CoChat
Sign Up
Cited by 27Cervical Cancer and HPV ResearchHead and Neck Cancer StudiesReproductive tract infections research

Human Papillomavirus Genotype Distribution in Invasive Cervical Cancer in Pakistan

Open access
Loya, Asif, Serrano, Beatriz, Rasheed, Farah, Tous, Sara, Hassan, Mariam, Clavero, Omar, Raza, Muhammad, De Sanjosé, Silvia +2 more·2016·Cancers
DOI 10.3390/cancers8080072PMC PMC4999781
Open this paper in CoChat — free accountOpen PDF

Abstract

Few studies have assessed the burden of human papillomavirus (HPV) infection in Pakistan. We aim to provide specific information on HPV-type distribution in invasive cervical cancer (ICC) in the country. A total of 280 formalin-fixed paraffin-embedded tissue blocks were consecutively selected from Shaukat Khanum Memorial Cancer Hospital and Research Centre (Lahore, Pakistan). HPV-DNA was detected by SPF10 broad-spectrum PCR followed by DNA enzyme immunoassay and genotyping by LiPA25. HPV-DNA prevalence was 87.5% (95%CI: 83.0–91.1), with 96.1% of cases histologically classified as squamous cell carcinoma. Most of the HPV-DNA positive cases presented single infections (95.9%). HPV16 was the most common type followed by HPV18 and 45. Among HPV-DNA positive, a significantly higher contribution of HPV16/18 was detected in Pakistan (78.4%; 72.7–83.3), compared to Asia (71.6%; 69.9–73.4) and worldwide (70.8%; 69.9–71.8) and a lower contribution of HPVs31/33/45/52/58 (11.1%; 7.9–15.7 vs. 19.8%; 18.3–21.3 and 18.5%; 17.7–19.3). HPV18 or HPV45 positive ICC cases were significantly younger than cases infected by HPV16 (mean age: 43.3, 44.4, 50.5 years, respectively). A routine cervical cancer screening and HPV vaccination program does not yet exist in Pakistan; however, the country could benefit from national integrated efforts for cervical cancer prevention and control. Calculated estimations based on our results show that current HPV vaccine could potentially prevent new ICC cases.

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 · 10.3390/cancers8080072

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?

  • The potential impact of the nonavalent vaccine in Asia and worldwide is 91.5% and 89.5%, respectively.

    “The potential impact of the nonavalent vaccine in Asia and worldwide are 91.5 and 89.5% respectively [44].”

    From HPV Genotypes distribution in Indian women with and without cervical carcinoma: Implication for HPV vaccination program in Odisha, Eastern India (2017) · cites this paper as [44]

    The Results (§2.2; page unavailable) estimate that HPV types covered by the nonavalent vaccine account for 91.4% of invasive cervical cancer cases in Asia and 89.3% worldwide. This supports the claimed potential impact in substance, but neither cited percentage—91.5% or 89.5%—matches the paper. (LLM, conf=0.88)

