Mammogram history in Nigerian women : Age-related risk factors for breast cancer and educational implications

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Background
Breast cancer accounts for 25% of diagnosed cancers and 20% of cancer-related mortality amongst women in sub-Saharan Africa. 1 Data from the International Agency for Research on Cancer suggest about 100 000 breast cancer cases are diagnosed annually in the African region, with the largest number of country-specific cases diagnosed in Nigeria (circa 14 000) yearly. 2 While the breast cancer incidence and mortality rates remain highest in fully industrialised nations, rates are rapidly increasing in developing countries.Thus, there is a dire need to detect cancer early, when it is more responsive to treatment. 3Mammography is a breast imaging method that employs low-dose x-rays to detect cancer early, thereby reducing the incidence of advanced cancers with poor prognosis. 3Mammography screening in Nigeria is offered to women aged from 40 to 70 years, 4 although women under 40 years may also be invited for mammograms if they have a strong family history of breast cancer. 5The efficacy of mammography in younger women is debatable (because of higher breast density). 6Nevertheless, missing a mammogram can significantly increase the likelihood of being diagnosed with cancer at a later stage. 7ckground: Breast cancer accounts for 25% of diagnosed cancers and 20% of cancer-related mortality in women from sub-Saharan Africa.Given the early onset of breast cancer in African women, there is a need to better understand how age-related risk factors contribute to mammography uptake in this population.
Aim: To identify age-related risk factors for breast cancer associated with previous uptake of mammograms in asymptomatic Nigerian women and consider implications for health education campaigns.
Method: Participants comprised 544 asymptomatic Nigerian women (aged 28-75 years) responding to breast cancer public awareness campaigns, by presenting for baseline or screening mammography at a local hospital.Information about mammography history and age-related risk factors (menarche, menopausal and chronological age) were obtained by interviewing the participants face-to-face, before proceeding with mammography.Hierarchical logistic regression was used to estimate the odds of previous mammograms based on the age-related risk factors.

Results:
The likelihood of previous mammography screening increased by a factor of 1.07 (95% confidence interval [CI]: 1.00-1.14)for every year older chronologically and decreased by a factor of 1.12 (95% CI: 1.24-1.01)for every year older at menarche.Age at menarche partly mediated the relationship between chronological age and mammography history (effect = -0.01,95% CI: -0.01, -0.00).Women with a history of breast cancer were 6.11 times more likely to have previously undertaken mammography screening (95% CI: 2.49-14.97).Age at menopause and age at first confinement were unrelated to mammography history.

Conclusions:
Nigerian women may recognise the need for mammograms because of adverse age-related risk factors for breast cancer, notably menarche and chronological age.However, awareness of menopausal age as a risk factor and basis for mammography screening may be deficient.It is therefore recommended that public awareness campaigns should emphasise the importance of older menopausal age in breast cancer risk and as a basis for requesting mammograms.

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Age-related risk factors
Several age-related risk factors for breast cancer have been identified. 8Therefore, these factors must be considered in health education initiatives to improve breast cancer awareness. 9Breast cancer patients from sub-Saharan Africa are often of a younger chronological age, with an average age of onset of 35-49 years, 10 compared to around 71 years in European women. 11The majority of breast cancer cases diagnosed in Africa occur in women aged ≤ 50 years. 12esearch also suggests age at menarche is critical in Nigerian women with younger age at first menstruation being associated with elevated breast cancer risk. 8,13Finally, age at menopause has also been implicated in breast cancer risk, with older age at menopause being associated with greater risk. 14Given the early onset of breast cancer in African women, there is a need to better understand the link between age-related risk factors and mammography uptake in this population.

Educaional challenges
The importance of education about breast cancer risk in Nigeria is underscored by the low levels of breast cancer awareness in this region, 15 even amongst health professionals, including medical doctors, nurses and radiographers. 16,17,18One study found only 38.2% of doctors and 18.9% of nurses knew that increasing age was a risk factor for breast cancer. 16Thus, Nigerian health workers may fail to offer mammography screening to women with negative age-related risk factors.Furthermore, Nigerian women may delay or decline mammograms partly because of knowledge deficits on breast cancer, 19 including age-related risk factors. 20Even amongst women who are more knowledgeable about breast cancer (e.g.those with higher education or professional jobs), 20 psychological theories of aging would suggest an age-related aversion to risk information may discourage utilisation of diagnostic medical services that may confirm the presence of a life-threatening illness. 21As many Nigerians view cancer as a spiritual ailment, older age may increase preference for traditional healers, who may present a more positive outlook for the future, through spiritual incantations and local herb preparations. 22ereas health promotion initiatives in many Western countries target women over 50 for breast cancer screening, 23 most sub-Saharan African countries lack a formal nation-wide breast cancer-screening programme. 22Thus, many women have little or no education about the importance of age-related risk factors in mammography screening. 15Nigerian women are disinclined to use medical services (e.g.visit a hospital) for menopause-related problems: one study found only 25.4% of women sought medical assistance because of menopause. 24hus, it is possible that older age at menopause may fail to encourage mammography, particularly given the low levels of cancer awareness. 20Evidence on menarche age and use of medical services by Nigerian women seems non-existent. 22hus, it is unclear whether women who are currently eligible for breast cancer screening will be motivated to undergo a mammogram as a result of having experienced menarche at a younger age in their youth.

