS for clinical diagnosis of PD, and to explore the association between sonographic manifestations and visual hallucinations (VH). A total of 226 subjects including 141 PD patients and 85 controls were recruited. All participants received TCS. A series of rating scales to evaluate motor and non-motor symptoms were performed in PD patients. Results showed that 172 subjects were successfully assessed by TCS. The area of SN was greater in PD patients than that in controls (P < 0.001). As receiver-operating characteristic (ROC) curve analysis showed, the best cutoff value for the larger SN echogenicity size was 23.5 mm2 (sensitivity 70.3%, specificity 77.0%). Patients with VH had larger SN area (P = 0.019), as well as higher Non-Motor Symptoms Scale (NMSS) scores (P = 0.018). Moreover, binary logistic regression analysis indicated that SN hyperechogenicity (odds ratio = 4.227, P = 0.012) and NMSS scores (odds ratio = 0.027, P = 0.042) could be the independent predictors for VH. In conclusion, TCS can be used as an auxiliary diagnostic tool for Parkinson’s disease. Increased SN echogenicity is correlated with VH in Parkinson’s disease, possibly because the brain stem is involved in the mechanism in the onset of VH. Further studies are needed to confirm these findings.
Literature
1.
go back to reference Stoessl AJ (2012) Neuroimaging in the early diagnosis of neurodegenerative disease. Transl neurodegener 1:5CrossRef Stoessl AJ (2012) Neuroimaging in the early diagnosis of neurodegenerative disease. Transl neurodegener 1:5CrossRef
2.
go back to reference Lees AJ, Hardy J, Revesz T (2009), Parkinson’s disease. Lancet (London, England) 373:2055-2066. Lees AJ, Hardy J, Revesz T (2009), Parkinson’s disease. Lancet (London, England) 373:2055-2066.
3.
go back to reference Stenc Bradvica I, Mihaljevic I, Butkovic-Soldo S, Kadojic D, Titlic M, Bradvica M, Kralik K (2015) Transcranial sonography and the pocket smell test in the differential diagnosis between Parkinson’s disease and essential tremor. Neurol Sci 36:1403–1410 Stenc Bradvica I, Mihaljevic I, Butkovic-Soldo S, Kadojic D, Titlic M, Bradvica M, Kralik K (2015) Transcranial sonography and the pocket smell test in the differential diagnosis between Parkinson’s disease and essential tremor. Neurol Sci 36:1403–1410
4.
go back to reference Tao A, Chen G, Deng Y, Xu R (2019) Accuracy of transcranial sonography of the substantia nigra for detection of Parkinson’s disease: a systematic review and meta-analysis. Ultrasound Med Biol 45:628–641CrossRef Tao A, Chen G, Deng Y, Xu R (2019) Accuracy of transcranial sonography of the substantia nigra for detection of Parkinson’s disease: a systematic review and meta-analysis. Ultrasound Med Biol 45:628–641CrossRef
5.
go back to reference Monaco D, Berg D, Thomas A, Di Stefano V, Barbone F, Vitale M, Ferrante C, Bonanni L et al (2018) The predictive power of transcranial sonography in movement disorders: a longitudinal cohort study. Neurol Sci 39:1887–1894 Monaco D, Berg D, Thomas A, Di Stefano V, Barbone F, Vitale M, Ferrante C, Bonanni L et al (2018) The predictive power of transcranial sonography in movement disorders: a longitudinal cohort study. Neurol Sci 39:1887–1894
6.
go back to reference Yu SY, Cao CJ, Zuo LJ, Chen ZJ, Lian TH, Wang F, Hu Y, Piao YS et al (2018) Clinical features and dysfunctions of iron metabolism in Parkinson disease patients with hyper echogenicity in substantia nigra: a cross-sectional study. BMC Neurol 18:9CrossRef Yu SY, Cao CJ, Zuo LJ, Chen ZJ, Lian TH, Wang F, Hu Y, Piao YS et al (2018) Clinical features and dysfunctions of iron metabolism in Parkinson disease patients with hyper echogenicity in substantia nigra: a cross-sectional study. BMC Neurol 18:9CrossRef
7.
go back to reference Bartova P, Skoloudik D, Ressner P, Langova K, Herzig R, Kanovsky P (2010) Correlation between substantia nigra features detected by sonography and Parkinson disease symptoms. J Ultras Med 29:37–42 Bartova P, Skoloudik D, Ressner P, Langova K, Herzig R, Kanovsky P (2010) Correlation between substantia nigra features detected by sonography and Parkinson disease symptoms. J Ultras Med 29:37–42
8.
