Journal of Cytology
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Year : 2012  |  Volume : 29  |  Issue : 1  |  Page : 20-25
Clinicopathological importance of Papanicolaou smears for the diagnosis of premalignant and malignant lesions of the cervix

Departemnt of Pathology, King Edward Medical University, Lahore, Pakistan

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Date of Web Publication27-Feb-2012


Background: Premalignant and malignant lesions are not uncommon in Pakistani women, especially in the older age-groups
Aim: This study was conducted to determine the clinicopathological importance of conventional Papanicolaou (Pap) smears for the diagnosis of premalignant and malignant lesions of the cervix.
Materials and Methods: Pap smears of 1000 women were examined from January 2007 to June 2009. Only cases with neoplastic cytology were included.
Results: The overall frequency of normal, inadequate, neoplastic, and infective smears was 50%, 1.8%, 10.2%, and 38.3%, respectively. Most of the patients (67%) were in the postmenopausal age-group, with the mean age being 44.7±15.63 years. The commonest clinical signs/symptoms seen among the 102 patients with neoplastic gynecological lesions were vaginal discharge and abnormal bleeding (93/102;(91.2% and 62/102;60.7%). Of the 102 cases with neoplastic lesions 46 patients (45%) had low-grade squamous cell intraepithelial lesions (LSILs), 22 (21.5%) had high-grade squamous cell intraepithelial lesions (HSILs), 14 (13.7%) had squamous cell carcinoma, and 6 (5.8%) showed features of adenocarcinoma. Ten (9.8%) cases showed cytology of atypical squamous cells of undetermined significance (ASCUS) and four (3.9%) cases had atypical glandular cells of undetermined significance (AGUS).
Conclusion: We conclude that cervical smear examination is well suited for diagnosing neoplastic disease. It is clear that cervical neoplastic lesions are becoming a problem in Pakistan.

Keywords: Neoplastic gynecological diseases; Papanicolaou smear; squamous cell intraepithelial lesion

How to cite this article:
Bukhari MH, Saba K, Qamar S, Majeed MM, Niazi S, Naeem S. Clinicopathological importance of Papanicolaou smears for the diagnosis of premalignant and malignant lesions of the cervix. J Cytol 2012;29:20-5

How to cite this URL:
Bukhari MH, Saba K, Qamar S, Majeed MM, Niazi S, Naeem S. Clinicopathological importance of Papanicolaou smears for the diagnosis of premalignant and malignant lesions of the cervix. J Cytol [serial online] 2012 [cited 2023 Mar 21];29:20-5. Available from:

   Introduction Top

Worldwide, malignant lesions of the cervix represents the most frequent cause of mortality and morbidity and the third most common cause of cancer deaths in females. [1] Pakistan, like other developing countries, is undergoing epidemiological transition and faces a double burden of disease. Cervical cancer is the fourth most common cancer among Pakistani women. [2] The incidence of cervical cancer in Pakistan is lower than in various western countries, but the mortality is higher. This higher rate of mortality is attributed to the late presentation of cervical cancers in Pakistan. [3]

The Papanicolaou (Pap) test is a screening test performed using cells from the uterine cervix. The Pap test was introduced as a cervical screening test in 1943 by George Papanicolaou, for whom it is named. The test is simple, quick, and painless. With the woman lying on an examination table, the clinician inserts a speculum into her vagina to open it and then, using a wooden scraper, takes a sample of cells from in and around the cervix; this is placed on a glass slide and rinsed in liquid fixative and sent to the laboratory for examination. The Papanicolaou cervical cytology test is capable of detecting cervical cancer at an early stage and is used widely in developed countries, where it has decreased both the incidence and mortality of cervical cancer. It has been estimated that the use of this simple and cost-effective technique has reduced the incidence of cervical cancer by at least 70%. Unfortunately, many developing countries lack the facility to carry out widespread Pap screening. [4],[5],[6]

This study was conducted to determine the clinicopathological importance of conventional  Pap smear More Detailss in the diagnosis of premalignant and malignant lesions of the uterine cervix.

