Effects of smoking on the genetic risk of obesity: The population architecture using genomics and epidemiology study

Megan D. Fesinmeyer; Kari E. North; Unhee Lim; Petra Bůžková; Dana C. Crawford; Jeffrey Haessler; Myron D. Gross; Jay H. Fowke; Robert Goodloe; Shelley Ann Love; Misa Graff; Christopher S. Carlson; Lewis H. Kuller; Tara C. Matise; Ching Ping Hong; Brian E. Henderson; Melissa Allen; Rebecca R. Rohde; Ping Mayo; Nathalie Schnetz-Boutaud; Kristine R. Monroe; Marylyn D. Ritchie; Ross L. Prentice; Lawrence N. Kolonel; Jo Ann E. Manson; James Pankow; Lucia A. Hindorff; Nora Franceschini; Lynne R. Wilkens; Christopher A. Haiman; Loic Le Marchand; Ulrike Peters

doi:10.1186/1471-2350-14-6

Effects of smoking on the genetic risk of obesity: The population architecture using genomics and epidemiology study

Megan D. Fesinmeyer, Kari E. North, Unhee Lim, Petra Bůžková, Dana C. Crawford, Jeffrey Haessler, Myron D. Gross, Jay H. Fowke, Robert Goodloe, Shelley Ann Love, Misa Graff, Christopher S. Carlson, Lewis H. Kuller, Tara C. Matise, Ching Ping Hong, Brian E. Henderson, Melissa Allen, Rebecca R. Rohde, Ping Mayo, Nathalie Schnetz-BoutaudKristine R. Monroe, Marylyn D. Ritchie, Ross L. Prentice, Lawrence N. Kolonel, Jo Ann E. Manson, James Pankow, Lucia A. Hindorff, Nora Franceschini, Lynne R. Wilkens, Christopher A. Haiman, Loic Le Marchand, Ulrike Peters

Research output: Contribution to journal › Article › peer-review

19 Scopus citations

Abstract

Background: Although smoking behavior is known to affect body mass index (BMI), the potential for smoking to influence genetic associations with BMI is largely unexplored.Methods: As part of the 'Population Architecture using Genomics and Epidemiology (PAGE)' Consortium, we investigated interaction between genetic risk factors associated with BMI and smoking for 10 single nucleotide polymorphisms (SNPs) previously identified in genome-wide association studies. We included 6 studies with a total of 56,466 subjects (16,750 African Americans (AA) and 39,716 European Americans (EA)). We assessed effect modification by testing an interaction term for each SNP and smoking (current vs. former/never) in the linear regression and by stratified analyses.Results: We did not observe strong evidence for interactions and only observed two interactions with p-values <0.1: for rs6548238/TMEM18, the risk allele (C) was associated with BMI only among AA females who were former/never smokers (β = 0.018, p = 0.002), vs. current smokers (β = 0.001, p = 0.95, p_interaction = 0.10). For rs9939609/FTO, the A allele was more strongly associated with BMI among current smoker EA females (β = 0.017, p = 3.5x10^-5), vs. former/never smokers (β = 0.006, p = 0.05, p_interaction = 0.08).Conclusions: These analyses provide limited evidence that smoking status may modify genetic effects of previously identified genetic risk factors for BMI. Larger studies are needed to follow up our results.Clinical Trial Registration: NCT00000611.

Original language	English (US)
Article number	6
Journal	BMC medical genetics
Volume	14
Issue number	1
DOIs	https://doi.org/10.1186/1471-2350-14-6
State	Published - Jan 11 2013

