Gynecologic Cytopathology

Acta Cytologica Received: September 11, 2017

Accepted after revision: September 19, 2017
DOI: 10.1159/000481654
Published online: November 8, 2017

Atypical Squamous Cells in Liquid-Based Cervical

Cytology: Microbiology, Inflammatory Infiltrate,
and Human Papillomavirus-DNA Testing
Geilson Gomes de Oliveira a Renata Mirian Nunes Eleutério b
Ana Katherine Silveira Gonçalves c Paulo César Giraldo d José Eleutério Jr. a–e
a
Department of Pathology, Faculty of Medicine, Federal University of Ceará, and b Department of Pharmacy, Federal
University of Ceará, Fortaleza, c Department of Obstetrics and Gynecology, Federal University of Rio Grande do
Norte, Natal, d Department of Obstetrics and Gynecology, State University of Campinas, Campinas, and
e
Department of Maternal and Child Health, Faculty of Medicine, Federal University of Ceará, Fortaleza, Brazil

Keywords microorganism was present, and Candida spp. was associ-

Atypical squamous cells of undetermined significance ·
Infection human papillomavirus · Cytology
Abstract
Objective: The aim of this study was to assess the correlation
between atypical squamous cells (ASC) and inflammatory in-
filtrate and vaginal microbiota using cervical liquid-based
cytological (SurePath®) and high-risk human papillomavirus
(HR-HPV) tests. Study Design: A cross-sectional study was
conducted using a 6-year database from a laboratory in For-
taleza (Brazil). Files from 1,346 ASC cases were divided into
subgroups and results concerning inflammation and vagi-
nal microorganisms diagnosed by cytology were compared
with HR-HPV test results. Results: An absence of specific mi-
croorganisms (ASM) was the most frequent finding (ASC of
undetermined significance, ASC-US = 74%; ASC – cannot ex-
clude high-grade squamous intraepithelial lesion, ASC-H =
68%), followed by bacterial vaginosis (ASC-US = 20%; ASC-
H = 25%) and Candida spp. (ASC-US = 6%; ASC-H = 5%).
Leukocyte infiltrate was present in 71% of ASC-US and 85%
of ASC-H (p = 0.0040), and in these specific cases HR-HPV
tests were positive for 65 and 64%, respectively. A positive
HR-HPV test was relatively more frequent when a specific
ated with HR-HPV-positive results (p = 0.0156), while an ASM
was associated with negative HR-HPV results (p = 0.0370).
Conclusion: ASC-US is associated with an absence of inflam-
mation or vaginosis, while ASC-H smears are associated with
Trichomonas vaginalis and inflammatory infiltrate. A positive
HR-HPV is associated with Candida spp. in ASC cytology.
© 2017 S. Karger AG, Basel
Introduction
In 2001, the Bethesda System review defined 2 catego-
ries for atypical squamous cells (ASC). The first is ASC of
undetermined significance (ASC-US), in which abnor-
mal cytological findings suggest a low grade. The second
is ASC – cannot exclude high-grade squamous intraepi-
thelial lesion (ASC-H), which is when the same doubt oc-
curs with suspicions of a high-grade squamous intraepi-
thelial lesion [1, 2]. Currently, these atypical findings are
the most common cytological abnormalities [3–5]. Al-
though these findings are uncertain, they can indicate an
inflammatory, reactive, or repair process of normal cytol-
ogy, but they can also signify an underlying precancerous
condition or even an invasive lesion [6].
129.127.145.240 - 11/16/2017 1:41:09 AM

© 2017 S. Karger AG, Basel Correspondence to: Dr. Geilson Gomes de Oliveira
Federal University of Ceará
Rua Aluisio Borba, 132, casa 4, Engenheiro Luciano Cavalcante
E-Mail karger@karger.com
Fortaleza, Ceará 60813-730 (Brazil)
www.karger.com/acy
Univ.of Adelaide
Downloaded by:

E-Mail geilson.ce @ gmail.com

 Color version available online
Fig. 1. ASC-US in LBC (SurePath®). Original magnification,
×1,000.
Several microorganisms coexist in the vaginal micro-
biota with exfoliated cells, transudates, and exudates, and
they vary according to the delicate balance of endoge-
nous and exogenous factors [7, 8]. Instability can lead to
the disordered growth of microorganisms, which can be-
come pathogenic and cause symptoms [9]. Cervicovagi-
nal infections are common in women and cause uncom-
fortable symptoms, such as vaginal discharge, odor, and
pruritus [9, 10]. Concomitant infections by multiple mi-
croorganisms are also common, and they may have sym-
biotic interactions [11]. Some of these pathogens can in-
fect the female genital mucosa and induce cytological
atypia [12]. Cervicitis and vaginitis are among the main
confounding factors for the diagnosis of squamous cel-
lular atypia [13]. Few studies have examined the poten-
tial risks of infectious agents that induce ASC cytology
[14].
Chronic or recurrent inflammation in cell prolifera-
tion has a well-known association with the processes of
cancer development. Chemical substances from inflam-
mation may favor both microbial colonization and po-
tentially transformed or truly neoplastic cells [15]. The
aim of this study was to assess the association between
ASC-specific pathogens, inflammatory infiltrate, and hu-
man papillomavirus (HPV)-DNA in cervical liquid-
based cytology (LBC). The subjects were women who at-
tended a private clinic in a large city in the northeast of
Brazil.
2 Acta Cytologica
DOI: 10.1159/000481654
Color version available online
Fig. 2. ASC-H in LBC (SurePath®). Original magnification, ×1,000.
Materials and Methods
A cross-sectional study was carried out using files on women
diagnosed with ASC in cervical LBC performed between January
2010 and July 2016 in the LABPEC database, which is a private
laboratory in Fortaleza, Brazil. Only ASC findings in LBC samples
were analyzed, regardless of patient age. Patients with immuno-
logical deficiency, pregnancy, or ASC findings in conventional cy-
tology were excluded. There were 2,458 cervical cytology cases
with ASC results, of which 1,346 records were included and 1,112
were excluded. The patients were then divided into 2 groups based
on findings of ASC-US and ASC-H.
The data collected were entered in a spreadsheet with informa-
tion about age, parity, gynecological examination findings, mor-
phological cytology findings, associated pathogens, and findings
correlated with ASC and HPV-DNA tests. LBC cytology was per-
formed using SurePath (BD, Franklin Lakes, NJ, USA). The slides
were interpreted according to the Bethesda System criteria. Cyto-
logical characterization of microorganisms was conducted in ac-
cordance with the Bethesda System and included Trichomonas
vaginalis (TV), fungal organisms morphologically consistent with
Candida species, a shift in flora suggestive of bacterial vaginosis
(BV), bacteria morphologically consistent with Actinomyces spe-
cies, and cellular changes consistent with herpes simplex virus. In-
flammatory infiltrate was defined by the presence of more than 5
polymorphonuclear leukocytes per epithelial cell in the high-pow-
er field (×1,000) [16].
Second-generation hybrid capture (Qiagen AG, Hom-
brechtikon, Switzerland) was performed using the microwell for-
mat and probes for high-risk (HR) genotypes (16, 18, 31, 33, 35,
39, 45, 51, 52, 56, 58, 59, 68). Expression was measured in reactive
light units. Polymerase chain reactions (PCR) were performed us-
ing a Cobas® 4800 system (Roche Diagnostics, Pleasanton, CA,
USA) with 3 channels (HPV16, HPV18, or 12 other HR-HPV
types) according to the manufacturer’s instructions.
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Gomes de Oliveira/Eleutério/Silveira
Gonçalves/Giraldo/Eleutério Jr.
Univ.of Adelaide
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Table 1. ASC in LBC (SurePath®) and
microbiological findings as suggested by ASC-US, ASC-H, p
the Bethesda System (n = 1,357) n (%) n (%)