   Materials and Methods Top

This was a hospital-based cross-sectional study on women aged 20-70 years. One thousand Pap smears were taken and sent to the department of pathology for analysis. Patients presenting with complaints of backache, hypogastric pain, painful sexual intercourse, vaginal discharge, or postcoital bleeding were included in the study. Those having vaginal bleeding other than postcoital and postmenopausal were excluded. History and other relevant information were recorded in a specially designed proforma. Written informed consent (in Urdu and English) was obtained from all patients (or the relative) before the smear was taken. This study was in accordance with the Declaration of Helsinki. Approval for the study was obtained from the review board of ethical committee of the University, Lahore. [7]

Before taking the Pap smear we ensured that the patient was not menstruating, had passed 10-20 days of her menstrual cycle, and had not douched or used tampons or vaginal medication for the preceding 24 hours.

The samples were smeared on two glass slides and were submitted to the pathology department for examination. The smears were stained using the conventional Papanicolaou technique, in which tinctorial dyes and acids are selectively retained by cells. Unstained cells cannot be visualised under the light microscope. The stains originally chosen by Papanicolau were selected to highlight cytoplasmic keratinisation, which actually has almost nothing to do with the nuclear features that are used to make the diagnosis these days. [8],[9]

After staining, the samples were examined by a qualified cytotechnologist and histopathologist under a light microscope. All the smears were classified according to Bethesda system 2001. [10]

Statistical analysis

Simple percentages of the lesions were calculated and compared with each other. Fisher's exact test was used (whenever there were small expected frequencies) to determine the statistical significance of the differences.

   Results Top

During this study 1000 Pap smears were examined in our laboratory and out of these 102 (10.2%) smears showed premalignant or malignant changes. The ages of the subjects ranged from 20 to 70 years, with a mean of 44.7 ± 15.63 years. The peak incidence of neoplastic gynecologucal lesions (NGL) (40/102; 39.2%) was found during 50-59 years. Out of 102 smears, 18 (1.8%) were inadequate for cytological examination [Table 1].

Among the 102 cases showing premalignant and malignant lesions, 62 (60.7%) patients were of postmenopausal age, 45 (44%) patients were of low socioeconomic status, 57 (55.8%) patients had history of early marriage, 69 (67.6%) patients had history of multiparity, and 93 (91.2%) patients had complaints of vaginal discharge. Only 15 (14.7%) patients had used oral contraceptives; 7 patients (6.8%) were smokers; and 7 (6.8%) patients had history of abortions. Only 9% of the women had had a Pap test within the previous 5 years; 91% said that they had never had this test before [Table 2].
Table 2: Frequency of known risk factors in 102 cases of neoplastic gynecological lesions

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Out of the102 cases with premalignant and malignant features, there were 10 (9.8%), 4 (3.9%), 46 (45%), and 22 (21.8%) cases of atypical squamous cells of undetermined significance (ASCUS), atypical glandular cells of undetermined significance (AGUS), low-grade squamous cell intraepithelial lesions (LSILs), and high-grade squamous cell intraepithelial lesions (HSILs), respectively. Fourteen patients (13.7%) had squamous cell carcinoma (SCC) and 6 patients (5.8%) had adenocarcinoma [Table 1] and [Figure 1]. Cases of ASCUS, AGUS, and LSIL were kept under follow-up.
Figure 1: (a) Squamous cell lesion of undetermined significance (Pap, ×400); (b) glandular cell lesion of undetermined significance (Pap, ×400); (c) low-grade squamous intaepithelial lesion with Human Papilloma Viral changes (Pap, ×400); and (d) high-grade squamous intraepithelial lesion (Pap, ×400)

