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  Table of Contents  
Year : 2021  |  Volume : 58  |  Issue : 3  |  Page : 317-325

Screening for cervical cancer in HIV-infected women: A review of literature

1 Department of Obstetrics and Gynecology, Deenanath Mangeshkar Hospital and Research Center, Pune, Maharashtra, India
2 Department of Research, Deenanath Mangeshkar Hospital and Research Center, Pune, Maharashtra, India

Date of Submission11-Oct-2019
Date of Decision13-Jul-2020
Date of Acceptance26-Sep-2020
Date of Web Publication07-Aug-2021

Correspondence Address:
Veena G Rahatgaonkar
Deenanath Mangeshkar Hospital and Research Center, Pune, Maharashtra
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ijc.IJC_888_19

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 » Abstract 

Globally, the cervical cancer burden is huge, more so in low-resource countries. Human immunodeficiency virus (HIV) infection increases a woman's risk of human papillomavirus (HPV) infection and cervical cancer. There is a lack of opportunistic, as well as, organized cervical cancer screening structure for HIV-positive women. A large proportion of women have invasive cervical cancer as their initial acquired immune deficiency syndrome (AIDS)-defining illness. There is an especially high-incidence in countries where there are no organized cervical cancer prevention programs. Additionally, there are cultural, social, psychological, and system barriers that women living with HIV have to overcome when accessing healthcare services. We believe that educating women and healthcare providers regarding the need for screening, early detection, and treatment is as important as bringing about a systematic change in healthcare services to improve participation of HIV-positive women in screening for cervical cancer.

Keywords: Cervical cancer, HIV infection, review, screening

How to cite this article:
Rahatgaonkar VG, Deshpande AA, Oka GA. Screening for cervical cancer in HIV-infected women: A review of literature. Indian J Cancer 2021;58:317-25

How to cite this URL:
Rahatgaonkar VG, Deshpande AA, Oka GA. Screening for cervical cancer in HIV-infected women: A review of literature. Indian J Cancer [serial online] 2021 [cited 2022 Sep 26];58:317-25. Available from:

 » Introduction Top

Cervical cancer is the fourth leading cause of female cancer in the world and the second most frequent cancer among women in India.[1],[2] Cervical cancer is a major contributing factor to mortality and morbidity in women.[1] Globally, the cervical cancer burden is huge, more so in low-resource countries. In the World Health Organization (WHO)-Institut Catala d'Oncologia (ICO) 2017 report on human papillomavirus (HPV) and related diseases, the standardized incidence rate of cervical cancer globally was reported as 14 per 100,000 populations. The incidence was lower at 9.9 for developed countries but as high as 15.7 in the less-developed countries. The standardized mortality rate of cervical cancer per 100,000 populations globally was 6.8, being 3.3 in developed and 8.3 in less developed countries.[1] As per the GLOBOCAN 2008 report, more than 85% of the global burden of cervical cancer cases and 87% of deaths due to cervical cancer have occurred in less-developed countries.[3],[4] Ten years later, these numbers have changed to 83% and 89% respectively, according to GLOBOCAN 2018.[5] Also, as per the same report, cervical cancer contributed to 9.23% of all cases of cancer incidence and 8.35% of all cancer deaths.[4],[6]

Biologically, HIV infection increases a woman's risk of HPV infection and cervical cancer.[1],[7] Although globally, new HIV infections have decreased (from 2.2 million in 2010 to 2.1 million in 2015), the burden of HIV infection is still high. Worldwide, there are an estimated 36.7 million people living with HIV.[8] A similar trend has been observed in India. In 2015, the total number of people living with HIV in India was estimated at 21.17 lakh with a decline in new HIV infections by 66% as compared to the year 2000. According to the same report, two-fifths (40.5%) of the total HIV infections were among females.[9] The global distribution of country-specific HIV prevalence matches the global distribution of cervical cancer incidence and mortality.[4],[10] More than half of the HIV-infected individuals are women and girls. In sub-Saharan Africa, more women than men are living with HIV.[11] In India, the disease burden among females in the age group 15–49 years is as high as in males. HIV prevalence estimated as per the National AIDS Control Organization (NACO) report of 2015 was 0.3% among males and 0.22% among females. In India, efforts of the NAC Program have been successful in reducing overall HIV incidence in the different states of the country by 32 to 50% during 2007 to 2015.[9] Although HIV prevalence was estimated at 0.31% in the general population, the proportion of HIV-positive women among the total reported HIV cases in India increased from 25% in 2001 to 39% in 2009.[9] The incidence of HPV infection and cervical cancerous and precancerous lesions among HIV-infected women is high. In the United States and Western Europe, women with HIV/AIDS have significantly higher rates of cervical cancer than women in the general population.[12] Linking the United States Agency for International Development (USAID) and Cancer Registry, the observed cervical cancer cases in HIV-infected women were up to 4-folds higher than the general population.[2] Screening for cervical cancer in HIV-positive women is extremely important due to the high burden of HIV disease in women.[9],[13],[14] Hence, prevention, early detection, and treatment of cervical neoplasia are integral components of the management of HIV-infected women.[7],[15]

