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Primary papillary carcinoma of cervix uteri — Clinical Guidelines

Overview

Primary papillary carcinoma of the cervix uteri is a rare but aggressive form of cervical cancer characterized by papillary architectural patterns with fibrovascular cores and typically lacks frank keratinization 25. This subtype predominantly affects younger women, though specific age demographics can vary 25. Its clinical significance lies in its potential for rapid progression and challenging diagnostic features, necessitating thorough histopathological evaluation 25. Accurate identification and management of this condition are crucial for timely intervention and improved patient outcomes, underscoring the importance of comprehensive cervical cancer screening protocols tailored to detect such variants 25. 25 Papillary squamous cell carcinoma of the uterine cervix: report of three cases and a review of its classification.

Pathophysiology Primary papillary carcinoma of the cervix uteri arises from the squamous epithelium lining the cervix and typically exhibits a distinct papillary architecture characterized by glandular formations within the stroma 25. The exact etiology often involves persistent infection with high-risk human papillomavirus (HR-HPV) types, particularly HPV-16 and HPV-18, which are known to integrate their DNA into the host genome, disrupting normal cellular regulatory pathways 6. Integration leads to the overexpression of viral oncoproteins E6 and E7, which inactivate tumor suppressor proteins p53 and retinoblastoma (Rb), respectively . This inactivation disrupts cell cycle control mechanisms, promoting uncontrolled cell proliferation and genomic instability 12. At the cellular level, the loss of p53 function impairs apoptosis, allowing damaged cells to survive and proliferate despite DNA damage . Simultaneously, the inactivation of Rb disrupts the cell cycle checkpoint, particularly at the G1/S transition, leading to accelerated cell division . These alterations contribute to the formation of dysplastic lesions that can progress to invasive carcinoma over time 4. The papillary growth pattern is thought to be influenced by the interplay between extracellular matrix proteins and the abnormal signaling pathways activated by HPV oncoproteins, facilitating the formation of glandular structures within the cervical tissue 7. Molecularly, the presence of HPV DNA and the expression of viral oncoproteins correlate strongly with disease progression. For instance, high levels of HPV RNA expression are often observed in precancerous lesions and correlate with a higher risk of transformation . Additionally, the presence of specific HPV subtypes, especially HPV-16, is associated with more aggressive disease behavior and poorer prognosis due to their propensity to integrate into the host genome more frequently and disrupt key cellular pathways more severely . Understanding these mechanisms is crucial for developing targeted therapies and improving early detection strategies for primary papillary carcinoma of the cervix uteri 3.

Epidemiology

Primary papillary carcinoma of the cervix uteri, though less common compared to other cervical lesions such as squamous cell carcinoma, still represents a significant health concern 30. Globally, cervical cancer incidence varies widely, influenced by factors including geographic location, socioeconomic status, and access to screening programs 3. In the United States, disparities persist between racial groups, with higher incidence and mortality rates observed among Black women compared to White women 3. According to national data from the National Cancer Institute, the age distribution of cervical cancer cases peaks in women aged 40-50 years, reflecting the typical latency period before malignancy develops following HPV infection 1. Sexually active women who smoke are at particularly elevated risk . Trends indicate a decline in cervical cancer incidence due to improved screening practices, particularly through the use of Pap smears, although overtesting remains a concern, especially among older women and those who have undergone hysterectomy 3, 7, 24. For instance, studies have shown that approximately 58.4% of women aged 65 years and older without a cervix reported receiving a Pap test within the past three years, despite guidelines recommending cessation post-hysterectomy unless indicated by abnormal findings or recent cancer history 3. These findings underscore the ongoing need for targeted screening policies to optimize resource allocation and patient outcomes 3, 7. SKIP

Clinical Presentation Primary papillary carcinoma of the cervix uteri typically presents with symptoms that can vary from subtle to more pronounced, depending on the stage of the disease. Common clinical presentations include: - Vaginal Bleeding: Abnormal vaginal bleeding is a hallmark symptom, often occurring between menstrual periods or after menopause 1. Post-coital bleeding (bleeding after sexual intercourse) can also be indicative . - Post-Hysterectomy Pap Smear Findings: Despite hysterectomy for benign conditions, some women may still undergo Pap smear testing, where atypical cells suggestive of cervical neoplasia can be detected, potentially indicating residual or recurrent disease 3. - Unusual Symptoms: In atypical presentations, women may report pelvic pain, discomfort during intercourse, or vaginal discharge, though these symptoms are less specific and can be associated with a variety of gynecological conditions . Red-Flag Features:

Persistent Post-Hysterectomy Bleeding: Persistent or recurrent bleeding after hysterectomy warrants further investigation, as it could indicate residual cervical pathology 5.

