ecancermedicalscience

Review

Determinants of breast cancer in Ethiopia: a systematic review and meta-analysis

Lencho Kajela Solbana1 and Eshetu Ejeta Chaka2

1College of Health Science, Assosa University, PO Box 018, Assosa, Ethiopia

2College of Medicine and Health Sciences, Ambo University, PO Box 19, Ambo, Ethiopia


Abstract

Background: Breast cancer (BC) is the first leading cancer sharing about 25% of the cancer burden among women globally. This study aimed to identify the determinants of BC in Ethiopia.

Methods: We comprehensively searched primary studies conducted in Ethiopia on associated factors of BC in PubMed, Cochrane Library, Hinari, Google, and Google Scholar) and available online until 2 June 2023. The necessary data were extracted from relevant studies and exported to STATA version 15 for analysis. The pooled odds ratio with its 95% confidence interval (CI) was estimated using a random effect model. The finding was reported following preferred reporting items for systematic reviews and meta-analyses guidelines.

Results: Five studies with 1,819 participants (792 cases and 1,027 controls) were included. The significant determinants of BC were age at menarche <12 years (adjusted odds ratio (AOR) = 3.36, 95% CI: 1.68–5.04), post-menopause (AOR = 2.37, 95% CI: 1.67–3.06), ever breastfeeding (AOR = 0.28, 95% CI: 0.15–0.42), and family history of cancer (AOR = 2.39, 95% CI: 1.29–3.44).

Conclusion: In Ethiopia, the significant determinants of BC among women were age at menarche <12 years, post-menopause, Ever breastfeeding, and family history of cancer. We recommend that the concerned organizations consider the aforementioned factors in addressing the problem of BC in Ethiopia by increasing community awareness, promoting breast self-examination, and developing programs to reduce the increasing burden of BC in the study setting.

Keywords: breast cancer, determinant, Ethiopia, women, meta-analysis

Correspondence to: Lencho Kajela Solbana
Email: lejch7@gmail.com

Published: 10/11/2023
Received: 29/06/2023

Publication costs for this article were supported by ecancer (UK Charity number 1176307).

Copyright: © the authors; licensee ecancermedicalscience. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.


Introduction

Breast cancer (BC) is a group of diseases in which cells in breast tissue change and divide uncontrolled, typically resulting in a lump or mass [1, 2]. It can be invasive or non-invasive. The invasive BC is where the cancer cells are only found in the ducts, which is known as ductal carcinoma in situ (DCIS) and the non-invasive BC is where the cancer cells have grown into surrounding tissue [3]. Types of BC depend on which cells in the breast turn into cancer [2]. Most BCs begin in the lobules (milk glands) or in the ducts that connect the lobules to the nipple [1]. It can spread outside the breast through blood vessels and lymph vessels. When this happens, it is said to have metastasized [2]. Less frequently occurring types of BC also occur in breast tissues, these cancers are called sarcomas and lymphomas [3].

Globally, BC accounts for 12.5% of cancer in the general population and shares 25.8% of cancer cases among women in 2020 [4]. It is the fifth leading cause of cancer mortality worldwide [5]. The International Agency for Research on Cancer (IARC) estimates there were more than 2.26 million new cases of BC and 685,000 deaths from it worldwide in 2020 [6]. In Sub-Saharan African (SSA) countries, BC was the most common cancer type among women [7]. In SSA lack of human resources and service delivery such as difficulty accessing health care, diagnostic errors, poor management, and treatment costs were the principal health system factors that influenced the diagnosis and treatment of women with BC [8].

Low-income countries have poorly developed health systems including cancer services indeed need up-grading [9]. In 2014 World Health Organization (WHO) report indicated that cancer is an increasing public health burden for Ethiopia [10]. In 2018, BC was the first leading cancer type which accounts for 22.6% and 17.0% of the morbidity and mortality of the cancer burden in the country [11]. The finding of the trend analysis done from 2010 to 2019 indicates the common killer cancers in Ethiopia were leukemia, BC, cervical cancer, and stomach cancer [12]. The other trend analysis done from 2013 to 2019 at Hawassa University Comprehensive Specialized Hospital shows there was a continuous increment in BC cases at the hospital [13].