Actinomyces spp. 4 (0.33) 0 (0) 1.0000

Candida spp. 71 (5.91) 7 (4.52) 0.5847
Cytopathic effect of HSV 2 (0.17) 0 (0.00) 1.0000
Suggestive of BV 237 (19.72) 39 (25.16) 0.9226
T. vaginalis 0 (0) 3 (1.94) 0.0015
Absence of specific microorganisms 888 (73.88) 106 (68.39) 0.1490
Total 1,202 (100.00) 155 (100.00)

Fisher exact test. ASC-US, atypical squamous cells of undetermined significance; ASC-
H, atypical squamous cells – cannot exclude high-grade squamous intraepithelial lesion;
HSV, herpes simplex virus; BV, bacterial vaginosis.

Table 2. Presence of inflammatory

infiltrate (>5 polymorphonuclear/ ASC-US, ASC-H, p Prevalence ratio
squamous cells) in ASC in LBC n (%) n (%) (95% CI)
(Surepath®) (n = 751)
Present 458 (70.57) 86 (84.31) 0.0040 2.045 (1.229 – 3.403)
Absent 191 (29.43) 16 (15.69)
Total 649 (100) 102 (100)

χ2 test. ASC-US, atypical squamous cells of undetermined significance; ASC-H, atypi-

cal squamous cells – cannot exclude high-grade squamous intraepithelial lesion.

Statistical analyses were carried out using the software Graph-
Pad Prism version 6.0 (GraphPad Software Inc., San Diego, CA,
USA). The results were compared using the Fisher exact or χ2 tests
with a significance level of less than 5% (p < 0.05) and 95% confi-
dence intervals (CI). The prevalence ratio was calculated when rel-
evant. All statistical tests were 2 sided. This study was approved by
the Research Ethics Committee of the Federal University of Ceará,
Brazil.
Results
Among the 1,346 results included in this study, we
found 1,192 (88.56%) cases of ASC-US and 154 (11.44%)
cases of ASC-H. The average age was 33.06 years (±11.59,
range 17–81) in the ASC-US group and 34.79 years
(±11.60, range 17–82) in the ASC-H group. The mean
parity for the ASC-US group was 1.17 ± 2.06 with a
range of 0–17 parturitions, while for the ASC-H group
the range was 0–7 parturitions with a mean of 1.65 ±
2.06.
Only 1,337 records had information about the general
descriptive analysis, including 1,183 for ASC-US (Fig. 1)
and 154 for ASC-H (Fig. 2). Of these, there were 878
(74.22%) smears described as inflammatory for ASC-US
and 114 (74.03%) for ASC-H.
For ASC-US, 237 (20.03%) cases were described as
compatible with BV, and 68 (5.75%) of the cytology cases
were described as normal. For ASC-H, about 39 (25.32%)
cases were described as BV and 1 (0.65%) was described
as normal. The microbiology findings included 1,357 re-
ported ASC smears. An absence of specific microorgan-
isms (ASM) was predominantly found in both groups
(ASC-US = 888; ASC-H = 106). BV was the next most
frequent (ASC-US = 237; ASC-H = 39), followed by Can-
dida spp. (ASC-US = 71; ASC-H = 7). An association was
found between microorganisms and the ASC subgroups,
as shown in Table 1.
Among the 992 smears described as inflammatory,
only 751 cytological smears were assessed for the pres-
ence of leukocyte infiltrate. There was a statistically sig-
nificant association between the ASC-H group and the
presence of inflammatory infiltrate (Table 2). There were
231 smears with a concomitant HR-HPV test, which were
positive in 132 ASC-US cases (101 Hybrid Capture 2 and
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ASC in LBC: Microbiology, Inflammatory Acta Cytologica 3

