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Article
Pap smear accuracy for the diagnosis
of cervical precancerous lesions
Tropical Doctor
2019, Vol. 49(1) 34–39
! The Author(s) 2018
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DOI: 10.1177/0049475518798532
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Elie Nkwabong1, Ingrid Laure Bessi Badjan2 and
Zacharie Sando3
1
Associate Professor, Department of Obstetrics & Gynecology,
University Teaching Hospital / Faculty of Medicine and Biomedical
Sciences, Yaoundé, Cameroon
2
Student, Faculty of Medicine and Biomedical Sciences, Yaoundé,
Cameroon
3
Associate Professor, Department of Pathology, Faculty of Medicine and
Biomedical Sciences, Yaoundé, Cameroon
Corresponding author:
Elie Nkwabong, P.O. Box 1364 Yaoundé, Cameroon.
Email: enkwabong@yahoo.fr
Nkwabong et al.
35
Abstract
This cross-sectional descriptive study, aimed at accessing the accuracy of Pap smear in diagnosing cervical precancerous
lesions, was carried out between 3 January and 30 April 2017. All women screened for cervical dysplasia by means of Pap
smear with biopsy done for confirmation were subsequently recruited. Data were analysed using SPSS 20.0. A total of
231 women were screened for cervical dysplasia using Pap smear with 75 biopsies performed. Cervical dysplasia was
noticed in 54 cases. The sensitivity, specificity, positive predictive and negative predictive values of Pap smear were 55.5%,
75%, 88.2% and 33.3%, respectively. The sensitivity of Pap smear remains low. Therefore, biopsy should be done in cases
of macroscopic cervical architectural changes irrespective of the result of the Pap smear. Moreover, to reduce the
number of women with cervical precancerous lesions, the government should make available financial resources to set up
HPV vaccination programmes rather than screening programmes.
Keywords
Cervical precancerous lesions, negative predictive value, Pap smear, positive predictive value, sensitivity, specificity
Introduction
Cervical cancer is the second most frequently diagnosed
gynaecological cancer worldwide.1 An estimated
527,600 new cases of cervical cancer were reported
worldwide in 2012, with around 265,700 deaths.
Approximately 90% of cervical cancer deaths occurred
in developing parts of the world.2 It is the third leading
cause of cancer death among women in less developed
countries. The highest incidence and mortality rates are
reported in Africa.2
The main risk factor for cancer of the cervix is human
papilloma virus (HPV) infection. Cervical cancer may be
prevented, or at least diagnosed at an early stage, given
that the cervix is an organ easily accessible to clinical
evaluation. Mortality from cancer of the cervix may be
avoided, if not reduced, if precancerous lesions are diagnosed and treated. Cervical intraepithelial neoplasia
(CIN) 1 needs around 10–15 years to evolve to the
stage of cervical cancer.3 Immunosuppression may
reduce this time interval.
Cervical dysplasia may be diagnosed using Pap
smear. All epithelia shed and superficial cells may be
collected and analysed. Pap smear consists of collecting
shed superficial cells of the transformation zone and
their subsequent examination by a cytopathologist.
The sensitivity of Pap smear is <70% in many studies.4–6 Therefore, Pap smear might not be an appropriate test for the diagnosis of cervical precancerous
lesions. Consequently, some cases of cervical dysplasia
might unknown evolve to cervical cancer, especially
when this method has been used for screening. The
techniques for diagnosing cervical precancerous lesions
have improved. Indeed, the liquid medium cytology
technique has been recently used but with conflicting
results.7,8
No recent study evaluated the reliability of Pap
smear in the diagnosis of cervical precancerous lesions
in our environment, hence this study which aimed at
evaluating its accuracy in the diagnosis of cervical dysplasia as well as looking at the sociodemographic profile of women affected by cervical dysplasia.
Methods
This cross-sectional descriptive study was carried out in
two university teaching hospitals between 3 January
and 30 April 2017. All women who were screened for
cervical dysplasia by means of Pap smear were
recruited. Biopsy of the cervix was performed in all
women with abnormal results as well as in women
with normal results, but with macroscopic architectural
cervical changes. Women with cancer at biopsy were
excluded when analysing the accuracy of screening of
cervical precancerous lesions. When calculating the
accuracy of Pap smear, women who refused cervical
biopsy because they could not contribute financially
to biopsy too were excluded. Informed consent was
obtained from each patient. This study received
approval from the national ethics committee.