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Of the 22 HSILs cases that were biopsied or underwent hysterectomies, one patient (4.5%) had low-grade dysplasia, seven (32%) had moderate dysplasia, and eleven (50%) had severe dysplasia/carcinoma in situ. One case was found with invasive cervical carcinoma (4.5%). Two cases (9%) were false positives. On histopathology of 20 malignant cases, nine of them were well-differentiated squamous cell carcinomas (WDSCCs), three cases were moderately differentiated squamous cell carcinomas (MDSCCs), two cases were poorly differentiated squamous cell carcinomas (PDSCCs), and six cases were adenocarcinomas. The overall specificity and accuracy for detection of malignant lesions (HSILs and carcinomas) was 100%; however, for grading of the different lesions the sensitivity, specificity, accuracy, positive predictive value (PPV), and negative predictive value (NPV) was 63%, 100%, 70%, 100%, and 40%, respectively [Table 3].
Table 3: Histopathological diagnosis of Papanicolaou-stained cervical smears

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The morphological features of all neoplastic lesions are given in detail in [Table 4] and [Figure 1].
Table 4: Cytological features of neoplastic lesions of female genital tract on Pap smear

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   Discussion Top

Abnormal vaginal discharge and postmenopausal bleeding was the commonest presentation among our patients [93/102; (91.2% and 62/102;60.7%] and the majority of our patients with neoplastic gynecological lesions (premalignant or malignant lesions) were in the age-group of 50-59 years.

Early marriage and multiparity were the two most common risk factors seen in our patients. Low-income women were found to be at high risk of developing cervical cancer, which is attributable not only to the higher prevalence of risk factors in this population but also to the lack of follow-up of abnormal Pap smears. Low socioeconomic status was commonly associated risk factor for neoplastic gynecological lesions and was seen in 44% Patients in our study. This is comparable to the study conducted in California which showed that low income women were at higher risk of developing cervical cancer. [11],[12] Awareness about the Pap test was poor in our study population, with only 9% ever having had a Pap test within the preceding 5 years.

The overall frequency of normal, inadequate, neoplastic, and infective smears was 50%, 1.8%, 10.2%, and 38.3%, respectively. Most of the patients (67%) were in the postmenopausal age-group, with the mean age being 44.7 ± 15.63 years. In the present study, out of 102 positive cases, 14 women (13.7%) had SCC (invasive) while 6 patients had adenocarcinoma. There were 10 (9.8%), 4 (3.9%), 46 (45%) and 22 (21.8%) cases of ASCUS, AGUS, LSIL, and HSIL, respectively.

The 22 cases of HSIL and the 14 cases of SCC were followed up till biopsy or hysterectomy and we found that only 9% of these cases had false positive Pap smears; 4.5% were found to be low grade on histopathology, whereas they had initially been diagnosed as HSIL on Pap smear cytology. ASCUS is the term used by patholo­gists to denote cellular changes that are more marked than that attributable to reactive changes but that are quantitatively or qualitatively insufficient for a definitive diagnosis of SIL. [10],[13],[14],[15] Ten (9.8%) of the Pap smears showed features of ASCUS, with enlargement of the nucleus (to 2.5-3 times the normal intermediate cell nucleus) and a slight increase in the nuclear/cytoplasmic ratio. There was marked variation in nuclear size and shape. Possible binucleation and mild hyperchromasia was also observed but the chromatin remained finely granular, with smooth and regular outline and limited irregularities.

Forty-six (45%) Pap smears revealed LSIL, with scattered or sheets of atypical cells seen against an inflammatory background. Nuclear abnormalities were generally confined to cells with 'mature' or superficial cell, with enlargement of the nucleus to at least three times the area of the normal intermediate nuclei, resulting in an increased nuclear/cytoplasmic ratio. There was moderate variation in nuclear size and shape, often with binucleation and multinucleation. The nucleoli were not seen and nuclear membranes was normal or having slight irregularities in some cells. There were regular distribution of chromatin in the nuclear areas. Cell borders in LSIL, were distinct with well-defined, clear cytoplasm or a peripheral dense rim of cytoplasm. It was important to note that cells showing perinuclear halos in the absence of nuclear abnormalities did not qualify for the diagnosis of LSIL.

