Literature DB >> 25783645

Risk factors for high-risk and multi-type Human Papillomavirus infections among women in Ho Chi Minh City, Vietnam: a cross-sectional study.

Ly Thi-Hai Tran1, Loi Thi Tran, Thanh Cong Bui, Dung Thi-Kieu Le, Alan G Nyitray, Christine M Markham, Michael D Swartz, Chau Bao Vu-Tran, Lu-Yu Hwang.   

Abstract

BACKGROUND: Concurrent infection with multiple types of Human Papillomavirus (HPV) is associated with an increased risk of cervical cancer; yet, little is known about risk factors for concurrent HPV infection in Vietnam. This study investigated the prevalence of and risk factors for high-risk-type HPV and multi-type HPV infections among women in Ho Chi Minh City, Vietnam.
METHODS: Data were collected from a population-based survey of 1,550 women (mean age = 42.4; SD = 9.5), using a multi-stage sampling process. Socio-demographic and behavioral variables were obtained by self-report. HPV genotypes in cervical specimens were identified using PCR protocols.
RESULTS: The prevalence of any high-risk HPV infection was 9.0%, and of multi-type HPV infection was 1.9%. In the HPV+ subsample, the percentage of high-risk HPV was 84% and of multi-type HPV was 20%. All multi-type HPV infections were high-risk-type. Lifetime smoking and older age of first sex were significantly associated with any high-risk and multi-type HPV infections. Regular condom use was inversely associated with high-risk and multi-type HPV infection.
CONCLUSIONS: Risk factors for high-risk and multi-type HPV infections were similar. Further research and intervention are needed to reduce HPV infections in order to prevent HPV-related cancers.

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Year:  2015        PMID: 25783645      PMCID: PMC4339249          DOI: 10.1186/s12905-015-0172-7

Source DB:  PubMed          Journal:  BMC Womens Health        ISSN: 1472-6874            Impact factor:   2.809


Background

Human Papillomavirus (HPV) infection, particularly persistent infection with high-risk types, is a major preventable causal agent of cervical cancer [1,2]. More than 100 types of HPVs are known, of which 18 types are classified as high risk (i.e., oncogenic) [3]. Persistent infection with high-risk HPV types has been shown to increase residual or recurrent cervical disease in women after surgical treatment for high-grade cervical lesions [4]. In the International Agency for Research on Cancer (IARC) data for Vietnam in 2003, the prevalence of any HPV genotype was 2.0% in Hanoi and 10.9% in Ho Chi Minh City (HCMC) [5]. Several studies have examined risk factors for genital HPV infection, particularly with high-risk types. These risk factors include lifetime number of sexual partners, having a new partner, and partner’s sexual history [6]. Other less consistent determinants are age of sexual debut, smoking, parity, and oral contraceptive use [2,6]. Concurrent infection with multiple HPV types is common. In a pooled analysis in 15 areas worldwide, the prevalence of multi-type HPV infection ranged from 0.3–11.8% [7]. Among HPV-positive women, this prevalence averaged about 25% and ranged from 18.5–46% [7-9]. A number of studies have observed associations between multi-type HPV infection and certain health consequences, such as abnormal Pap results [10,11], high-grade squamous intraepithelial lesions [12,13], and a nearly 5-fold higher proportion of failure in radiotherapy treatment in cervical cancer patients [14]. The increase in risk for cervical intraepithelial neoplasia and high-grade squamous intraepithelial lesions associated with multi-type HPV infection may be comparable to the sum of risk caused by individual types and there is no evidence for synergistic interactions [8]. Risk factors for multi-type infection have also been examined in a few studies. The variance in multi-type HPV prevalence in all surveyed women and in HPV+ women across different regions of the world suggested that there might be some different risk factors for multi-type HPV infection compared to any-type HPV infection. Higher numbers of sexual partners were observed for those who were infected with high-risk HPV and multi-type HPV compared to those who were infected with low-risk type and single-type, respectively; yet, these were not statistically significant [15]. An effect of condom use on single-type and multi-type HPV infections was also not statistically significant. Thus, it is necessary to continue investigating risk factors for multi-type HPV infections. Although a few studies have reported risk factors associated with general HPV infection in HCMC, Vietnam [5], little is known about risk factors of infection with high-risk and multiple HPV types. In our previous report, the unweighted HPV prevalence in women in HCMC was 10.8%, of which the most common types were 16, 18, and 58 [16]. The current analysis was conducted to investigate the weighted prevalence of and risk factors for high-risk-type and multi-type HPV infection. Because this survey employed probability sampling proportional to size sampling, the weighted procedure may produce more accurate results than unweighted analyses. Results of this analysis will contribute important evidence regarding knowledge of the determinants of HPV infection, particularly with multiple types, and may inform future prevention strategies to reduce HPV infection and subsequent cancer risks.

