Evidence map›Paper›PMID 30826282›Full record

ArticleThe lancet. HIV2019

Association of immunosuppression and HIV viraemia with non-Hodgkin lymphoma risk overall and by subtype in people living with HIV in Canada and the USA: a multicentre cohort study.

Raúl U Hernández-Ramírez, Li Qin, Haiqun Lin, Wendy Leyden, Romain S Neugebauer, Keri N Althoff, Chad J Achenbach, Nancy A Hessol, Gypsyamber D'Souza, Kelly A Gebo and 15 more

Open access · greenAbstract readMulticenter Study
PubMed Full text at PMC Publisher
In one paragraph

Article in The lancet. HIV, 2019. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 37 papers, 1 of them a synthesis that pooled it.

0numbers the graph read from it
0cells of the map it votes in
37citing papers in PubMed, 1 pooled it
4.1field-weighted citation impact, top 5% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

37 citing papers in PubMed, 1 synthesis or guideline pooled it, 64 citations in OpenAlex.

  1. Estimating the global burden of Epstein-Barr virus-related cancers.Journal of cancer research and clinical oncology · 2022
    Pooled it
  2. A proimmunotoxin nanodrug targeting AIDS-associated non-Hodgkin lymphoma.Journal of controlled release : official journal of the Controlled Release Society · 2026
    Article
  3. Article
  4. Review
  5. Risk of lymphoma among people with HIV in the United States, 2001-2019.Journal of the National Cancer Institute · 2025
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4 · The record

Corrections and comments

5 · Who and what money

Authors and funding

25 authors at 13 institutions in 3 countries.

Raúl U Hernández-RamírezDepartment of Chronic Disease Epidemiology, Yale School of Public Health, Yale School of Medicine, New Haven, CT, USA; Department of Biostatistics, Yale School of Public Health, Yale School of Medicine, New Haven, CT, USA. Electronic address: raul.hernandezramirez@yale.edu.
Li QinDepartment of Internal Medicine, Yale School of Medicine, New Haven, CT, USA.
Haiqun LinDepartment of Biostatistics, Yale School of Public Health, Yale School of Medicine, New Haven, CT, USA.
Wendy LeydenDivision of Research, Kaiser Permanente Northern California, Oakland, CA, USA.
Romain S NeugebauerDivision of Research, Kaiser Permanente Northern California, Oakland, CA, USA.
Keri N AlthoffDepartment of Epidemiology, Johns Hopkins University Bloomberg School of Public Health, Baltimore, MD, USA.
Chad J AchenbachDivision of Infectious Diseases, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.
Nancy A HessolDepartment of Clinical Pharmacy, University of California at San Francisco, San Francisco, CA, USA.
Gypsyamber D'SouzaDepartment of Epidemiology, Johns Hopkins University Bloomberg School of Public Health, Baltimore, MD, USA.
Kelly A GeboDepartment of Medicine, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
M John GillDepartment of Medicine, University of Calgary, Calgary, AB, Canada.
Surbhi GroverDepartment of Radiation Oncology, University of Pennsylvania Perelman School of Medicine, Philadelphia, PA, USA.
Michael A HorbergMid-Atlantic Permanente Research Institute, Kaiser Permanente Mid-Atlantic States, Rockville, MD, USA.
Jun LiEpidemiology Branch, Division of HIV/AIDS Prevention, Centers for Disease Control and Prevention, Atlanta, GA, USA.
W Christopher MathewsDepartment of Medicine, University of California San Diego, San Diego, CA, USA.
Angel M MayorRetrovirus Research Center, Universidad Central del Caribe School of Medicine, Bayamon, Puerto Rico.
Lesley S ParkStanford Center for Population Health Sciences, Stanford University School of Medicine, Palo Alto, CA, USA.
Charles S RabkinInfections and Immunoepidemiology Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD, USA.
Kate SaltersEpidemiology and Population Health, British Columbia Centre for Excellence in HIV/AIDS, Vancouver, BC, Canada.
Amy C JusticeDepartment of Health Policy and Management, Yale School of Public Health, Yale School of Medicine, New Haven, CT, USA; Department of Internal Medicine, Yale School of Medicine, New Haven, CT, USA; Research Service, Veterans Affairs Connecticut Healthcare System, West Haven, CT, USA.
Richard D MooreDepartment of Medicine, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
Eric A EngelsInfections and Immunoepidemiology Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD, USA.
Michael J SilverbergDivision of Research, Kaiser Permanente Northern California, Oakland, CA, USA.
Robert DubrowDepartment of Environmental Health Sciences, Yale School of Public Health, Yale School of Medicine, New Haven, CT, USA.
North American AIDS Cohort Collaboration on Research and Design of the International Epidemiologic Databases to Evaluate AIDS
Kaiser Permanente · USYale University · USJohns Hopkins University · USAIDS Vancouver · CANational Cancer Institute · USUniversity of California San Diego · USCenters for Disease Control and Prevention · USCentral University of the Caribbean · PRNorthwestern University · USStanford University · USUniversity of Calgary · CAUniversity of California, San Francisco · USUniversity of Pennsylvania · US