Twenty-two cases (21.5%) in our study showed HSIL morphology. The arrangement of the cells was variable: In some smears they were occurring scattered, while in others they were found arranged in sheets or in syncytial-like aggregates. The nuclear changes in HSIL were more pronounced than in LSIL. The nuclear abnormalities were observed predominantly as squamous cells with 'immature' lacy and delicate or a dense metaplastic cytoplasm; occasionally the cytoplasm was 'mature' and densely keratinized as in smears of cases with SCC. Nuclear enlargement was in the same range as that seen in LSIL but the cytoplasmic area was decreased, leading to a marked increase in the nuclear/cytoplasmic ratio. In cells with very high nuclear/cytoplasmic ratios, though the nuclear enlargement was often actually less than in LSIL cases, the overall HSIL cell size was smaller than in LSIL. Hyperchromasia was evident; the chromatin was finely or coarsely granular, with a more irregular distribution than in LSIL. Nucleoli were prominent in most of the neoplastic HSIL cells which were not seen in LSIL. Two features were more evident in HSIL cases: i.e., irregularities of nuclear membrane and irregular distribution of coarse chromatin in the nuclear areas. There was marked variation in cellular size and shape, with caudate and spindle cells that frequently contained dense orangeophilic cytoplasm. Their nuclei also varied markedly in size and configuration, with numerous dense opaque nuclear forms. The chromatin, when discernible, was coarsely granular and irregularly distributed with parachromatin clearing. There were many macronucleoli, though these were less common than in nonkeratinising SCC. Tumor diathesis was also present. Smears showing the above features were diagnosed as SCC with keratinisation.

SCC without keratinisation was seen scattered or in syncytical-like aggregates and the cells displayed all the features of HSIL but, in addition, they contained prominent macronucleoli and markedly irregular distribution of chromatin, including coarse chromatin clumping and parachromatin clearing. There was also an associated tumor diathesis, consisting of necrotic debris and old blood with macrocytosis, multinucleation, fine chromatin pattern, and hypochromatic or condensed macro-or micro-nuclei with karyopyknotic or karyorhexic changes [Table 4]. These cytological features were consistent with the criteria described by Koss, Höffken, and Smith et al. [16],[17],[18]

Our findings are consistent with that of Saha and Thapa, [19] who found sensitivity, specificity, PPV, NPV, and diagnostic accuracy for HSIL of 100%, 89.5%, 55.6%, 100%, and 90.7%, respectively. In our study the sensitivity, specificity, PPV, NPV and diagnostic accuracy was 100%.

The cytoplasm of the malignant cells of adenocarcinoma was denser, basophilic abundant, and clear and streaming effect was seen It was vacuolated (large vacuole) and granular (a lavender-violet granularity). There were irregularities, thickening, and swelling of cellular membranes. The prominent nuclear changes were chromatin margination towards the nuclear periphery (vesicular pattern), extreme variation in nuclear size and shape, and the presence of macronucleoli. These features were consistent with descriptions of Koss [20] and others. [18],[21],[22],[23],[24]

   Conclusion Top

Neoplastic gynecological diseases (NGD) are not uncommon in our setup and the Pap test is an effective modality for its diagnosis. To improve the coverage of the Pap test under the National Screening Program, information and awareness should be created about the utility of this important diagnostic modality to reduce the mortality due to cervical carcinoma.


Our population demonstrated very poor coverage with the Pap test, which may be due to poor awareness regarding the importance of this simple test. We would like to make the following recommendations for the benefit of patients and convenience of gynecologists with little modification in previous consensus. The focus is on how the management plan need to be different from that recommended by the American Society for Colposcopy and Cervical Pathology (ASCCP) due to the high-risk nature of the population and the high cost or poor availability of human papilloma virus (HPV) testing or colposcopy in developing countries.