Methods

Study design, population, and sampling

This study employed data from a population-based household survey of 1,550 women in HCMC, which was conducted from April 2008 to January 2009 to examine the predictive values of using an HPV test and/or a Pap smear in cervical cancer screening and diagnosis. Participants were selected through a two-stage sampling process. First, 10 districts (out of 24) and two communes (out of an average of 16) in each district in HCMC were randomly selected. Then, in each district, individuals were sampled where the probability of being selected was proportional to the size of the ward, based on the commune police registration lists. Women were eligible if they ever had sexual intercourse, were 18–69 years old, were registered residents of HCMC, and did not suffer from mental impairment. Exclusion criteria included women who were pregnant, had undergone a hysterectomy or a treatment for potential cervical cancer; had abnormal vaginal bleeding, or had any obstetrical/gynecological emergency. Selected women were fully informed about the purpose of the parent study, and the benefits/risks of participation. Women who agreed to participate provided written informed consents, and were invited to come to the commune health stations for a brief 15-minute interview and a gynecological examination, including collecting specimens for HPV tests and Pap tests. Interviews to obtain participants’ demographic and behavioral characteristics and medical history were conducted in Vietnamese in a private place (e.g., an empty room) at the commune health stations. Cervical specimens were then collected by trained gynecologists. Each participant received compensation (equivalent to $2.5 US dollars) for their time and transportation. Women who had a Pap result of ASCUS or higher (n = 33, 2.1%) were referred to OB/GYN hospitals in HCMC for further examination and diagnosis. The parent study protocol was approved by Ethical Review Committees of the University of Medicine and Pharmacy in HCMC and of the Department of Science and Technology in HCMC. Given the objectives of the parent study, a desired sample size of 1,566 was identified. A total of 1,566 eligible women were contacted, of whom 1,550 agreed to participate (response rate = 99%). Fifty participants who had no HPV test results were excluded from this analysis, resulting in a total sample size of 1,500.

Measures

Socio-demographic and behavioral variables used in this analysis were obtained from self-reported data via brief face-to-face interviews. These were participants’ factors and their husbands’ factors. Participants’ factors included age, parity, education level, marital status, age of first sexual intercourse, history of sexually transmitted infections (STIs), smoking history, lifetime number of sexual partners, and overall regular condom use. The husbands’ factors included education level, smoking history, and lifetime number of sexual partners. Current vaginitis or cervicitis was obtained from participants’ gynecological examination records. Specimens for HPV testing were obtained by cervical swab, placed in a sterile tube, and transferred to the Biology-Cell Laboratory of the University of Medicine and Pharmacy in HCMC on a daily basis for HPV DNA testing. L1 consensus PCR (MY09/11) was used to screen for HPV DNA. This test procedure could identify 25 HPV genotypes, including 8 low-risk types (6, 11, 42, 43, 61, 70, 71, 81), 16 high-risk types (16, 18, 31, 33, 35, 39, 45, 51, 52, 53, 56, 58, 59, 66, 68, 82), and one type with risk undetermined [17].

Statistical analysis

To account for the complex survey design, the data used in this analysis were weighted for the population sizes of the primary sampling units (i.e., communes), aided by survey procedures in Stata 11 (StataCorp LP, College Station, Texas, USA). Frequency distributions were used to examine the prevalence of HPV infection with any types, high-risk types, and multiple types. Chi-square and binary logistic regression were used to examine associations between demographic/behavioral characteristics and high-risk-type HPV infections. The bivariate association between each demographic/behavioral characteristic and multi-type HPV infection was examined by an ordinal logistic regression [18], in which the dependent variable (HPV infection) contained three ordinal values: no infection, single-type infection, and multi-type (≥2 types) infection. Variables which altered the OR point estimates by ≥10% in bivariate analyses were included in the multivariable logistic regression models for adjusted associations with HPV infection. Univariable and multivariable associations with HPV infection were assessed using the adjusted F test. All variables used for this analysis had less than 3% of missing values; these were ignored in analyses.

