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Association of Estimated Glomerular Filtration Rate and Albuminuria with Venous Thromboembolism

Zheng, Zhong; Pandit, Krutika; Chang, Alex R; Shin, Jung-Im; Charytan, David M; Grams, Morgan E; Surapaneni, Aditya
BACKGROUND:Chronic kidney disease (CKD) has been implicated as a risk factor for venous thromboembolism, but the evidence is limited to relatively healthy populations. The objective of the current study was to discern whether parameters of kidney function and damage are associated with the occurrence of venous thromboembolism after hospitalization. METHODS:We conducted a retrospective study including 23,899 and 11,552 adult individuals hospitalized within Geisinger Health System and NYU Langone Health from 2004 to 2019 and 2012 to 2022, respectively. A Poisson model was used to evaluate adjusted incidence rates of venous thromboembolism according to estimated glomerular filtration rate (eGFR) and albuminuria categories in each cohort. Cox proportional hazards models were used to analyze associations of eGFR and urinary albumin to creatinine ratio (UACR) with venous thromboembolism and hazard ratios were meta-analyzed across cohorts. RESULTS:Both lower eGFR and higher UACR were associated with higher risks of venous thromboembolism. In the Geisinger cohort, the incidence of venous thromboembolism after hospital discharge ranged from 10.7 (95% CI 9.2 - 12.6) events per 1000 person-years in individuals in G1A1 (eGFR >90 mL/min/1.73 m2 and UACR <30 mg/g) to 27.7 (95% CI 20.6 - 37.2) events per 1000 person-years in individuals with G4-5A3 (eGFR <30 mL/min/1.73 m2 and UACR >300 mg/g). A similar pattern was observed in the NYU cohort. Meta-analyses of the two cohorts showed that every 10 mL/min/1.73m2 reduction in eGFR below 60 mL/min/1.73m2 was associated with a 6% higher risk of venous thromboembolism (HR 1.06 [1.02 - 1.11], P = 0.01), and each two-fold higher UACR was associated with a 5% higher risk of venous thromboembolism (HR 1.05 [1.03 - 1.07], P <0.001). CONCLUSIONS:Both eGFR and UACR were independently associated with higher risk of venous thromboembolism after hospitalization. The incidence rate was higher with greater severity of CKD.
PMID: 37971889
ISSN: 1555-905x
CID: 5610872

Development and Validation of the American Heart Association Predicting Risk of Cardiovascular Disease EVENTs (PREVENT) Equations

Khan, Sadiya S; Matsushita, Kunihiro; Sang, Yingying; Ballew, Shoshana H; Grams, Morgan E; Surapaneni, Aditya; Blaha, Michael J; Carson, April P; Chang, Alexander R; Ciemins, Elizabeth; Go, Alan S; Gutierrez, Orlando M; Hwang, Shih-Jen; Jassal, Simerjot K; Kovesdy, Csaba P; Lloyd-Jones, Donald M; Shlipak, Michael G; Palaniappan, Latha P; Sperling, Laurence; Virani, Salim S; Tuttle, Katherine; Neeland, Ian J; Chow, Sheryl L; Rangaswami, Janani; Pencina, Michael J; Ndumele, Chiadi E; Coresh, Josef; ,
PMID: 37947085
ISSN: 1524-4539
CID: 5607782

Differences in the Circulating Proteome in Individuals with versus without Sickle Cell Trait