go back to reference Zhou HY, Sun Q, Tan YY, Hu YY, Zhan WW, Li DH, Wang Y, Xiao Q, Liu J, Chen SD (2016) Substantia nigra echogenicity correlated with clinical features of Parkinson’s disease. Parkinsonism Relat Disord 24:28–33CrossRef Zhou HY, Sun Q, Tan YY, Hu YY, Zhan WW, Li DH, Wang Y, Xiao Q, Liu J, Chen SD (2016) Substantia nigra echogenicity correlated with clinical features of Parkinson’s disease. Parkinsonism Relat Disord 24:28–33CrossRef
9.
go back to reference Aarsland D, Larsen JP, Cummins JL, Laake K (1999) Prevalence and clinical correlates of psychotic symptoms in Parkinson disease: a community-based study. Arch Neurol 56:595–601CrossRef Aarsland D, Larsen JP, Cummins JL, Laake K (1999) Prevalence and clinical correlates of psychotic symptoms in Parkinson disease: a community-based study. Arch Neurol 56:595–601CrossRef
10.
go back to reference Goetz CG, Stebbins GT, Ouyang B (2011) Visual plus nonvisual hallucinations in Parkinson’s disease: development and evolution over 10 years. Mov Disord 26:2196–2200 Goetz CG, Stebbins GT, Ouyang B (2011) Visual plus nonvisual hallucinations in Parkinson’s disease: development and evolution over 10 years. Mov Disord 26:2196–2200
11.
go back to reference Gibson G, Mottram PG, Burn DJ, Hindle JV, Landau S, Samuel M, Hurt CS, Brown RG, M Wilson KC (2013) Frequency, prevalence, incidence and risk factors associated with visual hallucinations in a sample of patients with Parkinson’s disease: a longitudinal 4-year study. Int J Geriatr Psych 28:626–631 Gibson G, Mottram PG, Burn DJ, Hindle JV, Landau S, Samuel M, Hurt CS, Brown RG, M Wilson KC (2013) Frequency, prevalence, incidence and risk factors associated with visual hallucinations in a sample of patients with Parkinson’s disease: a longitudinal 4-year study. Int J Geriatr Psych 28:626–631
12.
go back to reference McKeith IG, Dickson DW, Lowe J, Emre M, O'Brien JT, Feldman H, Cummings J, Duda JE, Lippa C, Perry EK, Aarsland D, Arai H, Ballard CG, Boeve B, Burn DJ, Costa D, del Ser T, Dubois B, Galasko D, Gauthier S, Goetz CG, Gomez-Tortosa E, Halliday G, Hansen LA, Hardy J, Iwatsubo T, Kalaria RN, Kaufer D, Kenny RA, Korczyn A, Kosaka K, Lee VM, Lees A, Litvan I, Londos E, Lopez OL, Minoshima S, Mizuno Y, Molina JA, Mukaetova-Ladinska EB, Pasquier F, Perry RH, Schulz JB, Trojanowski JQ, Yamada M, Consortium on DLB (2005) Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium. Neurology 65:1863–1872CrossRef McKeith IG, Dickson DW, Lowe J, Emre M, O'Brien JT, Feldman H, Cummings J, Duda JE, Lippa C, Perry EK, Aarsland D, Arai H, Ballard CG, Boeve B, Burn DJ, Costa D, del Ser T, Dubois B, Galasko D, Gauthier S, Goetz CG, Gomez-Tortosa E, Halliday G, Hansen LA, Hardy J, Iwatsubo T, Kalaria RN, Kaufer D, Kenny RA, Korczyn A, Kosaka K, Lee VM, Lees A, Litvan I, Londos E, Lopez OL, Minoshima S, Mizuno Y, Molina JA, Mukaetova-Ladinska EB, Pasquier F, Perry RH, Schulz JB, Trojanowski JQ, Yamada M, Consortium on DLB (2005) Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium. Neurology 65:1863–1872CrossRef
13.
go back to reference Fahn S, Elton RL (1987) Unified Parkinson’s disease rating scale. In: vol., pp. 153-163,293-304. Recent Developments in Parkinsons Disease, Vol 2 Florham Park, NJ: Macmillan Healthcare Information. Fahn S, Elton RL (1987) Unified Parkinson’s disease rating scale. In: vol., pp. 153-163,293-304. Recent Developments in Parkinsons Disease, Vol 2 Florham Park, NJ: Macmillan Healthcare Information.