Results

Of the 1,500 surveyed respondents who had HPV test results, the mean age of participants was 42.4 years (SD = 9.5 years). About half of participants had two children and the highest number of children was nine (Table 1). The percentage of participants with education levels of secondary school or less was higher than that of their spouses (53.2% and 42.5%, respectively). The majority of participants were married (95.2%). Age of first intercourse ranged from 13 to 46 years (mean = 23.8, SD = 4.4). Four percent of participants had more than one sexual partner during their lifetime; 9% reported that their husbands had more than one sexual partner during their lifetime, and 18% did not know their husbands’ lifetime number of sexual partners. More than half of participants’ husbands ever smoked while only 1.3% of participants were smokers. In this sample, 88% of women reported that they did not use condoms or used condoms infrequently.
Table 1

Prevalence and risk factors of high-risk HPV infections by demographic and behavioral characteristics

Characteristics Total High risk HPV infection
n a (%) b n a % high-risk HPV+ Unadjusted OR Adjusted OR
(95% CI) b (95% CI) b,e (95% CI) b,e
Total15001499.0(5.4-12.6)
Age1500149
 18-29136(9.1)188.7(3.5-14.0)11
 30–39454(30.3)354.6(2.6-6.6).51(.23-1.13).40(.18-.90)
 40–49534(35.6)6512.0(4.6-19.4)1.43(.54-3.74).76(.32-1.81)
 ≥50376(25.1)3110.1(1.1-19.1)1.17(.35-3.86).74(.27-2.01)
 p value (for trend).056 (.181).101 (.545)
Parity1500149
 Nulliparous54(3.6)45.3(0.9-11.4).61(.16-2.23)
 1365(24.3)418.4(5.1-11.7)1
 2669(44.6)539.6(3.0-16.1)1.15(.48-2.76)
 ≥3412(27.5)518.9(2.4-15.4)1.07(.43-2.64)
 p value (for trend).849 (.804)
Education level of participant1499149
 Secondary school or lower797(53.2)797.7(3.1-12.3)1
 High school or higher702(46.8)7011.3(5.5-17.0)1.52(.64-3.62)
 p value.340
Education level of husband1448144
 Secondary school or lower615(42.5)679.5(3.4-15.5)1
 High school or higher833(57.5)778.4(4.1-12.8).88(.36-2.18)
 p value.787
Marital status1426142
 Married1358(95.2)1348.1(4.8-11.5)1
 Widowed/divorced/never married68(4.8)88.5(1.2-15.8)1.06(.37-2.98)
 p value.918
Age of first intercourse1491149
 <20378(25.4)347.2(.7-13.8)11
 20-26744(49.9)776.2(4.5-8.0).85(.31-2.35)1.40(.80-2.45)
 >26369(24.8)3818.1(5.7-30.5)2.83(.78-10.23)4.69(1.83-12.03)
 p value (for trend) .030 (.159) .006 (.005)
Participant ever smoked cigarettes1493149
 Yes20(1.3)563.9(21.2-106.7)20.55(3.07-137.76)24.24(3.26-180.24)
 No1473(98.7)1447.9(4.8-11.1)11
 p value .002 .002
Husband ever smoked cigarettesc 1493149
 Yes838(56.1)816.8(3.2-10.4).50(.21-1.20).68(.31-1.49)
 No655(43.9)6812.6(5.3-19.9)11
 p value.123.340
History of STIs d 1179118
 No1091(92.5)1098.4(4.9-11.9)1
 Yes88(7.5)910.7(4.5-25.8)1.31(.25-6.82)
 p value.751
Current vaginitis or cervicitis1499149
 No1353(90.3)1309.4(5.3-13.5)1
 Yes146(9.7)196.1(2.3-9.8).63(.28-1.41)
 p value.258
Lifetime number of sexual partners1486146
 11423(95.8)1409.1(5.3-12.9)1
 >163(4.2)64.3(0.2-8.7).45(.14-1.44)
 p value.177
Husband’s lifetime number of sexual partners1494147
 11092(73.1)1078.1(4.8-11.5)1
 >1135(9.0)107.9(3.3-19.1).96(.19-4.80)
 Don’t know267(17.9)3013.5(.9-26.0)1.76(.55-5.64)
 p value.633
Overall condom use1494148
 Regular178(11.9)83.6(.5-6.7).36(.13-.99).41(.17-1.03)
 Not regular/ Do not use1316(88.1)1409.4(5.2-13.6)11
 p value .049 .057

aNumber of unweighted participants.

bAfter weighting was applied.

cIn participants who never smoked.

dIncluded Chlamydia, Gonorrhea, Syphilis, and Trichomoniasis.

eOdds ratio from logistic regressions.

