Human papillomavirus and risk factors for cervical adenocarcinoma in the state of Pernambuco, Brazil

Costa, Telma Maria Lubambo; Heráclio, Sandra; Amorim, Melania Maria Ramos; Souza, Paulo Roberto Eleutério; Lubambo, Natália; Souza, Gustavo Fonseca de Albuquerque; Souza, Alex Sandro Rolland

doi:10.1590/1806-93042019000300009

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ORIGINAL ARTICLES • Rev. Bras. Saude Mater. Infant. 19 (3) • Jul-Sep 2019 • https://doi.org/10.1590/1806-93042019000300009 copy

Human papillomavirus and risk factors for cervical adenocarcinoma in the state of Pernambuco, Brazil

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Objectives:

to determine the incidence of the main high oncogenic risk types of the human papillomavirus (HPV) ( 16, 18, 31 and 33) and the risk factors for cervical adenocarcinoma.

Methods:

a case-control study was carried out with 324 women (69 with adenocarcinoma and 260 healthy controls) between 2001 and 2014. Information on risk factors associated with adenocarcinomawere collected and the detection performed on HPVby using Polymerase Chain Reaction (PCR) method.

Results:

adenocarcinoma was associated with age ≥40 years old (OR=2.95; 95%CI=1.13-7.71), ≤3 years of schooling (OR=2.34; 95%CI=1.02-5.37), presence of HPV (OR=6.75; 95%CI=2.41-18.91),women in menopausal status (OR=4.76; 95%CI:1.70-13.31) black race (OR=6.71; 95%CI= 2.11-21.32) and never had undergone cervical cancer screening (OR=9.92; 95%CI:2.41-40.81). Andamong the HPV types detected, HPV 18 was observed to be strongly associated with adenocarcinoma of the cervix (OR=99.1; 95%CI=12.96-757.78).

Conclusions:

the factors associated with cervical adenocarcinoma were ≥40 years old, ≤3 years of schooling, black race, menopausal status, never had undergone cervical cancer screening and the presence of HPV.

Key words
Adenocarcinoma in situ; Papillomaviridae; Molecular biology; Risk factors; uterine cervical neoplasms