Bibliographical note

Funding Information:
The Population Architecture Using Genomics and Epidemiology (PAGE) program is funded by the National Human Genome Research Institute (NHGRI), supported by U01HG004803 (CALiCo), U01HG004798 (EAGLE), U01HG004802 (MEC), U01HG004790 (WHI), and U01HG004801 (Coordinating Center), and their respective NHGRI ARRA supplements. The contents of this paper are solely the responsibility of the authors and do not necessarily represent the official views of the NIH. The complete list of PAGE members can be found at http://www.pagestudy.org. The data and materials included in this report result from a collaboration between the following studies: The "Epidemiologic Architecture for Genes Linked to Environment (EAGLE)" is funded through the NHGRI PAGE program (U01HG004798-01 and its NHGRI ARRA supplement). Genotyping services for select NHANES III SNPs presented here were also provided by the Johns Hopkins University under federal contract number (N01-HV-48195) from NHLBI. The study participants derive from the National Health and Nutrition Examination Surveys (NHANES), and these studies are supported by the Centers for Disease Control and Prevention. The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention. The Multiethnic Cohort study (MEC) characterization of epidemiological architecture is funded through the NHGRI PAGE program (U01HG004802 and its NHGRI ARRA supplement). The MEC study is funded through the National Cancer Institute (R37CA54281, R01 CA63, P01CA33619, U01CA136792, and U01CA98758). Funding support for the “Epidemiology of putative genetic variants: The Women’s Health Initiative” study is provided through the NHGRI PAGE program (U01HG004790 and its NHGRI ARRA supplement). The WHI program is funded by the National Heart, Lung, and Blood Institute; NIH; and U.S. Department of Health and Human Services through contracts N01WH22110, 24152, 32100–2, 32105–6, 32108–9, 32111–13, 32115, 32118–32119, 32122, 42107–26, 42129–32, and 44221. The authors thank the WHI investigators and staff for their dedication, and the study participants for making the program possible. A full listing of WHI investigators can be found at: http:// www.whiscience.org/publications/ WHI_investigators_shortlist.pdf. Funding support for the Genetic Epidemiology of Causal Variants Across the Life Course (CALiCo) program was provided through the NHGRI PAGE program (U01HG004803 and its NHGRI ARRA supplement). The following studies contributed to this manuscript and are funded by the following agencies: The Atherosclerosis Risk in Communities (ARIC) Study is carried out as a collaborative study supported by National Heart, Lung, and Blood Institute contracts N01-HC-55015, N01-HC-55016, N01-HC-55018, N01-HC-55019, N01-HC-55020, N01-HC-55021, N01-HC-55022. The Coronary Artery Risk Development in Young Adults (CARDIA) study is supported by the following National Institutes of Health, National Heart, Lung and Blood Institute contracts: N01-HC-95095; N01-HC-48047; N01-HC-48048; N01-HC-48049; N01-HC-48050; N01-HC-45134; N01-HC-05187; and N01-HC-45205. The Cardiovascular Health Study (CHS) is supported by contracts HHSN268201200036C, N01-HC-85239, N01-HC-85079 through N01-HC-85086, N01-HC-35129, N01 HC-15103, N01 HC-55222, N01-HC-75150, N01-HC-45133, and grant HL080295 from the National Heart, Lung, and Blood Institute (NHLBI), with additional contribution from the National Institute of Neurological Disorders and Stroke (NINDS). Additional support was provided through AG-023629, AG-15928, AG-20098, and AG-027058 from the National Institute on Aging (NIA). The Strong Heart Study (SHS) is supported by NHLBI grants U01 HL65520, U01 HL41642, U01 HL41652, U01 HL41654, and U01 HL65521. The opinions expressed in this paper are those of the author(s) and do not necessarily reflect the views of the Indian Health Service. Assistance with phenotype harmonization, SNP selection and annotation, data cleaning, data management, integration and dissemination, and general study coordination was provided by the PAGE Coordinating Center (U01HG004801-01 and its NHGRI ARRA supplement). The National Institutes of Mental Health also contributes to the support for the Coordinating Center.

Keywords

Body mass index
Genetic epidemiology
Genetic risk factor
Genome-wide association study
Obesity
Smoking interactions

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1186/1471-2350-14-6

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Fesinmeyer, M. D., North, K. E., Lim, U., Bůžková, P., Crawford, D. C., Haessler, J., Gross, M. D., Fowke, J. H., Goodloe, R., Love, S. A., Graff, M., Carlson, C. S., Kuller, L. H., Matise, T. C., Hong, C. P., Henderson, B. E., Allen, M., Rohde, R. R., Mayo, P., ... Peters, U. (2013). Effects of smoking on the genetic risk of obesity: The population architecture using genomics and epidemiology study. BMC medical genetics, 14(1), [6]. https://doi.org/10.1186/1471-2350-14-6