The present study
Ages at menarche and menopause are particularly critical milestones in a woman's lifespan and linked to adverse biomedical (and psychosocial) outcomes. 25Menopausal age is the final stage in ovarian aging, while age at first menstruation marks the beginning of the female reproductive cycle. 26Women may seek or be offered mammography because of adverse age-related risk factors.However, these scenarios assume an adequate level of education about age-related risk factors for breast cancer, in both women and health professionals.Given the low level of breast cancer education in sub-Saharan Africa, 15,16,20 including knowledge of risk factors, 15,16 this study had two aims.The first objective was to determine whether women with adverse age-related risk factors for breast cancer are more likely to have a history of mammography screening.The second objective was to identify specific areas where education about age-related risk factors and importance of mammograms needs to be improved.

Methodology Sample
The cohort comprised 544 asymptomatic women (aged 28-75 years) presenting for screening mammography at the Shell-Iyienu Mission hospital breast cancer-screening programme in Anambra State, Nigeria, between January 2014 and December 2016.The programme accepts women aged 40 years and above for screening mammography, as well as women aged between 25 and 39 years with a positive history of breast cancer in the family.Although mammography screening in Nigeria targets women aged between 40 and 70 years, women under 40 years may be invited for a mammogram if they have a strong family history of breast cancer. 5

Mammography history and age-related risk factors
Past medical and family histories were obtained by interviewing the participants face-to-face and entering the information into a data form, before proceeding with mammography.After taking her clinical history, each woman underwent a physical breast examination, both carried out by trained registered nurse, followed by the mammography procedure.
Any women unable to provide definite responses to questions during the face-to-face interview were excluded from this study.

Data analysis
We used hierarchical logistic regression models to estimate the odds ratios ([ORs], 95% confidence intervals  2. To shed more light on possible direct and indirect associations involving age-related risk factors, we assessed the extent to which the association between chronological age and mammography screening was mediated by menarche or menopausal age. 25The analysis was performed using the PROCESS macro dialogue Statistical Package for the Social Sciences (SPSS) bootstrapping protocol. 27,28This generates unstandardised regression or path coefficients.We specified the generation of 1000 bootstrap samples, with a biascorrected CI method. 27,28For both predictor and mediator variables, 95% Ordinary Least Squares (OLS)-Maximum Likelihood (ML) Estimation CIs were specified.The conservative 'normal theory' (i.e.Sobel) test was used to establish the significance of any mediator effects. 29,30Statistical significance was based on α = 0.05.SPSS version 23 (IBM Corporation, Armonk, New York, USA), incorporating the PROCESS macro dialogue, 27 was used for data analysis.

Ethical consideraions
This work received approval from Liverpool John Moores University Research Ethics Committee (UREC) -Ethics Approval Reference 17/NSP/042.were less likely to have a palpable lump ( p < 0.001), more likely to have a history of breast cancer ( p < 0.001) and more likely to have had a previous biopsy ( p < 0.01).There was no group difference in familial risk, including having a first-degree relative with breast cancer.Women with a mammography history were more likely to be older than median menopausal age for the sample ( p < 0.001).These women were also chronologically older, but younger at menarche ( p < 0.05).There were no group differences in age at first confinement, age at menopause and height or weight data.

Mediator efect
Figure 1 illustrates the association between menarche age and mammography history in women who are currently eligible to screen (i.e.aged over 40, or aged 25 to 39 with a family history).The figure shows that women with a history of mammography screening were more likely to have had menarche at a younger age in their youth, notably at < 11 years (11.5% vs. 7.9%) and at 12 years (25% vs. 17%).We decided to exclude menopausal age from bootstrapping assessing mediator effects because of a large proportion of missing data (> 53 percentage of participants did not indicate their age at menopause).Bootstrapping using menarche age revealed a significant mediator effect, whereby age at first menstruation partly 'explained' the association between chronological age and mammography history (ab = −0.01,BCa CI: −0.01, −0.00). 28This mediator effect was significant based on the conservative 'normal' theory (i.e.Sobel) test (z = −2.04,p = 0.042). 30This mediator effect is illustrated in Figure 2. The figure shows that older women in general were more likely to have had a previous mammogram.However, this association was complicated by menarche age, in the sense that those older women who in their youth experienced menarche at an older age were less likely to have a prior history of mammography.Older age at menarche is associated with a lower risk of breast cancer, 8 which might make mammography screening seem unnecessary to some chronologically older women who are eligible for mammography screening.