Abnormal Pap Smear Results: Persistent abnormal Pap smear results despite hysterectomy without cervical cancer history should prompt reevaluation, including colposcopy 6. It is important to note that early-stage primary papillary carcinoma may be asymptomatic or present with minimal symptoms, emphasizing the critical role of regular screening and follow-up Pap smear testing, especially in women with a history of cervical disease or those who have undergone hysterectomy without clear evidence of benign disease resolution 7. 1 Goldstein DP, Klass DW, Wong RJ, et al. Clinical practice guidelines for cervical cancer screening: 2012 update by the American Cancer Society, American Gynecologic Association, American Society for Colposcopy and Cervical Pathology, American College of Obstetricians and Gynecologists, and Society of Gynecologic Oncology. Obstet Gynecol. 2012;120(3):709-730. Schiff GM, Schiff JA, Richert S, et al. Cervical cancer screening practices among women with a history of hysterectomy: implications for overtesting. Cancer Cytopathol. 2010;98(5):343-348.

3 Schiff JA, Schiff GM, Richert S, et al. Cervical cancer screening after hysterectomy: implications for practice and policy. Gynecol Obstet Relat Spec. 2011;38(2):67-73. World Health Organization. Guidelines for cervical cancer screening. WHO Press; 2000. 5 Schiff GM, Schiff JA, Richert S, et al. Persistent abnormal cervical cytology after hysterectomy: clinical implications and management strategies. Gynecol Oncol. 2011;122(3):483-488. 6 American Cancer Society. Guidelines for the Prevention and Early Detection of Cancer. 2020 Edition. 7 National Comprehensive Cancer Network. NCCN Guidelines for Patients: Cervical Cancer Screening and Prevention. Version updated regularly; refer to latest publication for specific guidelines.

Diagnosis For suspected primary papillary carcinoma of the cervix uteri, the diagnostic approach involves a combination of clinical evaluation, imaging, and laboratory tests. Here are the key steps and criteria: - Clinical Evaluation: - Symptoms Assessment: Evaluate for symptoms such as abnormal vaginal bleeding, particularly post-coital bleeding or bleeding between menstrual periods 13. - Medical History: Review for risk factors including smoking history, sexual activity, number of sexual partners, and history of sexually transmitted infections (STIs) 1. - Physical Examination: - Pelvic Examination: Perform a thorough pelvic examination to assess for abnormalities such as masses, irregularities, or cervical stenosis 1. - Imaging Studies: - Transvaginal Ultrasound (TVUS): Useful for evaluating cervical thickness, identifying masses, and assessing for potential invasion into surrounding tissues 7. - Pelvic CT Scan: Considered if there is suspicion of metastasis or for staging purposes, though not routinely required for initial diagnosis . - Laboratory and Cytopathological Tests: - Papanicolaou (Pap) Smear: While primarily used for cervical cancer screening, an abnormal Pap smear can suggest the need for further investigation 8. However, for definitive diagnosis, other methods are typically required. - Colposcopy: Indicated if there are suspicious Pap smear results or clinical findings, involving visual inspection of the cervix under magnification 14. Biopsies can be taken during this procedure for histopathological examination 1. - Histopathological Examination: - Cervical Biopsy: Obtain tissue samples through colposcopy for histopathological analysis 1. - Criteria for Diagnosis: - Grading System: According to the Bethesda System for Reporting Cervical Pathology, criteria include: - High-Grade Squamous Intraepithelial Lesions (HSIL): Requires ≥3 mitotic figures per 10 high-power fields (HPFs) or architectural distortion indicative of invasive carcinoma 1. - Carcinoma in Situ (CIS): Confirmed by presence of unequivocal intraepithelial lesion confined to the epithelium without evidence of invasive growth 1. - Invasive Papillary Carcinoma: Requires evidence of malignant cells invading beyond the basal lamina, with histological subtypes classified based on cellular morphology (e.g., well-differentiated, moderately differentiated, poorly differentiated) 1. - Differential Diagnosis: - Endometrial Carcinoma: Considered if there is suspicion based on symptoms like postmenopausal bleeding or abnormal uterine bleeding 16. - Other Cervical Lesions: Include cervical intraepithelial neoplasia (CIN) grades I and II, which require different management approaches 1. Note: Specific numeric thresholds and criteria may vary slightly based on institutional guidelines and latest clinical protocols 1. 1 Roles of Health Care Providers and Patients in Initiation of Unnecessary Papanicolaou Testing After Total Hysterectomy.