Prevalence and risk factors of high-risk HPV infections by demographic and behavioral characteristics aNumber of unweighted participants. bAfter weighting was applied. cIn participants who never smoked. dIncluded Chlamydia, Gonorrhea, Syphilis, and Trichomoniasis. eOdds ratio from logistic regressions. The prevalence of HPV was 9.7% for any-type infection, 9.0% for high-risk infection, and 1.9% for multi-type HPV infections (Figure 1). Among those who were infected with any type of HPV, the proportions of high-risk HPV infection was 84% (due to a higher total number of high-risk types detected by this test), and of multi-type HPV infection was 20%. For multi-type HPV cases, all were high risk-type, the most common two-type HPV concurrence was 16 & 18 (25/43, 58.1%) and 16 & 58 (2/43, 4.6%). The 16 &18 pair was also present in 4/7 (57%) cases who were concurrently infected with three or more types of HPV. No case was infected with four types or more.
Figure 1

HPV test results among participants. Note: Numbers were based on unweighted counts and proportions were calculated after weighting.

HPV test results among participants. Note: Numbers were based on unweighted counts and proportions were calculated after weighting. Table 1 presents bivariate associations between demographic and behavioral characteristics and HPV infections with any high-risk type(s). Participants’ age of first intercourse, lifetime smoking status, and frequency of condom use were significantly associated with high-risk HPV infection when compared to no infection. Because of the limited sample size of low risk type cases (n = 20), they were omitted from the analyses. Table 2 shows the prevalence of multi-type HPV infections by demographic and behavioral characteristics. Results from ordinal logistic regression in bivariate analyses suggested that HPV infections with one type (versus no infection) and with multi-type (versus with one type) were associated with participants’ smoking status and with irregular/no condom use. Prevalence of multi-type HPV infections varied across age groups of first intercourse (p = .030) but no specific trend could be confirmed (p-value for trend = .159). There was no difference in multi-type HPV infection by other characteristics of participants (e.g., age, parity, and lifetime number of sexual partners), and by characteristics of participants’ husbands (e.g., smoking status and lifetime number of sexual partners).
Table 2

Prevalence and risk factors of multi-type HPV infections by demographic and behavioral characteristics

Characteristics Multi-type HPV infection
n a % among HPV+ Unadjusted odd ratios Adjusted odd ratios
(95% CI) b (95% CI) b,e (95% CI) b,e
Total5020.1(10.8-29.4)
Age50
 18-291031.3(10.5-52.1)11
 30–391837.1(19.9-54.4)0.52(.24-1.13).43(.20-.91)
 40–491514.3(3.5-25.2)1.34(.54-3.53).74(.34-1.63)
 ≥50716.4(.1-34.0)1.12(.37-3.41).74(.30-1.84)
 p value (for trend).061 (.184).122 (.578)
Parity50
 Nulliparous116.4(4.1-46.9).59(.18-1.98)
 11633.6(18.4-48.8)1
 21915.2(3.1-27.3)1.02(.46-2.28)
 ≥31418.4(2.3-34.5).89(.37-2.13)
 p value (for trend).847 (.865)
Education level of participant50
 Secondary school or lower2719.1(6.1-32.1)1
 High school or higher2321.2(8.2-34.3)1.63(.74-3.57)
 p value.224
Education level of husband47
 Secondary school or lower2318.2(4.1-32.4)1
 High school or higher2419.9(8.2-31.6)1.01(.44-2.34)
 p value.981
Marital status49
 Married4522.0(11.6-32.4)1
 Widowed/divorced/never married442.0(10.3-73.6)1.28(.48-3.42)
 p value.630
Age of first intercourse50
 <201118.2(5.8-37.6)11
 20-262930.8(20.8-40.8).98(.37-2.60)1.62(.96-2.74)
 >261011.9(4.1-23.8)2.85(.86-9.48)4.58(1.94-10.83)
 p value (for trend) .037 (.178) .002 (.002)
Participant ever smoked cigarettes50
 Yes122.8(12.7-32.9)12.52(3.90-40.22)15.36(3.77-62.62)
 No492.0(0.3-7.3)11
 p value <.001 <.001
Husband ever smoked cigarettesc 50
 Yes2718.2(5.5-30.8).52(.24-1.16).70(.35-1.38)
 No2322.3(8.9-35.6)11
 p value.109.302
History of STIsd 35
 No2917.1(.6-44.9)1
 Yes618.3(9.0-27.5)1.20(.25-5.70)
 p value.823
Current vaginitis or cervicitis50
 No4620.0(10.0-30.1)1
 Yes420.5(18.0-39.1).65(.30-1.39)
 p value.265
Lifetime number of sexual partners49
 14820.0(12.1-31.1)1
 >118.6(1.1-43.8).67(.23-1.93)
 p value.288
Husband’s lifetime number of sexual partners49
 13323.0(11.5-34.5)1
 >1410.7(.5-27.8)1.01(.24-4. 16)
 Don’t know1218.1(.9-37.0)1.83(.65-5.13)
 p value.515
Overall condom use49
 Regular319.6(10.0-29.1).35(.13-.92).39(.16-.92)
 Not regular/ Do not use4626.3(.3-55.9)11
 p value .033 .032

