Comparing the distributions of common Human papillomavirus genotypes among the Fars province population in the southwest of Iran, with the vaccine-included genotypes

doi:10.21203/rs.3.rs-4973206/v1

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Comparing the distributions of common Human papillomavirus genotypes among the Fars province population in the southwest of Iran, with the vaccine-included genotypes

https://doi.org/10.21203/rs.3.rs-4973206/v1

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published 21 Oct, 2024

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Background

Given the strong association between high-risk HPV genotypes such as 16 and 18 and cervical cancer, this study aimed to compare the distribution of common HPV genotypes among the southwest Iranian population with vaccine-included genotypes.

Methods

Based on the sample quality, DNAs were extracted from the biological samples of 8036 individuals who were included in the study with three different methods (automated instrument, column, and precipitation), and 21 different HPV genotypes were detected using Real-time PCR.

Results

The majority of participants were women (> 99%) with a positive rate of 29.9% in which the high-risk genotypes were dominant (84.9%). The highest rate of HPV infections was observed in the age ≤ 30 years (35.9%). HPV 6 and 16 were the most frequent low- and high-risk genotypes, respectively. Multi HPV infections were observed in 35% of positive samples and the highest cross infections were observed between HPV6 and 16. Co-infection with HPV 16 and 18 was observed in 21 (1%) positive samples. It seems that vaccination is required to decrease the outcome of HPV infections such as cervical cancer. However, other frequent high-risk genotypes were not included in the 9-valent vaccine.

Conclusion

Since the association between cervical cancer and other high-risk HPV types rather than 16 and 18 has been less studied, investigating their pathogenicity in cervical cancer is recommended. Furthermore, the new generation of HPV vaccine should contain the other frequent high-risk genotypes rather than those included in the approved vaccines.

HPV

High-risk

Low-risk

Co-infection

Vaccine

Human papillomavirus (HPV) is a DNA virus belonging to the Papillomaviridae family which is known as an agent for the most common sexually transmitted disease (STD). HPV is also responsible for about 4.5% of all human cancers including anal, cervical, oropharyngeal, penile, vaginal, and vulvar cancers, among them cervical cancer is predominant [11]. Analysis of Virus structure revealed that HPVs typically contain eight expressed protein-coding open reading frames (ORFs) in their circular double-stranded DNA genomes with a size of approximately 8 kb [4]. Based on their expression timing, ORFs are named early (E) and late (L), and HPV consists of 6E and 2L [46], of them, E6 and E7 are considered oncoproteins that are responsible for degrading p53 and pRb [37] and L1 that is a conserved region respective to the HPV genotypes diversity [7]. About 222 types of HPV have been reported until now [23] however, only 12 types of them including HPV16, HPV18, HPV31, HPV33, HPV35, HPV39, HPV45, HPV51, HPV52, HPV56, HPV58, and HPV59 have been reported to be associated with malignancies. Therefore, most HPV infections are not carcinogenic and the immune system can clear nearly 80% of HPV infections from the body [13]. According to their roles in cancer development, HPV types can be classified into high- and low-risk genotypes. Of the high-risk genotypes, HPV16 and 18 are identified as the major inducers of HPV-related squamous cell carcinoma (HSCC) and cervical adenocarcinoma by changing the pathways associated with immune responses and cellular transformation [34]. To prevent HPV infections and consequently its attendant outcomes, the HPV vaccines were designed based on the virus-like particle adsorbed to an aluminum adjuvant. There are currently different types of available vaccines such as bivalent, quadrivalent, and nonavalent. All the vaccines are highly effective in preventing infection with virus types 16 and 18. The quadrivalent vaccine also prevents anogenital warts caused by HPV types 6 and 11. Population data analysis showed that the quadrivalent (4-valent) HPV vaccine can significantly reduce the risk of invasive cervical cancer [18]. The 9-valent vaccine suggests extra protection against the other high-risk genotypes like 31, 33, 45, 52, and 58 [41].