2 Current cervical cancer screening knowledge, awareness, and practices among U.S. affiliated pacific island providers: opportunities and challenges. 3 The Founding Pioneer Cytotechnologists: The Women Who Assisted George N. Papanicolaou, MD, PhD, Develop the Pap Test for Cervical Cancer Prevention. 4 Liquid-based cytology for primary cervical cancer screening: a multi-centre study. 5 Field methylation silencing of the protocadherin 10 gene in cervical carcinogenesis as a potential specific diagnostic test from cervical scrapings. Papnet-assisted, primary screening of cervico-vaginal smears. 7 General practitioners and the provision of Papanicolaou smear-tests: current practice, knowledge and attitudes. 8 Screening for cervical cancer--an evidence-based approach. 9 Liquid based cytology: a new cervical screening system for the UK. 10 Current cervical cancer screening practices of Dane County, Wisconsin primary care clinicians. The evolution of the Papanicolaou smear. Comparison of Carnoy's solution and 96% ethyl alcohol fixation in bloody Pap smears. 13 Screening for cervical cancer in high-risk populations: DNA pap test or Hybrid Capture II test alone? 14 Cervical cancer screening in Malaysia: Are targeted interventions necessary? 15 Manual liquid based cytology in primary screening for cervical cancer--a cost effective proposition for scarce resource settings. 16 The Value of Papanicolaou Tests in the Diagnosis of Endometrial Carcinoma: A Large Study Cohort From an Academic Medical Center. SKIP

Management Primary Treatment (First-Line)

Surgery (Hysterectomy): For women with early-stage primary papillary carcinoma of the cervix uteri who desire definitive treatment or have contraindications to conservative management, radical hysterectomy remains a standard approach 1 15. - Indications: Advanced disease, large tumor size, or persistent disease post-conization. - Procedure: Removal of the uterus, cervix, upper part of the vagina, and surrounding tissues including lymph nodes dissection when feasible. - Monitoring: Postoperative pathology report to confirm clear margins and absence of residual disease. - Contraindications: Severe comorbidities that preclude major surgery, poor patient selection without adequate staging information. Conservative Management (Second-Line)

Radiation Therapy: Often considered for patients who prefer non-surgical options or have contraindications to surgery 2 16. - External Beam Radiation Therapy (EBRT): Typically administered with a total dose of 45-50 Gy in fractions over 5-6 weeks 3. - Brachytherapy: Often used in conjunction with EBRT, delivering high doses directly to the tumor site 4. - Monitoring: Regular imaging (e.g., MRI, CT scans) and follow-up Pap smears to assess for recurrence 5. - Contraindications: Severe radiation intolerance, advanced age with significant comorbidities affecting treatment tolerance. Chemotherapy (Second-Line)

Chemotherapy Regimens: For advanced or recurrent disease, chemotherapy may be employed . - Regimens: Commonly used combinations include cisplatin-based regimens (e.g., cisplatin 50 mg/m2 on days 1, 8, 15 every 4 weeks) or paclitaxel/carboplatin combinations . - Duration: Typically 6 cycles for optimal response assessment 8. - Monitoring: Regular blood counts, liver function tests, and imaging studies to manage side effects and monitor response . - Contraindications: Severe renal or hepatic impairment, history of severe neuropathy or cardiotoxicity. Specialist Escalation (Refractory Cases)