    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: 27

  1. [2]De Martel C. Ferlay J. Franceschi S. Vignat J. Bray F. Forman D. Plummer M. Global burden of cancers attributable to infections in 2008: A review and synthetic analysis Lancet Oncol. 2012 13 607 615 10.1016/S1470-2045(12)70137-7 22575588 · DOI
  2. [3]IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. A Review of Human Carcinogens. Part B: Biological Agents, Volume 100 International Agency for Research on Cancer Lyon, France 2011 Available online: http://monographs.iarc.fr/ENG/Monographs/vol100B/mono100B.pdf (accessed on 15 February 2016)
  3. [4]Castellsagué X. Díaz M. de Sanjosé S. Muñoz N. Herrero R. Franceschi S. Peeling R.W. Ashley R. Smith J.S. Snijders P.J.F. Worldwide human papillomavirus etiology of cervical adenocarcinoma and its cofactors: Implications for screening and prevention J. Natl. Cancer Inst. 2006 98 303 315 16507827
  4. [5]Walboomers J.M. Jacobs M.V. Manos M.M. Bosch F.X. Kummer J.A. Shah K.V. Snijders P.J.F. Peto J. Meijer C.J.L.M. Muñoz N. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide J. Pathol. 1999 189 12 19 10.1002/(SICI)1096-9896(199909)189:1<12::AID-PATH431>3.0.CO;2-F 10451482 · DOI
  5. [6]Li N. Franceschi S. Howell-Jones R. Snijders P.J.F. Clifford G.M. Human papillomavirus type distribution in 30,848 invasive cervical cancers worldwide: Variation by geographical region, histological type and year of publication Int. J. Cancer. 2011 128 927 935 10.1002/ijc.25396 20473886 · DOI
  6. [7]De Sanjose S. Quint W.G. Alemany L. Geraets D.T. Klaustermeier J.E. Lloveras B. Tous S. Felix A. Bravo L.E. Shin H.R. Human papillomavirus genotype attribution in invasive cervical cancer: A retrospective cross-sectional worldwide study Lancet Oncol. 2010 11 1048 1056 10.1016/S1470-2045(10)70230-8 20952254 · DOI · Paper page
  7. [8]Guan P. Howell-Jones R. Li N. Bruni L. de Sanjosé S. Franceschi S. Clifford G.M. Human papillomavirus types in 115,789 HPV-positive women: A meta-analysis from cervical infection to cancer Int. J. Cancer. 2012 131 2349 2359 10.1002/ijc.27485 22323075 · DOI · Paper page
  8. [10]Gul S. Murad S. Javed A. Prevalence of High risk Human Papillomavirus in cervical dysplasia and cancer samples from twin cities in Pakistan Int. J. Infect. Dis. 2015 34 14 19 10.1016/j.ijid.2015.02.018 25725135 · DOI · Paper page
  9. [11]Siddiqa A. Zainab M. Qadri I. Bhatti M.F. Parish J.L. Prevalence and genotyping of high risk human papillomavirus in cervical cancer samples from Punjab, Pakistan Viruses 2014 6 2762 2777 10.3390/v6072762 25036463 PMC4113792 · DOI · Paper page
  10. [12]Raza S.A. Franceschi S. Pallardy S. Malik F.R. Avan B.I. Zafar A. Pervez S. Serajuddaula S. Snijders P.J.F. van Kemenade F.J. Human papillomavirus infection in women with and without cervical cancer in Karachi, Pakistan Br. J. Cancer 2010 102 1657 1660 10.1038/sj.bjc.6605664 20407442 PMC2883157 · DOI · Paper page
  11. [13]Yousuf S. Syed S. Moazzam A. Lucky M.H. Frequency of high risk human papillomavirus types in squamous cell carcinoma of cervix among women J. Pak. Med. Assoc. 2010 60 193 196 20225776
  12. [14]Khan S. Jaffer N.N. Khan M.N. Rai M.A. Shafiq M. Ali A. Pervez S. Khan N. Aziz A. Ali S.H. Human papillomavirus subtype 16 is common in Pakistani women with cervical carcinoma Int. J. Infect. Dis. 2007 11 313 317 10.1016/j.ijid.2006.06.007 17291804 · DOI · Paper page
  13. [15]Sancho-Garnier H. Khazraji Y.C. Cherif M.H. Mahnane A. Hsairi M. El Shalakamy A. Osgulg N. Tuncerg M. Jumaanh A.O. Seoudi M. Overview of cervical cancer screening practices in the extended Middle East and North Africa countries Vaccine 2013 31 G51 G57 10.1016/j.vaccine.2012.06.046 24331820 · DOI
  14. [17]Torre L.A. Bray F. Siegel R.L. Ferlay J. Lortet-Tieulent J. Jemal A. Global cancer statistics, 2012 CA Cancer J. Clin. 2015 65 87 108 10.3322/caac.21262 25651787 · DOI
