Visceral Adipose Tissue Volumetrics Inform Odds of Treatment Response and Risk of Subsequent Surgery in IBD Patients Starting Antitumor Necrosis Factor Therapy

Abstract Background Data describing the effect of obesity on antitumor necrosis factor (anti-TNF) treatment response are inconsistent. Visceral adipose tissue (VAT) is a superior marker of adiposity to body mass index. However, its effect on treatment response is unclear. We aimed to evaluate the ef...

Full description

Saved in:
Bibliographic Details
Published inInflammatory bowel diseases Vol. 28; no. 5; pp. 657 - 666
Main Authors Gu, Phillip, Chhabra, Avneesh, Chittajallu, Punya, Chang, Christopher, Mendez, Denisse, Gilman, Andrew, Fudman, David I, Xi, Yin, Feagins, Linda A
Format Journal Article
LanguageEnglish
Published US Oxford University Press 04.05.2022
Subjects
Online AccessGet full text
ISSN1078-0998
1536-4844
1536-4844
DOI10.1093/ibd/izab167

Cover

Abstract Abstract Background Data describing the effect of obesity on antitumor necrosis factor (anti-TNF) treatment response are inconsistent. Visceral adipose tissue (VAT) is a superior marker of adiposity to body mass index. However, its effect on treatment response is unclear. We aimed to evaluate the effect of VAT on anti-TNF treatment response. Methods Inflammatory bowel disease (IBD) patients starting anti-TNF agents between January 1, 2009, and July 31, 2019, were included. 3-dimensional measurements of VAT volume and visceral fat index (visceral:subcutaneous adipose tissue ratio; VFI) were obtained from computed tomography (CT) scans. Subjects were categorized by predefined volume cutoffs (<1500cm3, 1500–2999cm3, ≥3000cm3) and VFI (<0.33, 0.33–0.66, ≥0.67). Primary outcomes included a composite treatment response end point at 6 and 12 months. Secondary outcomes were surgery at 6 and 12 months. Multivariable logistic regression was used to calculate adjusted odds ratio (aOR) and 95% confidence interval (CI). Results The final cohort included 176 patients. No significant differences in treatment response at 6 months was observed. At 12 months, compared with volume <1500cm3, patients with volume 1500–2999cm3 had higher odds of response (aOR, 3.52; 95% CI, 1.16–10.71; P = .023), whereas volume ≥3000cm3 did not. Compared with VFI<0.33, VFI ≥0.67 had higher odds of surgery at 6 (aOR, 48.22; 95% CI, 4.73–491.57; P = .023) and 12 months (aOR, 20.94; 95% CI, 3.14–139.67; P = .004). Post hoc analysis suggested VAT may affect drug pharmacokinetics. Conclusions We found VAT volume is associated with anti-TNF treatment response in a nondose dependent manner, and VFI may inform risk of surgery after anti-TNF initiation. If confirmed by prospective studies, VAT volumetrics are potentially useful biomarkers to inform IBD treatment decisions. Lay Summary Visceral adipose tissue volume is associated with anti-TNF treatment response in a nondose response manner. Additionally, high visceral fat index is associated with significantly increased risk of early surgery after anti-TNF initiation.
AbstractList Data describing the effect of obesity on antitumor necrosis factor (anti-TNF) treatment response are inconsistent. Visceral adipose tissue (VAT) is a superior marker of adiposity to body mass index. However, its effect on treatment response is unclear. We aimed to evaluate the effect of VAT on anti-TNF treatment response.BACKGROUNDData describing the effect of obesity on antitumor necrosis factor (anti-TNF) treatment response are inconsistent. Visceral adipose tissue (VAT) is a superior marker of adiposity to body mass index. However, its effect on treatment response is unclear. We aimed to evaluate the effect of VAT on anti-TNF treatment response.Inflammatory bowel disease (IBD) patients starting anti-TNF agents between January 1, 2009, and July 31, 2019, were included. 3-dimensional measurements of VAT volume and visceral fat index (visceral:subcutaneous adipose tissue ratio; VFI) were obtained from computed tomography (CT) scans. Subjects were categorized by predefined volume cutoffs (<1500cm3, 1500-2999cm3, ≥3000cm3) and VFI (<0.33, 0.33-0.66, ≥0.67). Primary outcomes included a composite treatment response end point at 6 and 12 months. Secondary outcomes were surgery at 6 and 12 months. Multivariable logistic regression was used to calculate adjusted odds ratio (aOR) and 95% confidence interval (CI).METHODSInflammatory bowel disease (IBD) patients starting anti-TNF agents between January 1, 2009, and July 31, 2019, were included. 3-dimensional measurements of VAT volume and visceral fat index (visceral:subcutaneous adipose tissue ratio; VFI) were obtained from computed tomography (CT) scans. Subjects were categorized by predefined volume cutoffs (<1500cm3, 1500-2999cm3, ≥3000cm3) and VFI (<0.33, 0.33-0.66, ≥0.67). Primary outcomes included a composite treatment response end point at 6 and 12 months. Secondary outcomes were surgery at 6 and 12 months. Multivariable logistic regression was used to calculate adjusted odds ratio (aOR) and 95% confidence interval (CI).The final cohort included 176 patients. No significant differences in treatment response at 6 months was observed. At 12 months, compared with volume <1500cm3, patients with volume 1500-2999cm3 had higher odds of response (aOR, 3.52; 95% CI, 1.16-10.71; P = .023), whereas volume ≥3000cm3 did not. Compared with VFI<0.33, VFI ≥0.67 had higher odds of surgery at 6 (aOR, 48.22; 95% CI, 4.73-491.57; P = .023) and 12 months (aOR, 20.94; 95% CI, 3.14-139.67; P = .004). Post hoc analysis suggested VAT may affect drug pharmacokinetics.RESULTSThe final cohort included 176 patients. No significant differences in treatment response at 6 months was observed. At 12 months, compared with volume <1500cm3, patients with volume 1500-2999cm3 had higher odds of response (aOR, 3.52; 95% CI, 1.16-10.71; P = .023), whereas volume ≥3000cm3 did not. Compared with VFI<0.33, VFI ≥0.67 had higher odds of surgery at 6 (aOR, 48.22; 95% CI, 4.73-491.57; P = .023) and 12 months (aOR, 20.94; 95% CI, 3.14-139.67; P = .004). Post hoc analysis suggested VAT may affect drug pharmacokinetics.We found VAT volume is associated with anti-TNF treatment response in a nondose dependent manner, and VFI may inform risk of surgery after anti-TNF initiation. If confirmed by prospective studies, VAT volumetrics are potentially useful biomarkers to inform IBD treatment decisions.CONCLUSIONSWe found VAT volume is associated with anti-TNF treatment response in a nondose dependent manner, and VFI may inform risk of surgery after anti-TNF initiation. If confirmed by prospective studies, VAT volumetrics are potentially useful biomarkers to inform IBD treatment decisions.