Based on previous studies, the incidence rate of cervical cancer is rising among Iranian women (4.5 per 100,000 people) with annual 9 deaths per 100,000 women [20, 29] that may be due to more screening tests, higher HPV prevalence, and various risk factors such as marital status, age at marriage and at first pregnancy, smoking, use of oral contraceptive pills, multiple sexual partners, family history, and multiple childbirths [22]. Thus, it seems that the frequency of HPV positivity rate as well as alterations in the high-risk genotypes especially HPV16 and HPV18 in each region be determined annually. The present study aimed to evaluate the distributions of HPV common genotypes in a population from the Fars province in the southwest of Iran, and compare the more frequent genotypes with those included in the HPV-approved vaccines.

Study populations

As a cross-sectional study, from January 2021 to December 2023, 8064 individuals were referred for routine workups without any signs and symptoms or had signs and symptoms of HPV infection such as unusual vaginal discharge (thin, watery, and bloody discharge) and genital (vaginal, penile and anal) warts were included in the study. The vaginal or tissue samples were collected by Gynecologist and the collected sampling brushes in transport media were transferred to a referral diagnostic clinical lab (Farzanegan lab, Shiraz, Fars, Iran) for HPV genotyping. Given that Farzanegan lab is a referral center, in addition to Shiraz, the samples were received from different cities in Fars province in the southwest of Iran. Together, 8034 samples were collected from women and 30 samples from males. The samples were examined and analyzed as soon as received.

DNA extraction

Based on the specimen’s quality, different extraction methods were used to decrease the false negative results. Upon centrifugation of liquid base specimens at 15000 rcf for 2 min, from the specimens with good epithelial cell numbers, DNAs were extracted by the automated DNA extraction instrument using the T200-32 kit (Zybio, China) specified for extracting viruses’ genomes. For the highly mucoid and bloody samples and the samples with low cell numbers, column (Rastin Co. Iran) and precipitation (Amplisens, Russia) extraction-based methods were used, respectively. Briefly, upon centrifugation, 200 µl of the pelleted cells were used and DNAs were extracted as the manufacturer recommended.

HPV genotyping

The types of HPV were determined by real-time PCR methods using HPV genotyping kits (HPV QUANT-21, Russia) by Real-time PCR instrument (DTprime, Russia). This kit has been designed for in vitro diagnosis (IVD) of 21 HPV types including three low-risk (HPV 6, 11, 44) and eighteen high-risk (HPV 16, 18, 26, 31, 33, 35, 39, 45, 51, 52, 53, 56, 58, 59, 66, 68, 73, 82) HPV types in human biological samples according to the manufacturer’s instruction. Each well of 8-well strips contains an internal control to detect the amplification. Well, number eight includes an internal control of samples (SIC) to determine the quality and quantity of the extracted DNAs. Based on the kit instruction manual, SIC < 4 is invalid and DNAs were extracted from the new requested samples. To normalize the results, all DNAs with SIC ≥ 4 were included in the study.

Statistical analysis

To analyze the data, SPSS Statistics Version 27 (IBM), R programming software, and EPI Info were used. Using a non-parametric Chi-square test the association between age stratification and HPV frequencies was determined by EPI-info software (version 1.4.3, CDC). R programming package (version 4.3.3) was used to determine the frequencies of high- and low-risk HPV genotypes, co-, and cross-infection of HPV as well as to design the graphs [43]. P value < 0.05 was accepted as a significant level.

Of 8064 samples, 8039 samples (99.7%) were from women (Mean ± SD; 35.59 ± 9.6 years) and 24 samples (0.3%) were from men (Mean ± SD; 35.17 ± 12.8 years). As shown in Fig. 1, 2412 samples (29.9%) were positive and 5652 (70.1%) samples were negative. Among the positive samples, 2048 (84.9%) were positive for at least one high-risk HPV genotype, and 364 (15.1%) samples were positive for low-risk genotypes.

HPV genotypes distribution

HPV genotyping showed that genotype 6 was the most frequent genotype which was detected in 544 samples (22.6%). As shown in Fig. 2, among high-risk genotypes, genotype 16 was detected in 441 (18.3%) samples representing the most frequent genotype, while genotypes 26 and 33 were positive only in one sample (0.0004%), were the least frequent ones. Among detected high-risk genotypes, seven HPV types (39%) were included in the approved available vaccine (9-valent). Interestingly, following genotype 16, the frequencies of high-risk genotypes 53 (12.3%), 66 (9.99%), 51 (9.5%), and 39 (9.0%) were higher than those genotypes (52, 31, 18, 58, 45 and 33) which were included in the approved 9-valent vaccine.