Variable	Adenocarcinoma				OR	CI95%	p
	yes		no
	n	%	n	%
First sexual intercourse							0.62^* * Chi-square test,
< 20 years old	40	71.4	177	68.1	1.17	0.62-2.21
> 20 years old	16	28.6	83	31.9
Number of partners							0.04^* * Chi-square test,
< 2	40	71.2	147	56.5	1.92	1.02-3.61
> 2	16	28.6	113	43.5
Previous pregnancies							<0.001^* * Chi-square test,
>5	18	30.0	28	10.8	3.55	1.80-6.99
<5	42	70.0	232	89.2
Previous use of hormonal							<0.001^* * Chi-square test,
contraceptives
Yes	23	39.7	189	73.0	0.24	0.13-0.44
No	35	60.3	70	27.0
Menopause							<0.001^* * Chi-square test,
Yes	17	29.8	19	7.3	5.39	2.58-11.24
No	40	70.2	241	92.7
Condom use							0.16^ Fisher's exact test, STI= sexually transmitted infection, OR: Odds Ratio, CI95%= 95% confidence interval, HPV= human papillomavirus, BMI= body mass index.
Yes	1	1.8	20	7.7	0.21	0.03-1.63
No	56	98.2	240	92.3
Immunosuppressive drugs							0.7^ Fisher's exact test, STI= sexually transmitted infection, OR: Odds Ratio, CI95%= 95% confidence interval, HPV= human papillomavirus, BMI= body mass index.
Yes	0	0	5	1.9	-	-
No	60	100	255	98.1
Chronic disease							<0.001^* * Chi-square test,
Yes	41	65.1	95	36.7	3.22	1.81-5.72
No	22	34.9	164	63.3
STI							0.11^* * Chi-square test,
Yes	6	9.8	47	18.4	0.48	0.19-1.19
No	55	90.2	209	81.6
Current smoker							0.27^* * Chi-square test,
Yes	3	5.1	25	9.6	0.50	0.15-1.73
No	56	94.9	235	90.4
Former smoker							0.97^* * Chi-square test,
Yes	13	22.0	52	22.2	0.99	0.49-1.97
No	46	78.0	182	77.8
Smokes							0.24^* * Chi-square test,
Yes	13	22.0	77	29.7	0.67	0.34-1.31
No	46	78.0	182	70.3
Cancer screening							<0.001^ Fisher's exact test, STI= sexually transmitted infection, OR: Odds Ratio, CI95%= 95% confidence interval, HPV= human papillomavirus, BMI= body mass index.
No	17	29.3	6	2.3	17.5	6.54-47.12
Yes	41	70.7	254	97.7
HPV							<0.001^* * Chi-square test,
Yes	56	87.5	146	56.2	5.47	2.50-11.93
No	8	12.5	114	43.8
Age ≥40 years old							<0.001^* * Chi-square test,
Yes	51	79.7	133	51.2	3.74	1.94-7.22
No	13	20.3	127	48.8
Blackskin
Yes	9	16.4	15	5.8	3.19	1.32-7.74	0.02^ Fisher's exact test, STI= sexually transmitted infection, OR: Odds Ratio, CI95%= 95% confidence interval, HPV= human papillomavirus, BMI= body mass index.
No	46	83.6	245	94.2
BMI ≥25.0 kg/m²
Yes	25	64.1	138	56.8	1.34	0.67-2.74	0.39^* * Chi-square test,
No	14	35.9	105	43.2
Illiterate
Yes	9	17.6	11	4.2	4.85	1.89-12.41	0.004^ Fisher's exact test, STI= sexually transmitted infection, OR: Odds Ratio, CI95%= 95% confidence interval, HPV= human papillomavirus, BMI= body mass index.
No	42	82.4	249	95.8
Schooling ≤3 years
Yes	27	52.9	45	17.3	5.37	2.84-10.16	<0.001^* * Chi-square test,
No	24	47.1	215	82.7
No current partner
Yes	26	44.1	77	29.6	1.87	1.05-3.34	0.03^* * Chi-square test,
No	33	55.9	183	70.4
Lives in Recife or in the metropolitan region
Yes	43	67.2	218	83.8	0.39	0.21-0.73	0.002^* * Chi-square test,
No	21	32.8	42	16.2

Variables	Adenocarcinoma
Variables	Coefficient	Standard Error	OR	CI95%	p
Age ≥40 years old	1.08	0.49	2.95	1.13-7.71	0.03
Schooling ≤3 years	0.85	0.42	2.34	1.02-5.37	0.04
HPV	1.91	0.52	6.75	2.41-18.91	<0.001
Menopause	1.56	0.52	4.76	1.70-13.31	0.003
Blackskin	1.90	0.59	6.71	2.11-21.32	0.001
Never underwent screening	2.29	0.72	9.92	2.41-40.81	0.001
Constant	-4.80	0.62	-	-	<0.001