aNumber of unweighted participants.

bAfter weighting was applied.

cIn participants who never smoked.

dIncluded Chlamydia, Gonorrhea, Syphilis, and Trichomoniasis.

eOdds ratio from ordinal logistic regressions, in which we compare the odds of having multi-type HPV infection to the odds of having single-type HPV infection, and the odds of having single-type HPV infection to the odds of having no HPV infection.

Prevalence and risk factors of multi-type HPV infections by demographic and behavioral characteristics aNumber of unweighted participants. bAfter weighting was applied. cIn participants who never smoked. dIncluded Chlamydia, Gonorrhea, Syphilis, and Trichomoniasis. eOdds ratio from ordinal logistic regressions, in which we compare the odds of having multi-type HPV infection to the odds of having single-type HPV infection, and the odds of having single-type HPV infection to the odds of having no HPV infection. Based on findings from previous studies and the 10% change-in-estimate rule, we included participants’ age, participants’ age of first intercourse, participants’ lifetime smoking, husbands’ lifetime smoking and condom use in multivariable models. The association between age of first intercourse and high-risk HPV infection and multi-type HPV infection remained significant (all p-values < .05). Participants’ smoking status was strongly and significantly associated with the two HPV-infection outcomes. Using no HPV infection as the reference group, the odds of being infected with high-risk-type HPV were 24.2 in women who ever smoked compared to those who never smoked. Smoking also increased the odds of being infected with multiple types of HPV (OR = 15.4). Regular condom use was significantly associated with a lower likelihood of multi-type HPV infection (p = .032). When we further compared 50 multi-type high risk cases with 99 single-type high risk HPV cases, the results were comparable to previous findings.