14.
go back to reference Martinez-Martin P, Rodriguez-Blazquez C, Abe K, Bhattacharyya KB, Bloem BR, Carod-Artal FJ, Prakash R, Esselink RA, Falup-Pecurariu C, Gallardo M, Mir P, Naidu Y, Nicoletti A, Sethi K, Tsuboi Y, van Hilten J, Visser M, Zappia M, Chaudhuri KR (2009) International study on the psychometric attributes of the non-motor symptoms scale in Parkinson disease. Neurology 73:1584–1591CrossRef Martinez-Martin P, Rodriguez-Blazquez C, Abe K, Bhattacharyya KB, Bloem BR, Carod-Artal FJ, Prakash R, Esselink RA, Falup-Pecurariu C, Gallardo M, Mir P, Naidu Y, Nicoletti A, Sethi K, Tsuboi Y, van Hilten J, Visser M, Zappia M, Chaudhuri KR (2009) International study on the psychometric attributes of the non-motor symptoms scale in Parkinson disease. Neurology 73:1584–1591CrossRef
15.
go back to reference Chaudhuri KR, Pal S, DiMarco A, Whately-Smith C, Bridgman K, Mathew R, Pezzela FR, Forbes A et al (2002) The Parkinson’s disease sleep scale: a new instrument for assessing sleep and nocturnal disability in Parkinson’s disease. J Neurol Neurosurg Psychiatry 73:629–635CrossRef Chaudhuri KR, Pal S, DiMarco A, Whately-Smith C, Bridgman K, Mathew R, Pezzela FR, Forbes A et al (2002) The Parkinson’s disease sleep scale: a new instrument for assessing sleep and nocturnal disability in Parkinson’s disease. J Neurol Neurosurg Psychiatry 73:629–635CrossRef
16.
go back to reference Varma MG, Wang JY, Berian JR, Patterson TR, McCrea GL, Hart SL (2008) The constipation severity instrument: a validated measure. Dis Colon Rectum 51:162–172CrossRef Varma MG, Wang JY, Berian JR, Patterson TR, McCrea GL, Hart SL (2008) The constipation severity instrument: a validated measure. Dis Colon Rectum 51:162–172CrossRef
17.
go back to reference Nilsson MH, Bladh S, Hagell P (2013) Fatigue in Parkinson’s disease: measurement properties of a generic and a condition-specific rating scale. J Pain Symptom Manag 46:737–746CrossRef Nilsson MH, Bladh S, Hagell P (2013) Fatigue in Parkinson’s disease: measurement properties of a generic and a condition-specific rating scale. J Pain Symptom Manag 46:737–746CrossRef
18.
go back to reference Folstein MF, Folstein SE, McHugh PR (1975) Mini-mental state. A practical method for grading the cognitive state of patients for the clinician J Psychiatr Res 12:189–198 Folstein MF, Folstein SE, McHugh PR (1975) Mini-mental state. A practical method for grading the cognitive state of patients for the clinician J Psychiatr Res 12:189–198
19.
go back to reference Hamilton M (1960) A rating scale for depression. J Neurol Neurosurg Psychiatry 23:56–62CrossRef Hamilton M (1960) A rating scale for depression. J Neurol Neurosurg Psychiatry 23:56–62CrossRef
20.
go back to reference Hamilton M (1959) The assessment of anxiety states by rating. Br J Med Psychol 32:50–55 Hamilton M (1959) The assessment of anxiety states by rating. Br J Med Psychol 32:50–55
21.
go back to reference Peto V, Jenkinson C, Fitzpatrick R, Greenhall R (1995) The development and validation of a short measure of functioning and well being for individuals with Parkinson’s disease. Qual Life Res Int J Qual Life Asp Treat Care Rehab 4:241–248 Peto V, Jenkinson C, Fitzpatrick R, Greenhall R (1995) The development and validation of a short measure of functioning and well being for individuals with Parkinson’s disease. Qual Life Res Int J Qual Life Asp Treat Care Rehab 4:241–248
22.
go back to reference Emre M, Aarsland D, Brown R, Burn DJ, Duyckaerts C, Mizuno Y, Broe GA, Cummings J et al (2007) Clinical diagnostic criteria for dementia associated with Parkinson’s disease. Mov Disord 22:1689–1707 quiz 1837 Emre M, Aarsland D, Brown R, Burn DJ, Duyckaerts C, Mizuno Y, Broe GA, Cummings J et al (2007) Clinical diagnostic criteria for dementia associated with Parkinson’s disease. Mov Disord 22:1689–1707 quiz 1837
23.