Fesinmeyer, MD, North, KE, Lim, U, Bůžková, P, Crawford, DC, Haessler, J, Gross, MD, Fowke, JH, Goodloe, R, Love, SA, Graff, M, Carlson, CS, Kuller, LH, Matise, TC, Hong, CP, Henderson, BE, Allen, M, Rohde, RR, Mayo, P, Schnetz-Boutaud, N, Monroe, KR, Ritchie, MD, Prentice, RL, Kolonel, LN, Manson, JAE, Pankow, J, Hindorff, LA, Franceschini, N, Wilkens, LR, Haiman, CA, Le Marchand, L & Peters, U 2013, 'Effects of smoking on the genetic risk of obesity: The population architecture using genomics and epidemiology study', BMC medical genetics, vol. 14, no. 1, 6. https://doi.org/10.1186/1471-2350-14-6

@article{afd4c7d2cc8740198dc1432bf46cb0f7,

title = "Effects of smoking on the genetic risk of obesity: The population architecture using genomics and epidemiology study",

abstract = "Background: Although smoking behavior is known to affect body mass index (BMI), the potential for smoking to influence genetic associations with BMI is largely unexplored.Methods: As part of the 'Population Architecture using Genomics and Epidemiology (PAGE)' Consortium, we investigated interaction between genetic risk factors associated with BMI and smoking for 10 single nucleotide polymorphisms (SNPs) previously identified in genome-wide association studies. We included 6 studies with a total of 56,466 subjects (16,750 African Americans (AA) and 39,716 European Americans (EA)). We assessed effect modification by testing an interaction term for each SNP and smoking (current vs. former/never) in the linear regression and by stratified analyses.Results: We did not observe strong evidence for interactions and only observed two interactions with p-values <0.1: for rs6548238/TMEM18, the risk allele (C) was associated with BMI only among AA females who were former/never smokers (β = 0.018, p = 0.002), vs. current smokers (β = 0.001, p = 0.95, pinteraction = 0.10). For rs9939609/FTO, the A allele was more strongly associated with BMI among current smoker EA females (β = 0.017, p = 3.5x10-5), vs. former/never smokers (β = 0.006, p = 0.05, pinteraction = 0.08).Conclusions: These analyses provide limited evidence that smoking status may modify genetic effects of previously identified genetic risk factors for BMI. Larger studies are needed to follow up our results.Clinical Trial Registration: NCT00000611.",

keywords = "Body mass index, Genetic epidemiology, Genetic risk factor, Genome-wide association study, Obesity, Smoking interactions",

author = "Fesinmeyer, {Megan D.} and North, {Kari E.} and Unhee Lim and Petra Bů{\v z}kov{\'a} and Crawford, {Dana C.} and Jeffrey Haessler and Gross, {Myron D.} and Fowke, {Jay H.} and Robert Goodloe and Love, {Shelley Ann} and Misa Graff and Carlson, {Christopher S.} and Kuller, {Lewis H.} and Matise, {Tara C.} and Hong, {Ching Ping} and Henderson, {Brian E.} and Melissa Allen and Rohde, {Rebecca R.} and Ping Mayo and Nathalie Schnetz-Boutaud and Monroe, {Kristine R.} and Ritchie, {Marylyn D.} and Prentice, {Ross L.} and Kolonel, {Lawrence N.} and Manson, {Jo Ann E.} and James Pankow and Hindorff, {Lucia A.} and Nora Franceschini and Wilkens, {Lynne R.} and Haiman, {Christopher A.} and {Le Marchand}, Loic and Ulrike Peters",