Cai, Yanwei; Franceschini, Nora; Surapaneni, Aditya; Garrett, Melanie E; Tahir, Usman A; Hsu, Li; Telen, Marilyn J; Yu, Bing; Tang, Hua; Li, Yun; Liu, Simin; Gerszten, Robert E; Coresh, Josef; Manson, JoAnn E; Wojcik, Genevieve L; Kooperberg, Charles; Auer, Paul L; Foster, Matthew W; Grams, Morgan E; Ashley-Koch, Allison E; Raffield, Laura M; Reiner, Alex P
BACKGROUND:Sickle cell trait affects approximately 8% of Black individuals in the United States, along with many other individuals with ancestry from malaria-endemic regions worldwide. While traditionally considered a benign condition, recent evidence suggests that sickle cell trait is associated with lower eGFR and higher risk of kidney diseases, including kidney failure. The mechanisms underlying these associations remain poorly understood. We used proteomic profiling to gain insight into the pathobiology of sickle cell trait. METHODS:We measured proteomics ( N =1285 proteins assayed by Olink Explore) using baseline plasma samples from 592 Black participants with sickle cell trait and 1:1 age-matched Black participants without sickle cell trait from the prospective Women's Health Initiative cohort. Age-adjusted linear regression was used to assess the association between protein levels and sickle cell trait. RESULTS:In age-adjusted models, 35 proteins were significantly associated with sickle cell trait after correction for multiple testing. Several of the sickle cell trait-protein associations were replicated in Black participants from two independent cohorts (Atherosclerosis Risk in Communities study and Jackson Heart Study) assayed using an orthogonal aptamer-based proteomic platform (SomaScan). Many of the validated sickle cell trait-associated proteins are known biomarkers of kidney function or injury ( e.g. , hepatitis A virus cellular receptor 1 [HAVCR1]/kidney injury molecule-1 [KIM-1], uromodulin [UMOD], ephrins), related to red cell physiology or hemolysis (erythropoietin [EPO], heme oxygenase 1 [HMOX1], and α -hemoglobin stabilizing protein) and/or inflammation (fractalkine, C-C motif chemokine ligand 2/monocyte chemoattractant protein-1 [MCP-1], and urokinase plasminogen activator surface receptor [PLAUR]). A protein risk score constructed from the top sickle cell trait-associated biomarkers was associated with incident kidney failure among those with sickle cell trait during Women's Health Initiative follow-up (odds ratio, 1.32; 95% confidence interval, 1.10 to 1.58). CONCLUSIONS:We identified and replicated the association of sickle cell trait with a number of plasma proteins related to hemolysis, kidney injury, and inflammation.
PMID: 37533140
ISSN: 1555-905x
CID: 5609232

Proteomics of CKD progression in the chronic renal insufficiency cohort

Dubin, Ruth F; Deo, Rajat; Ren, Yue; Wang, Jianqiao; Zheng, Zihe; Shou, Haochang; Go, Alan S; Parsa, Afshin; Lash, James P; Rahman, Mahboob; Hsu, Chi-Yuan; Weir, Matthew R; Chen, Jing; Anderson, Amanda; Grams, Morgan E; Surapaneni, Aditya; Coresh, Josef; Li, Hongzhe; Kimmel, Paul L; Vasan, Ramachandran S; Feldman, Harold; Segal, Mark R; Ganz, Peter; ,; ,
Progression of chronic kidney disease (CKD) portends myriad complications, including kidney failure. In this study, we analyze associations of 4638 plasma proteins among 3235 participants of the Chronic Renal Insufficiency Cohort Study with the primary outcome of 50% decline in estimated glomerular filtration rate or kidney failure over 10 years. We validate key findings in the Atherosclerosis Risk in the Communities study. We identify 100 circulating proteins that are associated with the primary outcome after multivariable adjustment, using a Bonferroni statistical threshold of significance. Individual protein associations and biological pathway analyses highlight the roles of bone morphogenetic proteins, ephrin signaling, and prothrombin activation. A 65-protein risk model for the primary outcome has excellent discrimination (C-statistic[95%CI] 0.862 [0.835, 0.889]), and 14/65 proteins are druggable targets. Potentially causal associations for five proteins, to our knowledge not previously reported, are supported by Mendelian randomization: EGFL9, LRP-11, MXRA7, IL-1 sRII and ILT-2. Modifiable protein risk markers can guide therapeutic drug development aimed at slowing CKD progression.
PMCID:10564759
PMID: 37816758
ISSN: 2041-1723
CID: 5605032

Estimated Glomerular Filtration Rate, Albuminuria, and Adverse Outcomes: An Individual-Participant Data Meta-Analysis