Infiltrate, and HPV-DNA Testing DOI: 10.1159/000481654
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Table 3. HR-HPV-DNA and
inflammatory infiltrate Inflammatory infiltrate Inflammatory infiltrate p
(>5 polymorphonuclear/squamous cells) absent present
in ASC in LBC (SurePath®) (n = 138)
HR-HPV- HR-HPV- HR-HPV- HR-HPV-
DNA DNA DNA DNA
negative positive negative positive

ASC-US 20 (47.62) 22 (52.38) 28 (34.57) 53 (65.43) 0.1767

ASC-H 2 (50.00) 2 (50.00) 4 (36.36) 7 (63.64) 1.0000

Values are presented as n (%). Fisher exact test. HR-HPV-DNA in Hybrid Capture®
and Cobas 4800 Roche®. ASC-US, atypical squamous cells of undetermined significance;
ASC-H, atypical squamous cells – cannot exclude high-grade squamous intraepithelial
lesion.

Table 4. HR-HPV test and microbiology

in cases of ASC in LBC (SurePath®) HR-HPV HR-HPV p Prevalence ratio
(n = 231) positive negative (95% CI)

Candida spp. 10 (6.71) 0 (0.00) 0.0156 1.590 (1.437 – 1.759)

BV 32 (21.48) 13 (15.85) 0.3857 1.130 (0.9104 – 1.404)
Absence of specific
microorganisms 107 (71.81) 69 (84.15) 0.0370 1.659 (0.9965 – 2.761)
Total 149 (100) 82 (100)

Values are presented as n (%). Fisher exact test. BV, bacterial vaginosis.

31 PCR with a positivity of 64.39%) and 17 ASC-H cases Discussion

(12 Hybrid Capture 2 and 5 PCR with 65.38% positivity).
In only 138 of the 751 smears, there was an association
between inflammatory infiltrate and positivity for HR-
HPV. Inflammatory infiltrate was more frequent in the
event of HR-HPV for both ASCs, but the difference was
not statistically significant (Table 3).
We also investigated whether there is a correlation
between HR-HPV positivity and microbiology in ASC
cytology. Both HPV tests and microbiological agents
were indicated in 234 records. For HPV-negative sam-
ples, there were 69 (84.15%) cases of ASM and 13
(15.85%) cases of BV. For positive samples, we found
107 (71.81%) cases of ASM, 32 (21.48%) cases of BV, and
10 (6.71%) cases of Candida spp. ASM was more fre-
quently associated with negative HR-HPV-DNA with
statistical significance (p = 0.0370), while positivity in
the HR-HPV test was statistically more frequent for
Candida spp. (p = 0.0156). No cases were found for TV,
Actinomyces spp., and HSV with a concomitant HPV-
DNA test (Table 4).
An abnormal vaginal microbiota can be both a pitfall
in cytological results and a cofactor in preinvasive lesions
[17, 18]. Therefore, it is important to determine the cor-
relation between abnormal vaginal microbiological activ-
ity and atypical squamous cells [19]. Inflammatory cytol-
ogy may result from nonspecific cervical processes or
genital infections by Chlamydia trachomatis, Candida al-
bicans, TV, BV, and herpes simplex virus [20]. Cytology
is not the correct tool for diagnosing cervical and vaginal
pathogens, but in developing countries it is the only way
to assess genital microbiota [21].
About 74% of the smears in our study were inflamma-
tory in both groups, while there was no description of
vaginitis or vaginosis in smears in the minority of cases,
which was most significant for the ASC-US group. Re-
garding the relationship between microorganisms and
ASC cytology, ASM smears were more frequent for both
groups, but without significance. The frequency of a spe-
cific pathogen was higher in patients with ASC-US than
in patients in the ASC-H group in another study [22].
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4 Acta Cytologica Gomes de Oliveira/Eleutério/Silveira