 » HIV and Cervical Cancer Top

Immune-suppression is the main factor predisposing HIV-positive women to HPV infections.[16],[17] The weakened immune system due to HIV infection reduces the body's ability to fight infection with HPV leading to a high infection rate of HPV that can cause cervical cancer. Such immune-compromised women are less likely to clear cervical HPV than HIV-uninfected women.[2] In women treated with highly active antiretroviral therapy (HAART), there is a persistently high-risk of acquiring HPV infection because of impaired immune system function.[16],[17] Thus, AIDS-defining cancers like cervical cancer arise through loss of immunity against oncogenic viral infections. This fact has been proven by epidemiologic evidence.[2] Recent cohort data show a direct relationship between low CD4, T-lymphocyte cell count, and cervical cancer risk.[2],[12] Some data support that risk of cervical cancer increases with declining CD4 count.[2],[12] Cervical intraepithelial neoplasia (CIN) is more common in HIV-infected females with low CD4 count or AIDS. The use of ART did not reduce CIN rates in adolescents with perinatally or horizontally acquired HIV infection.[12] A study conducted between 2003 and 2009 in HIV-positive women in South Africa showed that women with lower CD4 counts were more likely to have abnormal Pap smears. Precancerous lesions were detected in 38% of women at the initial screening with Pap smear. These women had a median CD4 cell count of 254 cells/mm3, which was significantly lower than the median CD4 count of 351 cells/mm3 seen in women with normal Pap smear (P < 0.0001). The risk of low-grade and high-grade lesions reduced by 13% and 18%, respectively with each 100 cells/mm3 rise in CD4 cell count.[18] Similar results were seen in a study of HIV-positive women in Thailand which found that women with a CD4 count <350 cells/mm3 had a significant correlation with atypical squamous cells of undetermined significance (ASCUS) or worse cytology (P = 0.043).[19]

Cervical cancer in HIV-infected women shows the following features[4],[20],[a21]:

  1. Advanced stages at presentation
  2. Metastases in unusual locations
  3. Poor response to treatment
  4. Higher recurrence rate
  5. Shorter interval to death.

The interplay between HIV infection, HPV infection, and CIN or cervical cancer is complex.[2] HIV-related immunodeficiency is known to have an unfavorable impact on the natural history of HPV infection. It is associated with increased acquisition and persistence of HPV infection, as well as, with increased risk of precancerous lesions like CIN2 and CIN3. The decrease in cellular immunity caused by HIV increases the risk for new and persistent HPV infections, the primary cause of cervical cancers, and precancerous cervical lesions. This contributes to an accelerated incidence and progression of cervical neoplasia.[22],[23] Variations have been found in the prevalence of HPV according to geographical location, however, it is at least two folds higher among women living with HIV as compared to HIV-negative women: 62% versus 24% in sub-Saharan Africa, 30% versus 14% in Europe, and 30% versus 5% in North America.[24],[25]

Facts about the natural history of HPV infection and its progression to cervical cancer in HIV-positive women when compared with HIV-negative women[20],[25],[26]:

  1. HPV expression more common
  2. Persistence of HPV infection more common
  3. Infection by multiple types of HPV
  4. Five times more risk of progression to CIN
  5. Low cumulative incidence of the squamous intraepithelial lesion (SIL) among HIV-negative and HIV-positive women with CD4 count >500
  6. Increased risk of cervical cancer with a declining CD4 count
  7. When CD4 count >350, the incidence of SIL is similar in patients on HAART and not on HAART.