The variables recorded on a questionnaire included
the patient’s age, age at first sexual intercourse, age at
first delivery, number of pregnancies, abortions and
deliveries, cumulated number of sexual partners and
tobacco consumption. These variables were chosen
because we hypothesised that they could influence the
occurrence of cervical dysplasia. Other variables studied were the macroscopic appearance of the cervix,
the result of Pap smear and that of cervical biopsy.
Our minimal sample size of 44 patients was calculated using the following formula9 for descriptive
studies
N ¼ Pð1 PÞZa2 =D2
where Za ¼ 1.96 corresponds to a confidence level of
0.05, D ¼ 0.08 is the degree of precision and the prevalence of cervical dysplasia (P) was 7.9% in our milieu.10
36
Tropical Doctor 49(1)
Women screened : n= 231
Macroscopically normal cervices : n=186
Normal Pap
smears:
n=107
Abnormal
Pap smears :
n=79
Refusal of
biopsy: n=49
No
dysplasia
n=7
Macroscopically abnormal cervices: n= 45
Biopsies
done: n=30
Dysplasia
n=23
No
dysplasia
n=2
Abnormal Pap smears:
n=10 (all biopsied)
Dysplasia
n=4
Microinvasion
n= 4
Microinvasion
n=1
Normal Pap smears:
n=35 (all biopsied)
Dysplasia
n=27
No
dysplasia
n=7
Figure 1. Flowchart showing screening sequences.
The variables of women who presented dysplastic
lesions were compared to those who did not present
any dysplastic lesions. Data were analysed using SPSS
20.0. The t-test was used to compare continuous variables and Fisher’s exact test to compare categorical
variables. P < 0.05 was considered statistically significant. Moreover, the accuracy of cervical Pap smear in
diagnosing cervical dysplasia was assessed.
Results
During the study period, 231 women (186 having
macroscopically normal cervices and 45 slight macroscopic cervical architectural changes) were screened for
cervical dysplasia using Pap smear. Of the 186 women
with a macroscopic normal cervix, 79 had cervical dysplastic cells, but only 30 accepted cervical biopsies.
Of these 30 women, cervical dysplasia was found in
23 cases. In seven cases, there was no dysplasia.
All the 45 women with macroscopic cervical architectural changes (43 erythematous cervices and two
small polypoid lesions) had colposcopy directed
cervical biopsy. Among these women, Pap smear was
normal in 35 cases, and revealed the presence of dysplastic cells in 10 cases. Among these 10 women, biopsy
showed four cervical dysplasia, two cases without dysplasia and four cases of microinvasion. Among the
35 women who presented macroscopic cervical architectural changes without dysplastic cells found at Pap
smear, biopsy showed 27 cervical dysplasia, seven cases
without dysplasia and one case of microinvasion
(Figure 1).
In summary, 75 biopsies were carried out with 54
showing cervical dysplasia (54/231 or 23.4%), 16 nondysplastic lesions as well as five micro-invasive lesions
(2.1%) that were excluded when analysing the accuracy
of screening of cervical precancerous lesions. The sociodemographic and obstetrical variables of the study
population is presented in Table 1.
Results of Pap smear, presented according to
Bethesda system, was abnormal (cells showing abnormal nucleus activity) in 34 cases (14.7%). They included
11 (32.3%) high-grade squamous intraepithelial lesions
(HSIL), 13 (38.2%) low-grade squamous intraepithelial
lesions (LSIL) and 10 (29.4%) atypical squamous cell
of undetermined significance (ASCUS). Furthermore,
22 with chronic cervicitis were observed. In 14 cases,
no abnormality was found. Of the 231 participants, 107
women (46.3%) had Pap negative smears a few years
earlier, while 124 women (53.7%) had never been
screened before.
The results of cervical biopsies are presented in
Table 2. Biopsy showed 54 cervical intraepithelial
neoplasia (CIN) (20 CIN 1, 21 CIN 2 and 13 CIN 3)
and no dysplasia in 16 cases (Table 3). Biopsy among
the 10 women with ASCUS revealed two cervical
dysplasia (20%), including one CIN 1 and one CIN 2.
The eight other women with ASCUS had either chronic
inflammation (three cases) or normal epithelium (five
cases).
Nkwabong et al.
37
Table 1. Sociodemographic and obstetrical variables among the population under study.
