Human Papilloma Virus Infection in Iranian Women with Breast Cancer: A Systematic Review

authors:

avatar Abolfazl Jafari Sales ORCID 1 , 2 , avatar Mahdiyeh Ebrahimzadeh ORCID 3 , avatar Mehrdad Pashazadeh ORCID 4 , 5 , *

Department of Microbiology, Faculty of Basic Sciences, Islamic Azad University, Kazerun, Iran
Department of Microbiology, Faculty of Basic Sciences, Islamic Azad University, Tabriz, Iran
Department of Microbiology, Faculty of Basic Sciences, Islamic Azad University, Ahar, Iran
Department of Medical Laboratory Sciences and Microbiology, Faculty of Medical Sciences, Tabriz Medical Sciences, Islamic Azad University, Tabriz, Iran
Infectious Diseases Research Center, Tabriz Medical Sciences, Islamic Azad University, Tabriz, Iran

how to cite: Jafari Sales A, Ebrahimzadeh M, Pashazadeh M. Human Papilloma Virus Infection in Iranian Women with Breast Cancer: A Systematic Review. J Clin Res Paramed Sci. 2024;13(1):e139723. https://doi.org/10.5812/jcrps-139723.

Abstract

Background:

Breast cancer (BC) is one of the most common cancers and health problems in women under the age of 40.

Objectives:

This systematic study investigates the presence of human papilloma virus (HPV) in Iranian women with BC by searching various international and Iranian databases using standardized keywords.

Methods:

The inclusion and exclusion criteria were applied to select 22 articles with a total of 2445 BC samples for data extraction and analysis using Statistical Package for the Social Sciences (SPSS) software.

Results:

The results show that 21.10% of BC samples were HPV positive with Khuzestan, Shahrekord, Mashhad, and Karaj having the highest number of HPV-positive cases among women with BC. Polymerase chain reaction (PCR) was the most used method for detecting HPV in the studies. The distribution of BC samples was highest in Karaj, Tehran, and Golestan.

Conclusions:

This study provides valuable information about the prevalence of HPV in Iranian women with BC and the geographical distribution of positive cases.

1. Background

Breast cancer (BC) is one of the most common cancers and health problems in women under the age of 40, with a number of about 244 000 cases per year (1-4). In such a way that it constitutes more than 30% of important cancers in women (150 times more than men). The findings of the last few decades show that BC is the second cause of death in developing countries (44,800 deaths per year) and the third cause of death in developing countries (5-9). Breast cancer is caused by the abnormal proliferation of breast tissue cells, which mainly occurs in milk ducts and milk-producing glands, and may metastasize to distant areas of the body, or invade surrounding tissues (10). The world health organization (WHO) estimates that by 2050, at least 3.2 million women will be diagnosed with cancer (11, 12). The most frequent sites for BC metastasis include the bone, lung, liver, brain, and distant lymph nodes (13). The prevalence of BC in Iranian women is relatively high and accounts for 76% of common cancers in women (14). The researchers' findings show that the incidence of BC in the countries of Northern Europe and North America is higher than in Asia, Africa, South America and Southern Europe. This can be caused by the following factors: Aging, genetics, unhealthy behavior, types of radiation, smoking, geographical effects, number of pregnancies, late menopause, early menstruation, obesity, and differences in fertility patterns (15-19). Considering that various studies show that biological factors can be involved in 16% of human cancers (20). Women under the age of 45 account for 11 and 9% of BC in the United States and the United Kingdom (21). The cause of this increase can be due to various reasons such as changes in the status of social economic factors, increase in environmental risk factors, or improvement of diagnosis methods. Breast cancer can impose a lot of costs on the health system. Therefore, identifying the factors involved in the occurrence of cancer can be useful for the health system. Human papillomavirus (HPV) is a well-known sexually transmitted virus (22-25) that is primarily associated with cervical cancer, followed by anal, penile, and head and neck cancer. However, new evidence suggests a potential link between HPV infection and BC (26-30). Several studies have investigated the presence of HPV DNA in BC tissues with mixed results. Some studies have reported a higher prevalence of HPV DNA in BC samples compared to normal breast tissue, suggesting a possible role of HPV in breast carcinogenesis (31). However, other studies have failed to find a consistent association between HPV and BC (32). The potential mechanisms of HPV-mediated cancer development have not yet been proven, but it is hypothesized that HPV infection may cause BC through activation of oncogenic pathways, immune dysregulation, or direct integration of viral DNA into the host genome (33-35). In addition, HPV infection may interact with other risk factors, such as hormonal imbalance or genetic predisposition, to increase the risk of BC (36, 37). Understanding the relationship between HPV and BC is important for several reasons. First, if a causal relationship is established, it could have implications for prevention strategies, such as HPV vaccination, which have been successful in reducing the incidence of cervical cancer. Second, the detection of HPV DNA in BC tissues could potentially serve as a biomarker to identify subsets of BC patients who may benefit from targeted therapies or specific therapeutic approaches.

2. Objectives

The aim of this study was to systematically investigate the presence of HPV in women with BC in studies conducted in Iran.

3. Methods

3.1. Study Protocol

This article was written according to the PRISMA guidelines, which describe how to write systematic articles (38).