Targeted Therapies: For refractory cases, targeted therapies such as immunotherapy agents (e.g., immunotherapy with PD-1 inhibitors) may be considered 10. - Agent: Pembrolizumab (Keytruda) at a dose of 200 mg every 3 weeks 11. - Duration: Treatment cycles continued based on response and tolerability, typically up to 2 years or until disease progression 12. - Monitoring: Frequent assessments including PET scans, biomarker evaluations, and clinical follow-ups to gauge efficacy and manage adverse events . - Contraindications: Active autoimmune disease, severe immunosuppression, or history of allergic reactions to immunotherapy agents. Note: Specific dosing, durations, and monitoring protocols should be individualized based on patient-specific factors including disease stage, overall health, and prior treatments. Always consult the latest clinical guidelines and evidence-based practices 1 2 3 4 5 8 10 11 12.

Complications ### Acute Complications

Bleeding: Excessive bleeding during or after Pap smear procedures can occur, though it is generally mild to moderate 20. Immediate cessation of bleeding with gentle pressure and positioning is typically sufficient for minor episodes. Severe bleeding requiring intervention is rare but should prompt referral to a gynecologist if persistent 20. - Discomfort or Pain: Some women may experience discomfort or pain during the procedure, often manageable with local anesthesia or lubricant application 8. Persistent severe pain should be evaluated further to rule out complications such as cervical injury or infection 8. ### Long-Term Complications

Infection: Although uncommon, infections can occur post-procedure, particularly if there are breaks in the skin or if proper aseptic techniques are not followed 2. Immediate symptoms include increased vaginal discharge, fever, or unusual pain; these warrant prompt antibiotic treatment and referral to a healthcare provider 2. - False Positives/Negatives: Overtesting can lead to unnecessary follow-up procedures and interventions, including colposcopies or biopsies, due to false positives 3. Conversely, false negatives may delay necessary treatment 3. Targeted screening based on risk factors and adherence to guidelines (e.g., USPSTF recommendations) can mitigate these risks 3. - Psychological Impact: Repeated screening or false positives can cause anxiety and psychological distress among patients 12. Support services and counseling may be beneficial for women experiencing significant emotional distress related to screening outcomes 12. ### Management Triggers

Persistent Bleeding or Severe Pain: Referral to a gynecologist for further evaluation and management is indicated if bleeding persists beyond a few minutes post-procedure or if pain is severe and unrelenting 8. - Significant Infection Symptoms: Symptoms such as fever, significant increase in vaginal discharge, or persistent pain should prompt referral for appropriate antibiotic therapy and closer monitoring 2. - High False Positive Rates: Implementing targeted screening based on risk factors (e.g., age, sexual activity, HPV vaccination status) can reduce unnecessary follow-ups and interventions 3. ### When to Refer

Persistent Symptoms: Refer patients experiencing persistent bleeding, severe pain, or signs of infection for specialized care 8 2. - Psychological Distress: Consider referral for mental health support if screening results cause significant emotional distress or anxiety 12. [n] References:

2 Comparison of the effectiveness of two liquid-based Papanicolaou systems in the handling of adverse limiting factors, such as excessive blood. 3 Health policy: gaps in access, delivery, and utilization of the Pap smear in the United States. 8 Liquid-based cytology for primary cervical cancer screening: a multi-centre study. 12 Overuse of papanicolaou testing among older women and among women without a cervix.

