Cited by 72Viral-associated cancers and disordersHIV/AIDS Research and InterventionsCervical Cancer and HPV Research

The burden of cancers associated with HIV in the South African public health sector, 2004–2014: a record linkage study

Open access
Dhokotera, Tafadzwa, Bohlius, Julia, Spoerri, Adrian, Egger, Matthias, Ncayiyana, Jabulani, Olago, Victor, Singh, Elvira, Sengayi, Mazvita·2019·Infectious Agents and Cancer

Abstract

INTRODUCTION: The impact of South Africa's high human immunodeficiency virus (HIV) burden on cancer risk is not fully understood, particularly in the context of antiretroviral treatment (ART) availability. We examined national cancer trends and excess cancer risk in people living with HIV (PLHIV) compared to those who are HIV-negative. METHODS: We used probabilistic record linkage to match cancer records provided by the National Cancer Registry to HIV data provided by the National Health Laboratory Service (NHLS). We also used text search of specific HIV terms from the clinical section of pathology reports to determine HIV status of cancer patients. We used logistic and Joinpoint regression models to evaluate the risk and trends in cancers in PLHIV compared to HIV-negative patients from 2004 to 2014. In sensitivity analysis, we used inverse probability weighting (IPW) to correct for possible selection bias. RESULTS: = 30,486) with a known status were HIV-positive. PLHIV were at higher risk of AIDS-defining cancers (Kaposi sarcoma [adjusted OR:134, 95% CI:111-162], non-Hodgkin lymphoma [adjusted OR:2.73, 95% CI:2.56-2.91] and, cervix [adjusted OR:1.70, 95% CI:1.63-1.77], conjunctival cancer [adjusted OR:21.5, 95% CI:16.3-28.4] and human papilloma virus (HPV) related cancers (including; penis [adjusted OR:2.35, 95% CI:1.85-2.99], and vulva [adjusted OR:1.94, 95% CI:1.67-2.25]) compared to HIV-negative patients. Analysis using the IPW population yielded comparable results. CONCLUSION: There is need for improved awareness and screening of conjunctival cancer and HPV-associated cancers at HIV care centres. Further research and discussion is warranted on inclusive HPV vaccination in PLHIV.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1186/s13027-019-0228-7

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Women living with HIV face a six-to-tenfold increased risk of cervical cancer compared to HIV-negative women.

    “Women living with HIV (WLHIV) face an almost six-to-ten-fold increased risk of cervical cancer compared to HIV-negative women [8–10].”

    From HPV Screening in Women Living with HIV (WLHIV) in Karnataka, India: Can it be Integrated into ART Centres? (2025) · cites this paper as [9]

    The Results (Table 2; page unavailable) report a higher cervical-cancer association among people living with HIV, but the adjusted odds ratio is 1.70 (95% CI 1.63–1.77), not six- to tenfold. The paper also reports odds, rather than a six- to tenfold increase in risk. (LLM, conf=0.90)

    Checked by a reasoning model — may be wrong.

