Abstract
Purpose
The prevalence of pre-invasive lesions (PIL) of cervix in human immunodeficiency virus (HIV)-seropositive women ranges from 12.5 to 69%. Although Papanicolaou (PAP) test is the recommended screening method, it has concerns owing to high false-negative cytology in HIV-infected women and is associated with high attrition rates. The current study aims to compare the role of routine colposcopy with PAP test at initial visit for screening of pre-invasive lesions of cervix in HIV-seropositive women.
Methods
A cross-sectional study of 120 HIV-seropositive women aged 25–50 years and screened for PIL of cervix by PAP test and colposcopy simultaneously was conducted. Colposcopy-directed biopsy was taken if SWEDE score was ≥ 5, and the results were compared with PAP report as well as the histopathology findings.
Results
Out of the 120 women screened, abnormal colposcopy was found in 22 women (18.3%) out of which 12 (54.54%) were positive for PIL of cervix on biopsy as well. Abnormal PAP test was found in 6 women (5%), and all had abnormal colposcopy and histopathological findings suggestive of PIL as well. There were 6 women with PIL of cervix who would have been missed if only PAP test was to be used as the screening modality.
Conclusion
Colposcopy was superior in detection of PIL of cervix in HIV-seropositive women. Therefore, the authors conclude that colposcopy should be incorporated as a primary screening tool for pre-invasive lesions of cervix in HIV-seropositive women.
Keywords: PAP test, Colposcopy, Cervical cancer, SWEDE score, HIV
Introduction
Cervical cancer is a major public health problem and the third most common cause of cancer-related deaths in women across the world with nearly 90% of these cases occurring in developing countries [1]. This cancer has a well-defined pre-invasive stage lasting for approximately 10–15 years making it amenable for early detection. The most important risk factor for development of cervical cancer is chronic persistent human papilloma virus (HPV) infection. Women with HIV are more likely to have persistent HPV infection, making them prone to cervical abnormalities including cancer [2].
The PAP test is currently the most commonly used screening method for cervical cancer, but it has a low sensitivity of 55.4% in detection of cervical intraepithelial neoplasia (CIN) [3]. Co-testing with human papilloma virus deoxyribose nucleic acid (HPV-DNA) has greater sensitivity and is a better screening tool [4]. However, it is not cost-effective which makes it a limiting factor in developing countries.
Colposcopy has a high sensitivity, i.e., 80%, and specificity, i.e., 97.7%, in detecting pre-invasive lesions and may be the preferred screening tool in high-risk women where HPV testing is not feasible or available [9]. It is observed that the incidence of CIN, as confirmed by colposcopy, is four to five times higher in HIV-infected women compared with HIV-negative women [5].
Despite the increased risk of cervical cancer in HIV-positive women, there are no separate standard guidelines for screening in these women. Evidence is lacking regarding the preferred screening tool in these women. This study was thereby undertaken with the aim to compare the role of colposcopy with PAP test for detection of pre-invasive lesions of the cervix in HIV-seropositive women.
Methodology
This was a cross-sectional study conducted at the colposcopic clinic in a tertiary care health care facility with associated anti-retroviral therapy (ART) center in the vicinity from November 2019 to October 2021 after taking approval from institutional ethical committee. The sample size was 120 non-pregnant HIV-seropositive women within the age group of 25–50 years. Pregnant women, women with diagnosed carcinoma cervix or pre-invasive lesion of cervix in the past, women on immunosuppressive therapy, and women who had undergone hysterectomy in the past were excluded from the study.
All these women underwent simultaneous PAP (liquid-based cytology) testing and colposcopic assessment of the cervix. SWEDE score was calculated, and colposcopy-guided biopsies were obtained in cases where SWEDE score was equal to or more than 5 (Fig. 1). The SWEDE score is one of the well-known scoring systems that were designed to standardize colposcopic assessment and assist in the prediction of histological diagnosis. By evaluating 5 colposcopic features, i.e., lesion size degree of acetowhitening, lesion margin and surface configuration, pattern of vasculature, and degree of iodine staining, a maximum score of 10 can be obtained. A score of 0–4 indicates normal cervix or low-grade lesion (CIN1), score of 5–6 indicates high-grade and non-invasive lesions (CIN2+), and a score of 7–10 indicates high-grade lesion with suspected invasion [6]. Table 1 shows the details of SWEDE score.
Fig. 1.
Methodology of the Study
Table 1.