Data describing the effect of obesity on antitumor necrosis factor (anti-TNF) treatment response are inconsistent. Visceral adipose tissue (VAT) is a superior marker of adiposity to body mass index. However, its effect on treatment response is unclear. We aimed to evaluate the effect of VAT on anti-TNF treatment response. Inflammatory bowel disease (IBD) patients starting anti-TNF agents between January 1, 2009, and July 31, 2019, were included. 3-dimensional measurements of VAT volume and visceral fat index (visceral:subcutaneous adipose tissue ratio; VFI) were obtained from computed tomography (CT) scans. Subjects were categorized by predefined volume cutoffs (<1500cm3, 1500-2999cm3, ≥3000cm3) and VFI (<0.33, 0.33-0.66, ≥0.67). Primary outcomes included a composite treatment response end point at 6 and 12 months. Secondary outcomes were surgery at 6 and 12 months. Multivariable logistic regression was used to calculate adjusted odds ratio (aOR) and 95% confidence interval (CI). The final cohort included 176 patients. No significant differences in treatment response at 6 months was observed. At 12 months, compared with volume <1500cm3, patients with volume 1500-2999cm3 had higher odds of response (aOR, 3.52; 95% CI, 1.16-10.71; P = .023), whereas volume ≥3000cm3 did not. Compared with VFI<0.33, VFI ≥0.67 had higher odds of surgery at 6 (aOR, 48.22; 95% CI, 4.73-491.57; P = .023) and 12 months (aOR, 20.94; 95% CI, 3.14-139.67; P = .004). Post hoc analysis suggested VAT may affect drug pharmacokinetics. We found VAT volume is associated with anti-TNF treatment response in a nondose dependent manner, and VFI may inform risk of surgery after anti-TNF initiation. If confirmed by prospective studies, VAT volumetrics are potentially useful biomarkers to inform IBD treatment decisions.
Background Data describing the effect of obesity on antitumor necrosis factor (anti-TNF) treatment response are inconsistent. Visceral adipose tissue (VAT) is a superior marker of adiposity to body mass index. However, its effect on treatment response is unclear. We aimed to evaluate the effect of VAT on anti-TNF treatment response. Methods Inflammatory bowel disease (IBD) patients starting anti-TNF agents between January 1, 2009, and July 31, 2019, were included. 3-dimensional measurements of VAT volume and visceral fat index (visceral:subcutaneous adipose tissue ratio; VFI) were obtained from computed tomography (CT) scans. Subjects were categorized by predefined volume cutoffs (<1500cm3, 1500–2999cm3, ≥3000cm3) and VFI (<0.33, 0.33–0.66, ≥0.67). Primary outcomes included a composite treatment response end point at 6 and 12 months. Secondary outcomes were surgery at 6 and 12 months. Multivariable logistic regression was used to calculate adjusted odds ratio (aOR) and 95% confidence interval (CI). Results The final cohort included 176 patients. No significant differences in treatment response at 6 months was observed. At 12 months, compared with volume <1500cm3, patients with volume 1500–2999cm3 had higher odds of response (aOR, 3.52; 95% CI, 1.16–10.71; P = .023), whereas volume ≥3000cm3 did not. Compared with VFI<0.33, VFI ≥0.67 had higher odds of surgery at 6 (aOR, 48.22; 95% CI, 4.73–491.57; P = .023) and 12 months (aOR, 20.94; 95% CI, 3.14–139.67; P = .004). Post hoc analysis suggested VAT may affect drug pharmacokinetics. Conclusions We found VAT volume is associated with anti-TNF treatment response in a nondose dependent manner, and VFI may inform risk of surgery after anti-TNF initiation. If confirmed by prospective studies, VAT volumetrics are potentially useful biomarkers to inform IBD treatment decisions.
Abstract Background Data describing the effect of obesity on antitumor necrosis factor (anti-TNF) treatment response are inconsistent. Visceral adipose tissue (VAT) is a superior marker of adiposity to body mass index. However, its effect on treatment response is unclear. We aimed to evaluate the effect of VAT on anti-TNF treatment response. Methods Inflammatory bowel disease (IBD) patients starting anti-TNF agents between January 1, 2009, and July 31, 2019, were included. 3-dimensional measurements of VAT volume and visceral fat index (visceral:subcutaneous adipose tissue ratio; VFI) were obtained from computed tomography (CT) scans. Subjects were categorized by predefined volume cutoffs (<1500cm3, 1500–2999cm3, ≥3000cm3) and VFI (<0.33, 0.33–0.66, ≥0.67). Primary outcomes included a composite treatment response end point at 6 and 12 months. Secondary outcomes were surgery at 6 and 12 months. Multivariable logistic regression was used to calculate adjusted odds ratio (aOR) and 95% confidence interval (CI). Results The final cohort included 176 patients. No significant differences in treatment response at 6 months was observed. At 12 months, compared with volume <1500cm3, patients with volume 1500–2999cm3 had higher odds of response (aOR, 3.52; 95% CI, 1.16–10.71; P = .023), whereas volume ≥3000cm3 did not. Compared with VFI<0.33, VFI ≥0.67 had higher odds of surgery at 6 (aOR, 48.22; 95% CI, 4.73–491.57; P = .023) and 12 months (aOR, 20.94; 95% CI, 3.14–139.67; P = .004). Post hoc analysis suggested VAT may affect drug pharmacokinetics. Conclusions We found VAT volume is associated with anti-TNF treatment response in a nondose dependent manner, and VFI may inform risk of surgery after anti-TNF initiation. If confirmed by prospective studies, VAT volumetrics are potentially useful biomarkers to inform IBD treatment decisions. Lay Summary Visceral adipose tissue volume is associated with anti-TNF treatment response in a nondose response manner. Additionally, high visceral fat index is associated with significantly increased risk of early surgery after anti-TNF initiation.
