Human papillomavirus infection and seroprevalence among female university students in Mexico

Figures & data

Table 1. Clinical characteristics of the participants. IUD = Intrauterine device

Sample	HPV genotype	HPV risk	Age	Sexual debut age	Number of lifetime sexual partners	Vaccine doses	Contraceptive method	Medical consultation
M 1	18	High	18	15	2	0	Condom	Gynecological evaluation
M 2	18	High	19	17	8	0	Condom	IUD
M 3	51	High	21	17	10	0	Oral contraceptive	Vaginal infection and condylomatosis
M 4	Negative	Negative	22	15	3	0	Oral contraceptive	Subdermal contraceptive
M 5	31	High	22	14	5	0	Condom	Gynecological evaluation
M 6	Negative	Negative	20	17	4	2	Condom	Gynecological evaluation
M 7	6	Low	22	15	3	0	IUD	Cervical screening
M 8	6	Low	24	16	4	0	Condom	Cervical screening
M 9	16	High	19	16	Unknown	0	Condom	Cervical screening
M 10	18	High	19	17	4	2	None	Vaginal infection
M 11	51	High	25	17	10	0	IUD and Condom	Cervical screening
M 12	53	Low	19	16	6	0	None	Vaginal infection
M 13	6	Low	19	14	3	1	Condom and contraceptive injection	Cervical screening
M 14	6	Low	22	20	12	0	Condom	Cervical screening
M 15	68	High	21	18	2	0	Condom	Gynecological evaluation
M 16	18	High	19	16	Unknown	0	Subdermal contraceptive and Condom	Vaginal infection
M 17	Negative	Negative	24	20	2	1	Condom	Cervical screening
M 18	Negative	Negative	21	14	4	2	Condom	Cervical screening
M 19	18	High	22	18	7	1	Condom	Condylomatosis
M 20	51	High	20	19	Unknown	0	None	Vaginal infection
M 21	31	High	20	17	1	0	Condom	Gynecological evaluation
M 22	Negative	Negative	24	17	2	0	Condom	Vaginal infection
M 23	Negative	Negative	23	16	4	0	Condom	Cervical screening
M 24	16	High	23	18	6	0	Condom	Cervical screening
M 25	31	High	24	19	3	2	Condom	Vaginal infection
M 26	Negative	Negative	19	17	2	1	Condom	IUD
M 27	59	High	19	17	6	2	Condom	Vaginal infection
M 28	16	High	21	16	6	0	IUD and Condom	Cervical screening
M 29	59	High	19	15	1	2	Condom	Gynecological evaluation
M 30	Negative	Negative	19	17	2	0	Condom	Vaginal infection
M 31	51	High	22	20	4	0	None	Cervical screening
M 32	51	High	18	17	6	3	Condom	Vaginal infection
M 33	66	?	19	17	1	1	Subdermal contraceptive	Cervical screening
M 34	51	High	19	16	5	0	None	Estudio de papanicolaou
M 35	Negative	Negative	18	18	1	0	Condom	Gynecological evaluation
M 36	16	High	21	20	2	1	Condom	Vaginal infection
M 37	18	High	19	17	1	3	Condom	Gynecological evaluation
M 38	31	High	24	19	4	0	Condom	Cervical screening
M 39	31	High	20		1	0	Condom	Gynecological evaluation
M 40	6	Low	20	18	1	0	Condom	Gynecological evaluation
M 41	16	High	23	21	1	0	Condom	Gynecological evaluationpor lesión en mama
M 42	31	High	20	16	4	0	Oral contraceptive and Condom	Condylomatosis
M 43	51	High	20	16	5	2	Condom	Condylomatosis
M 44	18	High	20	16	5	0	Condom	Vaginal infection
M 45	6	Low	21	19	4	2	Condom	Gynecological evaluation
M 46	Negative	Negative	22	17	6	0	Condom	Cervical screening
M 47	18	High	19	16	6	1	Subdermal contraceptive	Condylomatosis
M 48	16	High	19	18	2	0	Condom	Vaginal infection
M 49	31	High	24	19	2	0	IUD	Gynecological evaluation
M 50	Negative	Negative	23	16	3	2	None	Cervical screening
M 51	Negative	Negative	23	21	1	0	Condom	Condylomatosis
M 52	6	Low	22	18	3	0	None	IUD
M 53	16	High	21	18	2	0	Condom	Condylomatosis
M 54	Negative	Negative	19	18	1	1	None	Vaginal infection
M 55	31	High	17	16	2	0	Condom	Cervical screening
M 56	31	High	21	20	2	0	Condom	IUD
M 57	Negative	Negative	21	15	3	1	Condom	Cervical screening
M 58	51	High	18	16	2	2	Condom	Cervical screening
M 59	51	High	22	17	4	0	Condom	Condylomatosis
M 60	Negative	Negative	24	20	2	0	None	Cervical screening
M 61	Negative	Negative	35	18	8	0	Condom	Gynecological evaluation
M 62	18	High	25	15	15	0	IUD	Cervical screening