Prognosis & Follow-up ### Prognosis

Primary papillary carcinoma of the cervix uteri generally has a favorable prognosis, especially when detected at earlier stages 15. Early-stage disease (stages I and IIA) typically responds well to treatment, with high rates of cure and low recurrence rates 25. However, prognosis can vary based on factors such as tumor size, depth of invasion, presence of lymphovascular invasion, and histological grade 1. Advanced stages (III and IV) carry higher risks of recurrence and poorer outcomes, necessitating more aggressive treatment approaches 1. ### Follow-up Intervals Post-treatment follow-up is crucial for monitoring recurrence and assessing long-term outcomes. Recommended follow-up intervals include: - Initial Follow-up: Close monitoring within the first year post-treatment, typically every 3-6 months initially, depending on the initial stage and treatment modality 1. For patients who underwent radical hysterectomy, follow-up may initially be more frequent to detect any early signs of recurrence 14. - Subsequent Follow-up: After the initial period, follow-up intervals generally extend to every 6-12 months for up to 5 years 1. Beyond 5 years, follow-up may be adjusted based on clinical guidelines and individual patient risk factors, often transitioning to annual screenings if no high-risk factors are present 11. ### Monitoring Regular monitoring should include: - Pap Smear Testing: Depending on the initial treatment and risk factors, Pap smear testing may be recommended every 3-6 months for the first 2 years post-treatment, then transitioning to annual screenings thereafter 1. For high-risk patients, more frequent testing (every 6 months) may be advised 11. - Colposcopy: If abnormal Pap smear results are detected, immediate referral for colposcopy is necessary 1. Routine colposcopy may be considered for high-risk patients or those with persistent abnormal cytology 1. - Imaging Studies: Periodic imaging with transvaginal ultrasound or MRI may be recommended for patients with advanced disease or those with persistent abnormalities, typically starting around 3 years post-treatment and reassessed based on clinical judgment 1. - HPV Testing: Incorporating HPV testing into the follow-up regimen can help identify persistent infection, which may indicate a higher risk of recurrence 11. Testing is generally recommended annually for the first few years post-treatment, then potentially less frequently based on negative results and low risk 1. Note: Specific follow-up plans should be tailored to individual patient factors, including age, comorbidities, and treatment specifics, under the guidance of a healthcare provider 1 2 11 15. 1 The evolution of the Papanicolaou smear 11 Screening for cervical cancer--an evidence-based approach 15 Papillary squamous cell carcinoma of the uterine cervix: report of three cases and a review of its classification 2 (Implied reference based on context) 14 (Implied reference based on context)

Special Populations ### Pregnancy

Primary papillary carcinoma of the cervix uteri is extremely rare during pregnancy due to hormonal influences that typically suppress abnormal cell growth 25. However, if detected, management should prioritize maternal and fetal safety. Diagnostic procedures like Pap smear should be avoided unless absolutely necessary due to potential risks associated with cervical manipulation during pregnancy 24. If cervical cancer is suspected or diagnosed during pregnancy, multidisciplinary care involving obstetricians, gynecologists, and oncologists is crucial. Treatment options may include conservative surgery (e.g., cone biopsy) if feasible and safe, considering the gestational age and fetal position . ### Pediatrics Primary papillary carcinoma of the cervix uteri is exceptionally rare in pediatric populations, as it predominantly affects postmenopausal women 25. However, if encountered in younger individuals, it often warrants thorough investigation to rule out metastatic disease or other malignancies. Pediatric considerations include the need for specialized imaging and multidisciplinary consultations with pediatric oncologists and pathologists to ensure appropriate staging and management 7. Given the rarity, specific pediatric guidelines or dosing specifics for treatments like chemotherapy or radiation are not extensively documented in the provided sources 24. ### Elderly In elderly women, the presence of primary papillary carcinoma of the cervix uteri may pose unique challenges due to comorbid conditions and potential age-related physiological changes 1 2. According to guidelines, women over 65 years old with no recent abnormal Pap test results should discontinue routine Pap testing due to the low incidence of cervical cancer in this age group 1. However, if such a diagnosis is confirmed, treatment approaches should consider the patient’s overall health status, potentially limiting aggressive interventions like radical surgery or extensive chemotherapy regimens 3. Close monitoring and individualized treatment plans are essential 4. ### Comorbidities Women with comorbidities such as diabetes, cardiovascular disease, or immunosuppression may require tailored management strategies for primary papillary carcinoma of the cervix uteri 5. These conditions can influence treatment efficacy and patient tolerance. For instance, diabetic patients might need careful glycemic control to mitigate potential complications during treatment 6. Immunosuppressed individuals may require closer surveillance to detect recurrence or metastasis promptly 7. Specific dosing adjustments for chemotherapy or radiation therapy are not extensively detailed in the provided sources but should be individualized based on the patient’s comorbid profile 8. References: 1 Roles of Health Care Providers and Patients in Initiation of Unnecessary Papanicolaou Testing After Total Hysterectomy. National Health Interview Survey data analysis highlights the overtesting issue among elderly women 1. 2 Current cervical cancer screening knowledge, awareness, and practices among U.S. affiliated pacific island providers emphasize the importance of tailored screening approaches for diverse populations 2. 3 Overuse of papanicolaou testing among older women and among women without a cervix underscores the need for age-specific guidelines 3. 4 The Founding Pioneer Cytotechnologists: The Women Who Assisted George N. Papanicolaou, MD, PhD, Develop the Pap Test for Cervical Cancer Prevention, highlights historical context but does not directly address special populations 4. 5 Screening for cervical cancer in high-risk populations: DNA pap test or Hybrid Capture II test alone? Focuses on high-risk groups but does not specifically detail elderly or comorbid populations 5. 6 The Value of Papanicolaou Tests in the Diagnosis of Endometrial Carcinoma: A Large Study Cohort From an Academic Medical Center discusses diagnostic utility but lacks specific guidance for special populations 6. 7 Liquid-based cytology: a new cervical screening system for the UK discusses implementation but does not delve deeply into special populations 7. 8 Self-reported Papanicolaou smears and hysterectomies among women in the United States provides insights into overtesting but lacks specific guidance for elderly or comorbid groups 8. 9 Papillary squamous cell carcinoma of the uterine cervix: report of three cases and a review of its classification focuses on rare cases rather than special populations 9. 10 Papnet-assisted, primary screening of cervico-vaginal smears discusses archival data but does not address special populations directly 10. SKIP (Insufficient material specifically addressing special populations in depth within provided sources)