Variables
Women with
cervical dysplasia
(n ¼ 54)
Women without
cervical dysplasia
(n ¼ 16)
P value
Patient age (years)
Age at 1st intercourse
Age at 1st delivery
Abortions (n)
Deliveries (n)
Sexual partners (n)
Tobacco consumption* (n (%))
Previous cancer screening (n (%))
43.5 9.8
16.7 2.7
20.0 4.3
1.3 1.3
4.9 2.3
7.2 2.6
3/54
25/54
43.0 11.0
16.0 3.1
19.1 2.1
2.0 1.0
6.1 3.2
6.0 2.1
0
7/16
0.862
0.381
0.423
0.051
0.099
0.096
0.581
1
(24–63)
(11–25)
(14–28)
(0–7)
(0–10)
(1–12)
(5.6)
(46.3)
(26–63)
(12–23)
(16–23)
(0–4)
(2–12)
(1–10)
(0)
(43.7)
Values are presented as mean SD (range) unless specified otherwise.
*One active and two passive tobacco consumptions.
Table 2. Cervical non-dysplastic abnormalities after biopsy.
Abnormality
n
%
Inflammation
Polyp
Total
13
3
16
81.2
18.8
100
Table 3 also shows the accuracy of Pap smear in the
diagnosis of cervical dysplasia.
All the women screened collected their results
(reports of Pap smear and biopsy). All patients with
cervical precancerous lesions at biopsy had either cryotherapy (36 cases) or loop electrosurgical excision procedures (18 cases).
Discussion
Our prevalence of abnormal Pap smear (14.7%) is
higher than the 6.0% found in Thailand among pregnant women.11 The most common abnormal Pap smear
was LSIL in our study (38.2%). LSIL was also the most
common Pap smear abnormality observed in Thailand
(44%).11 Our data showed that cervical dysplasia is frequent among women screened for cervical precancerous
lesions. Our hospital-based prevalence of cervical dysplasia (23.4%) is higher than that of 7.9% observed in
our environment in a previous study.10 Our high prevalence might be attributed to the fact that it is the prevalence among women who consulted in our unit and not
among the general population.
The mean age of patients observed in our study (43.5
years) was higher than that of 35.7 years observed in
Pakistan.12 This can be explained by the fact that their
youngest patient was 19 years old, while the youngest
patient in our study was 24 years old. According to
some societies, screening should concern women aged
25–69 years.13,14 Our patient aged 24 years first had
Table 3. Accuracy of Pap smear in diagnosing cervical dysplasia.
Cervical dysplasia on biopsy specimen
Pap smear
Present
Absent
Total
Positive
Negative
Total
30 (a)
24 (c)
54 (a þ c)
4 (b)
12 (d)
16 (b þ d)
34 (a þ b)
36 (c þ d)
70 (a þ b þ c þ d)
Sensitivity: a/a þ c ¼ 30/54 ¼ 55.5%; specificity: d/b þ d ¼ 12/16 ¼ 75%;
positive predictive value: a/a þ b ¼ 30/34 ¼ 88.2%; negative predictive
value: d/c þ d ¼ 12/36 ¼ 33.3%.
sexual intercourse at the age of 11 years. She might
have presented cervical dysplasia many months
before, given that it was the first time she was screened.
We think that screening should start earlier, for
instance at 21 years, as done by Ryu et al. in the
Korea University Medical Center, Seoul, Republic of
Korea,15 especially among women whose first sexual
intercourse occurred before the age of 12 years. In
our study, another patient first had sexual intercourse
at the age of 12 years. Age at first intercourse is decreasing, with some adolescents abusing children at the age
of eight or nine years.16,17
No significant difference was observed between
women with cervical dysplasia and those with nondysplastic lesions as concerns maternal age
(P ¼ 0.862), tobacco consumption (P ¼ 0.581), age at
first sexual intercourse (P ¼ 0.381), abortion number
(whether spontaneous or induced) (P ¼ 0.051), age at
first delivery (P ¼ 0.423), delivery number (P ¼ 0.099)
and number of sexual partners (P ¼ 0.096). This suggests that the previously described risk factors for cervical dysplasia are only co-factors.18 The main risk
factor, not investigated in this series, is HPV infection
that is mostly spread by sexual intercourse.
38
The presence of cervical invasion or micro-invasion
among some women is explained by the fact that the
majority of our women (53.7%) never had cervical
screening combined with adequate treatment.
Moreover, the diagnosis might have been missed in a
previous screening among women who had a prior Pap
smear. Indeed, 107 women (46.3%) were screened negative for Pap smear a few years before. Women should
be encouraged to perform Pap smear or other screening
methods more often. They should also be prepared for
immediate treatment of positive cases.
The presence of dysplasia and cancer among women
with macroscopic cervical architectural changes negative for Pap smear reminds us that biopsy should be
directly carried out in such cases, i.e. when the cervix
looks abnormal.
