AbstractMild cognitive impairment (MCI) is a prodromal stage in aging to possible progression to Alzheimer’s disease and related dementia (ADRD), where co-occurrence of major depressive disorder (MDD) accelerates the progression. Metabolic and mitochondrial abnormalities in ADRD and other neurodegenerative disorders have been widely suggested, while possible mitochondrial dysfunction has been associated with etiopathology of both MCI and MDD.

摘要轻度认知障碍（MCI）是衰老的前驱阶段，可能发展为阿尔茨海默病和相关痴呆（ADRD），其中重度抑郁症（MDD）的共同发生加速了进展。ADRD和其他神经退行性疾病的代谢和线粒体异常已被广泛提出，而可能的线粒体功能障碍与MCI和MDD的病因有关。

Hence, investigation of mitochondrial markers in MCI, MDD, and presence of both conditions is warranted. In total, 332 older adult participants were included: 168 with MCI, 108 with MCI plus remitted MDD (rMDD), and 56 with rMDD but without MCI. We measured plasma circulating mitochondrial DNA (ccf-mtDNA), lactate, and extracted nuclear mitochondrial encoded (NMt) single-nucleotide variants (SNVs) (n = 312).

因此，有必要研究MCI，MDD中的线粒体标志物以及这两种情况的存在。总共包括332名老年人参与者：168名患有MCI，108名患有MCI加缓解MDD（rMDD），56名患有rMDD但没有MCI。我们测量了血浆循环线粒体DNA（ccf mtDNA），乳酸和提取的核线粒体编码（NMt）单核苷酸变体（SNV）（n=312）。

Non-parametric statistical tests on ccf-mtDNA and lactate levels were performed on the diagnosis, clinical and cardiometabolic variables. Binary sequence kernel association test (SKAT-O) and burden test were performed on NMt-SNV, adjusted for age, race, gender, type II diabetes, and APOE genotype. Lower level of lactate was observed in MCI (KW χ2 = 14.8, P = 0.0024), more specifically, significant differences of lower plasma lactate between MCI only and rMDD, but not between MCI+rMDD and MCI were found, suggesting potential roles in MCI driving lactate lower levels.

对诊断，临床和心脏代谢变量进行了ccf mtDNA和乳酸水平的非参数统计检验。对NMt SNV进行了二元序列内核关联测试（SKAT-O）和负担测试，并根据年龄，种族，性别，II型糖尿病和APOE基因型进行了调整。。

While higher levels of ccf-mtDNA were observed in APOE-ε4 carrier (χ2 = 5.04, P = 0.05). This relationship was present only in MCI (P = 0.043) and MCI+rMDD groups (P = 0.023). No significant nuclear-encoded mitochondrial gene associations were observed with MCI or MDD. The results suggest decreased level of plasma lactate in individuals with MCI and MCI+rMDD, with i.

而在APOE-ε4载体中观察到更高水平的ccf mtDNA（χ2=5.04，P=0.05）。这种关系仅存在于MCI（P=0.043）和MCI+rMDD组（P=0.023）中。MCI或MDD未观察到明显的核编码线粒体基因关联。结果表明，MCI和MCI+rMDD患者的血浆乳酸水平降低。

IntroductionMild cognitive impairment (MCI) is a prodromal stage of dementia affecting up to 20% of older adults, where 10–20% of individuals with MCI progress to dementia annually [1]. While the progression of MCI to dementia is influenced by a range of factors, lifetime major depressive disorder (MDD) is one of most prevalent and influential clinical risk factors of developing late onset Alzheimer’s disease and related dementia (ADRD) [2].