HPV	Women with adenocarcinoma		Healthy women		OR	CI95%	p
HPV	n=64	%	n=219	%	OR	CI95%	p
16	34	53.1	90	41.1	1.62	0.93-2.84	0.09^* * Chi-square test,
18	20	31.3	1	0.5	99.1	12.96-757.78	<0.001^ Fisher's exact test, OR= Odds Ratio, CI95%= 95% confidence interval, HPV= human papillomavirus.
31	33	51.6	40	18.3	4.76	2.62-8.66	<0.001^* * Chi-square test,
33	27	42.2	7	3.2	22.10	8.97-54.45	<0.001^* * Chi-square test,
16 alone	13	20.3	58	26.5	0.71	0.36-1.39	0.32^* * Chi-square test,
31 alone	7	10.9	14	6.4	1.80	0.69-4.67	0.17^ Fisher's exact test, OR= Odds Ratio, CI95%= 95% confidence interval, HPV= human papillomavirus.
33 alone	4	6.3	0	0	-	-	0.004^ Fisher's exact test, OR= Odds Ratio, CI95%= 95% confidence interval, HPV= human papillomavirus.
16, 18 together	3	4.7	0	0	-	-	0.01^ Fisher's exact test, OR= Odds Ratio, CI95%= 95% confidence interval, HPV= human papillomavirus.
16, 18 associated with other types	14	21.9	0	0	-	-	<0.001^ Fisher's exact test, OR= Odds Ratio, CI95%= 95% confidence interval, HPV= human papillomavirus.
16, 31 together	1	1.6	25	11.4	0.12	0.02-0.93	0.04^ Fisher's exact test, OR= Odds Ratio, CI95%= 95% confidence interval, HPV= human papillomavirus.
16, 31 associated with other types	16	25.0	25	11.4	2.59	1.28-5.22	0.007^* * Chi-square test,
16, 33 together	0	0	7	3.2	-	-	0.32^ Fisher's exact test, OR= Odds Ratio, CI95%= 95% confidence interval, HPV= human papillomavirus.
16, 33 associated with other types	14	21.9	7	3.2	8.48	3.25-22.11	<0.001^ Fisher's exact test, OR= Odds Ratio, CI95%= 95% confidence interval, HPV= human papillomavirus.
18, 31 together	2	3.1	1	0.5	7.03	0.63-78.85	0.13^ Fisher's exact test, OR= Odds Ratio, CI95%= 95% confidence interval, HPV= human papillomavirus.
18, 31 associated with other types	14	21.9	1	0.5	61.04	7.84-475.07	<0.001^ Fisher's exact test, OR= Odds Ratio, CI95%= 95% confidence interval, HPV= human papillomavirus.
18,33 together	1	1.6	0	0	-	-	0.46^ Fisher's exact test, OR= Odds Ratio, CI95%= 95% confidence interval, HPV= human papillomavirus.
18, 33 associated with other types	12	18.8	0	0	-	-	<0.001^ Fisher's exact test, OR= Odds Ratio, CI95%= 95% confidence interval, HPV= human papillomavirus.
31, 33 together	5	7.8	0	0	-	-	0.001^ Fisher's exact test, OR= Odds Ratio, CI95%= 95% confidence interval, HPV= human papillomavirus.
31, 33 associated with other types	20	31.3	0	0	-	-	<0.001^ Fisher's exact test, OR= Odds Ratio, CI95%= 95% confidence interval, HPV= human papillomavirus.
16, 18, 31 together	9	14.1	0	0	-	-	<0.001^ Fisher's exact test, OR= Odds Ratio, CI95%= 95% confidence interval, HPV= human papillomavirus.
16, 18, 33 together	8	12.5	0	0	-	-	<0.001^ Fisher's exact test, OR= Odds Ratio, CI95%= 95% confidence interval, HPV= human papillomavirus.
16, 31, 33 together	12	18.8	0	0	-	-	<0.001^ Fisher's exact test, OR= Odds Ratio, CI95%= 95% confidence interval, HPV= human papillomavirus.
18, 31, 33 together	9	14.1	0	0	-	-	<0.001^ Fisher's exact test, OR= Odds Ratio, CI95%= 95% confidence interval, HPV= human papillomavirus.
16, 18, 31, 33 together	6	9.4	0	0	-	-	<0.001^ Fisher's exact test, OR= Odds Ratio, CI95%= 95% confidence interval, HPV= human papillomavirus.

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[1] Contribuições dos autores

Souza ASR and Amorim MMR - performed all the data handling and statistical analyses. Souza PRE contributed to the methodological discussions. Costa TML and Souza ASR - drafted the first version of the article. Souza ASR, Amorim MMR, Costa TML, Souza PRE, Heráclio S, Souza GFA and Lubambo N revised the article on several occasions. All authors approved the final version of the manuscript.