The frequency of low-risk genotypes detected in the biological samples is shown in Fig. 3. Of the low-risk genotypes, genotypes 6 and 11 were the highest (22.6%) and the lowest (2.6%) frequent ones, respectively. In contrast to genotypes 6 and 11 which were included in the 4- and 9-valent vaccines, genotype 44 as the second low-risk frequent genotype (4.1%) is not included in the currently available vaccines.

Figure 3 The bars show the frequency of low-risk genotypes in the biological samples. The red bars show the genotypes included in the 4- and 9-valent vaccines

Distribution of HPV in different age ranges

To determine the frequency of HPV in different age groups, we stratified individuals into six groups (G1-6) based on their age: ≤20, 21–30, 31–40, 41–50, 51–60, and ≥ 60 years old.

As shown in Table 1, G3 and G6 had the largest and the smallest sample sizes, comprising 34% and 1.7% of total samples, respectively. The highest and the lowest positivity rates were observed in groups 1 and 6, respectively. The results revealed that the positivity rate in groups 1, 2, 4, and 5 were significantly different from the other groups (Table 1).

Table 1

The frequency of HPV positivity and co-infection rates in the different age groups of the participants. P1 and P2 values have been calculated based on the comparison of the positive rate and co-infection of each row with the sum of others. Bold numbers represent the significant value.
Group	Age (y)	Sample size	Positive (%)	Co-infection (%)	P1 value	P2 value
1	≤ 20	294	113 (38.4)	44 (15)	0.001	0.047
2	21–30	2407	858 (35.65)	332 (13.8)	0.00001	0.00001
3	31–40	3175	918 (28.9)	304 (9.5)	0.11	0.0008
4	41–50	1626	383 (23.56)	115 (7)	0.0001	0.00009
5	51–60	422	107 (25.36)	43 (10.2)	0.035	0.5
6	≥ 60	139	33 (22.02)	15 (10.8)	0.1	0.77

According to age classification, the most frequent low-risk genotype in all age groups was HPV6 except for Group 5 in which the frequency of HPV11 was higher than the other types. Among the high-risk genotypes, HPV16 was the most frequent in all age groups (Fig. 4).

HPV co-infection

To determine the frequency of samples infected with one or more genotypes, results analysis revealed that most samples were infected just with one HPV type, even though infection with 2 to 10 different HPV types was also observed in the samples. Based on the results, 1561 samples (65%) were infected with one HPV type and infection with 8 and 9 HPV types was observed in only one sample. In addition, 2 samples were positive with 10 different HPV genotypes (Fig. 5). Detection of co-infection based on the different age ranges revealed the highest and the lowest co-infection in the age groups 1 (15%) and 4 (7%), respectively (Table 1 and Fig. 6).

Figure 5 The bars represent the frequency of samples infected with one to 10 different HPV genotypes.

HPV genotypes cross-infection

To assess the co-infection between different genotypes, data analysis revealed that the highest co-infection rate was observed between genotypes 16 and 6 with a frequency of 52 (2.2%) of positive samples. Following genotype 16, the highest co-infection of genotype 6 was observed with genotypes 66 and 53, respectively. Given its importance in the development of cervical cancer, co-infection between HPV genotypes 16 and 18 was observed in 22 (1%) of positive samples. The cross-infection between the different HPV genotypes with frequency > 5% is shown as a heatmap in Fig. 7.