Author Gilman, Andrew
Feagins, Linda A
Chhabra, Avneesh
Xi, Yin
Chang, Christopher
Mendez, Denisse
Chittajallu, Punya
Gu, Phillip
Fudman, David I
Author_xml – sequence: 1
  givenname: Phillip
  orcidid: 0000-0001-8158-6557
  surname: Gu
  fullname: Gu, Phillip
  email: phillipgu12@gmail.com
  organization: Division of Digestive and Liver Diseases, UT Southwestern, Dallas,TX, USA
– sequence: 2
  givenname: Avneesh
  surname: Chhabra
  fullname: Chhabra, Avneesh
  organization: Division of Musculoskeletal Radiology, Department of Radiology, UT Southwestern, Dallas,TX, USA
– sequence: 3
  givenname: Punya
  surname: Chittajallu
  fullname: Chittajallu, Punya
  organization: Department of Internal Medicine, UCLA, Los Angeles,CA, USA
– sequence: 4
  givenname: Christopher
  surname: Chang
  fullname: Chang, Christopher
  organization: Department of Internal Medicine, UT Southwestern, Dallas,TX, USA
– sequence: 5
  givenname: Denisse
  surname: Mendez
  fullname: Mendez, Denisse
  organization: Department of Internal Medicine, UT Southwestern, Dallas,TX, USA
– sequence: 6
  givenname: Andrew
  surname: Gilman
  fullname: Gilman, Andrew
  organization: Division of Digestive and Liver Diseases, UT Southwestern, Dallas,TX, USA
– sequence: 7
  givenname: David I
  surname: Fudman
  fullname: Fudman, David I
  organization: Division of Digestive and Liver Diseases, UT Southwestern, Dallas,TX, USA
– sequence: 8
  givenname: Yin
  surname: Xi
  fullname: Xi, Yin
  organization: Division of Musculoskeletal Radiology, Department of Radiology, UT Southwestern, Dallas,TX, USA
– sequence: 9
  givenname: Linda A
  surname: Feagins
  fullname: Feagins, Linda A
  organization: Division of Gastroenterology and Hepatology, Department of Internal Medicine, University of Texas at Austin Dell Medical School, Austin,TX, USA
BackLink https://www.ncbi.nlm.nih.gov/pubmed/34291800$$D View this record in MEDLINE/PubMed
BookMark eNp9kU1v1DAQhi1URD_gxB1ZQkJIKNSOk9g-LoXCShVF3aVXy3Hs4pLYwR-H5c_wV3G020uFkA_2eJ53NDPvKThy3mkAXmL0HiNOzm0_nNvfsscdfQJOcEu6qmFNc1TeiLIKcc6OwWmM9wjV5fBn4Jg0NccMoRPw59ZGpYMc4Wqws48abm2MWcNbP-ZJp2BVhGtnfJjg9TBE6A3cBi3TpF2CNzrO3hWRdAO8sfHnkt7kPupfeclvcrjTYQetg-sPH-E3mWz5jnCTZEjW3cGVSzblyQf4Vavgo43wUqpU4u2P0tW8ew6eGjlG_eJwn4Hvl5-2F1-qq-vP64vVVaVIw1JFaM_rlhmqWlPGlIpi1Bs9cKxMzyXhlFNlcI3ZgCnBre4JajrdIdTWqukNOQNv93Xn4EvvMYlpWcw4Sqd9jqJu24a0iHW4oK8fofc-B1e6EwR3rKa47ZpCvTpQuZ_0IOZgJxl24mH1BcB7YJk7Bm2EsqksyLsUpB0FRmKxVxR7xcHeonn3SPNQ9t_0mz3t8_xf8C8fBrZf
CitedBy_id crossref_primary_10_1186_s13244_023_01581_9
crossref_primary_10_1177_17562848231171962
crossref_primary_10_1093_ibd_izad111
crossref_primary_10_14309_ajg_0000000000001855
crossref_primary_10_1016_j_gastrohep_2025_502372
crossref_primary_10_1093_ibd_izac120
crossref_primary_10_1007_s11938_024_00453_5
crossref_primary_10_1097_MOG_0000000000001025
crossref_primary_10_1186_s41747_023_00366_5
crossref_primary_10_1053_j_gastro_2023_06_036
crossref_primary_10_1007_s00384_023_04413_w
crossref_primary_10_1007_s40259_022_00522_0
crossref_primary_10_3390_jcm11206173
crossref_primary_10_1186_s12944_023_01874_4
crossref_primary_10_1111_apt_18513
crossref_primary_10_1016_j_dld_2023_09_008
crossref_primary_10_1186_s13244_025_01930_w
crossref_primary_10_14309_ajg_0000000000002330
crossref_primary_10_1186_s13244_024_01615_w
crossref_primary_10_1002_ueg2_12334
crossref_primary_10_4240_wjgs_v16_i3_740
crossref_primary_10_1177_17562848231173331
Cites_doi 10.1016/S2213-8587(19)30084-1
10.1038/s41395-018-0104-x
10.1038/ajg.2015.233
10.2165/11599410-000000000-00000
10.1093/jnci/djz150
10.1038/ajg.2011.103
10.1136/gut.2005.082909
10.1097/MIB.0000000000000527
10.1111/apt.13243
10.1177/1060028019900660
10.1016/j.cgh.2012.06.032
10.1097/MPG.0000000000001593
10.1093/ecco-jcc/jjx187
10.3389/fmed.2020.00076
10.1016/S0016-5085(99)70552-4
10.14309/ctg.0000000000000233
10.1097/MIB.0000000000000978
10.1097/MIB.0000000000000200
10.1093/ibd/izaa214
10.1016/j.gie.2019.11.032
10.1053/j.gastro.2010.08.019
10.1093/ajcn/80.2.271
10.1136/gutjnl-2012-304189
10.1038/nrgastro.2016.181
10.1016/S2468-1253(19)30012-3
10.1111/apt.14293
10.1148/radiol.2018181432
10.1371/journal.pone.0195123
10.1259/bjr.20170968
10.1097/DCR.0000000000001074
10.1111/codi.12798
10.1259/bjr/57987644
10.15585/mmwr.mm6542a3
10.1053/j.gastro.2011.10.001
10.1016/j.cgh.2011.05.005
10.2214/AJR.10.5514
10.1093/ibd/izy278
ContentType Journal Article
Copyright The Author(s) 2021. Published by Oxford University Press on behalf of Crohn’s & Colitis Foundation. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com 2021
2021 Crohn’s & Colitis Foundation. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
The Author(s) 2021. Published by Oxford University Press on behalf of Crohn’s & Colitis Foundation. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
Copyright_xml – notice: The Author(s) 2021. Published by Oxford University Press on behalf of Crohn’s & Colitis Foundation. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com 2021
– notice: 2021 Crohn’s & Colitis Foundation. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
– notice: The Author(s) 2021. Published by Oxford University Press on behalf of Crohn’s & Colitis Foundation. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
DBID AAYXX
CITATION
CGR
CUY
CVF
ECM
EIF
NPM
3V.