  1. The mass media should be used to disseminate information and increase awareness about the importance of the Pap test for screening after marriage. Improving awareness is imperative before a coordinated cancer screening program, as advised by the ASCCP, can be implemented in developing countries. Education on proper sexual behavior and the risks associated with early marriage, multiparity, multiple partners, smoking, etc. should be given at high school level.
  2. A number of inexpensive community-based methods have been identified for improving awareness regarding cervical cancer screening, e.g., lectures, workshops, videos and graphic representation, radio broadcasts targeting rural women, and presentations to community nurses. Physicians also need to be proactive in educating their patients about such screening methods.
  3. There should be a proper communication between gynecologists and pathologists for proper diagnosis, early delivery of reports, maintenance of records of follow-up, and reporting of any unusual finding.
  4. A proforma should be designed for gynecologists that should be properly filled and returned to the pathology department to avoid ambiguities. A uniform reporting system should be used for cervical lesions; the nomenclature for reporting cervical cytology results has undergone several changes since the publication of the original Papanicolaou system and, therefore, the updated Bethesda system of reporting should be used for a uniform and smooth reporting system.
  5. There is no need of a repeat Pap test in women under 30 years with non-neoplastic and inflammatory smears; however, specific or nonspecific treatment of cervicitis is recommended.
  6. There is no need for urgent repeat Pap smear in women under 30 years with non-neoplastic and inflammatory smears, but annual screening must be performed.
  7. When an atypical Papanicolaou smear is seen in a young, sexually active, Pakistani woman, colposcopic evaluation is recommended without delay.
  8. If the Pap smear shows ASCUS/LSIL, the patient should be followed up and a repeat Pap smear done if the symptoms progress. If the repeat Pap test is negative then the patient can be placed in a routine cervical screening program. However, if such lesions are associated with high-risk HPV infection, the patient should be immediately referred for colposcopy. These patients should be kept under follow-up for 1 year.
  9. If the repeat smear shows persistence or progression of atypia, the patient should be immediately referred for colposcopic evaluation and biopsy of the cervix prior to any form of therapy.
  10. Women treated in the past for HSILs or cervical carcinomas remain at risk for persistence or recurrence for at least 20 years after treatment and should therefore continue to have annual screening for at least 20 years.