,; Grams, Morgan E; Coresh, Josef; Matsushita, Kunihiro; Ballew, Shoshana H; Sang, Yingying; Surapaneni, Aditya; Alencar de Pinho, Natalia; Anderson, Amanda; Appel, Lawrence J; Ärnlöv, Johan; Azizi, Fereidoun; Bansal, Nisha; Bell, Samira; Bilo, Henk J G; Brunskill, Nigel J; Carrero, Juan J; Chadban, Steve; Chalmers, John; Chen, Jing; Ciemins, Elizabeth; Cirillo, Massimo; Ebert, Natalie; Evans, Marie; Ferreiro, Alejandro; Fu, Edouard L; Fukagawa, Masafumi; Green, Jamie A; Gutierrez, Orlando M; Herrington, William G; Hwang, Shih-Jen; Inker, Lesley A; Iseki, Kunitoshi; Jafar, Tazeen; Jassal, Simerjot K; Jha, Vivekanand; Kadota, Aya; Katz, Ronit; Köttgen, Anna; Konta, Tsuneo; Kronenberg, Florian; Lee, Brian J; Lees, Jennifer; Levin, Adeera; Looker, Helen C; Major, Rupert; Melzer Cohen, Cheli; Mieno, Makiko; Miyazaki, Mariko; Moranne, Olivier; Muraki, Isao; Naimark, David; Nitsch, Dorothea; Oh, Wonsuk; Pena, Michelle; Purnell, Tanjala S; Sabanayagam, Charumathi; Satoh, Michihiro; Sawhney, Simon; Schaeffner, Elke; Schöttker, Ben; Shen, Jenny I; Shlipak, Michael G; Sinha, Smeeta; Stengel, Benedicte; Sumida, Keiichi; Tonelli, Marcello; Valdivielso, Jose M; van Zuilen, Arjan D; Visseren, Frank L J; Wang, Angela Yee-Moon; Wen, Chi-Pang; Wheeler, David C; Yatsuya, Hiroshi; Yamagata, Kunihiro; Yang, Jae Won; Young, Ann; Zhang, Haitao; Zhang, Luxia; Levey, Andrew S; Gansevoort, Ron T
IMPORTANCE:Chronic kidney disease (low estimated glomerular filtration rate [eGFR] or albuminuria) affects approximately 14% of adults in the US. OBJECTIVE:To evaluate associations of lower eGFR based on creatinine alone, lower eGFR based on creatinine combined with cystatin C, and more severe albuminuria with adverse kidney outcomes, cardiovascular outcomes, and other health outcomes. DESIGN, SETTING, AND PARTICIPANTS:Individual-participant data meta-analysis of 27 503 140 individuals from 114 global cohorts (eGFR based on creatinine alone) and 720 736 individuals from 20 cohorts (eGFR based on creatinine and cystatin C) and 9 067 753 individuals from 114 cohorts (albuminuria) from 1980 to 2021. EXPOSURES:The Chronic Kidney Disease Epidemiology Collaboration 2021 equations for eGFR based on creatinine alone and eGFR based on creatinine and cystatin C; and albuminuria estimated as urine albumin to creatinine ratio (UACR). MAIN OUTCOMES AND MEASURES:The risk of kidney failure requiring replacement therapy, all-cause mortality, cardiovascular mortality, acute kidney injury, any hospitalization, coronary heart disease, stroke, heart failure, atrial fibrillation, and peripheral artery disease. The analyses were performed within each cohort and summarized with random-effects meta-analyses. RESULTS:Within the population using eGFR based on creatinine alone (mean age, 54 years [SD, 17 years]; 51% were women; mean follow-up time, 4.8 years [SD, 3.3 years]), the mean eGFR was 90 mL/min/1.73 m2 (SD, 22 mL/min/1.73 m2) and the median UACR was 11 mg/g (IQR, 8-16 mg/g). Within the population using eGFR based on creatinine and cystatin C (mean age, 59 years [SD, 12 years]; 53% were women; mean follow-up time, 10.8 years [SD, 4.1 years]), the mean eGFR was 88 mL/min/1.73 m2 (SD, 22 mL/min/1.73 m2) and the median UACR was 9 mg/g (IQR, 6-18 mg/g). Lower eGFR (whether based on creatinine alone or based on creatinine and cystatin C) and higher UACR were each significantly associated with higher risk for each of the 10 adverse outcomes, including those in the mildest categories of chronic kidney disease. For example, among people with a UACR less than 10 mg/g, an eGFR of 45 to 59 mL/min/1.73 m2 based on creatinine alone was associated with significantly higher hospitalization rates compared with an eGFR of 90 to 104 mL/min/1.73 m2 (adjusted hazard ratio, 1.3 [95% CI, 1.2-1.3]; 161 vs 79 events per 1000 person-years; excess absolute risk, 22 events per 1000 person-years [95% CI, 19-25 events per 1000 person-years]). CONCLUSIONS AND RELEVANCE:In this retrospective analysis of 114 cohorts, lower eGFR based on creatinine alone, lower eGFR based on creatinine and cystatin C, and more severe UACR were each associated with increased rates of 10 adverse outcomes, including adverse kidney outcomes, cardiovascular diseases, and hospitalizations.
PMID: 37787795
ISSN: 1538-3598
CID: 5611022