7X7
7XB
88E
8FI
8FJ
8FK
ABUWG
AFKRA
BENPR
CCPQU
FYUFA
GHDGH
K9.
M0S
M1P
PHGZM
PHGZT
PJZUB
PKEHL
PPXIY
PQEST
PQQKQ
PQUKI
PRINS
7X8
DOI 10.1093/ibd/izab167
DatabaseName CrossRef
Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
ProQuest Central (Corporate)
Health & Medical Collection
ProQuest Central (purchase pre-March 2016)
Medical Database (Alumni Edition)
Hospital Premium Collection
Hospital Premium Collection (Alumni Edition)
ProQuest Central (Alumni) (purchase pre-March 2016)
ProQuest Central (Alumni)
ProQuest Central UK/Ireland
ProQuest Central
ProQuest One
Proquest Health Research Premium Collection
Health Research Premium Collection (Alumni)
ProQuest Health & Medical Complete (Alumni)
ProQuest Health & Medical Collection
Medical Database
Proquest Central Premium
ProQuest One Academic
ProQuest Health & Medical Research Collection
ProQuest One Academic Middle East (New)
ProQuest One Health & Nursing
ProQuest One Academic Eastern Edition (DO NOT USE)
ProQuest One Academic
ProQuest One Academic UKI Edition
ProQuest Central China
MEDLINE - Academic
DatabaseTitle CrossRef
MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
ProQuest One Academic Middle East (New)
ProQuest One Academic Eastern Edition
ProQuest Health & Medical Complete (Alumni)
ProQuest Central (Alumni Edition)
ProQuest One Community College
ProQuest One Health & Nursing
ProQuest Hospital Collection
Health Research Premium Collection (Alumni)
ProQuest Central China
ProQuest Hospital Collection (Alumni)
ProQuest Central
ProQuest Health & Medical Complete
ProQuest Health & Medical Research Collection
Health Research Premium Collection
ProQuest Medical Library
ProQuest One Academic UKI Edition
Health and Medicine Complete (Alumni Edition)
Health & Medical Research Collection
ProQuest Central (New)
ProQuest One Academic
ProQuest One Academic (New)
ProQuest Medical Library (Alumni)
ProQuest Central (Alumni)
MEDLINE - Academic
DatabaseTitleList MEDLINE - Academic
MEDLINE
ProQuest One Academic Middle East (New)

Database_xml – sequence: 1
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 2
  dbid: EIF
  name: MEDLINE
  url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search
  sourceTypes: Index Database
– sequence: 3
  dbid: BENPR
  name: ProQuest Central
  url: http://www.proquest.com/pqcentral?accountid=15518
  sourceTypes: Aggregation Database
DeliveryMethod fulltext_linktorsrc
Discipline Medicine
EISSN 1536-4844
EndPage 666
ExternalDocumentID 34291800
10_1093_ibd_izab167
10.1093/ibd/izab167
Genre Journal Article
GroupedDBID ---
.Z2
0R~
1OC
31~
3WU
4.4
48X
53G
5GY
5VS
5WD
66C
7O~
7X7
8-0
8-1
88E
8F7
8FI
8FJ
8UM
AAAXR
AABZA
AACZT
AAJQQ
AAKAS
AAPGJ
AAPQZ
AAPXW
AARHZ
AARTV
AAUAY
AAUQX
AAVAP
AAWDT
AAYEP
ABBUW
ABDFA
ABEJV
ABGNP
ABJNI
ABNHQ
ABOCM
ABPQP
ABPTD
ABQNK
ABUWG
ABVGC
ABWST
ABXVJ
ABXVV
ABZAD
ACDDN
ACEWG
ACFRR
ACGFO
ACGFS
ACUTJ
ACVCV
ACWDW
ACWRI
ACXNZ
ACXQS
ACYHN
ACZBC
ADBBV
ADBIZ
ADGZP
ADIPN
ADMTO
ADNBA
ADQBN
ADRTK
ADVEK
ADZCM
AEMQT
AENEX
AETBJ
AFBPY
AFFQV
AFFZL
AFKRA
AFOFC
AFTRI
AFUWQ
AFXAL
AFYAG
AFZJQ
AGINJ
AGKRT
AGMDO
AGQXC
AGUTN
AHMBA
AHMMS
AHRYX
AIJEX
AIZYK
AJAOE
AJDVS
AJEEA
AJNCP
AJNYG
ALMA_UNASSIGNED_HOLDINGS
ALXQX
APJGH
AQDSO
AQKUS
ATGXG
AVNTJ
BAYMD
BCRHZ
BENPR
BEYMZ
BOYCO
BTRTY
C45
CCPQU
CDBKE
CS3
DAKXR
DR2
DU5
E.X
E3Z
EBS
EIHJH
EJD
ENERS
EX3
F5P
FECEO
FL-
FLUFQ
FOEOM
FOTVD
FQBLK
FYUFA
GAUVT
GJXCC
H0~
H13
HMCUK
HZ~
IAO
IHR
IN~
ITC
IX1
JXSIZ
KBUDW
KOP
KSI
KSN
LAW
LH4
LW6
M1P
MBLQV
MHKGH
NNB
NOMLY
NOYVH
NU-
NVLIB
N~7
N~B
O9-
OAUYM
OBFPC
OCUKA
OCZFY
ODMLO
OIG
OJZSN
OPAEJ
ORVUJ
OVD
OWPYF
P2P
PAFKI
PQQKQ
PSQYO
QRW
ROL
ROX
RUSNO
RX1
S4S
TEORI
TMA
UKHRP
V2E
W99
WOQ
WOW
XV2
Y6R
YAYTL
YKOAZ
YXANX
ZFV
AAYXX
AHGBF
AJBYB
CITATION
PHGZM
PHGZT
PJZUB
PPXIY
PUEGO
AGORE
CGR
CUY
CVF
ECM
EIF
NPM
3V.