go back to reference Wan Y, Wang G, Zeng J, Laake K (2009) Investigation on prevalence and risk factors of visual hallucination in patients with Parkinson’s disease. J Shanghai Jiaotong Univ 29:862–865 Wan Y, Wang G, Zeng J, Laake K (2009) Investigation on prevalence and risk factors of visual hallucination in patients with Parkinson’s disease. J Shanghai Jiaotong Univ 29:862–865
24.
go back to reference Meppelink AM, de Jong BM, Renken R, Leenders KL, Cornelissen FW, van Laar T (2009), Impaired visual processing preceding image recognition in Parkinson’s disease patients with visual hallucinations. Brain: a journal of neurology 132:2980-2993. Meppelink AM, de Jong BM, Renken R, Leenders KL, Cornelissen FW, van Laar T (2009), Impaired visual processing preceding image recognition in Parkinson’s disease patients with visual hallucinations. Brain: a journal of neurology 132:2980-2993.
25.
go back to reference Ibarretxe-Bilbao N, Ramirez-Ruiz B, Junque C, Marti MJ, Valldeoriola F, Bargallo N, Juanes S, Tolosa E (2010) Differential progression of brain atrophy in Parkinson’s disease with and without visual hallucinations. J Neurol Neurosurg Psychiatry 81:650–657CrossRef Ibarretxe-Bilbao N, Ramirez-Ruiz B, Junque C, Marti MJ, Valldeoriola F, Bargallo N, Juanes S, Tolosa E (2010) Differential progression of brain atrophy in Parkinson’s disease with and without visual hallucinations. J Neurol Neurosurg Psychiatry 81:650–657CrossRef
26.
go back to reference Lenka A, Jhunjhunwala KR, Saini J, Pal PK (2015) Structural and functional neuroimaging in patients with Parkinson’s disease and visual hallucinations: a critical review. Parkinsonism Relat Disord 21:683–691CrossRef Lenka A, Jhunjhunwala KR, Saini J, Pal PK (2015) Structural and functional neuroimaging in patients with Parkinson’s disease and visual hallucinations: a critical review. Parkinsonism Relat Disord 21:683–691CrossRef
27.
go back to reference Ward RJ, Zucca FA, Duyn JH, Crichton RR, Zecca L (2014) The role of iron in brain ageing and neurodegenerative disorders. The Lancet Neurology 13:1045–1060CrossRef Ward RJ, Zucca FA, Duyn JH, Crichton RR, Zecca L (2014) The role of iron in brain ageing and neurodegenerative disorders. The Lancet Neurology 13:1045–1060CrossRef
28.
go back to reference Berg D, Grote C, Rausch WD, Maurer M, Wesemann W, Riederer P, Becker G (1999) Iron accumulation in the substantia nigra in rats visualized by ultrasound. Ultrasound Med Biol 25:901–904CrossRef Berg D, Grote C, Rausch WD, Maurer M, Wesemann W, Riederer P, Becker G (1999) Iron accumulation in the substantia nigra in rats visualized by ultrasound. Ultrasound Med Biol 25:901–904CrossRef
29.
go back to reference Berg D, Roggendorf W, Schroder U, Klein R, Tatschner T, Benz P, Tucha O, Preier M et al (2002) Echogenicity of the substantia nigra: association with increased iron content and marker for susceptibility to nigrostriatal injury. Arch Neurol 59:999–1005CrossRef Berg D, Roggendorf W, Schroder U, Klein R, Tatschner T, Benz P, Tucha O, Preier M et al (2002) Echogenicity of the substantia nigra: association with increased iron content and marker for susceptibility to nigrostriatal injury. Arch Neurol 59:999–1005CrossRef
30.
go back to reference Tuite PJ, Provias JP, Lang AE (1996) Atypical dopa responsive parkinsonism in a patient with megalencephaly, midbrain Lewy body disease, and some pathological features of Hallervorden-Spatz disease. J Neurol Neurosurg Psychiatry 61:523–527CrossRef Tuite PJ, Provias JP, Lang AE (1996) Atypical dopa responsive parkinsonism in a patient with megalencephaly, midbrain Lewy body disease, and some pathological features of Hallervorden-Spatz disease. J Neurol Neurosurg Psychiatry 61:523–527CrossRef
31.
go back to reference Berg D, Godau J, Riederer P, Gerlach M, Arzberger T (2010), Microglia activation is related to substantia nigra echogenicity. Journal of neural transmission (Vienna, Austria : 1996) 117:1287-1292. Berg D, Godau J, Riederer P, Gerlach M, Arzberger T (2010), Microglia activation is related to substantia nigra echogenicity. Journal of neural transmission (Vienna, Austria : 1996) 117:1287-1292.