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 29

  1. [3]Shisana O Rhele T Simbayi LC Zuma K Jooste S Zungu N South African national HIV prevalence, incidence and behaviour survey 2012 27002359
  2. [4]Dal Maso L Polesel J Serraino D Lise M Piselli P Falcini F Russo A Intrieri T Vercelli M Zambon P Tagliabue G Zanetti R Federico M Limina R M Mangone L De Lisi V Stracci F Ferretti S Piffer S Budroni M Donato A Giacomin A Bellù F Fusco M Madeddu A Vitarelli S Tessandori R Tumino R Suligoi B Franceschi S Pattern of cancer risk in persons with AIDS in Italy in the HAART era British Journal of Cancer 2009 100 5 840 847 10.1038/sj.bjc.6604923 19223894 PMC2653754 · DOI
  3. [5]Silverberg MJ Chao C Leyden WA Xu L Horberg MA Klein D HIV infection, immunodeficiency, viral replication, and the risk of cancer Cancer Epidemiol Biomark Prev 2011 20 2551 2559 10.1158/1055-9965.EPI-11-0777 PMC3237725 22109347 · DOI
  4. [6]Crum-Cianflone N Hullsiek KH Marconi V Weintrob A Ganesan A Barthel RV Trends in the incidence of cancers among HIV-infected persons and the impact of antiretroviral therapy: a 20-year cohort study AIDS. 2009 23 41 50 10.1097/QAD.0b013e328317cc2d 19050385 PMC2727153 · DOI
  5. [7]Albini L Calabresi A Gotti D Ferraresi A Festa A Donato F Burden of non-AIDS-defining and non-virus-related cancers among HIV-infected patients in the combined antiretroviral therapy era AIDS Res Hum Retrovir 2013 29 1097 1104 10.1089/aid.2012.0321 23581483 · DOI
  6. [8]Grulich AE van Leeuwen MT Falster MO Vajdic CM Incidence of cancers in people with HIV/AIDS compared with immunosuppressed transplant recipients: a meta-analysis Lancet. 2007 370 59 67 10.1016/S0140-6736(07)61050-2 17617273 · DOI
  7. [9]Bedimo RJ McGinnis KA Dunlap M Rodriguez-Barradas MC Justice AC Incidence of non-AIDS-defining malignancies in HIV-infected versus noninfected patients in the HAART era: impact of immunosuppression J Acquir Immune Defic Syndr 2009 52 203 208 10.1097/QAI.0b013e3181b033ab 19617846 PMC2814969 · DOI
  8. [10]Dryden-Peterson Scott Medhin Heluf Kebabonye-Pusoentsi Malebogo Seage George R. Suneja Gita Kayembe Mukendi K. A. Mmalane Mompati Rebbeck Timothy Rider Jennifer R. Essex Myron Lockman Shahin Cancer Incidence following Expansion of HIV Treatment in Botswana PLOS ONE 2015 10 8 e0135602 10.1371/journal.pone.0135602 26267867 PMC4534370 · DOI
  9. [11]Rohner E Valeri F Maskew M Prozesky H Rabie H Garone D Incidence rate of Kaposi sarcoma in HIV-infected patients on antiretroviral therapy in southern Africa JAIDS J Acquir Immune Defic Syndr 2014 67 547 554 10.1097/QAI.0000000000000360 25393941 PMC4231535 · DOI
  10. [12]Mbulaiteye Sam M. Katabira Elly T. Wabinga Henry Parkin Donald M. Virgo Phillip Ochai Robert Workneh Meklit Coutinho Alex Engels Eric A. Spectrum of cancers among HIV-infected persons in Africa: The Uganda AIDS-Cancer Registry Match Study International Journal of Cancer 2005 118 4 985 990 10.1002/ijc.21443 16106415 · DOI
  11. [13]Sengayi M Babb C Egger M Urban MI HIV testing and burden of HIV infection in black cancer patients in Johannesburg, South Africa: a cross-sectional study BMC Cancer 2015 15 144 10.1186/s12885-015-1171-7 25884599 PMC4434805 · DOI
  12. [14]Sengayi MM Kielkowski D Egger M Dreosti L Bohlius J Survival of patients with Kaposi’s sarcoma in the South African antiretroviral treatment era: a retrospective cohort study South African Med J 2017 107 871 10.7196/SAMJ.2017.v107i10.12362 PMC5913753 29022531 · DOI
  13. [17]Blecher M, Kollipara A, DeJager P, Zulu N. Health Financing. In: Padarath A, English R, editors. South African Health Review. 10th edition. Health Systems Trust; 2011. http://www.hst.org.za/publications/south-african-health-review-2011. Accessed 17 Feb 2018.
  14. [18]Harpaz Rave Callahan Alison Tamang Suzanne Low Yen Odgers David Finlayson Sam Jung Kenneth LePendu Paea Shah Nigam H. Text Mining for Adverse Drug Events: the Promise, Challenges, and State of the Art Drug Safety 2014 37 10 777 790 10.1007/s40264-014-0218-z 25151493 PMC4217510 · DOI
  15. [19]Bouvard V Baan R Straif K Grosse Y Secretan B Ghissassi F El, et al. a review of human carcinogens—part B: biological agents Lancet Oncol 2009 10 321 322 10.1016/S1470-2045(09)70096-8. 19350698 · DOI · Paper page
  16. [20]Newson Roger B. Attributable and Unattributable Risks and Fractions and other Scenario Comparisons The Stata Journal: Promoting communications on statistics and Stata 2013 13 4 672 698 10.1177/1536867X1301300402 · DOI
  17. [21]Stein L Urban MI O’Connell D Yu XQ Beral V Newton R The spectrum of human immunodeficiency virus-associated cancers in a South African black population: results from a case-control study, 1995-2004 Int J Cancer 2008 122 2260 2265 10.1002/ijc.23391 18241034 · DOI
  18. [24]Meyer-Rath G Johnson LF Pillay Y Blecher M Brennan AT Long L Changing the south African national antiretroviral therapy guidelines: the role of cost modelling PLoS One 2017 12 e0186557 10.1371/journal.pone.0186557 29084275 PMC5662079 · DOI
  19. [25]Hernández-Ramírez Raúl U Shiels Meredith S Dubrow Robert Engels Eric A Cancer risk in HIV-infected people in the USA from 1996 to 2012: a population-based, registry-linkage study The Lancet HIV 2017 4 11 e495 e504 10.1016/S2352-3018(17)30125-X 28803888 PMC5669995 · DOI
  20. [26]Sitas F. Newton R. Kaposi's Sarcoma in South Africa JNCI Monographs 2000 2000 28 1 4 10.1093/oxfordjournals.jncimonographs.a024250 11158199 · DOI
  21. [28]Shiels Meredith S. Pfeiffer Ruth M. Gail Mitchell H. Hall H. Irene Li Jianmin Chaturvedi Anil K. Bhatia Kishor Uldrick Thomas S. Yarchoan Robert Goedert James J. Engels Eric A. Cancer Burden in the HIV-Infected Population in the United States JNCI: Journal of the National Cancer Institute 2011 103 9 753 762 10.1093/jnci/djr076 21483021 PMC3086877 · DOI
  22. [29]Sasco AJ Jaquet A Boidin E Ekouevi DK Thouillot F Lemabec T The challenge of AIDS-related malignancies in sub-Saharan Africa PLoS One 2010 5 e8621 10.1371/journal.pone.0008621 20066157 PMC2799672 · DOI
  23. [30]Adler DH Wallace M Bennie T Mrubata M Abar B Meiring TL Cervical dysplasia and high-risk human papillomavirus infections among HIV-infected and HIV-uninfected adolescent females in South Africa Infect Dis Obstet Gynecol 2014 2014 498048 10.1155/2014/498048 25389377 PMC4217359 · DOI
  24. [31]Chokunonga E Borok MZ Chirenje ZM Nyakabau AM Parkin DM Trends in the incidence of cancer in the black population of Harare, Zimbabwe 1991-2010 Int J Cancer 2013 133 721 729 10.1002/ijc.28063 23364833 · DOI
  25. [32]Crum-Cianflone N Hullsiek KH Satter E Marconi V Weintrob A Ganesan A Cutaneous malignancies among HIV-infected persons Arch Intern Med 2009 169 1130 10.1001/archinternmed.2009.104 19546414 PMC2761839 · DOI
  26. [33]Lanoy E Costagliola D Engels EA Skin cancers associated with HIV infection and solid-organ transplantation among elderly adults Int J Cancer 2010 126 1724 1731 10.1002/ijc.24931 19810102 PMC2818159 · DOI
  27. [34]Bohlius J Valeri F Maskew M Prozesky H Garone D Sengayi M Kaposi’s sarcoma in HIV-infected patients in South Africa: multicohort study in the antiretroviral therapy era Int J Cancer 2014 135 2644 2652 10.1002/ijc.28894 24729433 PMC4415728 · DOI
  28. [35]Dandapani SV Eaton M Thomas CR Pagnini PG HIV- positive anal cancer: an update for the clinician J Gastrointest Oncol 2010 1 34 44 10.3978/j.issn.2078-6891.2010.005 22811803 PMC3397564 · DOI
  29. [36]Wong EY Jordan WC Malebranche DJ DeLaitsch LL Abravanel R Bermudez A HIV testing practices among black primary care physicians in the United States BMC Public Health 2013 13 96 10.1186/1471-2458-13-96 23375193 PMC3599058 · DOI