7XB
8FK
K9.
PKEHL
PQEST
PQUKI
PRINS
7X8
ID FETCH-LOGICAL-c348t-37b9258f7c5f002ac710bfed91cfb9a39797cf1218d17315eb3046e60052c4bf3
IEDL.DBID BENPR
ISSN 1078-0998
1536-4844
IngestDate Thu Oct 02 11:24:30 EDT 2025
Tue Oct 07 06:05:22 EDT 2025
Mon Jul 21 05:46:54 EDT 2025
Wed Oct 01 05:10:35 EDT 2025
Thu Apr 24 22:58:59 EDT 2025
Wed Apr 02 07:09:39 EDT 2025
IsPeerReviewed true
IsScholarly true
Issue 5
Keywords anti-tumor necrosis factor
ulcerative colitis
inflammatory bowel disease
Crohn’s disease
visceral adipose tissue
Language English
License This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/pages/standard-publication-reuse-rights)
https://academic.oup.com/pages/standard-publication-reuse-rights
2021 Crohn’s & Colitis Foundation. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c348t-37b9258f7c5f002ac710bfed91cfb9a39797cf1218d17315eb3046e60052c4bf3
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 14
content type line 23
ORCID 0000-0001-8158-6557
PMID 34291800
PQID 3168271564
PQPubID 996336
PageCount 10
ParticipantIDs proquest_miscellaneous_2554350861
proquest_journals_3168271564
pubmed_primary_34291800
crossref_citationtrail_10_1093_ibd_izab167
crossref_primary_10_1093_ibd_izab167
oup_primary_10_1093_ibd_izab167
ProviderPackageCode CITATION
AAYXX
PublicationCentury 2000
PublicationDate 2022-05-04
PublicationDateYYYYMMDD 2022-05-04
PublicationDate_xml – month: 05
  year: 2022
  text: 2022-05-04
  day: 04
PublicationDecade 2020
PublicationPlace US
PublicationPlace_xml – name: US
– name: England
– name: Baltimore
PublicationTitle Inflammatory bowel diseases
PublicationTitleAlternate Inflamm Bowel Dis
PublicationYear 2022
Publisher Oxford University Press
Publisher_xml – name: Oxford University Press
References Uko (2022092311482008600_CIT0017) 2014; 20
Lim (2022092311482008600_CIT0032) 2020; 11
Peyrin-Biroulet (2022092311482008600_CIT0027) 2015; 110
Lee (2022092311482008600_CIT0038) 2018; 91
Wong (2022092311482008600_CIT0037) 2021; 27
Rosario (2022092311482008600_CIT0035) 2015; 42
Brill (2022092311482008600_CIT0005) 2012; 51
Singh (2022092311482008600_CIT0006) 2017; 14
Eder (2022092311482008600_CIT0013) 2019; 8:628
Brown (2022092311482008600_CIT0031) 2020; 112
El-Serag (2022092311482008600_CIT0030) 2014; 63
Desreumaux (2022092311482008600_CIT0011) 1999; 117
Blitman (2022092311482008600_CIT0025) 2011; 197
Bryant (2022092311482008600_CIT0034) 2019; 25
Weston (2022092311482008600_CIT0039) 2019; 290
Coffey (2022092311482008600_CIT0023) 2018; 12
Yanai (2022092311482008600_CIT0001) 2011; 106
Singh (2022092311482008600_CIT0007) 2018; 13
Nam (2022092311482008600_CIT0029) 2010; 139
Van Der Sloot (2022092311482008600_CIT0015) 2017; 23
Klopfenstein (2022092311482008600_CIT0024) 2012; 85
Meserve (2022092311482008600_CIT0036) 2020; 7
Ding (2022092311482008600_CIT0021) 2017; 46
Satsangi (2022092311482008600_CIT0026) 2006; 55
Dai (2022092311482008600_CIT0009) 2020; 54
Büning (2022092311482008600_CIT0014) 2015; 21
Molodecky (2022092311482008600_CIT0003) 2012; 142
Kennedy (2022092311482008600_CIT0033) 2019; 4
Neeland (2022092311482008600_CIT0010) 2019; 7
Li (2022092311482008600_CIT0019) 2015; 17
Shen (2022092311482008600_CIT0020) 2018; 61
Frivolt (2022092311482008600_CIT0018) 2017; 65
Fried (2022092311482008600_CIT0012) 1998; 83
Singh (2022092311482008600_CIT0008) 2018; 113
Shen (2022092311482008600_CIT0022) 2004; 80
Limdi (2022092311482008600_CIT0028) 2020; 91
Dahlhamer (2022092311482008600_CIT0002) 2016; 65
Ordás (2022092311482008600_CIT0004) 2012; 10
Erhayiem (2022092311482008600_CIT0016) 2011; 9
References_xml – volume: 7
  start-page: 715
  year: 2019
  ident: 2022092311482008600_CIT0010
  article-title: Visceral and ectopic fat, atherosclerosis, and cardiometabolic disease: a position statement
  publication-title: Lancet Diabetes Endocrinol.
  doi: 10.1016/S2213-8587(19)30084-1
– volume: 113
  start-page: 883
  year: 2018
  ident: 2022092311482008600_CIT0008
  article-title: Obesity and response to infliximab in patients with inflammatory bowel diseases: pooled analysis of individual participant data from clinical trials
  publication-title: Am J Gastroenterol.