引言轻度认知障碍（MCI）是痴呆的前驱阶段，影响高达20%的老年人，其中10-20%的MCI患者每年进展为痴呆[1]。虽然MCI向痴呆的进展受到一系列因素的影响，但终生重度抑郁症（MDD）是发展迟发性阿尔茨海默病和相关痴呆（ADRD）的最普遍和最有影响的临床危险因素之一。

Lifetime history of MDD has been suggested to increase the risk of developing ADRD by twofold [3, 4]. Furthermore, both remitted and active late-life depression has been reported to accelerate the progression from MCI to AD by 20–40%, respectively [5, 6]. Lifetime occurrence of MDD is estimated up to 20%, while MCI affects up to 20% of older adults—together, individuals with MCI and MDD represents a large subgroup of patients with pre-dementia sharing neuropsychiatric considerations [7,8,9].Despite the identification of risk factors for developing sporadic forms of ADRD including genetic, biological, and environmental factors in recent years, understanding of the contribution and interactions of each factor to etiopathology remain largely elusive [10].

MDD的终生病史被认为会使发生ADRD的风险增加两倍[3，4]。此外，据报道，缓解型和活动性晚期抑郁症分别使MCI向AD的进展加速20-40%[5,6]。据估计，MDD的终生发生率高达20%，而MCI共同影响高达20%的老年人，MCI和MDD患者代表了痴呆前期患者的一大亚组，具有神经精神病学考虑[7,8,9]。尽管近年来确定了发展散发性ADRD的危险因素，包括遗传，生物和环境因素，但对每个因素对病因的贡献和相互作用的理解仍然很难理解（10）。

Previous investigations of MDD as a risk factor for dementia predominantly focused on symptomatology and active depression [3, 11]. Yet, careful considerations are required in the investigation and interpretation of depressive symptom as a neuropsychiatric feature of cognitive impairment, or rather, exacerbated impairment affected by pre-existing early to midlife MDD [12,13,14].

先前对MDD作为痴呆危险因素的研究主要集中在症状学和活动性抑郁症[3，11]。然而，在调查和解释抑郁症状作为认知障碍的神经精神病学特征时，需要仔细考虑，或者更确切地说，加剧了先前存在的早期至中年MDD的损害[12，13，14]。

Thus, further investigations on co-existing risk conditions and its interactions are required, while considering and controlling for semi-modifiable factors such as remission status and onset of depression.A c.

因此，需要进一步研究共存的风险状况及其相互作用，同时考虑和控制缓解状态和抑郁症发作等半可改变因素。A c。

ApoE-ε genotypingThe total count of successfully ApoE-genotyped individuals included in the analysis was 280 of 312, where rs4293558 genotyping was unsuccessful in 31 individuals, and inconsistency occurred in rs7412 quality control probes (3 total) which has been removed from the analysis. No statistical differences of ε4 or ε2 counts between diagnostic groups, age, race, and gender were found (Supplemental Table 2).Single-nucleotide variation quality control and nuclear-encoded mitochondrial gene extractionA total of 530,163 variants were genotyped, and upon initial quality control, 330,546 SNVs remained.

ApoE-ε基因分型分析中包括的成功ApoE基因分型个体总数为312个中的280个，其中rs4293558基因分型在31个个体中不成功，并且rs7412质量控制探针（总共3个）发生不一致，已从分析中删除。。单核苷酸变异质量控制和核编码线粒体基因提取对总共530163个变异进行了基因分型，在初始质量控制后，剩下330546个SNV。

The SNVs were pruned, and the remaining 123,328 SNVs were used for PCA. Upon extraction of NMt genes, a total of 4870 NMt SNVs were left for analysis.Principal component analysis of the pruned genome wide and mitochondrial SNVs demonstrated similar structures, separating self-identified races (Supplemental Table 2).

修剪了SNV，其余123328个SNV用于PCA。提取NMt基因后，总共剩下4870个NMt SNV进行分析。修剪后的全基因组和线粒体SNV的主成分分析显示出相似的结构，分离了自我鉴定的种族（补充表2）。

The first two PCs of the GW and NMt SNVs were linearly correlated (Pearson’s r2 > 0.98) and were used as covariates representing ancestry.Nuclear-encoded mitochondrial single nucleotide variantsThere were no NMt SNVs that were significantly associated with MCI or rMDD from logistic regression analysis.