According to a previous qualitative study done in southwest Ethiopia, misdiagnosis of BC, long distance to referral facilities, high cost of diagnostic services, long waiting time for diagnostic tests, and lack of screening and diagnostic tests in local facilities were identified as health-system-related barriers for late diagnosis of BC [14]. On the other hand, according to a systematic review and meta-analysis done in 2020, only 36.72% of women practice breast self-examination [15]. According to a study done at Tikur Anbessa Specialized Hospital in 2015, the treatment outcome of BC was mainly poor, so health education and sensitization on prevention were suggested [16]. The finding of a study done in the same area in 2016 indicates were BC, uterine cancer, colorectal cancer, uterine cancer, cervical cancer, esophageal cancer, osteosarcoma, squamous cell carcinoma were the leading cancer types among women aged 25–49 years [17].

The prevalence of BC is found to be increasing in Ethiopia as some studies indicate [12, 13]. However, women's awareness about the disease was low and there was also a problem of late diagnosis of the disease [14]. Late diagnosis of BC leads to poor treatment outcomes [16]. The findings of previous studies done on determinants of BC were inconsistent; and may vary from study to study. Therefore, this study aimed to identify common determinants of BC among Ethiopian women.


Methods

This study was conducted following preferred reporting items for systematic reviews and meta-analyses (PRISMA) guidelines.

PECOS framework

The population, exposure, comparisons, outcome, study design (PECOS) framework of the study is described in Table 1 below.

Table 1. Research question according to the PECOS framework.

Protocol registration

The protocol for this study was registered to the International Prospective Registry of Systematic Reviews (PROSPERO) with registration number CRD42023431578.

Search strategy and study selection

A comprehensive search of both published and unpublished primary studies was conducted using several databases (PubMed, Google Scholar, university research repository websites, Cochrane Library, Hinari, and Google). The search was done by combining various search phrases ((((((“Risk factor”[Title/Abstract]) OR (Determinant [Title/Abstract])) OR (“Associated factor”[Title/Abstract])) OR (“Modifiable factor”[Title/Abstract])) OR (Predictor [Title/Abstract])) AND ((“Breast cancer”[Title/Abstract]) OR (“Breast Neoplasms”[Mesh]))) AND (Ethiopia [Title/Abstract]).

Eligibility criteria

Primary observational studies done on associated factors of BC conducted at any time on women in Ethiopia and published in the English language and available online until 2 June 2023, were identified. The identified articles were first evaluated for their titles and abstracts. Then relevant studies were further evaluated by reading their full text. The quality of individual studies was assessed using the Newcastle-Ottawa scale (NOS) for case-control study [18], articles having a scale ≥7 were included in this meta-analysis (Table 2 and Figure 1).

Table 2. Risk of bias assessment.

Figure 1. PRISMA flow diagram of the included studies.

Exposures of interest

• History of ever breastfeeding (Yes versus No)

• Family history of cancer (Yes versus No)

• Age at menarche (<12 versus >15 years)

• Menopause status (post-menopause versus pre-menopause)

• Body mass index (≥25 versus <18.5 kg/m2)

Data extraction

Our review team prepared the data extraction form in Microsoft Excel before data extraction. Next, the necessary data from each included paper was extracted by both authors independently. The components of the data extraction formats include; the name of the first author, publication year, year of study, study design, study setting, study area, sample size, name of health facility (when institution-based), associated factors (or determinants), comparison group (reference group), adjusted odds ratio (AOR) with its lower level and upper level 95% confidence interval (CI) for the associated factors. In addition, when necessary data were not published together with the original studies, the corresponding author was requested to provide it.

Outcome

This study has one primary outcome; which was determinants of BC.