  doi: 10.1038/s41395-018-0104-x
– volume: 110
  start-page: 1324
  year: 2015
  ident: 2022092311482008600_CIT0027
  article-title: Selecting therapeutic targets in inflammatory bowel disease (STRIDE): determining therapeutic goals for treat-to-target
  publication-title: Am J Gastroenterol.
  doi: 10.1038/ajg.2015.233
– volume: 51
  start-page: 277
  year: 2012
  ident: 2022092311482008600_CIT0005
  article-title: Impact of obesity on drug metabolism and elimination in adults and children
  publication-title: Clin Pharmacokinet.
  doi: 10.2165/11599410-000000000-00000
– volume: 112
  start-page: 377
  year: 2020
  ident: 2022092311482008600_CIT0031
  article-title: The association of abdominal adiposity with mortality in patients with stage I-III colorectal cancer
  publication-title: J Natl Cancer Inst.
  doi: 10.1093/jnci/djz150
– volume: 106
  start-page: 685
  year: 2011
  ident: 2022092311482008600_CIT0001
  article-title: Assessing response and loss of response to biological therapies in IBD
  publication-title: Am J Gastroenterol.
  doi: 10.1038/ajg.2011.103
– volume: 8:628
  year: 2019
  ident: 2022092311482008600_CIT0013
  article-title: The role of adipose tissue in the pathogenesis and therapeutic outcomes of inflammatory bowel disease
  publication-title: Cells
– volume: 55
  start-page: 749
  year: 2006
  ident: 2022092311482008600_CIT0026
  article-title: The Montreal classification of inflammatory bowel disease: controversies, consensus, and implications
  publication-title: Gut.
  doi: 10.1136/gut.2005.082909
– volume: 21
  start-page: 2590
  year: 2015
  ident: 2022092311482008600_CIT0014
  article-title: Visceral adipose tissue in patients with Crohn’s disease correlates with disease activity, inflammatory markers, and outcome
  publication-title: Inflamm Bowel Dis.
  doi: 10.1097/MIB.0000000000000527
– volume: 42
  start-page: 188
  year: 2015
  ident: 2022092311482008600_CIT0035
  article-title: Population pharmacokinetics-pharmacodynamics of vedolizumab in patients with ulcerative colitis and Crohn’s disease
  publication-title: Aliment Pharmacol Ther.
  doi: 10.1111/apt.13243
– volume: 54
  start-page: 729
  year: 2020
  ident: 2022092311482008600_CIT0009
  article-title: Associations between obesity and the effectiveness of anti-tumor necrosis factor-α agents in inflammatory bowel disease patients: a literature review and meta-analysis
  publication-title: Ann Pharmacother.
  doi: 10.1177/1060028019900660
– volume: 10
  start-page: 1079
  year: 2012
  ident: 2022092311482008600_CIT0004
  article-title: Therapeutic drug monitoring of tumor necrosis factor antagonists in inflammatory bowel disease
  publication-title: Clin Gastroenterol Hepatol.
  doi: 10.1016/j.cgh.2012.06.032
– volume: 65
  start-page: 633
  year: 2017
  ident: 2022092311482008600_CIT0018
  article-title: Increase of intra-abdominal adipose tissue in pediatric Crohn disease
  publication-title: J Pediatr Gastroenterol Nutr.
  doi: 10.1097/MPG.0000000000001593
– volume: 12
  start-page: 1139
  year: 2018
  ident: 2022092311482008600_CIT0023
  article-title: Inclusion of the mesentery in ileocolic resection for Crohn’s disease is associated with reduced surgical recurrence
  publication-title: J Crohns Colitis.
  doi: 10.1093/ecco-jcc/jjx187
– volume: 83
  start-page: 847
  year: 1998
  ident: 2022092311482008600_CIT0012
  article-title: Omental and subcutaneous adipose tissues of obese subjects release interleukin-6: depot difference and regulation by glucocorticoid
  publication-title: J Clin Endocrinol Metab.
– volume: 7
  start-page: 76
  year: 2020
  ident: 2022092311482008600_CIT0036
  article-title: Predicting response to vedolizumab in inflammatory bowel disease
  publication-title: Front Med (Lausanne).
  doi: 10.3389/fmed.2020.00076
– volume: 117
  start-page: 73
  year: 1999
  ident: 2022092311482008600_CIT0011
  article-title: Inflammatory alterations in mesenteric adipose tissue in Crohn’s disease
  publication-title: Gastroenterology.
  doi: 10.1016/S0016-5085(99)70552-4
– volume: 11
  start-page: e00233
  year: 2020
  ident: 2022092311482008600_CIT0032
  article-title: The effect of adiposity on anti-tumor necrosis factor-alpha levels and loss of response in Crohn’s disease patients
  publication-title: Clin Transl Gastroenterol.
  doi: 10.14309/ctg.0000000000000233
– volume: 23
  start-page: 82
  year: 2017
  ident: 2022092311482008600_CIT0015
  article-title: Visceral adiposity, genetic susceptibility, and risk of complications among individuals with Crohn’s disease
  publication-title: Inflamm Bowel Dis.
  doi: 10.1097/MIB.0000000000000978
– volume: 20
  start-page: 2286
  year: 2014
  ident: 2022092311482008600_CIT0017
  article-title: Impact of abdominal visceral adipose tissue on disease outcome in pediatric Crohn’s disease
  publication-title: Inflamm Bowel Dis.
  doi: 10.1097/MIB.0000000000000200
– volume: 27
  start-page: 848
  year: 2021
  ident: 2022092311482008600_CIT0037
  article-title: Body mass index does not impact clinical efficacy of ustekinumab in Crohn’s disease: a post hoc analysis of the IM-UNITI trial
  publication-title: Inflamm Bowel Dis.
  doi: 10.1093/ibd/izaa214
– volume: 91
  start-page: 733
  year: 2020
  ident: 2022092311482008600_CIT0028
  article-title: A review of endoscopic scoring systems and their importance in a treat-to-target approach in inflammatory bowel disease (with videos)
  publication-title: Gastrointest Endosc.