3.2. Search Strategy

The present study is a systematic study that investigates the presence of HPV in Iranian women with BC. Therefore, Web of Science, Scopus, PubMed, ScienceDirect, EBESCO, Embase, Google Scholar, Magiran, SID, and Irandoc databases were used for searching. The WHO website was also used. The search was updated until 2 August 2023 among scientific articles published in Iranian and non-Iranian journals. Because the present study is related to Iranian women with BC, in addition to international databases, Iranian and Persian language databases were also used. To search the databases of the keywords of BC, HPV, prevalence, ferequency, genotype, cross sectional, seroprevalence, and Iranian women in Persian and English languages were used. Keywords were standardized using the MESH system. Studies consistent with a relationship between HPV and breast cancer have been searched.

3.3. Selection of Articles

First, a list of titles and abstracts of all searched articles in Farsi and English was prepared in ENDNOTE software. This work was done by two researchers independently (AJS and ME) and minor differences were resolved during joint meetings between the two researchers and with the cooperation of MP.

3.4. Inclusion and Exclusion Criteria

The inclusion criteria included: All research articles, thematic relevance, and complete articles. To increase the sensitivity of article selection, minimum inclusion criteria were used. Exclusion criteria included: Lack of relevance, systematic studies, reviews, case reports, animal studies lack of sufficient information, and lack of access to the full text. In the final stage, the content of the articles was examined in terms of methodology. The inclusion and exclusion criteria were controlled by MP researcher.

3.5. Data Extraction

To reduce possible biases, two researchers (ME and MP) independently extracted data from the articles. The data included the place of study, year, name of authors, language of publication, method, number of samples, number of positive samples, percentage of positive samples, and references of articles. Then the content of the articles was given in Table 1.

Table 1.

Comparison of HPV Infection in Women with BC According to the Study Area, Year of Publication, Names of Authors, Language of the Article, Type of Method and Odds Ratio

Study PlaceYearAuthorsPublication LanguageMethodNo. of CasePositive CaseP/N %Ref.
Rasht2023Fakour et al.ENPCR461532.61(39)
Tehran2023Khalilian et al.ENNested PCR2002412(40)
Kermanshah 2023Haghighi et al.ENPCR902325.56(41)
Karaj2022Hashemnejad et al.ENPCR50320139.96(42)
Tehran2021Golrokh Mofrad et al.ENNested PCR59711.86(43)
Khuzestan2020Hosseinpouri et al.PEPCR402562.5(44)
Shiraz2019Bakhtiarizadeh et alENPCR15000(45)
Shahrekord2019Khodabandehlou et al.ENPCR723548.61(46)
Tehran2019Kazemi Aghdam et al.ENNested PCR7500(47)
Tehran2018Ghaffari et al.ENNested PCR7245.56(48)
Kerman2018Malekpour Afshar et al.ENReal-Time PCR9888.16(49)
Yazd2016Doosti et al.ENNested PCR872022.99(50)
Sanandaj2016Karimi et al.ENPCR7022.86(51)
Tehran2015Aghakhani et al.ENNested PCR10000(52)
Tabriz2014Ahangar-Oskouee et al.ENNested PCR652233.85(53)
Karaj2014Doosti et al.PENested PCR872933.33(54)
Isfahan2014Manzouri et al.ENPCR551018.18(55)
Karaj2013Hossein et al.ENMultiplex PCR1505234.67(56)
Tehran2013Tahmasebi Fard et al.PEReal-Time PCR6600(57)
Sari2012Sigaroodi et al.ENPCR791518.99(58)
Mashad2009Seyedi Alavi et al.PEPCR502448(59)
Golestan2009Moradi et al.PEPCR23100(60)
Total244551621.10

3.6. Data Analysis

In this research, Statistical Package for the Social Sciences (SPSS) software (version 16) was used for statistical analysis of data (Average of samples).

3.7. Quality Assessment

The reviewed studies may have some risks of bias that need to be considered. Firstly, the inclusion and exclusion criteria were controlled by a single researcher, which may introduce bias in the selection process. Additionally, the data extraction was performed independently by two researchers, which could lead to potential biases in the interpretation of the data. Moreover, the methodological differences in the studies, such as the use of different PCR methods, could introduce bias in the comparison of results across different studies. Furthermore, the exclusion of articles due to the inappropriateness of the statement of the working method may have led to the exclusion of relevant studies, potentially introducing selection bias. Therefore, it is important to consider these potential biases when interpreting the findings of the reviewed studies. To reduce bias, the researchers used the risk of bias in non-randomized studies (ROBINS) strategy (61, 62) and the participation of all three researchers (AJS, ME, and MP) in the final analysis.