note = "Funding Information: The Population Architecture Using Genomics and Epidemiology (PAGE) program is funded by the National Human Genome Research Institute (NHGRI), supported by U01HG004803 (CALiCo), U01HG004798 (EAGLE), U01HG004802 (MEC), U01HG004790 (WHI), and U01HG004801 (Coordinating Center), and their respective NHGRI ARRA supplements. The contents of this paper are solely the responsibility of the authors and do not necessarily represent the official views of the NIH. The complete list of PAGE members can be found at http://www.pagestudy.org. The data and materials included in this report result from a collaboration between the following studies: The {"}Epidemiologic Architecture for Genes Linked to Environment (EAGLE){"} is funded through the NHGRI PAGE program (U01HG004798-01 and its NHGRI ARRA supplement). Genotyping services for select NHANES III SNPs presented here were also provided by the Johns Hopkins University under federal contract number (N01-HV-48195) from NHLBI. The study participants derive from the National Health and Nutrition Examination Surveys (NHANES), and these studies are supported by the Centers for Disease Control and Prevention. The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention. The Multiethnic Cohort study (MEC) characterization of epidemiological architecture is funded through the NHGRI PAGE program (U01HG004802 and its NHGRI ARRA supplement). The MEC study is funded through the National Cancer Institute (R37CA54281, R01 CA63, P01CA33619, U01CA136792, and U01CA98758). Funding support for the “Epidemiology of putative genetic variants: The Women{\textquoteright}s Health Initiative” study is provided through the NHGRI PAGE program (U01HG004790 and its NHGRI ARRA supplement). The WHI program is funded by the National Heart, Lung, and Blood Institute; NIH; and U.S. Department of Health and Human Services through contracts N01WH22110, 24152, 32100–2, 32105–6, 32108–9, 32111–13, 32115, 32118–32119, 32122, 42107–26, 42129–32, and 44221. The authors thank the WHI investigators and staff for their dedication, and the study participants for making the program possible. A full listing of WHI investigators can be found at: http:// www.whiscience.org/publications/ WHI_investigators_shortlist.pdf. Funding support for the Genetic Epidemiology of Causal Variants Across the Life Course (CALiCo) program was provided through the NHGRI PAGE program (U01HG004803 and its NHGRI ARRA supplement). The following studies contributed to this manuscript and are funded by the following agencies: The Atherosclerosis Risk in Communities (ARIC) Study is carried out as a collaborative study supported by National Heart, Lung, and Blood Institute contracts N01-HC-55015, N01-HC-55016, N01-HC-55018, N01-HC-55019, N01-HC-55020, N01-HC-55021, N01-HC-55022. The Coronary Artery Risk Development in Young Adults (CARDIA) study is supported by the following National Institutes of Health, National Heart, Lung and Blood Institute contracts: N01-HC-95095; N01-HC-48047; N01-HC-48048; N01-HC-48049; N01-HC-48050; N01-HC-45134; N01-HC-05187; and N01-HC-45205. The Cardiovascular Health Study (CHS) is supported by contracts HHSN268201200036C, N01-HC-85239, N01-HC-85079 through N01-HC-85086, N01-HC-35129, N01 HC-15103, N01 HC-55222, N01-HC-75150, N01-HC-45133, and grant HL080295 from the National Heart, Lung, and Blood Institute (NHLBI), with additional contribution from the National Institute of Neurological Disorders and Stroke (NINDS). Additional support was provided through AG-023629, AG-15928, AG-20098, and AG-027058 from the National Institute on Aging (NIA). The Strong Heart Study (SHS) is supported by NHLBI grants U01 HL65520, U01 HL41642, U01 HL41652, U01 HL41654, and U01 HL65521. The opinions expressed in this paper are those of the author(s) and do not necessarily reflect the views of the Indian Health Service. Assistance with phenotype harmonization, SNP selection and annotation, data cleaning, data management, integration and dissemination, and general study coordination was provided by the PAGE Coordinating Center (U01HG004801-01 and its NHGRI ARRA supplement). The National Institutes of Mental Health also contributes to the support for the Coordinating Center.",

year = "2013",

month = jan,

day = "11",

doi = "10.1186/1471-2350-14-6",

language = "English (US)",

volume = "14",

journal = "BMC Medical Genetics",

issn = "1471-2350",

publisher = "BioMed Central",

number = "1",

}

TY - JOUR

T1 - Effects of smoking on the genetic risk of obesity

T2 - The population architecture using genomics and epidemiology study

AU - Fesinmeyer, Megan D.

AU - North, Kari E.

AU - Lim, Unhee

AU - Bůžková, Petra

AU - Crawford, Dana C.

AU - Haessler, Jeffrey

AU - Gross, Myron D.

AU - Fowke, Jay H.

AU - Goodloe, Robert

AU - Love, Shelley Ann

AU - Graff, Misa

AU - Carlson, Christopher S.