SWEDE score
| SWEDE score | 0 | 1 | 2 |
|---|---|---|---|
| Acetouptake | Zero or transparent | Shady, milky, neither transparent nor opaque | Distinct, opaque, white |
| Vessels | Fine regular | Absent | Coarse or atypical vessels |
| Margins and surface | Diffuse | Sharp but irregular, jagged, geographical satellite | Sharper and evening in surface level including cutting |
| Lesion size | < 5 mm | 5–15 mm or two quadrants | 3–4 Quadrants or > 15 mm or endocervically |
| Iodine staining | Brown | Faintly or patchy brown | Distinct yellow |
The qualitative variables were summarized as frequencies/percentages and were compared using Chi-square test. Odds Ratio was calculated to quantify the impact of predictors on the outcome variable. A p-value < 0.05 was considered statistically significant. 'R' language and/or Statistical Package for Social Sciences (SPSS) version 16.0 was used for statistical analysis.
Results
The study was conducted on a total of 120 HIV-seropositive women who fulfilled the inclusion criteria. Most women were in the age group of 30–40 years. The average age at menarche was 13.25 years. The average age at first intercourse was 19 years. The mean parity was 2.40 ± 1.13.
81.66% (n = 98) women were asymptomatic, 10% (n = 12) had vaginal discharge, 7.5% (n = 9) had menstrual irregularities, and 0.83% (n = 1) had post-coital bleeding. All the patients were on anti-retro viral therapy. The duration of anti-retro viral therapy varied from 6 months to 21 years. The demographic profile is illustrated in Table 2.
Table 2.
Demographic profile of the study group
| Variables | Mean ± SD | Range | |
|---|---|---|---|
| Minimum | Maximum | ||
| Age | 33.42 ± 6.609 | 25 | 50 |
| Menarche [years] | 13.36 ± 1.43 | 10 | 17 |
| Age at first intercourse [years] | 19.31 ± 2.43 | 15 | 26 |
| Parity | 2.40 ± 1.13 | 0 | 6 |
| Duration [years] since HIV detection | 7.52 ± 4.57 | 0.5 | 21 |
| Duration [years] since anti- retroviral therapy | 5.81 ± 3.35 | 0.5 | 21 |
| CD4 count | 580 ± 279.23 | 110 | 1497 |
PAP test was found negative for intraepithelial lesion of malignancy in 114 women (95%). Among the six women (5%) with abnormal cytology, two were reported atypical squamous cells of undetermined significance (ASCUS), three high-grade squamous intraepithelial lesion (HSIL), and one keratinizing squamous cell carcinoma. No woman had atypical squamous cell - cannot exclude high-grade intraepithelial lesion (ASC-H) or low-grade squamous intraepithelial lesion (LSIL).
On colposcopy, 22 women (18.33%) had a SWEDE score of more than or equal to 5 in whom simultaneous biopsy was taken. Twelve women (54.54%) had positive histopathology report for pre-invasive/invasive lesions of the cervix. Five women (22.72%) had LSIL (CIN 1), 5 women (22.72%) had HSIL (CIN 2 & CIN3), and 2 women (9%) showed keratinizing squamous cervical cancer. Remaining 10 women were reported to have had chronic cervicitis (Table 3).
Table 3.
Frequency distribution of biopsy histopathology findings among the study group
| Biopsy | Number | Percentage (%) |
|---|---|---|
| Negative | 10 | 45.45 |
| CIN1 | 5 | 22.72 |
| CIN2 | 2 | 9.09 |
| CIN3 | 3 | 13.63 |
| Keratinizing squamous cell cancer (SCC) | 2 | 9 |
| Total | 22 | 100.0 |
The study included twenty-two women (n = 120) with abnormal colposcopic findings in whom biopsy was performed as well as six women with an abnormal PAP test. Sixteen women with negative PAP test had abnormal colposcopic findings; 6 of whom had a pre-invasive or invasive lesion of the cervix on biopsy. In short, abnormal PAP test was seen in 5% of women, abnormal colposcopy in 18.34% of women, and histopathologically confirmed pre-invasive and invasive lesions of the cervix in 10% of women.
Table 4 describes the characteristics of women who were diagnosed to have pre-invasive/invasive lesions of the cervix on histopathology (n = 12). Most women who were diagnosed with pre-invasive lesion of cervix were asymptomatic. Fifty percent of these women had negative PAP test but positive colposcopy and histopathologically proven pre-invasive lesion of cervix, i.e., 6 women could have been missed on screening and had colposcopy not been performed in them at their 1st visit.