4. Results

The initial search based on the prepared checklist included 341 articles, of which 170 articles were removed due to duplication. After the initial review of articles (171 articles), 102 related articles were selected and reviewed. 32 articles due to being specific to a certain age group, 16 articles due to overlapping with other studies, 14 articles due to lack of extractable data, 11 articles due to single case reports, 5 articles due to lack of epidemiological information, and 2 articles. They were excluded from the review process due to the inappropriateness of the statement of the working method. Finally, 22 published articles 5 (22.73%) articles in Persian language and 17 (77.27%) articles in English language) were reviewed and analyzed (Figure 1). In total, from 22 articles with 2445 BC samples, 21.10% (516 samples) were HPV positive. Khuzestan, Shahrekord, Mashhad, and Karaj had the highest number of HPV-positive cases among women with BC with odds ratio of 62.5%, 48.61%, 48%, and 38.11%, respectively (Figure 2). Among them, Golestan and Shiraz had a chance ratio of zero percent. PCR (50%), nested PCR (36.36%), real-time PCR (9.10%), and multiplex PCR (4.54%) were the most investigated methods in the studies. Out of 2445 BC samples, the most distribution was related to the cities of Karaj (740 samples), Tehran (572 samples), Golestan (231 samples), Shiraz (150 samples), Kerman (98), Kermanshah (90 samples), Yazd (87), Sari (79 samples), Shahrekord (72 samples), Sanandaj (70 samples), Tabriz (65 samples), Isfahan (55 samples), Mashhad (50 samples), Rasht (46 samples), and Khuzestan (40 samples).

Search flow diagram through databases
Search flow diagram through databases
Comparison of HPV infection in breast cancer classified according to study area
Comparison of HPV infection in breast cancer classified according to study area

5. Discussion

This systematic review was conducted with the aim of investigating the presence of HPV infection in Iranian women with BC. This study analyzed related studies conducted in Iran and evaluated the prevalence of HPV infection in BC tissues in Iranian women. From 22 related articles, a total of 2445 cases of BC were identified, and the overall prevalence of HPV in Iranian women with BC was 21.10%. This suggests that HPV infection may be associated with a higher risk of BC in Iranian women. Therefore, the findings of the systematic review show the potential relationship between HPV infection and BC in Iranian women. Several studies included in this review reported the presence of HPV DNA in BC tissues, indicating the possible involvement of HPV in breast carcinogenesis (33, 63). In the Middle East, studies have shown that HPV is present in BC tissues in Iraqi, Pakistani, Syrian, Turkish, and Qatar women (64-68). However, there are also studies from Tunisia that failed to detect HPV in BC tissues (69). The prevalence of HPV infection in BC may be different in different countries of the Middle East region. In Africa, countries such as Morocco, Algeria, Nigeria, and Congo reported the presence of HPV in women with BC (70-74). In their 2011 systematic review, Li et al. showed that 32.42%, 12.91%, 16.67%, 20%, and 42.11% of HPV-positive BC cases occurred in Asia, Europe, South America, North America, and Oceania (75). However, it is important to note that the results of the included studies were not consistent. Some studies reported a higher prevalence of HPV DNA in BC samples compared to normal breast tissue, while others found no significant association. These discrepancies may be attributed to variations in study design, sample size, diagnostic methods, and patient characteristics (63). The potential mechanisms by which HPV may contribute to the development of BC are not yet fully understood. It is hypothesized that HPV infection may activate oncogenic pathways, induce immune dysfunction, or directly integrate viral DNA into the host genome, leading to BC development (33-35). However, more research is needed to clarify the underlying mechanisms and establish a definitive link between HPV and BC. The findings of this systematic review have important implications for the prevention and management of BC in Iran. If the relationship between HPV and BC is established, it could have implications for HPV vaccination strategies, similar to the successful implementation of HPV vaccination to prevent cervical cancer. In addition, the detection of HPV DNA in BC tissues could potentially serve as a biomarker to identify a subset of BC patients who may benefit from targeted therapies or specific therapeutic approaches (76-79). It is worth mentioning that this systematic review is specifically focused on Iranian women with BC. Therefore, the findings may not be generalizable to other populations. Further research, including larger-scale studies and diverse populations, is needed to confirm the findings and determine the global relevance of the association between HPV infection and BC.

5.1. Conclusions

The present study shows the presence of HPV infection in Iranian women with BC and the potential relationship between HPV and BC in this population. Several studies included in this review reported the presence of HPV DNA in BC tissues, indicating a possible role of HPV in breast carcinogenesis. However, the results of the included studies were not consistent, and further research is needed to confirm this association and understand the underlying mechanisms. The findings of this systematic review have important implications for the prevention and management of BC in Iran. If a causal relationship between HPV and BC is established, it could have implications for HPV vaccination strategies and the development of targeted therapies for a subset of BC patients. However, it is important to note that the review specifically focused on Iranian women and more research in different populations is needed to confirm the findings and determine the universality of the association between HPV infection and BC.

References

  • 1.

    Mousavi SM, Montazeri A, Mohagheghi MA, Jarrahi AM, Harirchi I, Najafi M, et al. Breast cancer in Iran: An epidemiological review. Breast J. 2007;13(4):383-91. [PubMed ID: 17593043]. https://doi.org/10.1111/j.1524-4741.2007.00446.x.

  • 2.

    Parkin DM, Laara E, Muir CS. Estimates of the worldwide frequency of sixteen major cancers in 1980. Int J Cancer. 1988;41(2):184-97. [PubMed ID: 3338870]. https://doi.org/10.1002/ijc.2910410205.

  • 3.