GW和NMt SNV的前两个PC呈线性相关（Pearson的r2＞0.98），并被用作代表血统的协变量。核编码的线粒体单核苷酸变异从逻辑回归分析来看，没有NMt SNV与MCI或rMDD显着相关。

Of 4870 NMt SNVs, 135 variants were found in non-white participants. The average NMt alternative allele per individual was 2095 ± 137, and 0.43 ± 0.03 alleles per genotyped SNV. Burden and SKAT-O test for MCI as binary trait after adjusting for age, gender, rMDD, ccf-mtDNA, and lactate suggested difference by MCI (ncases = 262, ncontrols = 50) diagnosis status (Burden P = 0.011; SKAT-O P = 0.018), however, upon adjustment with the first 2 ancestry-related genetic PCs, no significance was found (Burden P = 0.21; SKAT-O P = 0.18).

在4870个NMt SNV中，在非白人参与者中发现了135个变体。每个个体的平均NMt替代等位基因为2095±137，每个基因型SNV的平均NMt替代等位基因为0.43±0.03。在调整年龄，性别，rMDD，ccf mtDNA和乳酸后，MCI作为二元性状的负担和SKAT-O检验表明MCI的差异（NCASE=262，ncontrols=50）诊断状态（负担P=0.011；SKAT-O P＝0.018），然而，在调整前2个祖先相关的遗传PC后，没有发现显着性（负担P＝0.21；SKAT-O P=0.18）。

The burden and SKAT-O test f.

负担和SKAT-O测试f。

Data availability

数据可用性

The data generated and analyzed in the current study is available from the corresponding author and the PACt-MD Study Group upon request.

本研究中生成和分析的数据可应要求从通讯作者和PACt MD研究小组获得。

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Download referencesAcknowledgementsThis work was made possible by a grant from the Canada Brain Research Fund of Brain Canada, with the financial support of Health Canada, the Chagnon Family, and the CAMH Discovery Fund. The PACt-MD Study Group comprised: Benoit H. Mulsant, MD, MS (Principal Investigator); Tarek K.

下载参考文献致谢这项工作是由加拿大大脑研究基金会（Canada Brain Research Fund of Brain Canada）资助的，并得到了加拿大卫生部，Chagnon家族和CAMH发现基金的财政支持。PACt MD研究小组包括：医学博士Benoit H.Mulsant，MS（首席研究员）；塔瑞克K。

Rajji, MD (Co-PI; site PI, Centre for Addiction and Mental Health, Lead, neurostimulation and neurophysiology); Nathan Herrmann, MD (Co-PI; site PI, Sunnybrook Health Sciences Centre), Bruce G. Pollock, MD, PhD (Co-PI); Daniel Blumberger, MD, MSc (Co-Investigator); Christopher Bowie, PhD, C.Psych (Co-Investigator; lead, cognitive remediation and neuropsychology); Meryl Butters, PhD (Consultant, neuropsychology); Corinne Fischer, MD (Co-Investigator; site PI, St.

医学博士Rajji（Co PI；site PI，成瘾和心理健康中心，铅，神经刺激和神经生理学）；医学博士Nathan Herrmann（联合PI；森尼布鲁克健康科学中心现场PI），医学博士Bruce G.Pollock博士（联合PI）；Daniel Blumberger，医学博士，理学硕士（联合研究员）；克里斯托弗·鲍伊（Christopher Bowie）博士，C.Psych（联合研究员；铅，认知修复和神经心理学）；Meryl Butters博士（神经心理学顾问）；。

Michael’s Hospital); Alastair Flint, MD (Co-Investigator; site PI, University Health Network); Angela Golas, MD (lead, CSF); Ariel Graff, MD (Lead, neurochemistry); James L. Kennedy, MD (Lead, genetics); Sanjeev Kumar, MD (Co-Investigator); Krista Lanctot, PhD, (site PI, Sunnybrook Health Sciences Centre), Lillian Lourenco, MPH (study co-manager), Linda Mah, MD, MHS (Co-Investigator; site PI, Baycrest Health Sciences); Shima Ovaysikia, MA (study co-manager); Mark Rapoport, MD (Co-Investigator); Kevin Thorpe, MSc (Biostatistician); Nicolaas P.L.G.