M 63	Negative	Negative	24	20	2	0	Condom	IUD
M 64	59	High	23	15	7	0	Condom	Cervical screening
M 65	31	High	19	14	29	0	IUD	Cervical screening
M 66	18	High	22	17	3	0	Condom	Gynecological evaluation
M 67	11	Low	23	15	5	0	Condom	Gynecological evaluation
M 68	6	Low	22	16	5	0	Condom	Cervical screening
M 69	Negative	Negative	19	18	3	0	Condom	Subdermal contraceptive
M 70	Negative	Negative	20	21	1	0	Condom	Vaginal infection
M 71	59	High	18	17	2	2	Condom	Condylomatosis
M 72	31	High	25	16	10	1	Subdermal contraceptive and Condom	Cervical screening
M 73	39	High	22	17	1	0	Condom	Vaginal infection
M 74	16	High	24	15	3	0	Oral contraceptive	Gynecological evaluation
M 75	Negative	Negative	21	20	1	2	Condom	Pregnancy test
M 76	18	High	25	18	4	0	Condom	Vaginal infection
M 77	45	High	23	22	1	0	Condom	Cervical screening
M 78	18	High	22	17	9	0	IUD	Vaginal infection
M 79	18	High	26	15	5	0	Condom	Gynecological evaluation
M 80	6	Low	20	14	8	0	Condom	IUD
M 81	6	Low	21	16	5	1	Condom	Gynecological evaluation
M 82	11	Low	22	16	10	0	Condom	Cervical screening
M 83	Negative	Negative	26	18	10	0	IUD	Cervical screening
M 84	16	High	19	17	1	1	Condom	Vaginal infection
M 85	16	High	20	15	3	2	Condom	Vaginal infection
M 86	18	High	28	17	1	0	Condon	Gynecological evaluation
M 87	31	High	28	24	5	0	Condom	Vaginal infection
M 88	6	Low	25	17	2	0	Contraceptive injection	Subdermal contraceptive
M 89	6	Low	19	16	1	0	Condom	Cervical screening
M 90	16	High	23	15	7	1	IUD	Cervical screening
M 91	18	High	21	14	5	0	IUD	Cervical screening
M 92	6	Low	18	15	7	0	None	Condylomatosis
M 93	Negative	Negative	23	16	3	0	Condom	IUD
M 94	6	Low	24	19	2	0	Oral contraceptive and Condom	Gynecological evaluation
M 95	Negative	Negative	25	21	2	0	Oral contraceptive	Estudio de papanicolaou
M 96	Negative	Negative	28	21	6	0	Oral contraceptive and Condom	Cervical screening
M 97	11	Low	19	15	2	1	Condom	Gynecological evaluation
M 98	59	High	24	18	2	0	Condon	Cervical screening
M 99	59	High	24	17	1	0	Condom	Cervical screening
M 100	51	High	23	17	4	0	Condom	Condylomatosis
M 101	Negative	Negative	29	19	20	3	Condom	Cervical screening
M 102	51	High	20	18	2	2	Condom	Cervical screening
M 103	11	Low	18	15	1	0	Condom	Condylomatosis
M 104	Negative	Negative	21	20	3	0	Condom	Gynecological evaluation
M 105	Negative	Negative	22	16	3	0	IUD	Gynecological evaluation
M 106	Negative	Negative	27	16	1	0	Oral contraceptive	Cervical screening
M 107	11	Low	17	16	1	2	Condom	Gynecological evaluation
M 108	6	Low	27	17	4	0	Oral contraceptive	Gynecological evaluation
M 109	18	High	24	22	3	1	Condom	Cervical screening
M 110	6	Low	20	15	10	2	Condom	Condylomatosis
M 111	31	High	20	17	2	1	Oral contraceptive and Condom	Subdermal contraceptive
M 112	6	Low	23	21	6	0	Condom	Gynecological evaluation
M 113	59	High	25	17	5	0	Condom	Gynecological evaluation
M 114	Negative	Negative					None	Gynecological evaluation
M 115	45	High	20	16	3	2	IUD	Gynecological evaluation
M 116	90	?	26	17	5	0	None	Vaginal infection
M 117	16	High	25	15	11	1	Subdermal contraceptive	Cervical screening
M 118	6	Low	25	17	2	0	Condom	Cervical screening
M 119	6	Low	24	17	5	0	Subdermal contraceptive and Condom	Cervical screening
M 120	51	High	24	16	1	0	Condom	Vaginal infection
M 121	18	High	20	19	1	2	Condom	Subdermal contraceptive
M 123	Negative	Negative	21	17	3	0	Oral contraceptive	Cervical screening
M125	Negative	Negative	20	18	2	0	Condom	Gynecological evaluation
M126	Negative		20	14	4	0	Condom	Cervical screening
M127	Negative	Negative	21	18	2	0	Condom	Cervical screening
M128	31	High	19	16	2	0	Condom	Gynecological evaluation
M129	18	High	19	17	3	3	Subdermal contraceptive	Gynecological evaluation
M124	6	ND	19	16	2	0	Condom	Cervical screening
M122	6					0	None	Gynecological evaluation