AU - Kuller, Lewis H.

AU - Matise, Tara C.

AU - Hong, Ching Ping

AU - Henderson, Brian E.

AU - Allen, Melissa

AU - Rohde, Rebecca R.

AU - Mayo, Ping

AU - Schnetz-Boutaud, Nathalie

AU - Monroe, Kristine R.

AU - Ritchie, Marylyn D.

AU - Prentice, Ross L.

AU - Kolonel, Lawrence N.

AU - Manson, Jo Ann E.

AU - Pankow, James

AU - Hindorff, Lucia A.

AU - Franceschini, Nora

AU - Wilkens, Lynne R.

AU - Haiman, Christopher A.

AU - Le Marchand, Loic

AU - Peters, Ulrike

N1 - Funding Information: The Population Architecture Using Genomics and Epidemiology (PAGE) program is funded by the National Human Genome Research Institute (NHGRI), supported by U01HG004803 (CALiCo), U01HG004798 (EAGLE), U01HG004802 (MEC), U01HG004790 (WHI), and U01HG004801 (Coordinating Center), and their respective NHGRI ARRA supplements. The contents of this paper are solely the responsibility of the authors and do not necessarily represent the official views of the NIH. The complete list of PAGE members can be found at http://www.pagestudy.org. The data and materials included in this report result from a collaboration between the following studies: The "Epidemiologic Architecture for Genes Linked to Environment (EAGLE)" is funded through the NHGRI PAGE program (U01HG004798-01 and its NHGRI ARRA supplement). Genotyping services for select NHANES III SNPs presented here were also provided by the Johns Hopkins University under federal contract number (N01-HV-48195) from NHLBI. The study participants derive from the National Health and Nutrition Examination Surveys (NHANES), and these studies are supported by the Centers for Disease Control and Prevention. The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention. The Multiethnic Cohort study (MEC) characterization of epidemiological architecture is funded through the NHGRI PAGE program (U01HG004802 and its NHGRI ARRA supplement). The MEC study is funded through the National Cancer Institute (R37CA54281, R01 CA63, P01CA33619, U01CA136792, and U01CA98758). Funding support for the “Epidemiology of putative genetic variants: The Women’s Health Initiative” study is provided through the NHGRI PAGE program (U01HG004790 and its NHGRI ARRA supplement). The WHI program is funded by the National Heart, Lung, and Blood Institute; NIH; and U.S. Department of Health and Human Services through contracts N01WH22110, 24152, 32100–2, 32105–6, 32108–9, 32111–13, 32115, 32118–32119, 32122, 42107–26, 42129–32, and 44221. The authors thank the WHI investigators and staff for their dedication, and the study participants for making the program possible. A full listing of WHI investigators can be found at: http:// www.whiscience.org/publications/ WHI_investigators_shortlist.pdf. Funding support for the Genetic Epidemiology of Causal Variants Across the Life Course (CALiCo) program was provided through the NHGRI PAGE program (U01HG004803 and its NHGRI ARRA supplement). The following studies contributed to this manuscript and are funded by the following agencies: The Atherosclerosis Risk in Communities (ARIC) Study is carried out as a collaborative study supported by National Heart, Lung, and Blood Institute contracts N01-HC-55015, N01-HC-55016, N01-HC-55018, N01-HC-55019, N01-HC-55020, N01-HC-55021, N01-HC-55022. The Coronary Artery Risk Development in Young Adults (CARDIA) study is supported by the following National Institutes of Health, National Heart, Lung and Blood Institute contracts: N01-HC-95095; N01-HC-48047; N01-HC-48048; N01-HC-48049; N01-HC-48050; N01-HC-45134; N01-HC-05187; and N01-HC-45205. The Cardiovascular Health Study (CHS) is supported by contracts HHSN268201200036C, N01-HC-85239, N01-HC-85079 through N01-HC-85086, N01-HC-35129, N01 HC-15103, N01 HC-55222, N01-HC-75150, N01-HC-45133, and grant HL080295 from the National Heart, Lung, and Blood Institute (NHLBI), with additional contribution from the National Institute of Neurological Disorders and Stroke (NINDS). Additional support was provided through AG-023629, AG-15928, AG-20098, and AG-027058 from the National Institute on Aging (NIA). The Strong Heart Study (SHS) is supported by NHLBI grants U01 HL65520, U01 HL41642, U01 HL41652, U01 HL41654, and U01 HL65521. The opinions expressed in this paper are those of the author(s) and do not necessarily reflect the views of the Indian Health Service. Assistance with phenotype harmonization, SNP selection and annotation, data cleaning, data management, integration and dissemination, and general study coordination was provided by the PAGE Coordinating Center (U01HG004801-01 and its NHGRI ARRA supplement). The National Institutes of Mental Health also contributes to the support for the Coordinating Center.