  15. [19]Arbyn M. Ronco G. Anttila A. Meijer C.J.L.M. Poljak M. Ogilvie G. Koliopoulos G. Naucler P. Sankaranarayanan R. Peto J. Evidence regarding human papillomavirus testing in secondary prevention of cervical cancer Vaccine 2012 30 F88 F99 10.1016/j.vaccine.2012.06.095 23199969 · DOI · Paper page
  16. [23]Shepherd J.P. Frampton G.K. Harris P. Interventions for encouraging sexual behaviours intended to prevent cervical cancer Cochrane Database Syst. Rev. 2011 13 CD001035 21491379 PMC4040418
  17. [24]Badar F. Anwar N. Vaccination against human papillomavirus for prevention of cervix uteri cancer in Pakistan—A public health perspective and debate J. Ayub Med. Coll. Abbottabad. 2011 23 186 24800378
  18. [25]Insinga R.P. Liaw K.L. Johnson L.G. Madeleine M.M. A systematic review of the prevalence and attribution of human papillomavirus types among cervical, vaginal, and vulvar precancers and cancers in the United States Cancer Epidemiol. Biomarkers Prev. 2008 17 1611 1622 10.1158/1055-9965.EPI-07-2922 18628412 PMC2587113 · DOI
  19. [26]Wentzensen N. Schiffman M. Dunn T. Zuna R.E. Gold M.A. Allen R.A. Zhang R. Sherman M.E. Wacholder S. Walker J. Multiple human papillomavirus genotype infections in cervical cancer progression in the study to understand cervical cancer early endpoints and determinants Int. J. Cancer 2009 125 2151 2158 10.1002/ijc.24528 19585494 PMC2755508 · DOI
  20. [27]Serrano B. Alemany L. Tous S. Bruni L. Clifford G.M. Weiss T. Bosch F.X. de Sanjosé S. Potential impact of a nine-valent vaccine in human papillomavirus related cervical disease Infect. Agents Cancer 2012 7 38 10.1186/1750-9378-7-38 23273245 PMC3554470 · DOI · Paper page
  21. [28]Safaeian M. Schiffman M. Gage J. Solomon D. Wheeler C.M. Castle P.E. Detection of precancerous cervical lesions is differential by human papillomavirus type Cancer Res. 2009 69 3262 3266 10.1158/0008-5472.CAN-08-4192 19351830 PMC3155840 · DOI
  22. [29]Bhurgri Y. Nazir K. Shaheen Y. Usman A. Faridi N. Bhurgri H. Kayani N. Pervez S. Hasan S.H. Setna F. Patho-epidemiology of Cancer Cervix in Karachi South Asian Pac. J. Cancer Prev. 2007 8 357 362 18159967
  23. [31]Goldie S.J. O’Shea M. Diaz M. Kim S.Y. Benefits, cost requirements and cost-effectiveness of the HPV16,18 vaccine for cervical cancer prevention in developing countries: Policy implications Reprod. Health Matters 2008 16 86 96 10.1016/S0968-8080(08)32409-4 19027626 · DOI
  24. [33]Brown D.R. Kjaer S.K. Sigurdsson K. Iversen O.E. Hernandez-Avila M. Wheeler C.M. Perez G. Koutsky L.A. Tay E.H. Garcia P. The impact of quadrivalent human papillomavirus (HPV; types 6, 11, 16, and 18) L1 virus-like particle vaccine on infection and disease due to oncogenic non vaccine HPV types in generally HPV-naive women aged 16–26 years J. Infect. Dis. 2009 199 926 935 10.1086/597307 19236279 · DOI
  25. [34]Wheeler C.M. Castellsagué X. Garland S.M. Szarewski A. Paavonen J. Naud P. Salmerón J. Chow S.N. Apter D. Kitchener H. Cross-protective efficacy of HPV-16/18 AS04-adjuvanted vaccine against cervical infection and precancer caused by non-vaccine oncogenic HPV types: 4-year end-of-study analysis of the randomised, double-blind PATRICIA trial Lancet Oncol. 2012 13 100 110 10.1016/S1470-2045(11)70287-X 22075170 · DOI
  26. [35]Malagón T. Drolet M. Boily M.C. Franco E.L. Jit M. Brisson J. Brisson M. Cross-protective efficacy of two human papillomavirus vaccines: A systematic review and meta-analysis Lancet Infect. Dis. 2012 12 781 789 10.1016/S1473-3099(12)70187-1 22920953 · DOI
  27. [37]Alemany L. Saunier M. Alvarado-Cabrero I. Quirós B. Salmeron J. Shin H.R. Pirog E.C. Guimerà N. Hernandez-Suarez G. Felix A. Human papillomavirus DNA prevalence and type distribution in anal carcinomas worldwide Int. J. Cancer 2015 136 98 107 10.1002/ijc.28963 24817381 PMC4270372 · DOI