Cited by

Sorted by citations

Authors
Dhokotera, T., Bohlius, J., Spoerri, A., Egger, M., Ncayiyana, J., Olago, V., Singh, E., & Sengayi, M.
Affiliations
  • National Health Laboratory Service (ZA)
  • University of Bern (CH)
  • University of Cape Town (ZA)
Corresponding author
Dhokotera, Tafadzwa
Venue
Infectious Agents and Cancer
Published
2019-05-03
Volume
14
Issue
1
Pages
12-12
ISSN
1750-9378 (ISSN-L)
OpenAlex
W2944332154
Cited by
72
References
1
Citations by year
2026: 4 · 2025: 6 · 2024: 14 · 2023: 11 · 2022: 15 · 2021: 12 · 2020: 9 · 2018: 1
FWCI
3.76
Type
journal article
Language
en
Open access
Locations
  • Infectious Agents and Cancer (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Bern Open Repository and Information System (University of Bern) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Open University of Cape Town (University of Cape Town) (submittedVersion)
  • Open Access CRIS of the University of Bern
Funders
  • CRDF Global (DAA3-16-62705-1)
  • National Institutes of Health (U01AI069924-09,)
  • Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (320030_169967)
Topics
  • Health Sciences › Medicine › Oncology › Viral-associated cancers and disorders
  • Health Sciences › Medicine › Infectious Diseases › HIV/AIDS Research and Interventions
  • Health Sciences › Medicine › Epidemiology › Cervical Cancer and HPV Research
Keywords
HIV-associated cancer, people living with HIV, AIDS-defining cancers, Kaposi's sarcoma, non-Hodgkin lymphoma, cervical cancer, HPV-associated cancers, penile cancer, vulvar cancer, cancer incidence trends, antiretroviral therapy, South Africa

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review