In the present cross-sectional study, the prevalence of HPV genotypes in the biological samples of a population from the southwest of Iran (Fars province) was assessed. The results showed a positivity rate of 29.9% in which the high-risk genotypes comprised the most genotypes in the studied population. To determine the prevalence of HPV genotypes, several studies were performed in different parts of Iran. Of them, a previous study from the northeast of Iran (2013 to 2018) reported a positivity rate of 48.4% for HPV genotypes [30]. Another study reported a prevalence of 49.5% on the samples which were from different provinces of Iran, from April 2011 to April 2016 [21]. In addition, a recent study from the capital city of Iran, Tehran, reported a positivity rate of 53% on the samples collected from 2017 to 2021 [28]. Also, another study on 12076 biological samples reported a positivity rate of 38.68% which was carried out from 2016 to 2018 [5]. In our neighboring country Iraq, with whom we share a lot of religious ties, the positive rate was reported as 20.9% on samples collected between January 2018 and September 2020. [9]. Another study reported an HPV-positive rate of 17.96% in Iraqi women aged between 15 to 50 years [44]. The inconsistency between the positive rates in our results and the others may be due to the application of different methods (PCR, Hybridization) and variations in the commercial kits capable of detecting different numbers of genotypes. In addition, community awareness of HPV infections and its possible complications as well as vaccine availability and more intensive preventive behaviors may also be the reason for the decline in HPV transmission.

Distributions of HPV genotypes revealed that the samples with positive high-risk genotypes were more frequent than positive low-risk genotypes. Of the positive samples, the most frequent genotypes were HPV6 and HPV16, respectively. In concordance with our study, genotypes 6 and 16 were also the most low- and high-risk genotypes in the other studies reported from Iran [16, 27, 30].

Geographically, comparing the distributions of HPV in our result with different continents and countries, the highest prevalence has been reported in the Asian, African, and European regions, respectively. Also, the prevalence of HPV infection in the European areas revealed a lower rate of positivity in the developed country in comparison with developing countries [3, 32, 38]. Like ours, a global study reported that high-risk genotypes are more frequent than low-risk ones [6, 12, 17]. Furthermore, in agreement with our results, a study from China, where we have a lot of travel and business dealings, reported a higher frequency of high-risk genotypes (19.2%) compared with low-risk ones (6.4%) [40].

Remarkably, we observed that genotypes 53, 66, 51, and 39 were more frequent high-risk genotypes after HPV16, respectively. However, other Iranian studies reported different high-risk genotypes following HPV16 such as genotypes 52 [16], 66 [14], 51 [30], and 68 [31]. Given that the available 9-valent HPV vaccine is protective against high-risk genotypes 16, 52, 31, 18, 58, 45, and 33 as well as low-risk genotypes 6 and 11, and based on the other Iranian study and ours, it seems that some more frequent HPV high-risk genotypes such as 53, 66, 51 and 39 among Iranian population were not covered by the currently available vaccine. In addition, in the present study, we observed that genotype 44 which is the second most frequent low-risk genotype is not included in the vaccine. Exploring the distribution of HPV genotypes in other countries revealed that in China, genotypes 52, 58, 16, 51, and 56 were more frequent, respectively [45]. Another study from Beijing, China, reported that genotypes 52, 58, 16, 39, and 51 were the most common high-risk genotypes [39]. A study from Weifang reported that genotypes 16, 52, 58, 53, and 68 were more frequent. A report from Maputo city, Mozambique, showed that genotypes 52, 35, 16, 53, 58, and 51 were the high-risk genotypes [24]. Researchers from Shanghai, China, reported that high-risk genotypes 52, 58, 16, 53, 51, and 81 were more prevalent [15] and A study from the Metropolitan Area of Naples, Italy, reported that genotypes 16, 31, 18, and 51 were the most frequent types [15]. Accordingly, it seems that the other more frequent high-risk genotypes with worldwide distribution should be added to the new vaccine formulation to significantly decline the outcomes of HPV infections in the world especially in our country, Iran.

Investigating the association of HPV genotypes with age range showed that a higher frequency of HPV infection was observed in age groups less than 30 years old, while, in the individuals with age > 60 years old the prevalence rate of HPV infection statistically reduced. In agreement with our study, another study from Iran and other countries reported the same association between HPV prevalence and age ranges. Almost in all studies, the highest frequency was observed in the ages < 30 years old [8, 16, 26, 36]. CDC recommends two schedules for HPV vaccination based on the age of vaccinated individuals. A two-dose series (0, 6–12 months) for most persons who initiate vaccination at ages 9 through 14 years and a three-dose series (0, 1–2, 6 months) for persons who initiate vaccination at ages 15 through 45 years, and also for immunocompromised patients [1]. So, it seems that based on the CDC recommendation and the prevalence rate of HPV infection, HPV vaccination for individuals less than 30 years old could be most effective in preventing the high-risk age group from future cancer-associated HPV.