    Ferlay J, Colombet M, Soerjomataram I, Parkin DM, Pineros M, Znaor A, et al. Cancer statistics for the year 2020: An overview. Int J Cancer. 2021. [PubMed ID: 33818764]. https://doi.org/10.1002/ijc.33588.

  • 4.

    Mahboobi A, Alvandi SH, Alizadeh Navaei R. An analytical survey on breast lesions in mammography. J Babol Univ Med Sci. 2004;6(2):52-5.

  • 5.

    Dean T, Armando E. Breast cancer. novak, Berek J, editors. Novak's gynecoloy. 13th. Philadelphia: Lippincott William & Wilkins; 2002.

  • 6.

    Mancino AT. Diseases of the Breast. Annals of Surgery. 2001;233(4). https://doi.org/10.1097/00000658-200104000-00018.

  • 7.

    YektaKooshali MH, Esmaeilpour-Bandboni M, Sharemi SH, Alipour Z. Survival rate and average age of the patients with breast cancer in iran: Systematic review and meta-analysis. J Babol Univ Med Sci. 2016;18(8):29-40.

  • 8.

    Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61(2):69-90. [PubMed ID: 21296855]. https://doi.org/10.3322/caac.20107.

  • 9.

    Ghoncheh M, Mohammadian-Hafshejani A, Salehiniya H. Incidence and mortality of breast cancer and their relationship to development in Asia. Asian Pac J Cancer Prev. 2015;16(14):6081-7. [PubMed ID: 26320499]. https://doi.org/10.7314/apjcp.2015.16.14.6081.

  • 10.

    Motovali-Bashi M, Amirmahani F, Ghatre Samani Z. Association between miR-152/148a polymorphisms and age of onset and progression of breast cancer in Isfahan population. Res Med. 2017;40(4):187-91.

  • 11.

    Hortobagyi GN, de la Garza Salazar J, Pritchard K, Amadori D, Haidinger R, Hudis CA, et al. The global breast cancer burden: Variations in epidemiology and survival. Clin Breast Cancer. 2005;6(5):391-401. [PubMed ID: 16381622]. https://doi.org/10.3816/cbc.2005.n.043.

  • 12.

    YektaKooshali MH, Esmaeilpour- Bandboni M, Ramezani A. The Scientific Production and Mapping of researchers in Breast Cancer during 1985– 2015 in Iran in Web of Sciences. 2016. https://doi.org/10.13140/RG.2.1.1085.8483.

  • 13.

    Jin X, Mu P. Targeting breast cancer metastasis. Breast Cancer (Auckl). 2015;9(Suppl 1):23-34. [PubMed ID: 26380552]. [PubMed Central ID: PMC4559199]. https://doi.org/10.4137/BCBCR.S25460.

  • 14.

    EnayatRad M, Salehinia H. An investigation of changing patterns in breast cancer incidence trends among Iranian women. J Sabzevar Univ Med Sci. 2015;22(1):27-35.

  • 15.

    Kelsey JL. A review of the epidemiology of human breast cancer. Epidemiol Rev. 1979;1:74-109. [PubMed ID: 398270]. https://doi.org/10.1093/oxfordjournals.epirev.a036215.

  • 16.

    Amini Sani N, Shamshir Garan M, Ghavam Nasiri M, Setayesh Y. The effect of active and passive smoking associated with breast cancer. J Babol Univ Med Sci. 2005;7(1):63-8.

  • 17.

    Hajian K, Gholizadehpasha A, Bozorgzadeh SH. Association of obesity and central obesity with breast cancer risk in pre-and postmenopausal women. J Babol Univ Med Sci. 2013;15(3):7-15.

  • 18.

    Lawson JS. Do viruses cause breast cancer? Methods Mol Biol. 2009;471:421-38. [PubMed ID: 19109792]. https://doi.org/10.1007/978-1-59745-416-2_21.

  • 19.

    Yaghmaei S, Bani Hashemi G, Ghorbani R. Survival rate following treatment of primary breast cancer in Semnan, Iran (1991-2002). Koomesh. 2008:111-6.

  • 20.

    de Martel C, Ferlay J, Franceschi S, Vignat J, Bray F, Forman D, et al. Global burden of cancers attributable to infections in 2008: A review and synthetic analysis. Lancet Oncol. 2012;13(6):607-15. [PubMed ID: 22575588]. https://doi.org/10.1016/S1470-2045(12)70137-7.

  • 21.

    Daly AA, Rolph R, Cutress RI, Copson ER. A review of modifiable risk factors in young women for the prevention of breast cancer. Breast Cancer (Dove Med Press). 2021;13:241-57. [PubMed ID: 33883932]. [PubMed Central ID: PMC8053601]. https://doi.org/10.2147/BCTT.S268401.

  • 22.

    Faghani Baladehi R, Yousef Memar M, Jafari Sales A, Bazmani A, Sadri Nahand J, Shiri Aghbash P, et al. The effect of oncogene proteins of human papillomaviruses on apoptosis pathways in prostate cancer. Oncologie. 2022;24(2):227-45. https://doi.org/10.32604/oncologie.2022.020648.

  • 23.