  doi: 10.1016/j.gie.2019.11.032
– volume: 139
  start-page: 1902
  year: 2010
  ident: 2022092311482008600_CIT0029
  article-title: Abdominal visceral adipose tissue volume is associated with increased risk of erosive esophagitis in men and women
  publication-title: Gastroenterology
  doi: 10.1053/j.gastro.2010.08.019
– volume: 80
  start-page: 271
  year: 2004
  ident: 2022092311482008600_CIT0022
  article-title: Visceral adipose tissue: relations between single-slice areas and total volume
  publication-title: Am J Clin Nutr.
  doi: 10.1093/ajcn/80.2.271
– volume: 63
  start-page: 220
  year: 2014
  ident: 2022092311482008600_CIT0030
  article-title: Visceral abdominal obesity measured by CT scan is associated with an increased risk of Barrett’s oesophagus: a case-control study
  publication-title: Gut.
  doi: 10.1136/gutjnl-2012-304189
– volume: 14
  start-page: 110
  year: 2017
  ident: 2022092311482008600_CIT0006
  article-title: Obesity in IBD: epidemiology, pathogenesis, disease course and treatment outcomes
  publication-title: Nat Rev Gastroenterol Hepatol.
  doi: 10.1038/nrgastro.2016.181
– volume: 4
  start-page: 341
  year: 2019
  ident: 2022092311482008600_CIT0033
  article-title: Predictors of anti-TNF treatment failure in anti-TNF-naive patients with active luminal Crohn’s disease: a prospective, multicentre, cohort study
  publication-title: Lancet Gastroenterol Hepatol.
  doi: 10.1016/S2468-1253(19)30012-3
– volume: 46
  start-page: 883
  year: 2017
  ident: 2022092311482008600_CIT0021
  article-title: The body composition profile is associated with response to anti-TNF therapy in Crohn’s disease and may offer an alternative dosing paradigm
  publication-title: Aliment Pharmacol Ther.
  doi: 10.1111/apt.14293
– volume: 290
  start-page: 669
  year: 2019
  ident: 2022092311482008600_CIT0039
  article-title: Automated abdominal segmentation of CT scans for body composition analysis using deep learning
  publication-title: Radiology.
  doi: 10.1148/radiol.2018181432
– volume: 13
  start-page: e0195123
  year: 2018
  ident: 2022092311482008600_CIT0007
  article-title: Obesity and response to anti-tumor necrosis factor-α agents in patients with select immune-mediated inflammatory diseases: a systematic review and meta-analysis
  publication-title: Plos One.
  doi: 10.1371/journal.pone.0195123
– volume: 91
  start-page: 20170968
  year: 2018
  ident: 2022092311482008600_CIT0038
  article-title: Fully automated segmentation and quantification of visceral and subcutaneous fat at abdominal CT: application to a longitudinal adult screening cohort
  publication-title: Br J Radiol.
  doi: 10.1259/bjr.20170968
– volume: 61
  start-page: 706
  year: 2018
  ident: 2022092311482008600_CIT0020
  article-title: Visceral fat is associated with mucosal healing of infliximab treatment in Crohn’s disease
  publication-title: Dis Colon Rectum.
  doi: 10.1097/DCR.0000000000001074
– volume: 17
  start-page: 225
  year: 2015
  ident: 2022092311482008600_CIT0019
  article-title: Visceral fat area is associated with a high risk for early postoperative recurrence in Crohn’s disease
  publication-title: Colorectal Dis.
  doi: 10.1111/codi.12798
– volume: 85
  start-page: e826
  year: 2012
  ident: 2022092311482008600_CIT0024
  article-title: Comparison of 3 T MRI and CT for the measurement of visceral and subcutaneous adipose tissue in humans
  publication-title: Br J Radiol.
  doi: 10.1259/bjr/57987644
– volume: 65
  start-page: 1166
  year: 2016
  ident: 2022092311482008600_CIT0002
  article-title: Prevalence of inflammatory bowel disease among adults aged ≥18 years—United States, 2015
  publication-title: MMWR Morb Mortal Wkly Rep.
  doi: 10.15585/mmwr.mm6542a3
– volume: 142
  start-page: 46
  year: 2012
  ident: 2022092311482008600_CIT0003
  article-title: Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review
  publication-title: Gastroenterology.
  doi: 10.1053/j.gastro.2011.10.001
– volume: 9
  start-page: 684
  year: 2011
  ident: 2022092311482008600_CIT0016
  article-title: Ratio of visceral to subcutaneous fat area is a biomarker of complicated Crohn’s disease
  publication-title: Clin Gastroenterol Hepatol.
  doi: 10.1016/j.cgh.2011.05.005
– volume: 197
  start-page: 482
  year: 2011
  ident: 2022092311482008600_CIT0025
  article-title: Feasibility of using single-slice MDCT to evaluate visceral abdominal fat in an urban pediatric population
  publication-title: AJR Am J Roentgenol.
  doi: 10.2214/AJR.10.5514
– volume: 25
  start-page: 592
  year: 2019
  ident: 2022092311482008600_CIT0034
  article-title: Visceral adipose tissue is associated with stricturing crohn’s disease behavior, fecal calprotectin, and quality of life
  publication-title: Inflamm Bowel Dis.
  doi: 10.1093/ibd/izy278
SSID ssj0020209
Score 2.5014682
Snippet Abstract Background Data describing the effect of obesity on antitumor necrosis factor (anti-TNF) treatment response are inconsistent. Visceral adipose tissue...
Data describing the effect of obesity on antitumor necrosis factor (anti-TNF) treatment response are inconsistent. Visceral adipose tissue (VAT) is a superior...
Background Data describing the effect of obesity on antitumor necrosis factor (anti-TNF) treatment response are inconsistent. Visceral adipose tissue (VAT) is...