32.
go back to reference Imamura K, Hishikawa N, Sawada M, Nagatsu T, Yoshida M, Hashizume Y (2003) Distribution of major histocompatibility complex class II-positive microglia and cytokine profile of Parkinson’s disease brains. Acta Neuropathol 106:518–526CrossRef Imamura K, Hishikawa N, Sawada M, Nagatsu T, Yoshida M, Hashizume Y (2003) Distribution of major histocompatibility complex class II-positive microglia and cytokine profile of Parkinson’s disease brains. Acta Neuropathol 106:518–526CrossRef
33.
go back to reference Zhu Y, Wang B, Tao K, Yang H, Wang Y, Zhou T, Yang Y, Yuan L et al (2017) Iron accumulation and microglia activation contribute to substantia nigra hyperechogenicity in the 6-OHDA-induced rat model of Parkinson's disease. Parkinsonism Relat Disord 36:76–82CrossRef Zhu Y, Wang B, Tao K, Yang H, Wang Y, Zhou T, Yang Y, Yuan L et al (2017) Iron accumulation and microglia activation contribute to substantia nigra hyperechogenicity in the 6-OHDA-induced rat model of Parkinson's disease. Parkinsonism Relat Disord 36:76–82CrossRef
34.
go back to reference Sakai K, Ikeda T, Ishida C, Komai K, Yamada M (2019), Delusions and visual hallucinations in a patient with Parkinson’s disease with dementia showing pronounced Lewy body pathology in the nucleus basalis of Meynert. Neuropathology: official journal of the Japanese Society of Neuropathology 39:319-323. Sakai K, Ikeda T, Ishida C, Komai K, Yamada M (2019), Delusions and visual hallucinations in a patient with Parkinson’s disease with dementia showing pronounced Lewy body pathology in the nucleus basalis of Meynert. Neuropathology: official journal of the Japanese Society of Neuropathology 39:319-323.
35.
go back to reference Zhu J, Shen B, Lu L, Lan W, Pan Y, Zhang L, Dong J, Wang M et al (2017) Prevalence and risk factors for visual hallucinations in Chinese patients with Parkinson’s disease. J Neurol Sci 372:471–476CrossRef Zhu J, Shen B, Lu L, Lan W, Pan Y, Zhang L, Dong J, Wang M et al (2017) Prevalence and risk factors for visual hallucinations in Chinese patients with Parkinson’s disease. J Neurol Sci 372:471–476CrossRef
36.
go back to reference Trojano L, Papagno C (2018), Cognitive and behavioral disorders in Parkinson’s disease: an update. II: behavioral disorders. Neurological sciences: official journal of the Italian Neurological Society and of the Italian Society of Clinical Neurophysiology 39:53-61. Trojano L, Papagno C (2018), Cognitive and behavioral disorders in Parkinson’s disease: an update. II: behavioral disorders. Neurological sciences: official journal of the Italian Neurological Society and of the Italian Society of Clinical Neurophysiology 39:53-61.
37.
go back to reference Walter U, Skoloudik D, Berg D (2010) Transcranial sonography findings related to non-motor features of Parkinson’s disease. J Neurol Sci 289:123–127CrossRef Walter U, Skoloudik D, Berg D (2010) Transcranial sonography findings related to non-motor features of Parkinson’s disease. J Neurol Sci 289:123–127CrossRef
38.
go back to reference Berg D, Siefker C, Becker G (2001) Echogenicity of the substantia nigra in Parkinson’s disease and its relation to clinical findings. J Neurol 248:684–689CrossRef Berg D, Siefker C, Becker G (2001) Echogenicity of the substantia nigra in Parkinson’s disease and its relation to clinical findings. J Neurol 248:684–689CrossRef
39.
go back to reference Kim JY, Kim ST, Jeon SH, Lee WY (2007), Midbrain transcranial sonography in Korean patients with Parkinson’s disease. Movement disorders: official journal of the Movement Disorder Society 22:1922-1926. Kim JY, Kim ST, Jeon SH, Lee WY (2007), Midbrain transcranial sonography in Korean patients with Parkinson’s disease. Movement disorders: official journal of the Movement Disorder Society 22:1922-1926.