Cervical cancer: An AIDS-defining illness

A large proportion of women have invasive cervical cancer as their initial AIDS-defining illness. The role of HAART in preventing CIN recurrence post-treatment is still controversial. A systematic review published in 2015 revealed that the incidence of invasive cervical cancer does not seem to have diminished after the advent of HAART like the other two AIDS-defining malignancies, namely, Kaposi's sarcoma and non-Hodgkin's lymphoma. In fact, there is an increased risk for the development of invasive cervical cancer even after the introduction of HAART (Relative Risk [RR]: 1.46; 95% Confidence Interval [CI]: 1.09—1.94).[16] Similar findings were noted by Gingues and Gillway back in 2006.[27] Cohort studies with data of individual patients on HAART use have shown conflicting results with a reduced risk associated with HAART reported in some, but not all studies.[16] Some studies found a decrease in persistence or progression of CIN with ART.[12] A population-based registry-linkage study which evaluated a cohort of HIV-infected people from Colorado, Connecticut, Georgia, Maryland, Michigan, New Jersey, New York, Puerto Rico, and Texas from 1996 to 2012 published in Lancet HIV in 2017 has reported a significant decrease in cervical and anal cancer in both men and women with HIV on ART.[12]

Importance of cervical cancer screening in HIV-infected women

Cancer risk increases with age. The longevity of people living with HIV is growing. Thus, the burden of HIV-infected people with cancer has grown markedly.[2] The prolongation of life due to ART leads to an increased cumulative incidence of cervical cancer. The prolonged life span leads to a potentially longer duration of HPV persistence thereby increasing the epigenetic changes in carcinogenesis.[12] The elevated risk of cervical cancer in HIV-infected women is partly due to increased sexual acquisition and persistence of HPV.[4] The incidence of cervical cancer is high among HIV-infected women, particularly in countries where there are no organized cervical cancer prevention programs.[2] This is clear from the following statistics from Africa: incidence of cervical cancer was high (42.7 per 100,000 women) in Eastern Africa, a high HIV-prevalence region with low screening coverage as compared to 30.6/100,000 in Middle Africa with moderate HIV prevalence and low screening. The cervical cancer incidence was low, at 6.6/100,000 in Northern Africa, a region of low HIV prevalence and moderate screening coverage.[4],[10] As per GLOBOCAN 2018 report, the cervical cancer burden is still high (40.1/100,000 in Eastern Africa, 26.8/100,000 in Middle Africa, and 7.2/100,000 in Northern Africa) indicating the need for effective screening coverage. There is a lack of opportunistic, as well as, organized screening program among HIV-positive women.[28]

Increasing the use of HPV vaccination in adolescents and young adults may reduce the risk of HPV-associated cancers later in life in persons with HIV but, effective HPV vaccination in low-resource countries is lacking.[12] Hence, despite HPV vaccination, the role of screening in HIV-positive women for secondary prevention cannot be undermined.

Prevalence of HPV-16 and HPV-18

Globally, it has been seen that the prevalence of HPV-16 and HPV-18 is most common in cervical cancer pathogenesis. As per WHO/ICO report 2017, the prevalence of HPV-16 and 18 in low-grade squamous intraepithelial lesion (CIN I) was 25.8%, in high-grade squamous intraepithelial lesion (CIN II and III) was 51.9% and in cervical cancer was 69.4%.[1] Similarly, in India and neighboring countries of South Asia, HPV-16 and 18 have a higher prevalence in cervical pre-cancer and cancer.[29]