Statistical analysis and presenting findings

The extracted data were exported to STATA version 15.0 software for analysis. The pooled odds ratio was conducted using a random effect model. When the 95% CI of the pooled odds ratio did not include 1, the factors were considered to be significantly associated (Figure 2). The characteristics of individual studies and the syntheses were presented using tables, figures, and statements.


Results

Study selection

A total of 52 studies (35 from electronic databases and 17 other sources) were identified. After 29 duplicates were removed, 23 studies were screened for titles and abstracts. Eight studies were excluded since found to be irrelevant and 15 studies were assessed for full text. Nine studies were excluded after reviewing full texts, and six studies were evaluated against NOS quality. Finally, one study was excluded by quality score and five studies were included in the final analysis (Table 2).

Figure 2. Forest plot revealing determinants of BC in Ethiopia.

Characteristics of the included studies

All the included studies were conducted from 2013 to 2020 [1923]. The study design of all the studies was case-control, whose study area was Addis Ababa [1923]. In addition, all studies were institution based [1923]. The sample size of the studies ranges from 220 to 434, with varying control-to-case ratios among the included studies [1923]. All the included studies were those identified from different journals (published studies) (Table 3).

Synthesis of results

In the present study, five studies having 1,819 total participants (792 cases and 1,027 controls) were included. The significant determinants of BC were age at menarche <12 years (AOR = 3.36, 95% CI: 1.68–5.04), post-menopause (AOR = 2.37, 95% CI: 1.67–3.06), ever breastfeeding (AOR = 0.28, 95% CI: 0.15–0.42), and family history of cancer (AOR = 2.39, 95% CI: 1.29–3.44) (Figure 2).

Table 3. Characteristics of studies included studies.


Discussion

This study aimed to identify determinants of BC in Ethiopian women. Age at menarche <12 years, post menopause, not ever breastfeeding a baby, and having a family history of cancer increased the odds of developing BC.

Ever breastfeeding

It was identified that a history of ever breastfeeding decreased the odds of developing BC by 72% (AOR = 0.28, 95% CI: 0.15–0.42) which is supported by findings of previous meta-analyses done in other countries [25, 26]. Breastfeeding reduces BC risk biologically through lower levels of systemic estrogen and progesterone levels during breastfeeding and the excretion of estrogen and carcinogens from the breast ducts [21]. However, when breastfeeding stops, fatty tissue replaces the mammary gland, increasing the risk of BC [27].

For a variety of reasons, including working outside the home, employed Ethiopian women choose bottle feeding to breastfeeding [28]. Lack of workplace breastfeeding laws, arrangements, and support hinders mothers’ freedom to practice optimal breastfeeding, according to a 2021 study that compared breastfeeding in Ethiopia to the international standard [29]. Therefore, policymakers, the government, and other concerned bodies should pay close attention to the facilitation of arrangements to enable employed mothers to practice optimal breastfeeding upon return to work; strengthening breastfeeding has a dual benefit for mothers and their babies.

Age at menarche <12 years old

The finding of this study indicates that age at menarche of <12 years old increased the odds of developing BC by 3.36 times more likely as compared to age at menarche after 15 years (AOR = 3.36, 95% CI: 1.68–5.04). This is supported by a systematic review and meta-analysis done on case-control studies in Iran at different times [5, 30]. It is also supported by pooled analysis of 117 epidemiologic studies [2]. According to one theory, the association between early menarche and BC is caused by breast tissue being exposed to cyclic hormonal stimulation over longer periods [31]. Being exposed for a long time and/or to high levels of estrogen hormone has been linked to an increased risk of BC [32]. Although early menarche is a non-modifiable risk factor for BC, improving early screening, diagnosis, and breast self-examination for those women is possible to reduce the disease's progression. However, only 36.72% of women in Ethiopia Practice breast self-examination as identified by one systematic review and meta-analysis done in 2021 [15]. According to one study, one of the important factors for advanced-stage diagnosis of BC in Ethiopia is a lack of breast self-examination [33]. Therefore, increasing women’s and adolescents’ awareness about BC knowledge and encouraging breast self-examination is important.