Circulating Proteins and Mortality in CKD: A Proteomics Study of the AASK and ARIC Cohorts

Srialluri, Nityasree; Surapaneni, Aditya; Schlosser, Pascal; Chen, Teresa K; Schmidt, Insa M; Rhee, Eugene P; Coresh, Josef; Grams, Morgan E
RATIONALE & OBJECTIVE/UNASSIGNED:Proteomics could provide pathophysiologic insight into the increased risk of mortality in patients with chronic kidney disease (CKD). This study aimed to investigate associations between the circulating proteome and all-cause mortality among patients with CKD. STUDY DESIGN/UNASSIGNED:Observational cohort study. SETTING & PARTICIPANTS/UNASSIGNED:Primary analysis in 703 participants in the African American Study of Kidney Disease and Hypertension (AASK) and validation in 1,628 participants with CKD in the Atherosclerosis Risk in Communities (ARIC) study who attended visit 5. EXPOSURE/UNASSIGNED:Circulating proteins. OUTCOME/UNASSIGNED:All-cause mortality. ANALYTICAL APPROACH/UNASSIGNED:Among AASK participants, we evaluated the associations of 6,790 circulating proteins with all-cause mortality using multivariable Cox proportional hazards models. Proteins with significant associations were further studied in ARIC Visit 5 participants with CKD. RESULTS/UNASSIGNED:-microglobulin, spondin-1, and N-terminal pro-brain natriuretic peptide) were available in the ARIC data, with all 3 significantly associated with death in ARIC. LIMITATIONS/UNASSIGNED:Possibility of unmeasured confounding. Cause of death was not known. CONCLUSIONS/UNASSIGNED:Using large-scale proteomic analysis, proteins were reproducibly associated with mortality in 2 cohorts of participants with CKD. PLAIN-LANGUAGE SUMMARY/UNASSIGNED:-microglobulin, spondin-1, and N-terminal pro-brain natriuretic peptide (BNP)) were also measured in ARIC and were significantly associated with death. Additional studies assessing biomarkers associated with mortality among patients with CKD are needed to evaluate their use in clinical practice.
PMCID:10498294
PMID: 37711886
ISSN: 2590-0595
CID: 5583272

Discrepancies between Cystatin C-Based and Creatinine-Based eGFR

Farrington, Danielle K; Surapaneni, Aditya; Matsushita, Kunihiro; Seegmiller, Jesse C; Coresh, Josef; Grams, Morgan E
BACKGROUND:Recent guidance suggests clinicians increase use of cystatin C for the estimation of GFR. Discrepant levels of creatinine-versus cystatin C-based eGFR (eGFRcr versus eGFRcys) can occur and might signify inaccurate estimation of GFR using creatinine alone. This study sought to enhance the knowledge of the risk factors and clinical implications of having a large eGFR discrepancy. METHODS:Participants in the Atherosclerosis Risk in Communities Study, a prospective cohort study of US adults, were followed over 25 years. eGFR discrepancy was measured at five clinical visits and defined as eGFRcys either 30% lower or higher than eGFRcr, the current clinical standard of care. The associations between eGFR discrepancies and kidney-related laboratory parameters were assessed using linear and logistic regression and long-term adverse outcomes, including kidney failure, AKI, heart failure, and death, using Cox proportional hazards models. RESULTS:Among 13,197 individuals (mean age 57 [SD 6] years, 56% women, 25% Black race), 7% had eGFRcys 30% lower than eGFRcr at visit 2 (1990-1992), and this proportion increased over time to 23% by visit 6 (2016-2017). By contrast, the percent with eGFRcys 30% higher than eGFRcr was relatively stable (3%-1%). Independent risk factors for having eGFRcys 30% lower than eGFRcr included older age, female sex, non-Black race, higher eGFRcr, higher body mass index, weight loss, and current smoking. Those with eGFRcys 30% lower than eGFRcr had more anemia and higher uric acid, fibroblast growth factor 23, and phosphate levels as well as higher risk of subsequent mortality, kidney failure, AKI, and heart failure compared with those with similar eGFRcr and eGFRcys values. CONCLUSIONS:Having eGFRcys lower than eGFRcr was associated with worse kidney-related laboratory derangements and a higher risk of adverse health outcomes.
PMID: 37339177
ISSN: 1555-905x
CID: 5542622