Funding

Statistical and Data Management Center (SDMC), AIDS Clinical Trials Group (ACTG)UM1AI068634 · NIAID · HARVARD UNIVERSITY D/B/A HARVARD SCHOOL OF PUBLIC HEALTH · PI Marlene Ann Cooper, Michael David Hughes · 2011 to 2026
$246.6M
WOMEN'S HEALTH AGENDAU01AI038858 · NIAID · SOCIAL AND SCIENTIFIC SYSTEMS, INC. · PI BENSON, CONSTANCE ANN · 1996 to 2008
$157.5M
AIDS Clinical Trials Group NetworkU01AI068636 · NIAID · SOCIAL AND SCIENTIFIC SYSTEMS, INC. · PI KURITZKES, DANIEL R. · 2006 to 2010
$147.1M
UCSF CLINICAL AND TRANSLATIONAL SCIENCE INSTITUTEUL1RR024131 · NCRR · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI JOHNSTON, S. CLAIBORNE · 2006 to 2011
$111.2M
University of Washington/Fred Hutch Center for AIDS ResearchP30AI027757 · NIAID · UNIVERSITY OF WASHINGTON · PI Judith Tsui · 1988 to 2026
$104.9M
Yale Clinical and Translational Science Award (U Component)UL1TR001863 · NCATS · YALE UNIVERSITY · PI John H. Krystal, LUCILA OHNO-MACHADO · 2016 to 2026
$102.9M
Unsolicited R24 for the CFAR-Network of Integrated Clinical Sciences, CNICSR24AI067039 · NIAID · UNIVERSITY OF ALABAMA AT BIRMINGHAM · PI Michael S. Saag · 2006 to 2026
$99.4M
Virology CoreP30AI027763 · NIAID · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI STEVEN Grant DEEKS · 1988 to 2026
$93.6M
Implementing a Maternal health and PRegnancy Outcomes Vision for Everyone (IMPROVE)UL1TR002378 · NCATS · EMORY UNIVERSITY · PI Andres J Garcia, Elizabeth O. Ofili · 2017 to 2026
$92.1M
Virology CoreP30AI027767 · NIAID · UNIVERSITY OF ALABAMA AT BIRMINGHAM · PI OLAF KUTSCH · 1988 to 2026
$84.1M
STATISTICAL AND DATA MANAGEMENT CENTERU01AI038855 · NIAID · HARVARD UNIVERSITY (SCH OF PUBLIC HLTH) · PI HUGHES, MICHAEL DAVID · 1996 to 2006
$78.1M
Engaging University of California Stakeholders for Biorespository ResearchUL1TR000004 · NCATS · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI GRANDIS, JENNIFER RUBIN · 2012 to 2015
$78.0M
Intramural NIH HHS Z01 CP010176Intramural NIH HHS ZIA CP010214NCATS NIH HHS KL2 TR000421NCATS NIH HHS KL2 TR002317NCATS NIH HHS UL1 TR000004NCATS NIH HHS UL1 TR000083NCATS NIH HHS UL1 TR000454NCATS NIH HHS UL1 TR001863NCATS NIH HHS UL1 TR002378NCI NIH HHS N01 CP001004NCI NIH HHS N02 CP055504NCI NIH HHS R01 CA165937NCRR NIH HHS M01 RR000052NCRR NIH HHS UL1 RR024131NEI NIH HHS K23 EY013707NEI NIH HHS U10 EY008052NEI NIH HHS U10 EY008057NEI NIH HHS U10 EY008067NHLBI NIH HHS U01 HL146194NHLBI NIH HHS U01 HL146201NHLBI NIH HHS U01 HL146203NHLBI NIH HHS U01 HL146205NHLBI NIH HHS U01 HL146242NHLBI NIH HHS U01 HL146245NIAAA NIH HHS R01 AA016893NIAAA NIH HHS U01 AA013566NIAAA NIH HHS U01 AA020790NIAAA NIH HHS U01 AA026224NIAAA NIH HHS U24 AA020794NIAID NIH HHS F31 AI124794NIAID NIH HHS K01 AI093197NIAID NIH HHS K01 AI131895NIAID NIH HHS K24 AI065298NIAID NIH HHS K24 AI118591NIAID NIH HHS P30 AI027757NIAID NIH HHS P30 AI027763NIAID NIH HHS P30 AI027767NIAID NIH HHS P30 AI036219NIAID NIH HHS P30 AI050410NIAID NIH HHS P30 AI094189NIAID NIH HHS P30 AI110527NIAID NIH HHS R24 AI067039NIAID NIH HHS R38 AI140299NIAID NIH HHS U01 AI031834NIAID NIH HHS U01 AI034989NIAID NIH HHS U01 AI034993NIAID NIH HHS U01 AI034994NIAID NIH HHS U01 AI035004NIAID NIH HHS U01 AI035039NIAID NIH HHS U01 AI035040NIAID NIH HHS U01 AI035041NIAID NIH HHS U01 AI035042NIAID NIH HHS U01 AI037613NIAID NIH HHS U01 AI037984NIAID NIH HHS U01 AI038855NIAID NIH HHS U01 AI038858NIAID NIH HHS U01 AI042590NIAID NIH HHS U01 AI068634NIAID NIH HHS U01 AI068636NIAID NIH HHS U01 AI069432NIAID NIH HHS U01 AI069434NIAID NIH HHS U01 AI069918NIAID NIH HHS U01 AI103390NIAID NIH HHS U01 AI103397NIAID NIH HHS U01 AI103401NIAID NIH HHS U01 AI103408NIAID NIH HHS UM1 AI035043NIAID NIH HHS UM1 AI068634NIAID NIH HHS UM1 AI069432NIA NIH HHS R01 AG053100NIA NIH HHS R21 AG059505NIA NIH HHS U54 AG062334NICHD NIH HHS U01 HD032632NIDA NIH HHS F31 DA037788NIDA NIH HHS K24 DA000432NIDA NIH HHS R01 DA011602NIDA NIH HHS R01 DA012568NIDA NIH HHS U01 DA036297NIDA NIH HHS U01 DA036935NIMHD NIH HHS G12 MD007583NIMHD NIH HHS U54 MD007587NIMH NIH HHS P30 MH062246
6 · The paper itself