    Faghany Baladehi R, Bazmani A, Ahangar Oskouee M, Jafari Sales A, Pirzadeh T, Shokouhi B, et al. Frequency of human papilloma virus 16/18 patients with prostate cancer by polymerase chain reaction method in hospitals of Tabriz City, Iran. Journal of Inflammatory Diseases. 2022;26(1):19-26. https://doi.org/10.32598/jid.26.1.2.

  • 24.

    Jafari-Sales A, Jafari B, Khaneshpour H, Sadeghi-Deylamdeh Z, Shariat A, Bannazadeh-Baghi H, et al. Helicobacter pylori: A systematic review of drug resistance in Iran. Reviews Research in Med Microbiol. 2022:10.1097.

  • 25.

    Jafari-Sales A, Shariat A, Bannazadeh Baghi H, Baradaran B, Jafari B. The presence of human papillomavirus and epstein-barr virus infection in gastric cancer: A systematic study. Oncologie. 2022;24(3):413-26. https://doi.org/10.32604/oncologie.2022.024161.

  • 26.

    Bansal A, Singh MP, Rai B. Human papillomavirus-associated cancers: A growing global problem. Int J Appl Basic Med Res. 2016;6(2):84-9. [PubMed ID: 27127735]. [PubMed Central ID: PMC4830161]. https://doi.org/10.4103/2229-516X.179027.

  • 27.

    Lekoane KMB, Kuupiel D, Mashamba-Thompson TP, Ginindza TG. Evidence on the prevalence, incidence, mortality and trends of human papilloma virus-associated cancers in sub-Saharan Africa: Systematic scoping review. BMC Cancer. 2019;19(1):563. [PubMed ID: 31185951]. [PubMed Central ID: PMC6558783]. https://doi.org/10.1186/s12885-019-5781-3.

  • 28.

    Sofiani VH, Veisi P, Rukerd MRZ, Ghazi R, Nakhaie M. The complexity of human papilloma virus in cancers: A narrative review. Infect Agent Cancer. 2023;18(1):13. [PubMed ID: 36843070]. [PubMed Central ID: PMC9969657]. https://doi.org/10.1186/s13027-023-00488-w.

  • 29.

    Lawson JS, Salmons B, Glenn WK. Oncogenic viruses and breast cancer: Mouse mammary tumor virus (MMTV), Bovine Leukemia Virus (BLV), Human Papilloma Virus (HPV), and Epstein-Barr Virus (EBV). Front Oncol. 2018;8:1. [PubMed ID: 29404275]. [PubMed Central ID: PMC5786831]. https://doi.org/10.3389/fonc.2018.00001.

  • 30.

    Jafari-Sales A, Shariat A, Bannazadeh-Baghi H, Baradaran B, Jafari B. Human Papillomavirus (HPV) Prevalence and E6 Protein Expression in Gastric Cancer Tissue Samples Compared with Non-malignant and Control Groups in East Azerbaijan Province, Iran, 2021. Iranian J Med Microbiol. 2023;17(1):58-65. https://doi.org/10.30699/ijmm.17.1.58.

  • 31.

    Lawson JS, Glenn WK, Heng B, Ye Y, Tran B, Lutze-Mann L, et al. Koilocytes indicate a role for human papilloma virus in breast cancer. Br J Cancer. 2009;101(8):1351-6. [PubMed ID: 19773762]. [PubMed Central ID: PMC2768439]. https://doi.org/10.1038/sj.bjc.6605328.

  • 32.

    Tsai JH, Tsai CH, Cheng MH, Lin SJ, Xu FL, Yang CC. Association of viral factors with non-familial breast cancer in Taiwan by comparison with non-cancerous, fibroadenoma, and thyroid tumor tissues. J Med Virol. 2005;75(2):276-81. [PubMed ID: 15602723]. https://doi.org/10.1002/jmv.20267.

  • 33.

    Simoes PW, Medeiros LR, Simoes Pires PD, Edelweiss MI, Rosa DD, Silva FR, et al. Prevalence of human papillomavirus in breast cancer: A systematic review. Int J Gynecol Cancer. 2012;22(3):343-7. [PubMed ID: 22214962]. https://doi.org/10.1097/IGC.0b013e31823c712e.

  • 34.

    Williams VM, Filippova M, Soto U, Duerksen-Hughes PJ. HPV-DNA integration and carcinogenesis: Putative roles for inflammation and oxidative stress. Future Virol. 2011;6(1):45-57. [PubMed ID: 21318095]. [PubMed Central ID: PMC3037184]. https://doi.org/10.2217/fvl.10.73.

  • 35.

    Lin C, Tsai SC, Huang JY, Lin FC. HPV infection and breast cancer risk: Insights from a nationwide population study in Taiwan. Front Oncol. 2023;13:1210381. [PubMed ID: 37519781]. [PubMed Central ID: PMC10379647]. https://doi.org/10.3389/fonc.2023.1210381.

  • 36.

    Purrahman D, Avarvand AY, Paradowska-Gorycka A, Saki N, Karimpourian H, Jodat H, et al. Association of human papillomavirus with breast cancer: A new perspective on an old debate. Future Oncol. 2022;18(22):2483-94. [PubMed ID: 35695559]. https://doi.org/10.2217/fon-2021-1158.