Table 4.
Characteristics of women with pre-invasive lesions/invasive lesions of the cervix included in the study group
| S.No. | Age (year) | Menarche (year) | Age of 1st intercourse (year) | Parity | Year since diagnosis | Symptom | Duration of ART (year) | CD4 count | PAP SMEAR | SWEDE score | HPE finding |
|---|---|---|---|---|---|---|---|---|---|---|---|
| 1 | 27 | 14 | 22 | 2 | 2 | No | 2 | 764 | NILM | 5 | CIN1 |
| 2 | 35 | 12 | 19 | 3 | 1 | No | 14 | 514 | NILM | 6 | CIN1 |
| 3 | 40 | 14 | 17 | 3 | 6 | No | 6 | 529 | K.SCC | 8 | SCC |
| 4 | 42 | 15 | 18 | 3 | 6 | Yes | 5 | 911 | ASCUS | 6 | CIN1 |
| 5 | 43 | 14 | 18 | 5 | 5 | Yes | 10 | 1170 | HSIL | 7 | CIN3 |
| 6 | 36 | 13 | 17 | 3 | 10 | No | 6 | 658 | ASCUS | 6 | CIN2 |
| 7 | 26 | 12 | 23 | 1 | 3 | No | 3 | 845 | NILM | 6 | CIN2 |
| 8 | 39 | 14 | 20 | 2 | 3 | No | 2 | 581 | HSIL | 8 | CIN3 |
| 9 | 31 | 12 | 18 | 2 | 18 | No | 17 | 671 | NILM | 5 | CIN 1 |
| 10 | 26 | 13 | 18 | 2 | 3 | No | 3 | 466 | HSIL | 5 | HSIL |
| 11 | 34 | 12 | 17 | 4 | 8 | No | 8 | 411 | SCC | 7 | ICC |
| 12 | 25 | 16 | 20 | 2 | 4 | No | 2 | 485 | NILM | 6 | CIN1 |
Discussion
Cervical cancer is most frequently diagnosed at an average age of 50 years. Immunosuppression by HIV enhances the oncogenic potential of HPV leading to faster progression of the disease, and hence, women with HIV who develop pre-invasive lesions of the cervix are much younger [7]. Additionally, the use of ART increases the longevity of life of women infected with HIV which in turn leads to longer persistence of HPV infection thereby increasing epigenetic alteration in carcinogenesis [8]. In our study, average age of women with pre-invasive lesion of cervix was 33 years. Studies by Georgette et al. (39 years), Singh DK et al. (34 years) and Kapambwe S et al. (35 years) had similar observations reflecting the need of early and vigorous screening in these high-risk women [9, 10].
Higher parity irrespective of immunocompromised state is an established high risk of pre-invasive/ invasive lesions of the cervix as per the American Cancer Society (ACS) [11]. In our study, all women with pre-invasive / invasive lesions of the cervix had a parity ranging from 1 to 5 with an average of 2.6, thereby reflecting that HIV-seropositive women are in general at a high risk of developing pre-invasive lesion of cervix irrespective of the parity. Earlier age at first intercourse is considered a significant risk factor in the pathogenesis of cervical cancer as per the American Cancer Society [11]. In our study, the age at first sexual intercourse among the affected women was 18.9 years which was comparable to the study by Bhutia et al. and Macharia et al. where the women with pre-invasive lesions of the cervix were found to have a mean age at first intercourse of 18.9 ± 2.6 and 18.7 years, respectively [12, 13]. Pre-invasive lesions of the cervix and even cervical cancer may not give rise to any symptoms in an affected woman till the time malignancy advances. Out of the 12 women detected to have pre-invasive lesions of the cervix or invasive cervical cancer, 2 (16.67%) had symptoms, while the rest 10 (83.33%) patients were asymptomatic. In a study by Srivastava et al. among women who were diagnosed with pre-invasive lesions of the cervix, 36.1% of the women were asymptomatic and the rest had either vaginal discharge or menstrual irregularities [14]. Similarly, Zosia Kmietowicz et al. found only 31.25% of the patient with cancer cervix to be symptomatic in the form of abnormal vaginal bleeding and post-coital bleeding. Based on these studies, it may be inferred that most of the pre-invasive/invasive cervical cancer in HIV-seropositive women are asymptomatic, and hence, cervical cancer screening should be done in all HIV-seropositive women beyond 25 years of age irrespective of the symptoms. The role of ART in HPV related lesions and cervical cancer is still debated and requires more research. In our study, no co-relation was found between the duration of the ART and the presence or severity of disease.