Menopause status

Being in post-menopause was associated with 2.37 times higher odds of developing BC as compared to the pre-menopausal period (AOR = 2.37, 95% CI: 1.67–3.06). This finding is supported by findings of systematic review and meta-analysis done in southeast Asia [34]. However, according to a study done in Iran, there was no association between menopause status and BC [30]. The reason for the discrepancy might be socioeconomic and lifestyle differences. However, the finding of 117 epidemiological analyses of the Lancet report indicates that premenopausal women had a greater risk of BC than postmenopausal women of an identical age [35]. The possibility exists that post-menopause increased risk of BC in this study might be brought on by age-related factors [1, 36]. Therefore, improving post-menopausal women's health-seeking behavior enables early disease detection and timely treatment of BC for better treatment outcomes.

Family history of cancer

Having a family history of cancer was associated with 2.39 times higher odds of developing BC as compared to their counterpart (AOR = 2.39, 95% CI: 1.29–3.44); which is supported by findings of systematic review and meta-analysis done in southwest Asia and Iran [30, 34]. Therefore, women having a family history of cancer should be closely checked for their health status compared to other communities.

Body mass index

In the present study, the pooled analysis of odds ratios doesn’t show a significant association between body mass index and odds of developing BC. However, many meta-analyses indicate that there is an association [34]. The reason for the discrepancy might be due to a smaller study in Ethiopia investigating the association between BMI and the odds of BC. High body mass index and BC association is mainly due to obesity-related factors. Obesity raises the risk of BC because of fat tissue that creates an excess of estrogen; which is associated with an increased risk of BC [36, 37]. As a result, it has implications for lifestyle modification.


Limitations of the study

Even though this study brought recent evidence on determinants of BC in Ethiopian women it has some limitations. Even if many studies indicate oral contraceptive use [5, 25, 38], smoking [39], dietary fiber consumption [40, 41], physical exercise [25, 42], history of abortion [5], drinking alcohol [25], red meat consumption [25, 39], overweight or obesity [25], use of skin lighteners and hair relaxers [43], and a number of parity [34] were found to be associated with BC, the present study didn’t include these variables. This is because of a lack of studies carried out in Ethiopia on the association between the risk of getting BC and those variables. Therefore, further studies should be conducted in Ethiopia by incorporating the above-listed variables.


Conclusion

The significant determinants of BC in the study area are early menarche, family history of cancer, post-menopausal status, and not ever breastfeeding. Therefore, it is recommended that the Ministry of Health, regional health, zonal and district health departments, and other interested non-profit organizations should work cooperatively to reduce the risk of BC. In addition, the aforementioned factors should be targeted in addressing the problem of BC in Ethiopia by increasing community awareness, promoting breast self-examination, and developing programmes to increase women's knowledge to reduce the increasing burden of BC in Ethiopia.

Furthermore, we recommend that additional studies be conducted in the country to assess the association between BC and oral contraceptive use, obesity, smoking, alcohol consumption, red meat consumption, abortion, physical activity, and dietary fiber consumption, which have not yet been studied in Ethiopia, even if studies from other countries have shown an association.


List of abbreviations

BMI: body mass index; AOR: adjusted odds ratio; PECOS: population, exposure, comparisons, outcome, study design.


Conflicts of interest

The authors declare that they have no competing interests.


Funding

This work was not funded by any organization.


Author contributions

LKS was involved in conceptualizing, protocol registration process, searching, data extraction, formal analysis, and manuscript writing, and EEC was involved in searching, data extraction, formal analysis, and manuscript writing. All authors reviewed the manuscript.


Availability of data and materials

The dataset analyzed for this study's findings is available online (https://figshare.com/s/7ec253e86a75d5b4ffd3).