  • 37.

    Blanco R, Carrillo-Beltran D, Munoz JP, Corvalan AH, Calaf GM, Aguayo F. Human papillomavirus in breast carcinogenesis: A passenger, a cofactor, or a causal agent? Biology (Basel). 2021;10(8). [PubMed ID: 34440036]. [PubMed Central ID: PMC8389583]. https://doi.org/10.3390/biology10080804.

  • 38.

    Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. Int J Surg. 2021;88:105906. [PubMed ID: 33789826]. https://doi.org/10.1016/j.ijsu.2021.105906.

  • 39.

    Fakour F, Rafiei Sorouri Z, Hajizadeh Fallah A, Mousavi A, Farahmand M. Association of breast cancer with human papillomavirus types 16 and 18 in the North of Iran. J Obstetrics, Gynecology Cancer Res. 2023;8(2):173-80. https://doi.org/10.30699/jogcr.8.2.173.

  • 40.

    Khalilian M, Hosseini SM, Vahidi Emami H, Madadgar O. High Frequency of HPV Genotypes 16 and 18 Found in breast cancer patients: Evidence for a more comprehensive hpv vaccination program in Iran. J Advanced Biomed Sci. 2023. https://doi.org/10.18502/jabs.v13i2.12729.

  • 41.

    Haghighi ZMS, Tabatabaei T, Rafigh M, Karampour R, Babaei F, Amjad ZS, et al. Human papillomavirus maybe is a critical player in the regulation of chemoresistance related factors (P53, Rb, TWIST, Bcl-2, Bcl-XL, c-IAP2, cytochrome C, and caspase 3) in breast cancer. Pathol Res Pract. 2023;248:154653. [PubMed ID: 37454490]. https://doi.org/10.1016/j.prp.2023.154653.

  • 42.

    Hashemnejad M, Mirmajidi R, Rahimzadeh M, Ataei M. The prevalence of high-risk human papillomavirus genotypes and related risk factors among Iranian women. J Med Life. 2022;15(11):1340-6. [PubMed ID: 36567834]. [PubMed Central ID: PMC9762374]. https://doi.org/10.25122/jml-2022-0031.

  • 43.

    Golrokh Mofrad M, Sadigh ZA, Ainechi S, Faghihloo E. Detection of human papillomavirus genotypes, herpes simplex, varicella zoster and cytomegalovirus in breast cancer patients. Virol J. 2021;18(1):25. [PubMed ID: 33482849]. [PubMed Central ID: PMC7821692]. https://doi.org/10.1186/s12985-021-01498-z.

  • 44.

    Hosseinpouri P, Hejazi SH, Hadi F. Relationship between human papillomavirus and breast cancer in women with this cancer in Khuzestan province. Iranian J Obstetrics, Gynecology Infertility. 2020;23(8):66-74.

  • 45.

    Bakhtiyrizadeh S, Hosseini SY, Yaghobi R, Safaei A, Sarvari J. Almost complete lack of human cytomegalovirus and human papillomaviruses genome in benign and malignant breast lesions in Shiraz, Southwest of Iran. Asian Pacific J Cancer Prevention: Apjcp. 2017;18(12):3319.

  • 46.

    Khodabandehlou N, Mostafaei S, Etemadi A, Ghasemi A, Payandeh M, Hadifar S, et al. Human papilloma virus and breast cancer: The role of inflammation and viral expressed proteins. BMC Cancer. 2019;19(1):61. [PubMed ID: 30642295]. [PubMed Central ID: PMC6332859]. https://doi.org/10.1186/s12885-019-5286-0.

  • 47.

    Kazemi Aghdam M, Nadji SA, Alvandimanesh A, Maliheh M, Khademi Y. Absence of Human Papillomavirus in Benign and Malignant Breast Tissue. Iran J Pathol. 2019;14(4):279-83. [PubMed ID: 31754356]. [PubMed Central ID: PMC6824765]. https://doi.org/10.30699/ijp.2019.89684.1847.

  • 48.

    Ghaffari H, Nafissi N, Hashemi-Bahremani M, Alebouyeh MR, Tavakoli A, Javanmard D, et al. Molecular prevalence of human papillomavirus infection among Iranian women with breast cancer. Breast Dis. 2018;37(4):207-13. [PubMed ID: 30124441]. https://doi.org/10.3233/BD-180333.

  • 49.

    Malekpour Afshar R, Balar N, Mollaei HR, Arabzadeh SA, Iranpour M. Low Prevalence of Human Papilloma Virus in Patients with Breast Cancer, Kerman; Iran. Asian Pac J Cancer Prev. 2018;19(11):3039-44. [PubMed ID: 30485938]. [PubMed Central ID: PMC6318420]. https://doi.org/10.31557/APJCP.2018.19.11.3039.

  • 50.

    Doosti M, Bakhshesh M, Zahir ST, Shayestehpour M, Karimi-Zarchi M. Lack of evidence for a relationship between high risk human papillomaviruses and breast cancer in Iranian patients. Asian Pacific J Cancer Prevention. 2016;17(9):4357-61.

  • 51.