Proteomics analysis of plasma from middle-aged adults identifies protein markers of dementia risk in later life

Walker, Keenan A; Chen, Jingsha; Shi, Liu; Yang, Yunju; Fornage, Myriam; Zhou, Linda; Schlosser, Pascal; Surapaneni, Aditya; Grams, Morgan E; Duggan, Michael R; Peng, Zhongsheng; Gomez, Gabriela T; Tin, Adrienne; Hoogeveen, Ron C; Sullivan, Kevin J; Ganz, Peter; Lindbohm, Joni V; Kivimaki, Mika; Nevado-Holgado, Alejo J; Buckley, Noel; Gottesman, Rebecca F; Mosley, Thomas H; Boerwinkle, Eric; Ballantyne, Christie M; Coresh, Josef
A diverse set of biological processes have been implicated in the pathophysiology of Alzheimer's disease (AD) and related dementias. However, there is limited understanding of the peripheral biological mechanisms relevant in the earliest phases of the disease. Here, we used a large-scale proteomics platform to examine the association of 4877 plasma proteins with 25-year dementia risk in 10,981 middle-aged adults. We found 32 dementia-associated plasma proteins that were involved in proteostasis, immunity, synaptic function, and extracellular matrix organization. We then replicated the association between 15 of these proteins and clinically relevant neurocognitive outcomes in two independent cohorts. We demonstrated that 12 of these 32 dementia-associated proteins were associated with cerebrospinal fluid (CSF) biomarkers of AD, neurodegeneration, or neuroinflammation. We found that eight of these candidate protein markers were abnormally expressed in human postmortem brain tissue from patients with AD, although some of the proteins that were most strongly associated with dementia risk, such as GDF15, were not detected in these brain tissue samples. Using network analyses, we found a protein signature for dementia risk that was characterized by dysregulation of specific immune and proteostasis/autophagy pathways in adults in midlife ~20 years before dementia onset, as well as abnormal coagulation and complement signaling ~10 years before dementia onset. Bidirectional two-sample Mendelian randomization genetically validated nine of our candidate proteins as markers of AD in midlife and inferred causality of SERPINA3 in AD pathogenesis. Last, we prioritized a set of candidate markers for AD and dementia risk prediction in midlife.
PMCID:10665113
PMID: 37467317
ISSN: 1946-6242
CID: 5587212

Unbiased Human Kidney Tissue Proteomics Identifies Matrix Metalloproteinase 7 as a Kidney Disease Biomarker