Infection with multiple HPV types is detected more often in HIV-infected women as compared to non-infected women with HPV types other than 16 and 18 accounting for a substantial proportion of cervical cancer in HIV-infected women. As per a meta-analysis published in 2017, data from various parts of the world, namely, Africa, Asia, Latin America, North America, and Europe showed that along with HPV-16 and 18, HPV-45 accounted for a greater proportion of HPV infections in invasive cervical cancers in HIV-positive women.[25] Another meta-analysis showed that in the United States, 12% of women living with HIV were infected with multiple HPV types. HPV-16 was the most commonly detected type, followed by HPV-58, HPV-18, HPV-52, HPV-31, and HPV-33.[24] Worldwide, the prevalence of multiple genotypes has varied widely (between 12%–87%), as reported by Mane et al. in 2012.[30] In India, limited data is available on the epidemiology of various HPV types among HIV-infected women. The study conducted by the National AIDS Research Institute (NARI), Pune and National institute of Epidemiology (NIE), Chennai regarding HPV genotype distribution in CIN lesions in HIV-infected women found that 50.7% had multiple HPV genotypes. Multiple genotypes have been found to be associated with high-risk sexual behaviors of HIV-infected women or their partners. Decreased immune response leads to the reactivation of latent HPV genotypes.[30] Infection with multiple HPV genotypes in HIV-infected women increases the risk of progression to invasive cervical cancer disease.[30]

 » Current Recommendations Top

Evidence-based cervical cancer screening strategies in HIV-positive women are still being investigated. The World Health Organization (WHO) 2006 guidelines on sexual and reproductive health for women living with HIV included cervical cancer prevention as a topic area, but not as a part of essential service for HIV-positive women.[4],[31] In 2009, WHO recommendations were made to integrate family planning, prevention of sexually transmitted infection (STI), and prevention of mother-to-child transmission, but cervical cancer was still not mentioned.[32] As research into the integration of reproductive health and HIV services evolved, more focus was placed on the provision of comprehensive care for women living with HIV in low-middle-income countries. Considering the lack of stand-alone cervical cancer prevention clinics, integration of cervical cancer prevention services into existing HIV care programs seems important. Such integration will facilitate improved access to, and uptake of, cervical cancer screening services by the high-risk population due to the reduction of visit burden and loss to follow-up. According to ACOG (American Congress of Obstetricians and Gynecologists) guidelines (2016) for the prevention and treatment of opportunistic infections in HIV-infected adults and adolescents, screening protocols have been defined for two groups of women according to age groups.[33]

Screening for women below 30 years

Cervical cytology is the primary mode of cervical cancer screening for women with HIV below the age of 30 years [Figure 1]. It is known that 20-60% of Pap smears in HIV-infected women are abnormal with 15–40% smears indicative of CIN, mostly low-grade lesions. Cytological abnormalities detected in women with HIV are 10–12 times more than in HIV-negative women. Brogly and colleagues found that 30% of female adolescents with HIV infections acquired from their mothers had an abnormality on their first Pap smear as ASCUS or greater.[12],[34] In HIV-positive women, the rate of progression of abnormalities of epithelial cells is higher.[35]
Figure 1: This algorithm is for women below 30 years

Click here to view

Screening should begin within 1 year of onset of sexual activity regardless of the mode of HIV transmission below the age of 21 years. Women with HIV aged 21 to 29 years should have a Pap test at the time of the initial diagnosis of HIV. Provided the initial Pap test for a newly diagnosed woman with HIV is normal, the next Pap test should be done in 12 months (level of evidence BII). If the results of three consecutive Pap tests done yearly are normal, follow-up Pap tests should be done every 3 years (level of evidence BII).[12],[36]

 » Abnormal Pap test results Top

If the Pap test report is ASCUS, then repeat cytology in 6–12 months is recommended. For any result equal to or greater than ASCUS on repeat cytology, referral to colposcopy is recommended (level of evidence AII). For low-grade squamous intraepithelial lesion (LSIL) (including atypical glandular cells [AGC] and high-grade squamous intraepithelial lesions (HSIL) referral to colposcopy is recommended.[12]

Screening for women above 30 years

Cervical cancer screening in women with HIV should continue throughout a woman's life and should not stop at 65 years as in the general population, as women with HIV are at high-risk of cervical cancer [Figure 2]. However, clinicians should consider other factors such as the life expectancy of the patient and the risk for developing cervical cancer at that age.[12] Screening by testing for HPV DNA has recently been introduced as a preferred method in HIV-infected women. Current guidelines from the American Cancer Society and the US Preventive Services Task Force advocate the use of HPV co-testing with cytology for screening in women above the age of 30 years. A negative HPV test predicts a prolonged low risk of cancer. In women with negative co-testing, a prolonged screening interval can be allowed.[12],[37] In women with HIV, there is a high-incidence of HPV infection and its progression to CIN so, HPV DNA testing in the triage of abnormal Pap smear is of limited value. Colposcopy is indicated when a Pap smear reveals abnormalities of epithelial cells.[15]
Figure 2: This is the algorithm for women above 30 years