    Karimi M, Khodabandehloo M, Nikkhoo B, Ghaderi E. No significant association between human papillomavirus and breast cancer, Sanandaj, Iran. Asian Pacific J Cancer Prevention: APJCP. 2016;17(10):4741.

  • 52.

    Aghakhani A, Hamkar R, Ramezani A, Bidari-Zerehpoosh F, Sabeti S, Ghavami N, et al. Lack of human papillomavirus DNA in colon adenocarcinama and adenoma. J Cancer Res Ther. 2014;10(3):531-4. [PubMed ID: 25313733]. https://doi.org/10.4103/0973-1482.137674.

  • 53.

    Ahangar-Oskouee M, Shahmahmoodi S, Jalilvand S, Mahmoodi M, Ziaee AA, Esmaeili HA, et al. No detection of 'high-risk' human papillomaviruses in a group of Iranian women with breast cancer. Asian Pac J Cancer Prev. 2014;15(9):4061-5. [PubMed ID: 24935597]. https://doi.org/10.7314/apjcp.2014.15.9.4061.

  • 54.

    Doosti M, Bakhshesh M, Taghipour-Zahir S, Hatami A, Shayestehpour M, Moghimi M. The relationship of low-risk (6, 11) and high-risk types (16, 18) of papilloma virus and human breast cancer in women. J Isfahan Med School. 2014;32(279):368-77.

  • 55.

    Manzouri L, Salehi R, Shariatpanahi S, Rezaie P. Prevalence of human papilloma virus among women with breast cancer since 2005-2009 in Isfahan. Adv Biomed Res. 2014;3:75. [PubMed ID: 24627883]. [PubMed Central ID: PMC3950802]. https://doi.org/10.4103/2277-9175.125873.

  • 56.

    Hossein R, Behzad S, Tahar M, Azadeh NA. Prevalence of human papillomavirus genotypes associated with cervical and breast cancers in iran. Monoclon Antib Immunodiagn Immunother. 2013;32(6):399-403. [PubMed ID: 24328743]. https://doi.org/10.1089/mab.2013.0047.

  • 57.

    Tahmasebi Fard Z, Abdirad A, Saatian M, Arefian L. Association between human Papillomavirus (HPV) and breast cancer in Iranian patients. Med Sci J Islamic Azad Univesity-Tehran Medical Branch. 2013;23(2):120-6.

  • 58.

    Sigaroodi A, Nadji SA, Naghshvar F, Nategh R, Emami H, Velayati AA. Human papillomavirus is associated with breast cancer in the north part of Iran. ScientificWorldJournal. 2012;2012:837191. [PubMed ID: 22566779]. [PubMed Central ID: PMC3329875]. https://doi.org/10.1100/2012/837191.

  • 59.

    Seyedi Alavi G, Sharifi N, Sadeghian A, Jabari H, Bahreyni M, Bagheri H. Presence of human papilloma virus sequences in breast cancer tissues and association with histopathological features. Iranian J Obstetrics, Gynecology Infertility. 2009;12(2):1-4.

  • 60.

    Moradi A, Mobasheri E, Tabarraei A, Bakhshandeh Nosrat S, Azarhosh R, Alizadeh SH, et al. Molecular epidemiology of Human Papillomaviruses in breast cancer, Golestan province of Iran. Medical Laboratory J. 2009;3(1):0.

  • 61.

    Morgan RL, Thayer KA, Santesso N, Holloway AC, Blain R, Eftim SE, et al. Evaluation of the risk of bias in non-randomized studies of interventions (ROBINS-I) and the 'target experiment' concept in studies of exposures: Rationale and preliminary instrument development. Environ Int. 2018;120:382-7. [PubMed ID: 30125855]. [PubMed Central ID: PMC9581061]. https://doi.org/10.1016/j.envint.2018.08.018.

  • 62.

    Sterne JA, Hernan MA, Reeves BC, Savovic J, Berkman ND, Viswanathan M, et al. ROBINS-I: A tool for assessing risk of bias in non-randomised studies of interventions. BMJ. 2016;355. i4919. [PubMed ID: 27733354]. [PubMed Central ID: PMC5062054]. https://doi.org/10.1136/bmj.i4919.

  • 63.

    Bae JM, Kim EH. Human papillomavirus infection and risk of breast cancer: A meta-analysis of case-control studies. Infect Agent Cancer. 2016;11:14. [PubMed ID: 26981149]. [PubMed Central ID: PMC4791894]. https://doi.org/10.1186/s13027-016-0058-9.

  • 64.

    Ali SH, Al-Alwan NA, Al-Alwany SH. Detection and genotyping of human papillomavirus in breast cancer tissues from Iraqi patients. East Mediterr Health J. 2014;20(6):372-7. [PubMed ID: 24960513].

  • 65.

    Naushad W, Surriya O, Sadia H. Prevalence of EBV, HPV and MMTV in Pakistani breast cancer patients: A possible etiological role of viruses in breast cancer. Infect Genet Evol. 2017;54:230-7. [PubMed ID: 28705719]. https://doi.org/10.1016/j.meegid.2017.07.010.

  • 66.