Cited by

Sorted by citations

Authors
Loya, A., Serrano, B., Rasheed, F., Tous, S., Hassan, M., Clavero, O., Raza, M., De Sanjosé, S., Bosch, F., & Alemany, L.
Affiliations
  • Shaukat Khanum Memorial Cancer Hospital and Research Center (PK)
  • Institut d'Investigació Biomédica de Bellvitge (ES)
  • Department of Pathology, Shaukat Khanum Memorial Cancer Hospital and Research Centre Lahore, Punjab 54000, Pakistan
  • Unit of Infections and Cancer (UNIC), Cancer Epidemiology Research Programme, Catalan Institute of Oncology (ICO)–IDIBELL, L’Hospitalet de Llobregat, Gran Via de l’Hospitalet, 199-203, 08908 L’Hospitalet de Llobregat, Barcelona, Spain; CIBER Epidemiología y Salud Pública (CIBERESP). Madrid, Spain
Corresponding author
Alemany, Laia
ORCID
Venue
Cancers
Publisher
MDPI AG
Published
2016-07-30
Volume
8
Issue
8
Pages
72
ISSN
2072-6694 (ISSN-L)
DOI
10.3390/cancers8080072
PMC
PMC4999781
OpenAlex
W2491786767
Cited by
27
References
1
Citations by year
2026: 2 · 2025: 1 · 2024: 6 · 2023: 2 · 2022: 2 · 2021: 3 · 2020: 2 · 2019: 3 · 2018: 1 · 2017: 5
FWCI
2.81
Type
journal article
Language
en
Open access
Licence
Locations
  • Cancers (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • RECERCAT (Consorci de Serveis Universitaris de Catalunya) (publishedVersion, other-oa)
  • Dipòsit Digital de la Universitat de Barcelona (Universitat de Barcelona) (submittedVersion, cc-by)
Funders
  • Eli Lilly and Company
  • Agència de Gestió d'Ajuts Universitaris i de Recerca (RTIC RD06/0020/0095, RCESP C03/09, RTICESP C03/10, 2005SGR00695, RD12/0036/0056, 2009SGR126, 2014SGR1077)
  • Instituto de Salud Carlos III (RD06/0020, C03/09, FIS PI061246, C03/10, PI030240, PI061246, RD12/0036/0056), RCESP C03/09, 051530, FIS PI030240, 2005SGR00695, RTIC RD06/0020/0095, Marató de TV3, RTICESP C03/10)
Topics
  • Health Sciences › Medicine › Epidemiology › Cervical Cancer and HPV Research
  • Health Sciences › Medicine › Otorhinolaryngology › Head and Neck Cancer Studies
  • Life Sciences › Immunology and Microbiology › Microbiology › Reproductive tract infections research
Keywords
human papillomavirus, HPV genotypes, invasive cervical cancer, HPV16, HPV 18, HPV45, squamous cell carcinoma, HPV prevalence, cervical cancer screening, HPV vaccination, cervical cancer prevention, Pakistan

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