References

1. American Cancer Society (2020) Breast Cancer Facts & Figures 2019-2020 (Atlanta: American Cancer Society) pp 1–31

2. Center of for Disease Control and Prevention (CDC) (2023) What Is Breast Cancer? [Internet] p 1 [https://www.cdc.gov/cancer/breast/basic_info/what-is-breast-cancer.htm] Date accessed: 14/09/23

3. American Cancer Society (2022) Breast Cancer What is Breast Cancer? (Atlanta: American Cancer Society) [Internet] pp 1–19 [http://www.cancer.org/cancer/breast-cancer/about/what-is-breast-cancer.html]

4. Ngwa W, Addai BW, and Adewole I, et al (2022) Cancer in sub-Saharan Africa: a Lancet Oncology Commission Lancet Oncol [Internet] 23(6) e251–e312 [http://www.thelancet.com/article/S1470204521007208/fulltext] Date accessed: 31/05/23 https://doi.org/10.1016/S1470-2045(21)00720-8 PMID: 35550267 PMCID: 9393090

5. Khoramdad M, Dodaran MS, and Kabir A, et al (2022) Breast cancer risk factors in Iranian women: a systematic review and meta-analysis of matched case–control studies Eur J Med Res [Internet] 1–31

6. International Agency for Research on Cancer (IARC) (2021) Breast cancer awareness month 2021 [Internet] [https://www.iarc.who.int/featured-news/breast-cancer-awareness-month-2021/#:~:text=Breast cancer became the most commonly diagnosed cancer,fifth most common cause of cancer death overall] Date accessed: 14/09/23

7. IARC (2022) Cancer in sub-Saharan Africa: building local capacity for data production, analysis, and interpretation Int Agency Res Cancer [Internet] 2045(5) 1–2

8. Gbenonsi G, Boucham M, and Belrhiti Z, et al (2021) Health system factors that influence diagnostic and treatment intervals in women with breast cancer in sub-Saharan Africa: a systematic review BMC Public Health 21(1) 1–20 https://doi.org/10.1186/s12889-021-11296-5

9. Morgan GW, Foster K, and Huynh V, et al (2018) Improving health and cancer services in low-resource countries to attain the sustainable development goals target 3.4 for noncommunicable diseases J Glob Oncol 2018(4)

10. World Health Organization (WHO) (2014) Cancer – a growing public health concern for Ethiopia [Internet] [https://www.afro.who.int/news/cancer-growing-public-health-concern-ethiopia#:~:text=Cancer is an increasing public health burden for,four per cent of all deaths in Ethiopia] Date accessed: 14/09/23

11. World Health Organization (2020) Cancer Ethiopia 2020 Country Profile (Geneva: WHO) pp 2019–2020

12. Awedew AF, Asefa Z, and Belay WB (2022) National Burden and Trend of Cancer in Ethiopia, 2010 – 2019: a systemic analysis for Global burden of disease study Sci Rep [Internet] 12(1) 12736 https://doi.org/10.1038/s41598-022-17128-9 PMID: 35882895 PMCID: 9325704

13. Gebretsadik A, Bogale N, and Negera DG (2021) Epidemiological trends of breast cancer in Southern Ethiopia: a seven-year retrospective review SAGE 28 1–7

14. Getachew S, Tesfaw A, and Kaba M, et al (2020) Perceived barriers to early diagnosis of breast cancer in south and southwestern Ethiopia: a qualitative study BMC Womens Health 1–8

15. Gizachew Y, Id Y, and Kassa GM, et al (2021) Breast self-examination practice and its determinants among women in Ethiopia: a systematic review and meta-analysis PLoS One [Internet] 1–25

16. Dagne S, Abate SM, and Tigeneh W, et al (2019) Assessment of breast cancer treatment outcome at Tikur Anbessa Specialized Hospital Adult Eur J Oncol Pharm 0(February)

17. Woldu MA, Legese DA, and Abamecha FE, et al (2017) The prevalence of cancer and its associated risk factors among patients cancer science & therapy the prevalence of cancer and its associated risk factors among patients visiting oncology unit, Tikur Anbessa Specialized Hospital, Addis Ababa-Ethiopia J Cancer Sci Ther

18. Palmeri V, Colamesta V, and Torre LL (2016) OPE AC evaluation of methodological quality of studies Senses Sci [Internet] 3(3) 235–241 [www.sensesandsciences.com]