The prognosis of pre-invasive lesion of cervix is largely based on early detection and management. To achieve this, PAP test has been used worldwide as a screening tool of choice. Table 5 shows the results of PAP test (LBC) of various studies compared with the present study which highlights the increased prevalence of abnormal cytology in HIV-infected women [15–20].
Table 5.
Comparison between epithelial cell abnormalities on PAP test results of various studies in HIV-seropositive women
| Studies | Year | Type of study | Study group (HIV-seropositive women) (n) | Percentage positive (%) |
|---|---|---|---|---|
| Singh KN et al | 2017 | Cross-sectional | 70 | 8.57 |
| Gupta et al | 2019 | Retrospective | 150 | 12 |
| Jha et al | 2012 | Cross-sectional | 407 | 8.34 |
| Vani et al | 2017 | Cross-sectional | 100 | 20 |
| Madan et al | 2016 | Cross-sectional | 250 | 12 |
| Tansupswatdikul et al | 2009 | Cross-sectional | 280 | 21.3 |
| Present study | 2021 | Cross-sectional | 120 | 5 |
In our study, it was observed that the incidence of false-negative result on PAP test was high. This was observed in a study by Massad et al. where he found the sensitivity and specificity of PAP test 68% and 78%, respectively, in this population of HIV-seropositive women as compared to the HIV-seronegative women [21]. Spinillo et al. also reported the rate of false-negative results (i.e., normal PAP test finding with abnormal colposcopy and biopsy findings) as 26.6% for 241 HIV-seropositive women as compared to 16.2% for the control of 404 HIV-seronegative women [22]. Madan et al. in his study further pointed out the need of regular and frequent follow-up in HIV-seropositive women as they are subject to high attrition rate [19].
Colposcopy although is expensive, time-consuming, and needs a proper setup, it has a high sensitivity, i.e., 80%, and specificity, i.e., 97.7%, in detecting high-grade cervical lesions [21]. A meta-analysis that included eight longitudinal studies observed a high accuracy of colposcopy (89%) in detection of pre-invasive lesions of the cervix. This study also recommended colposcopy as a triage test in cervical cancer prevention [23, 24].
Nongyao et al. 2008, in their study on Underlying Histopathology of HIV-infected Women with Squamous Cell Abnormalities on Cervical Cytology, showed the importance of additional test at an early age after an abnormal PAP result. In their study, they observed that HIV-infected women with abnormal PAP smears of any grade had approximately 2.6 times the risk of having CIN II or higher (95% CI = 1.21–5.40, P = 0.01) compared to HIV negative women [25]. Because of the higher risk of harboring such significant lesions, once abnormal cervical cytology is diagnosed, these HIV-infected women warrant further appropriate evaluation and immediate colposcopy as a feasible test and may be adopted in developing countries.
Although most literatures display the added advantage of colposcopy, certain studies have stated that colposcopy increases the likelihood of unnecessary biopsies and that it should not be used as a screening modality for cancer cervix [26, 27]. To overcome this shortcoming, SWEDE score evaluation and cut-off score to consider a biopsy have been studied.
In our study, 22 women (n = 120) had abnormal colposcopy (SWEDE Score ≥ 5) and biopsy was taken in their 1st visit. Out of them, 12 had histologically proven CIN of cervix. However, only 6 of the 12 had abnormal cytology, suggesting that 50% of women would have been missed if only cytology was to be used for screening in these women. However, PAP was found very sensitive as all 6 positive cases on PAP test had pre-invasive lesion of cervix. The comparison between PAP test and colposcopy by kappa coefficient (0.37) was found to have fair agreement with the 95% confidence interval ranging from 0.157 to 0.601, meaning that colposcopy and PAP test are not interchangeable for the screening of pre-invasive lesions of cervix. This suggests that the benefits of colposcopy cannot be extrapolate to PAP test and that colposcopy has a definite role in screening of these high-risk patients which is better than PAP test. Further, it was observed that the false-negative case with PAP test was associated with low- as well as high-grade pre-invasive cervical lesion suggesting a need for more intense and repeated screening in these women. Moreover, this population has a high prevalence and persistent HPV infection which can cause rapid progression of these low-grade lesion into high-grade lesion thereby demanding its early detection and treatment. Hence, in our study, we found colposcopy to be better than PAP smear (LBC) in the detection of pre-invasive lesions of the cervix and cervical cancer.