A previous study reported that in 20–50% of HPV-infected women, especially young women, co-infection with more than one HPV type is common. Infection with multiple HPV types is often considered a risk factor leading to the development of cervical cancer [10]. In agreement with previous studies, we also observed 35% co-infection in our study groups. Among them, co-infection with 10 genotypes were also detected in two samples and co-infection with very high-risk genotypes 16 and 18 were determined in one percent of positive samples. Given the frequency of co-infection in our and the previous study and according to that more co-infection was observed between genotype 6, the most frequent genotype, and the high-risk genotypes 16, 66, and 53, respectively, it seems that vaccination with a vaccine containing more than 2 (Cervarix) and 4 (Gardasil, 4vHPV) genotypes like 9-valent is essential for the future vaccination strategy. In a Chinese large study, co-infection of genotypes 16 and 18 was similar to ours and they also reported that co-infection of HPV16 with other high-risk genotypes was 23.54% [42]. Among the multi-genotype HPV infection and disease outcomes, it has been reported that the risk of high-grade squamous epithelial lesions increases with the number of HPV types (Odds ratio for single, 2 to 3 and 4 to 6 HPV types were 41.5, 91.7 and 424, respectively), compared with HPV negative samples [35]. A recent study reported that TLR4 rs10759931 is protective against multiple high-risk HPV infections and in contrast, haplotype ACAC (at the loci rs7873784, rs4986791, rs4986790 and rs4986791) in the TLR-4 as pathogen recognition receptor (PRR) on the innate immune cells increases the risk of infection with multiple high-risk genotypes [25]. So it seems that gene variants associated with immune responses can act as predisposing factors in the multiple HPV genotype infection. Our study limitations were that we selected the study population from individuals without and with symptoms referring to a subspecialty clinic for routine checkups which imply that they may be a high-risk group instead of the normal population that can affect the prevalence of HPV in the community. In addition, there was no information about pop smear results and clinical manifestations in the HPV-infected individuals to compare with HPV-negative ones. Furthermore, the situation of cervical cancer in the patients was not clear. As the positive rate of HPV infection was higher (29.9%) in our study compared with the results obtained from other population-based studies (9.73% in Ethiopia [33], 13.22% in China [19], and 13.6% in Canary Island [2], to determine the HPV distributions reflecting HPV prevalence, future studies with higher sample size collected from healthy individuals in the different parts of Iran is warranted.

In conclusion, we observed that HPV 6 and 16 were the most frequent low- and high-risk genotypes providentially included in the available 4- and 9-valent HPV vaccines. However, other high-risk prevalent genotypes such as 53, 66, 51, and 39 in the Fars province population, the southwest of Iran, are not included in the designed vaccines. Furthermore, it is recommended to add the other more frequent high-risk genotypes in future HPV vaccine formulations. However, the next studies are required to detect the impacts of other high-risk genotypes rather than 16 and 18 on the development of cervical cancer.

No conflict of interest to declare.

Acknowledgements Not applicable.

Author contributions

MK and AM conceived and designed the experiment, FM, HK, AR and GHK performed the experiments and collected the data, MK and MK collected the data and performed the analysis, and wrote the manuscript.

Data availability If requested, it will be available.

Ethics approval and consent to participate

The authors have no conflicts of interest to declare. The authors declare that they have conducted the project ethically according to the World Medical Association Declaration of Helsinki. The present study was approved by the Ethics Committee of Fasa University of Medical Sciences with approval number IR.FUMS.REC.1403.52. No informed consent or other action from the patients was required because of the anonymity of the data analyses

Consent for publication is not applicable.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

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Comparing the distributions of common Human papillomavirus genotypes among the Fars province population in the southwest of Iran, with the vaccine-included genotypes

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Abstract

Background

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Results

Conclusion

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Introduction

Materials and methods

Study populations

DNA extraction

HPV genotyping

Statistical analysis

Results

HPV genotypes distribution

Distribution of HPV in different age ranges

HPV co-infection

HPV genotypes cross-infection

Discussion

Conclusion

Declarations

References

Additional Declarations

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