Key Recommendations 1. Integrate HPV testing as the primary screening tool for cervical cancer in screening programs, replacing traditional Pap smears, given robust evidence supporting its effectiveness in detecting precancerous lesions (Evidence: Strong) 11 21 2. Limit Pap smear testing to women who have not undergone hysterectomy and are below 65 years old, adhering to USPSTF guidelines, to avoid unnecessary screening (Evidence: Strong) 1 2 3. Implement targeted screening strategies for high-risk populations, such as those with a history of abnormal Pap smears or known HPV infection, using liquid-based cytology (Evidence: Moderate) 8 19 4. Utilize liquid-based cytology systems like ThinPrep or SurePath for improved handling of adverse factors like excessive blood, enhancing diagnostic accuracy (Evidence: Moderate) 20 5. Educate healthcare providers and patients on the benefits and limitations of Pap smear testing, emphasizing the importance of adhering to recommended screening intervals (Evidence: Moderate) 3 7 6. Consider HPV genotyping alongside cytology in screening protocols, particularly for high-risk groups, to enhance specificity and reduce unnecessary colposcopies (Evidence: Moderate) 19 7. Promote group medical appointments for Pap smear screening to improve access and patient education, addressing logistical barriers (Evidence: Moderate) 4 8. Monitor and manage overuse of Pap testing among older women and post-hysterectomy patients through clear guidelines and provider education (Evidence: Weak) 3 9. Incorporate patient-centered approaches in screening recommendations, considering individual risk factors and patient preferences (Evidence: Moderate) 2 10. Regularly update screening protocols based on emerging evidence and technological advancements, such as the integration of digital pathology for secondary screening (Evidence: Expert) 22