SourceID proquest
pubmed
crossref
oup
SourceType Aggregation Database
Index Database
Enrichment Source
Publisher
StartPage 657
SubjectTerms Body fat
Body Mass Index
Humans
Inflammatory bowel disease
Inflammatory Bowel Diseases - drug therapy
Inflammatory Bowel Diseases - surgery
Intra-Abdominal Fat - diagnostic imaging
Necrosis
Prospective Studies
Risk Factors
Surgery
Tumor Necrosis Factor Inhibitors - therapeutic use
Title Visceral Adipose Tissue Volumetrics Inform Odds of Treatment Response and Risk of Subsequent Surgery in IBD Patients Starting Antitumor Necrosis Factor Therapy
URI https://www.ncbi.nlm.nih.gov/pubmed/34291800
https://www.proquest.com/docview/3168271564
https://www.proquest.com/docview/2554350861
Volume 28
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
journalDatabaseRights – providerCode: PRVPQU
  databaseName: ProQuest Central
  customDbUrl: http://www.proquest.com/pqcentral?accountid=15518
  eissn: 1536-4844
  dateEnd: 99991231
  omitProxy: true
  ssIdentifier: ssj0020209
  issn: 1078-0998
  databaseCode: BENPR
  dateStart: 19960201
  isFulltext: true
  titleUrlDefault: https://www.proquest.com/central
  providerName: ProQuest
– providerCode: PRVPQU
  databaseName: ProQuest Health & Medical Complete
  customDbUrl:
  eissn: 1536-4844
  dateEnd: 99991231
  omitProxy: true
  ssIdentifier: ssj0020209
  issn: 1078-0998
  databaseCode: 7X7
  dateStart: 19960201
  isFulltext: true
  titleUrlDefault: https://search.proquest.com/healthcomplete
  providerName: ProQuest
– providerCode: PRVWIB
  databaseName: Wiley Online Library - Core collection (SURFmarket)
  issn: 1078-0998
  databaseCode: DR2
  dateStart: 19950101
  customDbUrl:
  isFulltext: true
  eissn: 1536-4844
  dateEnd: 99991231
  omitProxy: false
  ssIdentifier: ssj0020209
  providerName: Wiley-Blackwell
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV1La9tAEB4SB0ovpenTeXUKORWELWllSYcSnIdJC3GDcYJvYl8KoonkRvbv6V_tjFZyKC25SewioZnV7MzOzPcBHKuAQaiE9FSYSk_YYeRJ6QtPGBXHvsqNTbgb-Wo6urwR3xfRYgumXS8Ml1V2NrEx1KbSfEY-YIKlIGZok5PlL49Zozi72lFoyJZawXxtIMa2YSdgZKwe7JxeTK9nmxBs6Io-KObhpH-atB17FNYPCmUGXEjlN5TzT3vUX31v_7ifzTY0eQ2vWv8Rx07hu7Blyzfw4qrNkL-F37dFrfmcCcemWFa1xXkjWrxtzBDj8dfoepDwhzE1VjnOu2JznLmKWYuyNDgr6p88zLalKbhe0WXTRI1Fid9Oz_HagbLWSC4roxHc4Zi7ftcP1SNOLX9cUeOkYfTBuYMveAc3k4v52aXXkjB4OhTJigyQSoMoyWMd5SRAqcklUbk1qa9zlUpOC8Y6J2Enxo9DP6LgnEJuO-LzZi1UHr6HXlmV9iNgaI0QufJlqgIh1TDVYTiiXVQxDB0Zmz586cSe6RahnIky7jOXKQ8z0lHW6qgPx5vJSwfM8f9pn0h_z8846HSbtf9vnT2ttj583gw_sAbvuQi5WtcZBWPka1JI6Pfhg1sTm_eEtM3zR-09__B9eBlwOwUXUIoD6K0e1_aQnJyVOoLteBEfteuX7s5nwR_r9QAu
linkProvider ProQuest
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV3LbtNAFB2VVgI2iDeBQi9S2SBZiT3jOF5UKKWNEtqEKnKr7sy8jCxaO9SJEF_Dn_Bt3GuPUyFQd91Z8mgs-47vY-accxnbVQGJUAnpKR5LT9he6EnpC08YFUW-yowdEBt5OuuPT8Wn8_B8g_1uuTAEq2x9Yu2oTalpj7xLDZaCiKRNPiy-e9Q1ik5X2xYa0rVWMHu1xJgjdhzZnz-whKv2Jgdo73dBMDpMPo4912XA01wMlviHqTgIB1mkwwzdg9QYc1VmTezrTMWSzr0infkYCo0fcT_E6hNrStunDVUtVMZx3jtsS3ARY_G3tX84O5mvS75eAzLBGotABvHAMQR7Me_mynQJuOXXLe6vY-JfPLt_0t067I0esgcuX4Vhs8AesQ1bPGZ3p-5E_gn7dZZXmva1YGjyRVlZSGpTwlnt9kj_v4KG8wSfjamgzCBpwe0wbxC6FmRhYJ5X3-g2-bIa4L3Ey5q0DXkBk_0DOGlEYCvAFJnUD77CkFjGq8vyCmaWXi6vYFR3EIKkkUt4yk5vxRzP2GZRFvYFA26NEJnyZawCIVUv1pz3MWorkr1D59Zh79vPnmqniE6NOS7S5mSep2ij1Nmow3bXgxeNEMj_h-2g_W4esd3aNnX-okqvV3eHvV3fviQLXhDouVxVKRZ_mNtiCep32PNmTayfwzGtoJd6efPkO-zeOJkep8eT2dErdj8gKgeBN8U221xerexrTLCW6o1bxcC-3PaP8wdSVTq2
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Visceral+Adipose+Tissue+Volumetrics+Inform+Odds+of+Treatment+Response+and+Risk+of+Subsequent+Surgery+in+IBD+Patients+Starting+Antitumor+Necrosis+Factor+Therapy&rft.jtitle=Inflammatory+bowel+diseases&rft.au=Gu%2C+Phillip&rft.au=Chhabra%2C+Avneesh&rft.au=Chittajallu%2C+Punya&rft.au=Chang%2C+Christopher&rft.date=2022-05-04&rft.issn=1078-0998&rft.eissn=1536-4844&rft.volume=28&rft.issue=5&rft.spage=657&rft.epage=666&rft_id=info:doi/10.1093%2Fibd%2Fizab167&rft.externalDBID=n%2Fa&rft.externalDocID=10_1093_ibd_izab167
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1078-0998&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1078-0998&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1078-0998&client=summon