The limitation of our study was small sample size. Histopathology which is considered as the gold standard for the diagnosis could not be done in all the women as biopsy is an invasive test and doing so would be ethically unacceptable. Therefore, sensitivity, specificity, positive predictive value, negative predictive value, and diagnostic accuracy could not be calculated for the present study. Thus, the findings of the study cannot be generalized and more robust studies with larger sample size are needed to formulate screening guidelines for this high-risk group of HIV-seropositive women.
Conclusion
HIV-seropositive women are at a higher risk of development of carcinoma cervix as evident by high percentage of positivity in our study group (10%). It was also found that 50% of the women positive for pre-invasive lesion of cancer would have been missed if PAP test was used as the sole screening method for these women. Thus, colposcopy was found to be better than PAP test in the detection of pre-invasive lesions of the cervix and cervical cancer in women with HIV (kappa coefficient value of 0.37). The authors thus conclude that colposcopy should be included in the screening of HIV-seropositive women at the initial visit.
Funding
There was no financial support.
Declarations
Conflict of interest
The authors report no conflict of interest.
Ethical Approval
This is to certify that the study has been approved by the Ethical Committee for Human Research (ECHR) at Lady Hardinge Medical College. Date: 28 October 2019.
Footnotes
Swati Agrawal is a Professor; Anju Seth is a Director Professor; Smita Singh is a Professor
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
References
- 1.Ferlay J, Soerjomataram I, Ervik M, et al. GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC Cancer Base No. 11 [online].Lyon, France: International Agency for Research on Cancer; 2013. Available from: http://globocan.iarc.fr. Accessed 12 May 2021.
- 2.Bowring J, Strander B, Young M, et al. The Swede score: evaluation of a scoring system designed to improve the predictive value of colposcopy. Am Soc Colposc Cerv Pathol J Lower Genit Tract Dis. 2010;14:301–5. 10.1097/LGT.0b013e3181d77756 [DOI] [PubMed] [Google Scholar]
- 3.Mayrand MH, Duarte-Franco E, Rodrigues I, et al. Human papillomavirus DNA versus Papanicolaou screening tests for cervical cancer. N Engl J Med. 2007;357(16):1579–88. 10.1056/NEJMoa071430 [DOI] [PubMed] [Google Scholar]
- 4.Madeddu G, Mameli G, Capobianco G, et al. HPV infection in HIV- positive females: the need for cervical cancer screening including HPV-DNA detection despite successful HAART. Eur Rev Med Pharmacol Sci. 2014;18:1277–85. [PubMed] [Google Scholar]
- 5.Bornstein J, Bentley J, Bosze P, et al. 2011 colposcopic terminology of the international federation for cervical pathology and colposcopy. Obstet Gynecol. 2012;120(1):166–72. 10.1097/AOG.0b013e318254f90c [DOI] [PubMed] [Google Scholar]
- 6.Bowring J, Strander B, Young M, et al. The SWEDE score: evaluation of a scoring system designed to improve the predictive value of colposcopy. J Low Genit Tract Dis. 2010;14(4):301–5. 10.1097/LGT.0b013e3181d77756 [DOI] [PubMed] [Google Scholar]
- 7.Anderson-Jean EL, Sanghvi H. Cervical cancer screening and prevention for HIV infected women in the developing world Cancer prevention from mechanisms to translational benefits. Best Prac Red Clin Obstet Gynaecol. 2012;26(2):189–96. [Google Scholar]
- 8.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. 10.4103/ijc.IJC_888_19 [DOI] [PubMed] [Google Scholar]
- 9.Singh DK, Anastos K, Hoover DR, et al. Human papillomavirus infection and cervical cytology in HIV-infected and HIV-uninfected Rwandan women. J Infect Dis. 2009;199(12):1851–61. 10.1086/599123 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Kapambwe S, Sahasrabuddhe VV, Blevins M, et al. Implementation and operational research: age distribution and determinants of invasive cervical Cancer in a “screen-and-treat” program integrated with HIV/AIDS Care in Zambia. J Acquir Immune Defic Syndr. 2015;70(1):e20–6. 10.1097/QAI.0000000000000685 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.American Cancer Society. Global Cancer facts and figures 3rd Edition Atlanta: American Cancer Society; 2015. Available at: https://www.cancer.org/content/dam/cancer.org/research/cancer-facts-and-statistics/global-cancer-facts-andfigures/global-cancer-facts-and-figures-3rd-editionpdf. Accessed 19 June 2023.