DOI: 10.1159/000481654 Gonçalves/Giraldo/Eleutério Jr.
Univ.of Adelaide
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Paba et al. [23] corroborated the correlation between cy-
tology classified as ASC-US and cervicovaginal infec-
tions. They suggested that some of these results are due to
genital infection and that these patients should be treated
prior to cytology and HPV testing.
BV was described in 20% of the ASC-US group and
25% of the ASC-H group. Other studies have also report-
ed a predominance of BV but with different frequencies
[19, 20]. The characteristic “clue cells” may hide the atyp-
ical character of real lesions, and the satisfied criteria
would be indicative of ASC.
No association was found between Candida spp. and
ASC in our study, but another report described a pre-
dominance of this pathogen in ASC-US smears prepared
by the ThinPrep automated method [14]. Interestingly,
the finding of TV showed statistical significance for the
ASC-H group. Another study found an association be-
tween ASC-US and these vaginal protozoa when compar-
ing LBC results (SurePath®) and using real-time PCR for
TV, but no cases of ASC-H were reported with this patho-
gen [11]. This discrepancy in the results can be explained
by the more sensitive method used in that study, as well
as the different populations examined.
In our study, an inflammatory infiltrate was found in
75% of ASC-US cases and 80% of ASC-H cases, and it was
more significant for ASC-H cases. A previous study ob-
served histopathological intraepithelial lesions in half of
the cases of highly inflammatory cytology [24]. It is im-
portant to evaluate inflammation due to the risk of it hid-
ing HPV cytopathy. Another study showed that cytomor-
phological findings suspected of HPV infection were
significantly masked by the presence of moderate and
marked inflammation [10]. Our study indicated no sta-
tistical correlation between inflammatory infiltrate and
the presence of HR-HPV for ASC smears. However, we
compared ASC-US with ASC-H, but not with normal
smears. A recent study found significantly more leuko-
cytes in conventional Pap smears of women who tested
positive for HPV-DNA [25].
In their Latin American Screening Study (LAMS),
Longatto-Filho et al. [26] suggested that vaginal infec-
tions most likely promotes HPV disease in women from
developing countries. When correlating the vaginal mi-
crobiota with HR-HPV in ASC-US cytology, we observed
a predominance of BV, but there was no statistically sig-
nificant difference with HR-HPV positivity. Other stud-
ies have pointed out an association between BV and HR-
HPV infection, suggesting BV may be a cofactor for squa-
mous intraepithelial lesions due the action of pathogens
causing inflammatory processes and microabrasions on
ASC in LBC: Microbiology, Inflammatory
Infiltrate, and HPV-DNA Testing
the cervical epithelium [19]. A significantly higher fre-
quency for Candida spp. and HR-HPV positivity was ob-
served, in agreement with a previous study that assessed
the prevalence of the vaginal microbiome in women with
known HPV outcomes [25]. On the other hand, the pres-
ence of Candida spp. was correlated more frequently with
a negative HPV-DNA in a cross-sectional study on the
influence of HPV on cytological vaginitis with LSIL [27].
Another report considered that Candida spp. had no as-
sociation with HR-HPV [15].
Our study has various limitations. First, we evaluated
data from files in a private laboratory. Furthermore, we
studied the microbiota using only the morphology, which
has a lower sensitivity than biomolecular methods. HPV-
DNA tests were not used in all cases. Although we used 2
HPV detection tests, a report pointed out that sensitivity
and specificity was similar among them [28]. A better
study design, such as a prospective model, is essential to
confirm our findings.
We conclude that ASC-US is significantly more fre-
quent than ASC-H in the absence of inflammation or vag-
inosis. TV was significantly more prevalent in ASC-H
smears, but the number of records was insufficient for a
better definition. Inflammatory infiltrate was associated
with the ASC-H group, but no association was found be-
tween the presence of vaginal leukocytes and HR-HPV
positivity. Positive HR-HPV results are associated with
the presence of Candida spp. in the ASC cytology.
Disclosure Statement
The authors have no potential conflicts of interest in relation to
this article.
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