Figure 1. The overall prevalence of HPV genotypes in female university students. a) The infection prevalence is expressed as the number of individual positives for each genotype. From 129 samples, 74.41% (96 students) were positive for HPV (gray bar). b) Comparison of the most common HPV genotypes detected in all samples. The prevalence of most common high-risk HPV was HPV-18 13.95%; HPV-31 10.85%; HPV-16 9.3%, HPV-51 9.3%; and HPV-59 5.4%. c) Age distribution of sexual debut among students. The median age of coitarche for HPV- was 17.5 and for HPV+ girls was 17 years, which were used as a cutoff value for stratification of the girls by age. Fisher’s exact test showed that girls over 17 years old have a higher risk of HPV infection (P = .016). d) Comparison of the distribution of sexual partners among HPV- and HPV+ girls showed a statistically significant association between HPV infection and an increased number of lifetime sexual partners (Fisher’s exact test, P = .038). The cutoff value was the median number of lifetime sexual partners that was 3 for HPV- girls and 3.5 for HPV+ girls.

Figure 2. HPV-vaccination decrease the prevalence of some HPV types. a) The effect of HPV vaccination was evaluated in girls who received one, two or three doses of the vaccine in comparison with non-vaccinated girls. The percentages of infections were for HPV6 16% (12/75 girls), 12% (2/17), 12% (2/17) and 0% for unvaccinated, one dose, two doses and three doses of the vaccine, respectively. For HPV16 were 9% (7/75),18% (3/17), 6% (1/17), and 0%; for HPV18 were 12% (9/75), 18% (3/17), 12% (2/17), and 50% (2/4); for HPV31 were 15% (11/75), 12% (2/17), 6% (1/17), and 0%; and for HPV51 were 8% (6/75), 0%, 12% (2/17), and 25% (1/4). Data were analyzed by Fisher’s exact test. P-values less than 0.05 were considered statistically significant (*P < .05; **P < .01; ***P < .001). b) Percentage of seropositive individuals for HPV-16-specific IgG antibodies (left graph), and IgG anti-HPV-18 antibodies (right graph) in girls based on their vaccination status. Forty-three percent (32 of 75) of unvaccinated girls were seropositive for HPV16 and 41% (31/75) for HPV18. Forty-four percent (7/16) of vaccinated girls were seropositive for HPV16 after one dose of the HPV vaccine, 56% (9/16) for two doses, and 75% (3/4) for three doses. For HPV18 38% (6/16) of vaccinated girls were seropositive for one dose of the vaccine, while 56% (9/16) and 75% (3/4) were seropositive after two and three doses, respectively. c) Prevalence (percentage) of specific HPV infection in girls that were seropositive for HPV16 (left graph) or HPV18 antibodies (right graph). White bars represent unvaccinated girls and gray bar vaccinated girls. Data were analyzed by Fisher’s exact test. P-values less than 0.05 were considered statistically significant (*P < .05; **P < .01; ***P < .001).

Figure 3. Heatmap analysis of seroprevalence, infection, and vaccination. Analysis of the levels of specific antibodies against HPV16 and 18, and their association with the presence of HPV infection and vaccination status were analyzed by heatmap. For the antibody levels the scoring star with blue color for negative or low levels and change to red color for higher amounts of antibodies detected by ELISA. For the vaccination status, the blue color represents unvaccinated girls and the increasing intensity in red represents 1, 2, or 3 doses of the HPV vaccine. Finally, for HPV infection blue color represent HPV- girls and light red color represent girls with HPV infection (any HPV). Each horizontal line represents one girl, and the sample number is indicated in the left side of the graph. Rectangles 1 and 2 show unvaccinated double seropositive girls, while rectangles 3 and 4 show vaccinated double seropositive girls.

Figure 4. HPV seropositivity according to cervical HPV infection status. Percentages of HPV16 or HPV18 seropositive girls, which were grouped in those negative for HPV (HPV-), positive for any HPV (HPV+), and positive only for HPV-16 (HPV-16+) or HPV-18 (HPV-18+). Data were analyzed by Fisher’s exact test. P-values less than 0.05 were considered statistically significant (*P < .05; **P < .01).

Data availability statement

The data sets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.