Abstract

backgroundResearch is needed to better understand relations between immunosuppression and HIV viraemia and risk for non-Hodgkin lymphoma, a common cancer in people living with HIV. We aimed to identify key CD4 count and HIV RNA (viral load) predictors of risk for non-Hodgkin lymphoma, overall and by subtype.

methodsWe studied people living with HIV during 1996-2014 from 21 Canadian and US cohorts participating in the North American AIDS Cohort Collaboration on Research and Design. To determine key independent predictors of risk for non-Hodgkin lymphoma, we assessed associations with time-updated recent, past, cumulative, and nadir or peak measures of CD4 count and viral load, using demographics-adjusted, cohort-stratified Cox models, and we compared models using Akaike's information criterion.

findingsOf 102 131 people living with HIV during the study period, 712 people developed non-Hodgkin lymphoma. The key independent predictors of risk for overall non-Hodgkin lymphoma were recent CD4 count (ie, lagged by 6 months; <50 cells per μL vs ≥500 cells per μL, hazard ratio [HR] 3·2, 95% CI 2·2-4·7) and average viral load during a 3-year window lagged by 6 months (a cumulative measure; ≥100 000 copies per mL vs ≤500 copies per mL, HR 9·6, 95% CI 6·5-14·0). These measures were also the key predictors of risk for diffuse large B-cell lymphoma (recent CD4 count <50 cells per μL vs ≥500 cells per μL, HR 2·4, 95% CI 1·4-4·2; average viral load ≥100 000 copies per mL vs ≤500 copies per mL, HR 7·5, 95% CI 4·5-12·7). However, recent CD4 count was the sole key predictor of risk for CNS non-Hodgkin lymphoma (<50 cells per μL vs ≥500 cells per μL, HR 426·3, 95% CI 58·1-3126·4), and proportion of time viral load was greater than 500 copies per mL during the 3-year window (a cumulative measure) was the sole key predictor for Burkitt lymphoma (100% vs 0%, HR 41·1, 95% CI 9·1-186·6).

interpretationBoth recent immunosuppression and prolonged HIV viraemia have important independent roles in the development of non-Hodgkin lymphoma, with likely subtype heterogeneity. Early and sustained antiretroviral therapy to decrease HIV replication, dampen B-cell activation, and restore overall immune function is crucial for preventing non-Hodgkin lymphoma.

fundingNational Institutes of Health, Centers for Disease Control and Prevention, US Agency for Healthcare Research and Quality, US Health Resources and Services Administration, Canadian Institutes of Health Research, Ontario Ministry of Health and Long Term Care, and the Government of Alberta.

Indexed as

Immune ToleranceAdolescentAdultAgedAged, 80 and overCanadaCD4 Lymphocyte CountCohort StudiesFemaleHIV InfectionsHumansLymphoma, Non-HodgkinMaleMiddle AgedRisk AssessmentUnited States

Identifiers

PMID30826282
PMCPMC6531288
OpenAlexW2915081447

What OpenQuestion holds

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Read underepoch 390

Registered trials

None linked

Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.