Click here to view

Screening by co-testing

Co-testing can be done at the time of diagnosis or at the age of 30 years (level of evidence BII). Co-test negative women should have a repeat screening test after 3 years. Those with normal Pap tests but positive for HPV should have repeat co-testing in 1 year. If either of the co-test at 1 year is abnormal (i.e., abnormal cytology or positive HPV), referral to colposcopy is recommended. If the initial HPV test is positive and there is the availability of HPV genotyping, then genotype-specific testing for HPV-16 or 18 is done. If the HPV testing is positive, but the genotype-specific testing for HPV-16 or HPV-16 or 18 is negative, then repeat co-testing in 1 year is recommended. If genotype testing is positive, then referral to colposcopy is recommended.[37] If either of the co-tests at 1 year is abnormal (i.e., abnormal cytology or positive HPV), referral to colposcopy is recommended.[12]

Screening by Pap smear test only

In the case of nonavailability or non-affordability, screening by Pap test alone is accepted. Pap test at the time of HIV diagnosis and then every year is advised (level of evidence BII). If three consecutive Pap tests are normal, then a follow-up Pap test should be done every 3 years (level of evidence BII). Pap smear alone as a screening tool is controversial due to some limitations. It has low sensitivity for the detection of cytological abnormalities. In conventional cytology, there is more chance of inadequate smear due to cellular debris. Liquid-based cytology (LBC) decreases inadequate smears and one can perform HPV testing using the LBC specimen.[33] The reduction of inadequate smears from 9% to 1.6% was observed when LBC was used.[34] LBC does not perform better than the conventional Pap test in terms of relative sensitivity and positive predictive value for the detection of cervical cancer precursors. The sensitivity and specificity of Pap smear in detecting CIN2+ in HIV-positive women have been shown to be between 45–76% and 58–98%, respectively.[7],[35]

Abnormal Pap tests

For the ASCUS Pap test, repeat cytology in 6–12 months is recommended (level of evidence AII). For any result equal to or greater than ASCUS on repeat cytology, referral to colposcopy is advised. If the Pap test report is LSIL or worse, referral to colposcopy is recommended.[12]

Visual screening method

An alternative low-cost approach using visual screening methods like visual inspection with acetic acid (VIA) and visual inspection with Lugol's Iodine (VILI) for early detection of precancerous lesions is advocated for low-resource settings. The sensitivity of VIA is 50–88% and specificity is between 65% and 83% in detecting CIN2+ lesion in HIV-positive women. Using a combination of VIA and VILI in detecting CIN2+ in HIV-positive women resulted in increased clinical performance with a sensitivity of 81% and specificity of 93.2%.[38] “See & Treat” approach using VIA for screening and treatment by cryotherapy or loop electrosurgical excision procedure (LEEP) in the same sitting is adopted in many centers in low-resource settings.[15] The screening interval needs to be decreased in conditions like previous abnormal Pap smear, HPV infection, symptomatic HIV disease, CD4 count <200, and past treatment of CIN.

Barriers for cervical cancer screening

While the value of Pap smear as a preventive health tool is clearly defined, there are cultural, social, psychological, and system barriers that women living with HIV often have to overcome when accessing healthcare services. A negligible number of women come for follow-up visits required after abnormal screening tests. The dropout rates of women in screening programs are very high. As organized cervical cancer screening is not prioritized in low- and middle-income countries, the screening is either improper or unavailable.[39]

Women attending HIV clinics to obtain ART may not give the same importance to cervical cancer screening.[39] Women living with HIV rarely receive cervical cancer screening as a result of cultural or social barriers like resistance from their partners. The main limitation of screening in HIV-infected women is the lack of awareness regarding the severity and nature of the disease. Most of the HIV-infected women are unaware of the fact that cervical cancer is a significant health threat.