19. Tolessa L, Sendo EG, and Dinegde NG, et al (2021) Risk factors associated with breast cancer among women in Addis Ababa, Ethiopia: unmatched case–control study Int J Womens Health 13 101–110 https://doi.org/10.2147/IJWH.S292588 PMCID: 7822084

20. Hassen F, Enquselassie F, and Ali A, et al (2022) Association of risk factors and breast cancer among women treated at Tikur Anbessa Specialized Hospital, Addis Ababa, Ethiopia: a case-control study BMJ Open 12(9) 1–8 https://doi.org/10.1136/bmjopen-2021-060636

21. Duche H, Tsegay AT, and Tamirat KS (2021) Identifying risk factors of breast cancer among women attending selected hospitals of addis ababa city: Hospital-based unmatched case-control study Breast Cancer Targets Ther 13 189–197 https://doi.org/10.2147/BCTT.S293867

22. Letta G and Addissie A (2013) Magnitude of breast and cervical cancer and associated risk factors of breast cancer in Addis Ababa, Ethiopia, Masters Thesis, Addis Ababa University, Addis Ababa Addis Abeba Univ Res Repos

23. Mengesha H and Seme A (2015) Association of non breast feeding and breast cancer among patients on chemotherapy and radiotherapy at Tikur Anbessa Specialized Hospital: a case-control study, Masters Thesis, Addis Abeba University, Addis Ababa Addis Abeba Univ Res Repos

24. Hassen F, Enquselassie F, and Ali A, et al (2021) Socio-demographic and haematological determinants of breast cancer in a Tertiary Health Care and Teaching Hospital in Addis Ababa, Ethiopia Ethiop J Heal Dev 35(2) 1–8

25. Poorolajal J, Heidarimoghis F, and Karami M, et al (2021) Factors for the primary prevention of breast cancer: a meta-analysis of prospective cohort studies J Res Health Sci 21(3) https://doi.org/10.34172/jrhs.2021.57

26. Bernier MO, Bossard N, and Ayzac L, et al (2000) Breast feeding and risk of breast cancer: a meta-analysis of published studies Eur Soc Hum Reprod Embrol 6(4) 374–386

27. Stordal B (2023) Breastfeeding reduces the risk of breast cancer: a call for action in high-income countries with low rates of breastfeeding Cancer Med 12(4) 4616–4625 https://doi.org/10.1002/cam4.5288 PMCID: 9972148

28. Kebebe T and Assaye H (2017) Intention, magnitude and factors associated with bottle feeding among mothers of 0-23 months old children in Holeta town, Central Ethiopia: a cross sectional study BMC Nutr 3(1) 1–7 https://doi.org/10.1186/s40795-017-0174-y

29. Kebede EM and Seifu B (2021) Breastfeeding and employed mothers in Ethiopia: legal protection, arrangement, and support Int Breastfeed J 16(1) 10–13 https://doi.org/10.1186/s13006-021-00392-2

30. Shamshirian A, Heydari K, and Shams Z, et al (2020) Breast cancer risk factors in Iran: a systematic review & meta-analysis Horm Mol Biol Clin Investig 41(4) PMID: 33079703

31. Olsson HL and Olsson ML (2020) The menstrual cycle and risk of breast cancer: a review Front Oncol 10(January) 10–13 https://doi.org/10.3389/fonc.2020.00021

32. National Cancer Institute (2015) Cancer causes and prevention [Internet] [https://www.cancer.gov/about-cancer/causes-prevention/risk/hormones#:~:text=Studies have also shown that a woman’s risk,linked to an increased risk of breast cancer] Date accessed: 16/09/23

33. Tesfaw A, Tiruneh M, and Tamire T, et al (2021) Factors associated with advanced-stage diagnosis of breast cancer in north-west Ethiopia: a cross-sectional study Ecancermedicalscience 15 1–13 https://doi.org/10.3332/ecancer.2021.1214