40.
go back to reference Luo WF, Zhang YC, Sheng YJ, Fang JC, Liu CF (2012), Transcranial sonography on Parkinson’s disease and essential tremor in a Chinese population. Neurological sciences: official journal of the Italian Neurological Society and of the Italian Society of Clinical Neurophysiology 33:1005-1009. Luo WF, Zhang YC, Sheng YJ, Fang JC, Liu CF (2012), Transcranial sonography on Parkinson’s disease and essential tremor in a Chinese population. Neurological sciences: official journal of the Italian Neurological Society and of the Italian Society of Clinical Neurophysiology 33:1005-1009.
41.
go back to reference Hagenah J, Konig IR, Sperner J, Wessel L, Seidel G, Condefer K, Saunders-Pullman R, Klein C et al (2010) Life-long increase of substantia nigra hyperechogenicity in transcranial sonography. NeuroImage 51:28–32CrossRef Hagenah J, Konig IR, Sperner J, Wessel L, Seidel G, Condefer K, Saunders-Pullman R, Klein C et al (2010) Life-long increase of substantia nigra hyperechogenicity in transcranial sonography. NeuroImage 51:28–32CrossRef
42.
go back to reference Bor-Seng-Shu E, Pedroso JL, Felicio AC, de Andrade DC, Teixeira MJ, Braga-Neto P, Batista IR, Barsottini OG, Borges V, Ferraz HB, Shih MC, Bressan RA, de Andrade LA, Walter U (2014) Substantia nigra echogenicity and imaging of striatal dopamine transporters in Parkinson’s disease: a cross-sectional study. Parkinsonism Relat Disord 20:477–481CrossRef Bor-Seng-Shu E, Pedroso JL, Felicio AC, de Andrade DC, Teixeira MJ, Braga-Neto P, Batista IR, Barsottini OG, Borges V, Ferraz HB, Shih MC, Bressan RA, de Andrade LA, Walter U (2014) Substantia nigra echogenicity and imaging of striatal dopamine transporters in Parkinson’s disease: a cross-sectional study. Parkinsonism Relat Disord 20:477–481CrossRef
43.
go back to reference Mahlknecht P, Stockner H, Kiechl S, Willeit J, Rastner V, Gasperi A, Rungger G, Poewe W, et al. (2012), Is transcranial sonography useful to distinguish drug-induced parkinsonism from Parkinson’s disease? Movement disorders: official journal of the Movement Disorder Society 27:1194-1196. Mahlknecht P, Stockner H, Kiechl S, Willeit J, Rastner V, Gasperi A, Rungger G, Poewe W, et al. (2012), Is transcranial sonography useful to distinguish drug-induced parkinsonism from Parkinson’s disease? Movement disorders: official journal of the Movement Disorder Society 27:1194-1196.
44.
go back to reference Hershkovitz I, Greenwald C, Rothschild BM, Latimer B, Dutour O, Jellema LM, Wish-Baratz S (1999) Hyperostosis frontalis interna: an anthropological perspective. Am J Phys Anthropol 109:303–325CrossRef Hershkovitz I, Greenwald C, Rothschild BM, Latimer B, Dutour O, Jellema LM, Wish-Baratz S (1999) Hyperostosis frontalis interna: an anthropological perspective. Am J Phys Anthropol 109:303–325CrossRef
Metadata
Title
Increased substantia nigra echogenicity correlated with visual hallucinations in Parkinson’s disease: a Chinese population-based study
Authors
Ting Li
Jing Shi
Bin Qin
Dongsheng Fan
Na Liu
Jingnian Ni
Tianqing Zhang
Hufang Zhou
Xiaoqing Xu
Mingqing Wei
Xuekai Zhang
Xiangzhu Wang
Jianping Liu
Yongyan Wang
Jinzhou Tian
Publication date
01-03-2020
Publisher
Springer International Publishing
Published in
Neurological Sciences / Issue 3/2020
Print ISSN: 1590-1874
Electronic ISSN: 1590-3478
DOI
https://doi.org/10.1007/s10072-019-04110-z

Other articles of this Issue 3/2020

Neurological Sciences 3/2020 Go to the issue