   References Top

1.Spinelli A. Preinvasive diseases of the cervix, vulva, and vagina. Semin Oncol Nurs 2002;18:184-92.  Back to cited text no. 1
2.Ferlay J, Bray F, Pisani P, Parkin DM. GLOBOCAN 2002: Cancer incidence, mortality and prevalence worldwide, version 2.0. IARC Cancer Base No. 5. Vol. 10. Lyon: IARC Press; 2004. p. 1741-52.  Back to cited text no. 2
3.Badar F, Anwar N, Meerza F, Sultan F. Cervical carcinoma in a Muslim community. Asian Pac J Cancer Prev 2007;8:24-6.  Back to cited text no. 3
4.Zamani N. Management of abnormal cervical cytology. J Coll Physc Surg Pak 1994;4:28-9.  Back to cited text no. 4
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6.Singh P, Ilancheran A. The 'Pap' or cervical smear and the role of colposcopy in screening for carcinoma of the cervix. Singapore Med J 1989;30:302-5.  Back to cited text no. 6
7.WMA. World Medical Association Declaration of Helsinki: Ethical principles of medical research involving human subjects. [Available from:]. [Last cited on 2010 March 21]. 2004; Available from: [Available at:]. [Last cited on 2010 March 21].  Back to cited text no. 7
8.Coste J, Cochand-Priollet B, de Cremoux P, Le Gales C, Cartier I, Molinie V, et al. Cross sectional study of conventional cervical smear, monolayer cytology, and human papillomavirus DNA testing for cervical cancer screening. BMJ 2003;326:733.  Back to cited text no. 8
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10.Solomon D, Davey D, Kurman R, Moriarty A, O'Connor D, Prey M, et al. The 2001 Bethesda System: Terminology for reporting results of cervical cytology. JAMA 2002;287:2114-9.  Back to cited text no. 10
11.Coker AL, Eggleston KS, Meyer TE, Luchok K, Das IP. What predicts adherence to follow-up recommendations for abnormal Pap tests among older women? Gynecol Oncol 2007;105:74-80.  Back to cited text no. 11
12.Engelstad LP, Stewart SL, Nguyen BH, Bedeian KL, Rubin MM, Pasick RJ, et al. Abnormal Pap smear follow-up in a high-risk population. Cancer Epidemiol Biomarkers Prev 2001;10:1015-20.  Back to cited text no. 12
13.Davey DD, Neal MH, Wilbur DC, Colgan TJ, Styer PE, Mody DR. Bethesda 2001 implementation and reporting rates: 2003 practices of participants in the College of American pathologists interlaboratory comparison program in cervicovaginal cytology. Arch Pathol Lab Med 2004;128:1224-9.  Back to cited text no. 13
14.Davey DD, Woodhouse S, Styer P, Stastny J, Mody D. Atypical epithelial cells and specimen adequacy: Current laboratory practices of participants in the college of American pathologists interlaboratory comparison program in cervicovaginal cytology. Arch Pathol Lab Med 2000;124:203-11.  Back to cited text no. 14
15.Solomon D, Frable WJ, Vooijs GP, Wilbur DC, Amma NS, Collins RJ, et al. ASCUS and AGUS criteria. International academy of cytology task force summary. Diagnostic Cytology Towards the 21 st Century: An International expert conference and tutorial. Acta Cytol 1998;42:16-24.  Back to cited text no. 15
16.Hoffken H. Comparison of cytological features in keratinizing dysplasia and keratinizing squamous carcinoma (author's transl). Geburtshilfe Frauenheilkd 1978;38:431-7.  Back to cited text no. 16
17.Koss L, Melamed M. Squamous cell carcinoma of the Uterine cervix and related precacerous lesions in Diagnostic cytology of organs. In: Koss' diagnostic cytology and its histopathologic bases. 5 th ed. Philidelphia: JB Lippincot Company; 2005. p. 282-395.  Back to cited text no. 17
18.Smith P. Cervical intraepithelial neoplasia and squamous cell carcinoma of the cervix. In: Gray W, Mckee G, editors. Diagnostic cytopathology, 2nd ed. New York: Churchill Livingstone; 2002. p. 721-53.  Back to cited text no. 18
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20.Koss L, Melamed M. Adenocarcinoma and related tumors of the uterine cervix in diagnostic cytology of organs. In: Koss' diagnostic cytology and its histopathologic bases. 5 th ed. Philadelphia: JB Lippincot Company; 2005. p. 395-421.  Back to cited text no. 20
21.Belsley NA, Tambouret RH, Misdraji J, Muzikansky A, Russell DK, Wilbur DC. Cytologic features of endocervical glandular lesions: Comparison of sure path, ThinPrep, and conventional smear specimen preparations. Diagn Cytopathol 2008;36:232-7.  Back to cited text no. 21
22.Thiryayi SA, Marshall J, Rana DN. Differentiating between endocervical glandular neoplasia and high-grade squamous intraepithelial lesions in endocervical crypts: Cytological features in ThinPrep and SurePath cervical cytology samples. Diagn Cytopathol 2009;37:315-9.  Back to cited text no. 22
23.Young RH, Clement PB. Endocervical adenocarcinoma and its variants: Their morphology and differential diagnosis. Histopathology 2002;41:185-207.  Back to cited text no. 23
24.Crasta JA, Chaitra V, Simi CM, Correa M. An audit of cervicovaginal cytology in a teaching hospital: Are atypical glandular cells under-recognised on cytological screening? JOC 2009;26:69-73.  Back to cited text no. 24

Correspondence Address:
Mulazim Hussain Bukhari
Professor of Pathology and Director PhD Program, King Edward Medical University, Lahore
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Source of Support: King Edward Medical University, Lahore, Conflict of Interest: None

DOI: 10.4103/0970-9371.93213

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  [Figure 1]

  [Table 1], [Table 2], [Table 3], [Table 4]

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