；医学博士Alastair Flint（联合研究员；大学健康网络PI站点）；医学博士Angela Golas（CSF负责人）；医学博士Ariel Graff（领导，神经化学）；James L.Kennedy，医学博士（遗传学负责人）；Sanjeev Kumar，医学博士（联合研究员）；Krista Lanctot博士（森尼布鲁克健康科学中心PI站点），Lillian Lourenco，MPH（研究联合经理），Linda Mah，MD，MHS（联合研究员；Baycrest Health Sciences PI站点）；马萨诸塞州Shima Ovaysikia（研究共同经理）；医学博士Mark Rapoport（联合研究员）；凯文·索普，理学硕士（生物统计学家）；尼古拉斯P.L.G。

Verhoeff, MD, PhD (Co-Investigator); Aristotle Voineskos, MD, PhD (Lead, neuroimaging). This study was funded by Canadian Institute for Health Research to ACA, and Mitacs to JC. We also acknowledge the contribution of Kathleen Bingham, MD; Lina Chiuccariello, PhD; Tiffany Chow, MD; Pallavi Dham, MD; Breno Diniz, MD, PhD; Dielle Miranda, Carmela Tartaglia, MD; and the PACt-MD Research Staff.Author informationAuthors and AffiliationsDepartment o.

Verhoeff，医学博士，博士（联合研究员）；亚里士多德·沃因斯科斯（Aristotle Voineskos），医学博士（Lead，neuroimaging）。这项研究由加拿大健康研究所资助ACA，Mitacs资助JC。我们也感谢医学博士Kathleen Bingham的贡献；Lina Chiuccariello博士；蒂芙尼·周，医学博士；医学博士Pallavi Dham；医学博士Breno Diniz；Dielle Miranda，医学博士Carmela Tartaglia；和PACt MD研究人员。作者信息作者和附属机构o。

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PubMed Google ScholarConsortiathe PACt-MD Study GroupContributionsJC contributed to conceptualization, design, data curation, investigation, analysis and interpretation of the data, and original draft of the study. TC and ELB contributed in data curation, investigation, validation, analysis of data, review and editing.

PubMed Google ScholarConsortiathe PACt MD研究小组贡献JC为数据的概念化，设计，数据管理，调查，分析和解释以及研究的原始草案做出了贡献。TC和ELB在数据管理，调查，验证，数据分析，审查和编辑方面做出了贡献。

HJB contributed to the data curation, investigation, analysis of data, review and editing. JLK, CEF, AJF, NH, KLL, LM, BHM, and BGP contributed to the study design, analysis and interpretation of data, manuscript review and editing. TKR and ACA supervised the study, and performed conceptualization, design, analysis and interpretation of the data, review and edit of the manuscript.Corresponding authorCorrespondence to.

HJB为数据管理、调查、数据分析、审查和编辑做出了贡献。JLK，CEF，AJF，NH，KLL，LM，BHM和BGP为研究设计，数据分析和解释，稿件审查和编辑做出了贡献。TKR和ACA监督了这项研究，并对数据进行了概念化，设计，分析和解释，审查和编辑了手稿。对应作者对应。

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All participants provided written informed consent as approved by the University of local Research Ethics Boards (University of Toronto REB# 42061, Centre for Addiction and Mental Health protocol# 1333) and Clinical Trials Ontario. All research activities and methods were performed in accordance with the guidelines and regulations..

所有参与者均提供了经当地研究大学伦理委员会（多伦多大学REB#42061，成瘾与心理健康协议中心#1333）和安大略省临床试验批准的书面知情同意书。所有研究活动和方法均按照指南和规定进行。。

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Reprints and permissionsAbout this articleCite this articleChoi, J., Beroncal, E.L., Chernega, T. et al. Exploring mitochondrial blood-based and genetic markers in older adults with mild cognitive impairment and remitted major depressive disorder.

转载和许可本文引用本文Choi，J.，Beroncal，E.L.，Chernega，T。等人探索轻度认知障碍和缓解型重度抑郁症老年人的线粒体血液和遗传标记。

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