Discussion

Our study results revealed that the prevalence of HPV in a population-based sample of women in HCMC, Vietnam was 9.0% for infection with high-risk types, and 1.9% for infection with multiple types of HPV. The prevalence of high-risk HPV infection in our study is comparable to previous results of vaginal-cervical HPV infection in a similar population in HCMC [5,7]; however, the prevalence of multi-type HPV infection is lower (1.9%) in our study compared to 4.5% in the IARC data in HCMC [5]. As reported in a previous publication using the same dataset, the most prevalent high-risk types of HPV were 16, 18, and 58 (which accounted for 40.7%, 26.2%, and 8.1% of all HPV infections, respectively) [16]. In this analysis, these three HPV types were also the most prevalent in multi-type HPV infection. There is no strong evidence to support type-clustering tendency in multiple infections [7,19]. In this study, the high prevalence of 16 &18 pairs was likely due to common behavioral risk factors for all HPV types, rather than because of the possibility of a biological interaction or clustering between 16 &18 types. Also, it was suggested that co-infecting HPV types might be related to HPV genetic similarity and to the testing procedure, which might be more likely to detect or miss certain HPV types with similar gene(s). For example, enzyme immunoassay, which was used in our study, is more likely to detect the excess of multiple HPV infections, compared to reverse line blot analysis [7]. Intervention or management to reduce high-risk HPV infection is important because of its oncogenic potential. Several studies have examined risk factors of high-risk HPV infection at the vaginal or cervical sites; however, evidence regarding risk factors other than sexual behavioral risks is inconsistent [6]. Although low education, high parity, and a history of STIs (e.g., Chlamydia or HSV-2) have been found to be associated with high-risk HPV infection [6,20-22], these associations were not observed in our study. Age of first sexual intercourse, which was also inconsistently related to HPV risk in previous studies, was associated with HPV prevalence in our results. In multivariable logistic regression models, our results suggested that older age of first sexual intercourse was a risk factor for high-risk HPV infection and multiple HPV infection. The effect of condom use in preventing HPV transmission and infection has not been fully established, although more studies have suggested a protective effect [22]. Our findings showed that regular condom use was associated with a lower likelihood of both high-risk-type and multi-type HPV infections. Similar to several previous studies [23,24], our findings indicated that smoking was strongly associated with increased risk of HPV infection - with high-risk types or multiple types. Most Vietnamese women generally do not smoke; the prevalence of current tobacco smokers in reproductive-aged women was 0.8% [25]. Targeting smoking is particularly important because smoking does not only increase the likelihood of HPV infection but also contributes to the progression to HPV-related cancers [23,24]. Therefore, interventions to reduce smoking in women are needed for cervical cancer prevention. In this analysis, however, we could not examine tobacco use in detail (e.g., current smoking, numbers of cigarette smoked per day) due to the limited type of smoking related variables in the data set. Further studies are needed to explore the role of tobacco use and HPV infection in this population. Although the proportions of multi-type HPV infection were not statistically different by most demographic and behavioral characteristics (possibly due to the small number of observed cases), the significant odds ratios of ordinal logistic regression suggested that irregular condom use and smoking increased the risk of being infected with multiple HPV types. In other words, risk factors of multi-type HPV infection in this study were very similar to the risk factors of high-risk type HPV infections. Although previous studies suggested that multi-type HPV infection was particularly more common in young women and women with multiple sexual partners [7,8,26], these associations were not observed in our results. The non-association between lifetime numbers of sexual partners and multi-type HPV infection might be due to the small number of participants who had more than one sexual partner in our predominantly married-women sample, given the taboos on premarital sex and extramarital sex for women in Vietnam [27,28]. It may be interesting to examine risk factors of multi-type HPV infection in younger female populations, in which sexual attitudes and practices may have taken a more liberal turn [27,29]. It is also important for future research or intervention projects to conduct HPV testing with main male sexual partner(s) in order to more comprehensively investigate the risk factors for multi-type HPV infections. Our study has some limitations. Given the cross-sectional nature of the data, causality between risk factors and HPV outcomes cannot be established. However, most genital HPV infection is current and transient [6]; so HPV infection is unlikely to precede lifetime behavioral risks. Moreover, as we discussed above, factors such as smoking or irregular condom use have been suggested as risk determinants of high-risk-type or multi-type HPV infections in other prospective studies. Sexual and other behavioral risk factors were obtained from self-reports and hence might be subject to recall bias or under-reporting. To reduce potential biases of self-report, interviews were conducted in a private place, and interviewers were trained to aid participants in recalling their behaviors in different ways. The reliability of self-report might have been more compromised for responses related to risk behaviors of participants’ male sexual partners. This might explain why some husbands’ risk factors, such as husbands’ lifetime numbers of sexual partners, were not associated with high-risk or multi-type HPV infections in our analysis, although they have been significantly associated with HPV infection in other studies [15]. We did neither screen participants for their recent treatments of HPV (e.g., condylome), which might have influenced their current HPV presence, nor exclude them. However, the prevalence of cases with symptomatic HPV infection (e.g., types 6 & 11) who might have recently received a treatment was very low in the general population; and treatments for asymptomatic HPV infection (i.e., most high-risk types) were not available or recommended in Vietnam. Because in our study multi-type HPV infection included only high-risk types, future studies should investigate multi-type HPV infection which comprises of multiple high-risk only, multiple low-risk only, and multiple with both high-and low-risk. Despite our relatively large sample size, the low HPV prevalence, particularly with multiple types, limited statistical power to detect associations and hence generated wide confidence intervals. Future prospective cohort studies are also needed to longitudinally investigate risk factors of multi-type HPV infection, interactions, and persistence.