    Akil N, Yasmeen A, Kassab A, Ghabreau L, Darnel AD, Al Moustafa AE. High-risk human papillomavirus infections in breast cancer in Syrian women and their association with Id-1 expression: A tissue microarray study. Br J Cancer. 2008;99(3):404-7. [PubMed ID: 18648363]. [PubMed Central ID: PMC2527786]. https://doi.org/10.1038/sj.bjc.6604503.

  • 67.

    Gumus MAHMUT, Yumuk PF, Salepci T, Aliustaoglu M, Dane FAYSAL, Ekenel M, et al. HPV DNA frequency and subset analysis in human breast cancer patients' normal and tumoral tissue samples. J Experimental Clinical Cancer Research: CR. 2006;25(4):515-21.

  • 68.

    Sher G, Salman NA, Kulinski M, Fadel RA, Gupta VK, Anand A, et al. Prevalence and Type Distribution of High-Risk Human Papillomavirus (HPV) in Breast Cancer: A Qatar Based Study. Cancers (Basel). 2020;12(6). [PubMed ID: 32532107]. [PubMed Central ID: PMC7352582]. https://doi.org/10.3390/cancers12061528.

  • 69.

    Hachana M, Ziadi S, Amara K, Toumi I, Korbi S, Trimeche M. No evidence of human papillomavirus DNA in breast carcinoma in Tunisian patients. Breast. 2010;19(6):541-4. [PubMed ID: 20547456]. https://doi.org/10.1016/j.breast.2010.05.007.

  • 70.

    Habyarimana T, Attaleb M, Mazarati JB, Bakri Y, El Mzibri M. Detection of human papillomavirus DNA in tumors from Rwandese breast cancer patients. Breast Cancer. 2018;25(2):127-33. [PubMed ID: 29350329]. https://doi.org/10.1007/s12282-018-0831-2.

  • 71.

    Corbex M, Bouzbid S, Traverse-Glehen A, Aouras H, McKay-Chopin S, Carreira C, et al. Prevalence of papillomaviruses, polyomaviruses, and herpesviruses in triple-negative and inflammatory breast tumors from algeria compared with other types of breast cancer tumors. PLoS One. 2014;9(12). e114559. [PubMed ID: 25478862]. [PubMed Central ID: PMC4257687]. https://doi.org/10.1371/journal.pone.0114559.

  • 72.

    ElAmrani A, Gheit T, Benhessou M, McKay-Chopin S, Attaleb M, Sahraoui S, et al. Prevalence of mucosal and cutaneous human papillomavirus in Moroccan breast cancer. Papillomavirus Res. 2018;5:150-5. [PubMed ID: 29660489]. [PubMed Central ID: PMC5909064]. https://doi.org/10.1016/j.pvr.2018.04.003.

  • 73.

    Chigbu CO, Onyebuchi AK, Onyeka TC, Odugu BU, Dim CC. The impact of community health educators on uptake of cervical and breast cancer prevention services in Nigeria. Int J Gynaecol Obstet. 2017;137(3):319-24. [PubMed ID: 28295268]. https://doi.org/10.1002/ijgo.12150.

  • 74.

    Boumba ALM, Malanda Mboungou Moudiongui D, Ngatali SFC, Takale RP, Moukassa D, Peko JF. Oncogenic human papillomavirus in breast cancer: Molecular prevalence in a group of Congolese patients. Access Microbiol. 2021;3(3):216. [PubMed ID: 34151168]. [PubMed Central ID: PMC8209706]. https://doi.org/10.1099/acmi.0.000216.

  • 75.

    Li N, Bi X, Zhang Y, Zhao P, Zheng T, Dai M. Human papillomavirus infection and sporadic breast carcinoma risk: A meta-analysis. Breast Cancer Res Treat. 2011;126(2):515-20. [PubMed ID: 20740311]. [PubMed Central ID: PMC3164261]. https://doi.org/10.1007/s10549-010-1128-0.

  • 76.

    Sharma P. Biology and management of patients with triple-negative breast cancer. Oncologist. 2016;21(9):1050-62. [PubMed ID: 27401886]. [PubMed Central ID: PMC5016071]. https://doi.org/10.1634/theoncologist.2016-0067.

  • 77.

    Sahasrabuddhe VV, Luhn P, Wentzensen N. Human papillomavirus and cervical cancer: Biomarkers for improved prevention efforts. Future Microbiol. 2011;6(9):1083-98. [PubMed ID: 21958146]. [PubMed Central ID: PMC3809085]. https://doi.org/10.2217/fmb.11.87.

  • 78.

    Widschwendter A, Brunhuber T, Wiedemair A, Mueller-Holzner E, Marth C. Detection of human papillomavirus DNA in breast cancer of patients with cervical cancer history. J Clin Virol. 2004;31(4):292-7. [PubMed ID: 15494272]. https://doi.org/10.1016/j.jcv.2004.06.009.

  • 79.

    De Carolis S, Storci G, Ceccarelli C, Savini C, Gallucci L, Sansone P, et al. HPV DNA associates with breast cancer malignancy and it is transferred to breast cancer stromal cells by extracellular vesicles. Front Oncol. 2019;9:860. [PubMed ID: 31608222]. [PubMed Central ID: PMC6756191]. https://doi.org/10.3389/fonc.2019.00860.