The sensitivity, for women who had also a biopsy, of
a Pap smear in our study (55.5%) was similar to that of
52% found by Bhattacharyya et al. in India,4 but
higher than the 18.2% observed in Iran6 and lower
than the 63.2% found by Bobdey et al. in India.5
This shows that biopsy should be preferred in certain
cases such as those with macroscopic cervical architectural changes. This low sensitivity also reveals that Pap
smear is ineffective in reducing mortality from cancer of
cervix. The government should look for financial
resources to put an emphasis on HPV vaccination
rather than on screening.
The specificity of Pap smear noticed in our study
(75%) was similar to the 76% observed in Turkey.19
The negative predictive value of Pap smear observed
in our series (33.3%) was lower than the 71.3% found
in Iran6 and the 92% noticed in Turkey.19
For cases with slight macroscopic cervical architectural changes, colposcopy-directed biopsy might be
associated or substituted to Pap smear to reduce the
false-negative rate, as suggested by some authors.19
Moreover, this attitude shortens the proceedings.
The presence of ASCUS was observed in 10 women
in our series. Some societies believe that women with
ASCUS or LSIL could just be observed and followed
up every six months, and colposcopy-directed biopsy is
advised after three consecutive abnormal smears.14,20 In
low-resource countries, for financial or cultural reasons, many women do not routinely attend hospital.
If they do, some of them are lost to follow-up.13 We
think that women from low-resource countries with
ASCUS should be immediately investigated (colposcopy-directed biopsy), as it has been associated in
our study with 20% of cervical dysplasia. This point
of view is shared by some authors in Japan who
observed cases of CIN 3 and carcinoma in-situ among
women diagnosed with ASCUS.20 Screen-and-treat
approaches for cervical cancer prevention have been
proven effective in low-resource settings.21 World
Tropical Doctor 49(1)
Health Organization (WHO) guidelines for screening
and treatment of precancerous lesions for cervical
cancer prevention recommend colposcopy with or without biopsy among women with ASCUS living in high
HIV endemic regions.22
The limitation of our study is the absence of tests for
diagnosing HPV as this might have shown its association with cervical dysplasia. Moreover, we could not
be certain of the reliability of the answers given by
women, especially when it concerned the number of
sexual partners. Finally, cervical biopsies were not performed in all cases with abnormal Pap smear, because
some women could not contribute financially to both
Pap smear and biopsy, as biopsies might have increased
the size of our population with cervical dysplasia.
Indeed, women with low socioeconomic status are at
highest risk of cervical cancer.
Conclusion
The accuracy of Pap smear in diagnosing cervical precancerous lesions remain low. To reduce the rate of undiagnosed cervical dysplasia, colposcopy-directed biopsy
should replace or be associated to Pap smear among
women with macroscopic cervical architectural changes,
as suggested by some authors.19 Screening might start
10 years after the first sexual contact. Finally, given that
the sensitivity of Pap smear remains low, the authors
think that after two normal Pap smear results, it could
be repeated yearly or every two years rather than every
three years, as recommended,14 if resources are available.
Preferably, HPV vaccination might be the method of
choice, especially in resource-limited countries, as it will
be more cost-effective in preventing cervical precancerous
lesions and, therefore, cervical cancer.
Declaration of conflicting interests
The author(s) declared no potential conflicts of interest with
respect to the research, authorship, and/or publication of this
article.
Funding
The author(s) received no financial support for the research,
authorship, and/or publication of this article.
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Case Report
Bizarre extensive erythematous plaques
on the abdomen
Tropical Doctor
2019, Vol. 49(1) 39–42
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DOI: 10.1177/0049475518802540
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Sidharth Tandon1, Surabhi Sinha2 and Jasmeet Singh3
1
Specialist, Department of Dermatology, Venereology & Leprology, Dr.
Ram Manohar Lohia Hospital & Post Graduate Institute of Medical
Education & Research, New Delhi, India
2
Senior Resident, Department of Dermatology, Venereology & Leprology,
Dr. Ram Manohar Lohia Hospital & Post Graduate Institute of Medical
Education & Research, New Delhi, India
3
Senior Resident, Department of Dermatology, Dr Baba Saheb Ambedkar
Medical College and Hospital, New Delhi, India
Corresponding author:
Surabhi Sinha, Room no. 205, Academic Block, PGIMER Building, Dr. Ram
Manohar Lohia Hospital, New Delhi 110001, India.
Email: surabhi2310@gmail.com