Conclusions

Our population-based survey suggested that risk factors for multi-type HPV infection in women in HCMC, Vietnam, were similar to risk factors for high-risk-type HPV infections. Risk factors, which showed a statistically strong association, included women’s smoking status, and older age of first sexual debut. Regular condom use was inversely associated with high-risk and multi-type HPV infection. Future research and intervention projects (e.g., related to HPV vaccination) are needed to reduce high-risk-type and multi-type HPV infections in order to prevent consequent HPV-related cancers.
  24 in total

1.  Improved amplification of genital human papillomaviruses.

Authors:  P E Gravitt; C L Peyton; T Q Alessi; C M Wheeler; F Coutlée; A Hildesheim; M H Schiffman; D R Scott; R J Apple
Journal:  J Clin Microbiol       Date:  2000-01       Impact factor: 5.948

Review 2.  Factors affecting transmission of mucosal human papillomavirus.

Authors:  Nienke J Veldhuijzen; Peter Jf Snijders; Peter Reiss; Chris Jlm Meijer; Janneke Hhm van de Wijgert
Journal:  Lancet Infect Dis       Date:  2010-11-11       Impact factor: 25.071

3.  Human papillomavirus infections with multiple types and risk of cervical neoplasia.

Authors:  Helen Trottier; Salaheddin Mahmud; Maria Cecilia Costa; João P Sobrinho; Eliane Duarte-Franco; Thomas E Rohan; Alex Ferenczy; Luisa L Villa; Eduardo L Franco
Journal:  Cancer Epidemiol Biomarkers Prev       Date:  2006-07       Impact factor: 4.254

4.  Worldwide human papillomavirus etiology of cervical adenocarcinoma and its cofactors: implications for screening and prevention.

Authors:  Xavier Castellsagué; Mireia Díaz; Silvia de Sanjosé; Nubia Muñoz; Rolando Herrero; Silvia Franceschi; Rosanna W Peeling; Rhoda Ashley; Jennifer S Smith; Peter J F Snijders; Chris J L M Meijer; F Xavier Bosch
Journal:  J Natl Cancer Inst       Date:  2006-03-01       Impact factor: 13.506

5.  Human papillomavirus infection with multiple types: pattern of coinfection and risk of cervical disease.

Authors:  Anil K Chaturvedi; Hormuzd A Katki; Allan Hildesheim; Ana Cecilia Rodríguez; Wim Quint; Mark Schiffman; Leen-Jan Van Doorn; Carolina Porras; Sholom Wacholder; Paula Gonzalez; Mark E Sherman; Rolando Herrero
Journal:  J Infect Dis       Date:  2011-04-01       Impact factor: 5.226

6.  Continuity and change in premarital sex in Vietnam.

Authors:  Sharon Ghuman; Vu Manh Loi; Vu Tuan Huy; John Knodel
Journal:  Int Fam Plan Perspect       Date:  2006-12

7.  Tobacco smoking and chewing as risk factors for multiple human papillomavirus infections and cervical squamous intraepithelial lesions in two countries (Côte d'Ivoire and Finland) with different tobacco exposure.

Authors:  Aline Simen-Kapeu; Guy La Ruche; Vesa Kataja; Merja Yliskoski; Christine Bergeron; Apollinaire Horo; Kari Syrjänen; Seppo Saarikoski; Matti Lehtinen; François Dabis; Annie J Sasco
Journal:  Cancer Causes Control       Date:  2008-09-24       Impact factor: 2.506

8.  Sexual behavior, condom use, and human papillomavirus: pooled analysis of the IARC human papillomavirus prevalence surveys.

Authors:  Salvatore Vaccarella; Silvia Franceschi; Rolando Herrero; Nubia Muñoz; Peter J F Snijders; Gary M Clifford; Jennifer S Smith; Eduardo Lazcano-Ponce; Sukhon Sukvirach; Hai-Rim Shin; Silvia de Sanjosé; Monica Molano; Elena Matos; Catterina Ferreccio; Pham Thi Hoang Anh; Jaiye O Thomas; Chris J L M Meijer
Journal:  Cancer Epidemiol Biomarkers Prev       Date:  2006-02       Impact factor: 4.254

9.  Current tobacco use and secondhand smoke exposure among women of reproductive age--14 countries, 2008-2010.

Authors: 
Journal:  MMWR Morb Mortal Wkly Rep       Date:  2012-11-02       Impact factor: 17.586

10.  Correlation of high-risk human papillomavirus genotypes persistence and risk of residual or recurrent cervical disease after surgical treatment.