- 12.Bhutia K, Puri M, Gami N, et al. Persistent inflammation on Pap smear: Does it warrant evaluation? Indian J Cancer. 2011;48:220–2. 10.4103/0019-509X.82901 [DOI] [PubMed] [Google Scholar]
- 13.Macharia H, Cheserem EJ, Bukusi E, et al. A comparative analysis of conventional Pap smear cytology, liquid based cytology and colposcopy clinical impression with colposcopy biopsy histology as gold standard in women undergoing colposcopy in Kenyatta National Hospital. Int J Reprod Contracept Obstet Gynecol. 2014;3(1):58–63. [Google Scholar]
- 14.Srivastava AN, Misra JS. Significance of inflammation in cervical cytology smears in rural women of India: An observational study. Indian J Obstet Gynecol Res. 2018;5(4):520–4. [Google Scholar]
- 15.Singh KN, Achale S, Ghanghoriya V. A study on HPV mRNA test and colposcopy in HIV positive women for early detection of cervical intraepithelial lesions. Int J Reprod Contracept Obstet Gynecol. 2017;6(6):2522–6. 10.18203/2320-1770.ijrcog20172344 [DOI] [Google Scholar]
- 16.Gupta K, Philipose CS, Rai S, et al. A study of Pap smears in HIV positive and HIV- negative women from a tertiary care centre in South India. Acta Cytol. 2019;63(1):50–5. 10.1159/000496211 [DOI] [PubMed] [Google Scholar]
- 17.Jha BM, Patel M, Patel K, et al. A study on cervical Pap smear examination in patient living with HIV. Natl J Med Res. 2012;2(1):81–4. [Google Scholar]
- 18.Vani YS, Priyadarshini M. A study of prevalence of Pap smear abnormalities in HIV seropositive women. IAIM. 2017;4:75–81. [Google Scholar]
- 19.Madan A, Patil S, Nakate L. A Study of Pap smear in HIV-positive females. J Obstet Gynaecol India. 2016;66(6):453–9. 10.1007/s13224-016-0908-9 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Tansupswatdikul P, Piyaman S. Prevalence and predictors of abnormal cervical cytology in HIV-infected patients at the anonymous clinic, Chonburi Hospital. Thai J Obstet Gynaecol. 2009;17:51–6. [Google Scholar]
- 21.Massad LS, D’Souza G, Tian F, et al. Negative predictive value of pap testing: implications for screening intervals for women with human immunodeficiency virus. Obstet Gynecol. 2012;1204(4):791–7. 10.1097/AOG.0b013e31826a8bbd [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Spinillo A, Capuzzo E, Tenti P, et al. Adequacy of screening cervical cytology among human immunodeficiency virus-seropositive women. Gynecol Oncol. 1998;69(2):109–13. 10.1006/gyno.1998.4985 [DOI] [PubMed] [Google Scholar]
- 23.Karimi-Zarchi M, Zanbagh L, Shafii A. Comparison of Pap smear and colposcopy in screening for cervical cancer in patients with secondary immunodeficiency. Electron Physician. 2015;7(7):1542–8. 10.19082/1542 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Akhter S, Bari A, Hayat Z. Variability study between Pap smear, colposcopy and cervical histopathology findings. J Pak Med Assoc. 2015;65(12):1295–9. [PubMed] [Google Scholar]
- 25.Suwankanta N, Kietpeerakool C, Srisomboon J, et al. Underlying histopathology of HIV-infected women with squamous cell abnormalities on cervical cytology. Asian Pac J Cancer Prev. 2008;9:441. [PubMed] [Google Scholar]
- 26.Branca M, Garbuglia AR, Benedetto A, et al. Factors predicting the persistence of genital human papillomavirus infections and PAP smear abnormality in HIV-positive and HIV-negative women during prospective follow-up. Int J STD AIDS. 2003;14(6):417–25. 10.1258/095646203765371321 [DOI] [PubMed] [Google Scholar]
- 27.Cantor SB, Cárdenas-Turanzas M, Cox DD, et al. Accuracy of colposcopy in the diagnostic setting compared with the screening setting. Obstet Gynaecol. 2008;111(1):7–14. 10.1097/01.AOG.0000295870.67752.b4 [DOI] [PubMed] [Google Scholar]