PY - 2013/1/11

Y1 - 2013/1/11

N2 - Background: Although smoking behavior is known to affect body mass index (BMI), the potential for smoking to influence genetic associations with BMI is largely unexplored.Methods: As part of the 'Population Architecture using Genomics and Epidemiology (PAGE)' Consortium, we investigated interaction between genetic risk factors associated with BMI and smoking for 10 single nucleotide polymorphisms (SNPs) previously identified in genome-wide association studies. We included 6 studies with a total of 56,466 subjects (16,750 African Americans (AA) and 39,716 European Americans (EA)). We assessed effect modification by testing an interaction term for each SNP and smoking (current vs. former/never) in the linear regression and by stratified analyses.Results: We did not observe strong evidence for interactions and only observed two interactions with p-values <0.1: for rs6548238/TMEM18, the risk allele (C) was associated with BMI only among AA females who were former/never smokers (β = 0.018, p = 0.002), vs. current smokers (β = 0.001, p = 0.95, pinteraction = 0.10). For rs9939609/FTO, the A allele was more strongly associated with BMI among current smoker EA females (β = 0.017, p = 3.5x10-5), vs. former/never smokers (β = 0.006, p = 0.05, pinteraction = 0.08).Conclusions: These analyses provide limited evidence that smoking status may modify genetic effects of previously identified genetic risk factors for BMI. Larger studies are needed to follow up our results.Clinical Trial Registration: NCT00000611.

AB - Background: Although smoking behavior is known to affect body mass index (BMI), the potential for smoking to influence genetic associations with BMI is largely unexplored.Methods: As part of the 'Population Architecture using Genomics and Epidemiology (PAGE)' Consortium, we investigated interaction between genetic risk factors associated with BMI and smoking for 10 single nucleotide polymorphisms (SNPs) previously identified in genome-wide association studies. We included 6 studies with a total of 56,466 subjects (16,750 African Americans (AA) and 39,716 European Americans (EA)). We assessed effect modification by testing an interaction term for each SNP and smoking (current vs. former/never) in the linear regression and by stratified analyses.Results: We did not observe strong evidence for interactions and only observed two interactions with p-values <0.1: for rs6548238/TMEM18, the risk allele (C) was associated with BMI only among AA females who were former/never smokers (β = 0.018, p = 0.002), vs. current smokers (β = 0.001, p = 0.95, pinteraction = 0.10). For rs9939609/FTO, the A allele was more strongly associated with BMI among current smoker EA females (β = 0.017, p = 3.5x10-5), vs. former/never smokers (β = 0.006, p = 0.05, pinteraction = 0.08).Conclusions: These analyses provide limited evidence that smoking status may modify genetic effects of previously identified genetic risk factors for BMI. Larger studies are needed to follow up our results.Clinical Trial Registration: NCT00000611.

KW - Body mass index

KW - Genetic epidemiology

KW - Genetic risk factor

KW - Genome-wide association study

KW - Obesity

KW - Smoking interactions

UR - http://www.scopus.com/inward/record.url?scp=84872156946&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84872156946&partnerID=8YFLogxK

U2 - 10.1186/1471-2350-14-6

DO - 10.1186/1471-2350-14-6

M3 - Article

C2 - 23311614

AN - SCOPUS:84872156946

SN - 1471-2350

VL - 14

JO - BMC Medical Genetics

JF - BMC Medical Genetics

IS - 1

M1 - 6

ER -

Effects of smoking on the genetic risk of obesity: The population architecture using genomics and epidemiology study

Abstract

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Keywords

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