34. Nindrea RD, Aryandono T, and Lazuardi L (2017) Breast cancer risk from modifiable and non-modifiable risk factors among women in Southeast Asia: a meta-analysis Asian Pac J Cancer Prev 18(12) 3201–3206 PMID: 29281867 PMCID: 5980871

35. Hamajima N, Hirose K, and Tajima K, et al (2012) Menarche, menopause, and breast cancer risk: individual participant meta-analysis, including 118 964 women with breast cancer from 117 epidemiological studies Lancet Oncol [Internet] 13(11) 1141–1151 https://doi.org/10.1016/S1470-2045(12)70425-4

36. Łukasiewicz S, Czeczelewski M, and Forma A, et al (2021) Breast cancer – epidemiology, risk factors, classification, prognostic markers, and current treatment strategies – an updated review MDPI Cancers 1–30

37. Liu XZ, Pedersen L, and Halberg N (2021) Cellular mechanisms linking cancers to obesity Cell Stress 5(5) 55–72 https://doi.org/10.15698/cst2021.05.248 PMID: 33987528 PMCID: 8090860

38. Rushton L and Jones DR (1992) Oral contraceptive use and breast cancer risk: a meta‐analysis of variations with age at diagnosis, parity and total duration of oral contraceptive use BJOG Int J Obstet Gynaecol 99(3) 239–246 https://doi.org/10.1111/j.1471-0528.1992.tb14506.x

39. Namiranian N, Moradi-Lakeh M, and Razavi-Ratki SK, et al (2014) Risk factors of breast cancer in the eastern mediterranean region: a systematic review and meta-analysis Asian Pacific J Cancer Prev 15(21) 9535–9541 https://doi.org/10.7314/APJCP.2014.15.21.9535

40. Farvid MS, Spence ND, and Holmes MD, et al (2020) Fiber consumption and breast cancer incidence: a systematic review and meta-analysis of prospective studies Cancer 126(13) 3061–3075 https://doi.org/10.1002/cncr.32816 PMID: 32249416

41. Chen S, Chen Y, and Ma S, et al (2016) Dietary fibre intake and risk of breast cancer: a systematic review and meta-analysis of epidemiological studies Oncotarget [Internet] 7(49) 80980–80989 [www.impactjournals.com/oncotarget/] https://doi.org/10.18632/oncotarget.13140 PMID: 27829237 PMCID: 5348370

42. Pizot C, Boniol M, and Mullie P, et al (2016) Physical activity, hormone replacement therapy and breast cancer risk: a meta-analysis of prospective studies Eur J Cancer 52 138–154 https://doi.org/10.1016/j.ejca.2015.10.063

43. Brinton LA, Figueroa JD, and Ansong D, et al (2018) Skin lighteners and hair relaxers as risk factors for breast cancer: results from the Ghana breast health study Carcinogenesis 39(4) 571–579 https://doi.org/10.1093/carcin/bgy002 PMID: 29324997 PMCID: 6248529

Related Articles

Natalia Camejo, Cecilia Castillo, Diego Santana, Lucia Argenzio, Dahiana Amarillo, Guadalupe Herrera, Maria Guerrina, Gabriel Krygier
Fernanda J Martin, Isabel M Saffie, Mabel A Hurtado, Diana Avila-Jaque, Rodrigo A Lagos, Carolina A Selman, Jonathan Z Huserman, Valentina A Castillo, Badir J Chahuán
Raja Pramanik, Sindhura Chitikela, SVS Deo, Ajay Gogia, Atul Batra, Akash Kumar, Ritu Gupta, Deepshi Thakral, Vedam L Ramprasad, Sandeep Mathur, DN Sharma, Aparna Sharma, Ashutosh Mishra, Babul Bansal
Dana Narvaez, Jorge Nadal, Adrian Nervo, Victoria Costanzo, Claudio Paletta, Fernando Petracci, Sergio Rivero, Alexis Ostinelli, Federico Coló, Loza Martín, Veronica Fabiano, Luciana Sabatini, Azul Perazzolo, Mora Amat, Matias Chacon, Federico Waisberg
Table of Contents
Table of Contents