Hirohama, Daigoro; Abedini, Amin; Moon, Salina; Surapaneni, Aditya; Dillon, Simon T; Vassalotti, Allison; Liu, Hongbo; Doke, Tomohito; Martinez, Victor; Md Dom, Zaipul; Karihaloo, Anil; Palmer, Matthew B; Coresh, Josef; Grams, Morgan E; Niewczas, Monika A; Susztak, Katalin
SIGNIFICANCE STATEMENT:Although gene expression changes have been characterized in human diabetic kidney disease (DKD), unbiased tissue proteomics information for this condition is lacking. The authors conducted an unbiased aptamer-based proteomic analysis of samples from patients with DKD and healthy controls, identifying proteins with levels that associate with kidney function (eGFR) or fibrosis, after adjusting for key covariates. Overall, tissue gene expression only modestly correlated with tissue protein levels. Kidney protein and RNA levels of matrix metalloproteinase 7 (MMP7) strongly correlated with fibrosis and with eGFR. Single-cell RNA sequencing indicated that kidney tubule cells are an important source of MMP7. Furthermore, plasma MMP7 levels predicted future kidney function decline. These findings identify kidney tissue MMP7 as a biomarker of fibrosis and blood MMP7 as a biomarker for future kidney function decline. BACKGROUND:Diabetic kidney disease (DKD) is responsible for close to half of all ESKD cases. Although unbiased gene expression changes have been extensively characterized in human kidney tissue samples, unbiased protein-level information is not available. METHODS:We collected human kidney samples from 23 individuals with DKD and ten healthy controls, gathered associated clinical and demographics information, and implemented histologic analysis. We performed unbiased proteomics using the SomaScan platform and quantified the level of 1305 proteins and analyzed gene expression levels by bulk RNA and single-cell RNA sequencing (scRNA-seq). We validated protein levels in a separate cohort of kidney tissue samples as well as in 11,030 blood samples. RESULTS:Globally, human kidney transcript and protein levels showed only modest correlation. Our analysis identified 14 proteins with kidney tissue levels that correlated with eGFR and found that the levels of 152 proteins correlated with interstitial fibrosis. Of the identified proteins, matrix metalloprotease 7 (MMP7) showed the strongest association with both fibrosis and eGFR. The correlation between tissue MMP7 protein expression and kidney function was validated in external datasets. The levels of MMP7 RNA correlated with fibrosis in the primary and validation datasets. Findings from scRNA-seq pointed to proximal tubules, connecting tubules, and principal cells as likely cellular sources of increased tissue MMP7 expression. Furthermore, plasma MMP7 levels correlated not only with kidney function but also associated with prospective kidney function decline. CONCLUSIONS:Our findings, which underscore the value of human kidney tissue proteomics analysis, identify kidney tissue MMP7 as a diagnostic marker of kidney fibrosis and blood MMP7 as a biomarker for future kidney function decline.
PMCID:10356165
PMID: 37022120
ISSN: 1533-3450
CID: 5587132

Alterations in the Circulating Proteome Associated with Albuminuria

Kiernan, Elizabeth; Surapaneni, Aditya; Zhou, Linda; Schlosser, Pascal; Walker, Keenan A; Rhee, Eugene P; Ballantyne, Christie M; Deo, Rajat; Dubin, Ruth F; Ganz, Peter; Coresh, Josef; Grams, Morgan E
SIGNIFICANCE STATEMENT:We describe circulating proteins associated with albuminuria in a population of African American Study of Kidney Disease and Hypertension with CKD (AASK) using the largest proteomic platform to date: nearly 7000 circulating proteins, representing approximately 2000 new targets. Findings were replicated in a subset of a general population cohort with kidney disease (ARIC) and a population with CKD Chronic Renal Insufficiency Cohort (CRIC). In cross-sectional analysis, 104 proteins were significantly associated with albuminuria in the Black group, of which 67 of 77 available proteins were replicated in ARIC and 68 of 71 available proteins in CRIC. LMAN2, TNFSFR1B, and members of the ephrin superfamily had the strongest associations. Pathway analysis also demonstrated enrichment of ephrin family proteins. BACKGROUND:Proteomic techniques have facilitated understanding of pathways that mediate decline in GFR. Albuminuria is a key component of CKD diagnosis, staging, and prognosis but has been less studied than GFR. We sought to investigate circulating proteins associated with higher albuminuria. METHODS:We evaluated the cross-sectional associations of the blood proteome with albuminuria and longitudinally with doubling of albuminuria in the African American Study of Kidney Disease and Hypertension (AASK; 38% female; mean GFR 46; median urine protein-to-creatinine ratio 81 mg/g; n =703) and replicated in two external cohorts: a subset of the Atherosclerosis Risk in Communities (ARIC) study with CKD and the Chronic Renal Insufficiency Cohort (CRIC). RESULTS:In cross-sectional analysis, 104 proteins were significantly associated with albuminuria in AASK, of which 67 of 77 available proteins were replicated in ARIC and 68 of 71 available proteins in CRIC. Proteins with the strongest associations included LMAN2, TNFSFR1B, and members of the ephrin superfamily. Pathway analysis also demonstrated enrichment of ephrin family proteins. Five proteins were significantly associated with worsening albuminuria in AASK, including LMAN2 and EFNA4, which were replicated in ARIC and CRIC. CONCLUSIONS:Among individuals with CKD, large-scale proteomic analysis identified known and novel proteins associated with albuminuria and suggested a role for ephrin signaling in albuminuria progression.
PMID: 36890639
ISSN: 1533-3450
CID: 5541462