Authors:  Simona Venturoli; Simone Ambretti; Monica Cricca; Elisa Leo; Silvano Costa; Monica Musiani; Marialuisa Zerbini
Journal:  J Med Virol       Date:  2008-08       Impact factor: 2.327

View more
  9 in total

1.  Prevalence of and risk factors for high-risk human papillomavirus infection: a population-based study from Hetian, Xinjiang, China.

Authors:  Mayinuer Niyazi; Sulaiya Husaiyin; Lili Han; Huduyum Mamat; Kundus Husaiyin; Lin Wang
Journal:  Bosn J Basic Med Sci       Date:  2016-01-01       Impact factor: 3.363

2.  Is Pap Test Awareness Critical to Pap Test Uptake in Women Living in Rural Vietnam?

Authors:  Hee Yun Lee; Qingyi Li; Yan Luo; Kun Wang; Sara Hendrix; Jongwook Lee; Sangchul Yoon; Quoc Huy Nguyen Vu
Journal:  Asian Pac J Cancer Prev       Date:  2021-03-01

3.  Prevalence of human papillomavirus infection among women from quilombo communities in northeastern Brazil.

Authors:  Maria do Desterro Soares Brandão Nascimento; Flávia Castello Branco Vidal; Marcos Antonio Custódio Neto da Silva; José Eduardo Batista; Maria do Carmo Lacerda Barbosa; Walbert Edson Muniz Filho; Geusa Felipa de Barros Bezerra; Graça Maria de Castro Viana; Rebeca Costa Castelo Branco; Luciane Maria Oliveira Brito
Journal:  BMC Womens Health       Date:  2018-01-02       Impact factor: 2.809

4.  Awareness of Cervical Cancer and Pap Smear Testing Among Omani Women

Authors:  Alwahaibi Nasar; Alsalami Waad; Alzaabi Atheer; Alramadhani Nasra
Journal:  Asian Pac J Cancer Prev       Date:  2016-11-01

5.  Factors associated with high-risk HPV infection and cervical cancer screening methods among rural Uyghur women aged > 30 years in Xinjiang.

Authors:  Sulaiya Husaiyin; Lili Han; Lin Wang; Chunhua Ma; Zumurelaiti Ainiwaer; Nuermanguli Rouzi; Mireguli Akemujiang; Hatiguli Simayil; Zumulaiti Aniwa; Rouzi Nurimanguli; Mayinuer Niyazi
Journal:  BMC Cancer       Date:  2018-11-23       Impact factor: 4.430

6.  Performance of HPV16/18 in Triage of Cytological Atypical Squamous Cells of Undetermined Significance.

Authors:  Xiaoqin Cao; Shuzheng Liu; Manman Jia; Hongmin Chen; Dongmei Zhao; Bing Dong; Zhen Guo; Lingyan Ren; Shaokai Zhang; Xibin Sun
Journal:  Anal Cell Pathol (Amst)       Date:  2019-12-16       Impact factor: 2.916

Review 7.  Prevalence of human papillomavirus detection in ovarian cancer: a meta-analysis.

Authors:  Soumia Cherif; Abdessamad Amine; Sarah Thies; Eliane T Taube; Elena Ioana Braicu; Jalid Sehouli; Andreas M Kaufmann
Journal:  Eur J Clin Microbiol Infect Dis       Date:  2021-06-04       Impact factor: 3.267

8.  Possible Synergistic Interactions Among Multiple HPV Genotypes in Women Suffering from Genital Neoplasia

Authors:  Massoud Hajia; Amir Sohrabi
Journal:  Asian Pac J Cancer Prev       Date:  2018-03-27

9.  Positivity and prevalence of human papillomavirus among a large population of women in southeastern China.

Authors:  Sudong Liu; Xiaodong Gu; Ruiqiang Weng; Jing Liu; Zhixiong Zhong
Journal:  J Int Med Res       Date:  2019-09-06       Impact factor: 1.671

  9 in total

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