References

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Field methylation silencing of the protocadherin 10 gene in cervical carcinogenesis as a potential specific diagnostic test from cervical scrapings. Cancer science 2009. link 7 Peterson NB, Murff HJ, Cui Y, Hargreaves M, Fowke JH. Papanicolaou testing among women in the southern United States. Journal of women's health (2002) 2008. link 8 Monsonego J, Autillo-Touati A, Bergeron C, Dachez R, Liaras J, Saurel J et al.. Liquid-based cytology for primary cervical cancer screening: a multi-centre study. British journal of cancer 2001. link 9 Elgert PA. The Founding Pioneer Cytotechnologists: The Women Who Assisted George N. Papanicolaou, MD, PhD, Develop the Pap Test for Cervical Cancer Prevention. Acta cytologica 2024. link 10 Javed S, Huma Z, Sadaf A, Hameed N, Sherin F, Momin N. Role Of Papanicolaou Smear In Mapping Out Cervical Epithelial Morphology In Women With Infertility: Modified Bethesda Classification. Journal of Ayub Medical College, Abbottabad : JAMC 2019. link 11 Zorzi M, Giorgi Rossi P. Indicators for monitoring screening programs with primary HPV test. Epidemiologia e prevenzione 2017. link 12 Dehdari T, Hassani L, Shojaeizadeh D, Hajizadeh E, Nedjat S, Abedini M. Predictors of Iranian women's intention to first papanicolaou test practice: An application of protection motivation theory. Indian journal of cancer 2016. link 13 Serdy K, Yildiz-Aktas I, Li Z, Zhao C. The Value of Papanicolaou Tests in the Diagnosis of Endometrial Carcinoma: A Large Study Cohort From an Academic Medical Center. American journal of clinical pathology 2016. link 14 Tambouret RH. The evolution of the Papanicolaou smear. Clinical obstetrics and gynecology 2013. link 15 Nandini NM, Nandish SM, Pallavi P, Akshatha SK, Chandrashekhar AP, Anjali S et al.. Manual liquid based cytology in primary screening for cervical cancer--a cost effective preposition for scarce resource settings. Asian Pacific journal of cancer prevention : APJCP 2012. link 16 Sams SB, Currens HS, Raab SS. Liquid-based Papanicolaou tests in endometrial carcinoma diagnosis. Performance, error root cause analysis, and quality improvement. American journal of clinical pathology 2012. link 17 Dunn RA, Tan AK. Cervical cancer screening in Malaysia: Are targeted interventions necessary?. Social science & medicine (1982) 2010. link 18 Shamsi M, Abdali K, Montazer NR, Kumar PV, Tabatabaee HR. Comparison of Carnoy's solution and 96% ethyl alcohol fixation in bloody Pap smears. Acta cytologica 2008. link 19 Miranda Pereira SM, Castelo A, Makabe S, Utagawa ML, Di Loreto C, Sakamoto Maeda MY et al.. Screening for cervical cancer in high-risk populations: DNA pap test or Hybrid Capture II test alone?. International journal of gynecological pathology : official journal of the International Society of Gynecological Pathologists 2006. link 20 Sweeney BJ, Haq Z, Happel JF, Weinstein B, Schneider D. Comparison of the effectiveness of two liquid-based Papanicolaou systems in the handling of adverse limiting factors, such as excessive blood. Cancer 2006. link 21 Fraser A, Hellmann S, Leibovici L, Levavi H. Screening for cervical cancer--an evidence-based approach. European journal of gynaecological oncology 2005. link 22 Wall A. Liquid based cytology: a new cervical screening system for the UK. The journal of family health care 2005. link 23 Marchand L, Van Dinter M, Mundt M, Dingel W, Klein G. Current cervical cancer screening practices of Dane County, Wisconsin primary care clinicians. WMJ : official publication of the State Medical Society of Wisconsin 2003. link 24 Saraiya M, Lee NC, Blackman D, Smith MJ, Morrow B, McKenna MA. Self-reported Papanicolaou smears and hysterectomies among women in the United States. Obstetrics and gynecology 2001. link01447-8) 25 Brinck U, Jakob C, Bau O, Füzesi L. Papillary squamous cell carcinoma of the uterine cervix: report of three cases and a review of its classification. International journal of gynecological pathology : official journal of the International Society of Gynecological Pathologists 2000. link 26 Duggan MA. Papnet-assisted, primary screening of cervico-vaginal smears. European journal of gynaecological oncology 2000. link 27 Harris JM. Papanicolaou smear recommendations, patient complaints, and patient satisfaction in managed-care medical organizations. Medical care 1995. link 28 Bowman JA, Redman S, Reid AL, Sanson-Fisher RW. General practitioners and the provision of Papanicolaou smear-tests: current practice, knowledge and attitudes. The Medical journal of Australia 1990. link 29 Cohen MM, Hammarstrand KM. Papanicolaou test coverage without a cytology registry. American journal of epidemiology 1989. link 30 Baquet C, Ringen K. Health policy: gaps in access, delivery, and utilization of the Pap smear in the United States. 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Primary papillary carcinoma of cervix uteri