Psychological barriers like fear of diagnosis of cervical cancer and anxiety and fear regarding the procedure of screening were reported in one of the review articles published in 2019 as the main limitation for screening.[39] Members of the Cervical Cancer Screening Subgroup of the AIDS Education and Training Centers (AETC), Women's Health and Wellness Workgroup developed a guide book to address system barriers to cervical cancer screening for HIV-infected women and strategies to overcome them.[40] System barriers such as lack of provider training, insufficient equipment, and lack of availability of follow-up procedures limit the effective participation of women in cervical cancer screening. Screening uptake rates are influenced by the available infrastructure at screening centers like cleanliness, the presence of trained staff, and properly functioning equipment. Other structural barriers like the cost of the test, lack of transport facility to the screening centers, and insufficient medical advice from community healthcare providers limit the uptake of screening services.[39]

Recommendations for improvement of screening for cervical cancer in HIV-infected women

A two-pronged approach to increase the cervical cancer screening rate is suggested. One, educate women and healthcare providers regarding the need for screening, early detection, and treatment and two, system changes, that is, changes in the healthcare services to improve participation of women in screening.

A) Education

The healthcare providers must be educated as per the following facts:

  • The high prevalence of high-risk HPV infection, STIs, and cervical lesions among women living with HIV makes regular screening of these women particularly important.
  • HIV care providers should be educated about the screening of all women, especially of older age, low CD4 count, and who undergo Pap test elsewhere
  • Primary healthcare providers and gynecologists should be trained regarding differences in screening schedules and recommendations for HIV-infected women and the general population.
  • WHO recommends that women and girls who test positive for HIV should be screened for cervical cancer and undergo annual screening.[31],[37]
  • Social workers, HIV healthcare providers, and gynecologists should join hands for the effective participation of HIV-infected women in screening programs.
  • Healthcare workers should inform HIV-infected women about the importance of frequent screening.

B) System change

  • HIV care and gynecological care should be integrated to increase the screening coverage of cervical cancer.
  • Along with the development of an implementation strategy, there is a need of developing a monitoring and evaluation program to measure the coverage achieved and the quality of cervical cancer prevention services provided as part of the comprehensive sexual and reproductive health services for HIV-positive women.[10] The infrastructure developed for HIV prevention, testing, and treatment could be used as a platform to arrest the morbidity and mortality associated with cervical cancer.
  • Screening of HIV-positive women should be included as an integral aspect of the existing National Programme for Prevention and Control of Cancer, Diabetes, Cardiovascular Diseases and Stroke (NPCDCS) in India.
  • In 2006, Zambia used its HIV program infrastructure to introduce the Cervical Cancer Prevention Program in Zambia, a nurse-driven cervical cancer screening and treatment program that was integrated into public sector clinics as a routine healthcare service. The program initially focused on women living with HIV. It later recruited and trained women from the community to promote the service and inform other women about cervical cancer screening and treatment. Nurses were trained to perform cervical cancer screening and offer HIV testing services to women undergoing cervical cancer screening who did not know their HIV status. Newly diagnosed women living with HIV were referred to nearby clinics for HIV treatment, care, and support. Within 5 years, the program provided services to over 58,000 women.[8] Greater levels of guiding knowledge are needed for the development of cervical cancer screening uptake. Advanced research into the tools by which screening uptake will increase is needed for the future so that they help to update policies in low-middle-income countries.[39]

 » Conclusion Top

Women infected with HIV are living longer due to access to HAART, and hence, are at increased risk of contracting cervical cancer. Easy access to antiretroviral therapy has started reducing AIDS mortality worldwide, but women treated for AIDS could end up with death due to cervical cancer. For HIV-infected women, infection with HPV is a major challenge that requires heightened prevention, screening, and treatment efforts. For effective participation of HIV-infected women in screening, successful integration of cervical cancer control programs and HIV care is a must. In HIV prevalent areas, HPV vaccination and frequent screening is the most successful strategy for cervical cancer prevention. For the integration of healthcare, sexual and reproductive health services should be included in the basket of services that are funded while allocating HIV/AIDS funding. HIV-infected women and healthcare workers need to be educated on the link between HIV and cervical cancer and the importance of early detection of disease by screening. The current cervical cancer screening policy should be expanded for the essential screening of HIV-infected women.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

 » References Top

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