Discussion
The data show that certain age-related risk factors are implicated in previous mammography uptake in Nigerian women.It suggests health education initiatives to promote breast cancer awareness and the need for early detection may be having some success in encouraging mammograms for breast screening in asymptomatic women who have age-related risk factors for breast cancer.The data are

Educaional implicaions for chronological age
Chronologically older women were more likely to undergo mammograms.This is consistent with evidence from Western populations. 23Nevertheless, it is important for health education programmes to emphasise that breast cancer tends to be diagnosed at a young age amongst Nigerian women (aged below 50 years), 12 albeit the efficacy of mammography screening in younger women is questionable (because of greater breast density).Although knowledge of breast cancer risk factors in Nigerian women is low, and this has been implicated in low levels of mammography uptake, 15 the positive relationship between chronological age and mammography history suggests older women were motivated to seek mammograms as a result of awareness of age-related risk factors. 19The public awareness jingles used by health workers seemed particularly helpful in this context.Even women younger than 50 years should be specifically targeted by such health promotion campaigns, given the lower age of breast cancer onset in Nigerian women. 12Lower uptake of mammography amongst younger women may contribute to the high proportion of advanced (stage III or IV) breast cancer cases reported in Nigeria (the highest in Africa), 10 because breast pathology may remain undetected for years.

Educaional implicaions for age at menarche
Previous studies suggest younger age of menarche is associated with elevated breast cancer risk in Nigerian women. 13The present findings indicate menarche age also relates to mammography history, with previous mammograms more likely in women of a younger menarche age.Again, this arguably depicts efforts by health providers to increase breast cancer awareness or deliberate efforts by the women themselves to seek mammography (given their elevated risk) in response to the health promotion jingles.Previous studies show low or modest knowledge of risk factors for breast cancer in Nigerian women, 15,19,20 which in turn is blamed for low levels of mammography uptake. 15Although the present findings suggest women of younger menarche age were motivated to request mammograms, presumably in response to the public awareness jingles, it is still necessary for health campaigns to address the patriarchal aspects of Nigerian society, where women are less able to take the initiative for their own health care. 22The mediating effect of menarche age reinforces the need to educate older women who are eligible for screening about the importance of obtaining a mammogram even if they feel their risk of breast cancer is lower because of being older at menarche in their youth. 31

Educaional implicaions for menopausal age
The lack of association between menopausal age and mammography history is worrying 9 and may highlight a knowledge deficit about breast cancer risk in Nigerian women. 20It perhaps indicates the need for public awareness jingles that explicitly emphasise the importance of menopausal age in breast cancer risk. 24Evidence suggests women who seek mammograms tend to be individuals with a family history of breast cancer, women with a history of breast pathologies or those who had already experienced clinical breast examination. 15Thus, educational initiatives should encourage women to seek mammography based on older menopausal age.This is particularly critical given that use of medical services for menopause-related problems is low amongst Nigerian women. 24Hence, awareness of a link between older menopausal age and breast cancer seems unlikely to motivate women to visit a hospital for mammography, unless more educational resources are committed to bridge the gap between knowledge and behaviour. 15Factors such as poverty, limited access to health services and reliance on traditional healers may present further challenges, diminishing likelihood of mammography.

Limitaions
The cross-sectional design negates conclusive inferences about possible directions of causality.The sample is also biased.Much of the Shell-Iyienu Mission breast cancerscreening programme is subsidised, making it affordable to many women within the catchment area.However, some women in the locality are unable to afford fees to participate in the programme, thus limiting the sample size.The study population would have been much larger had the programme been cost free.The sample comprised women within southeastern Nigeria, and hence may not necessarily reflect the country as a whole.

Conclusions
In summary, the present study associates certain age-related risk factors (age at menarche and chronological age) for breast cancer with a history of mammography uptake in Nigerian women.This link may partly denote the effect of a public awareness jingle to improve knowledge of breast cancer in Nigerian women.Women may have been motivated to request mammograms because of age-related concerns, notwithstanding previous research suggesting knowledge of risk factors for breast cancer is low amongst Nigerian women.The lack of an association between menopausal age and mammography history is a concern and may partly reflect cultural taboos and sensitivities.Research shows that Nigerian women are disinclined to use medical services for health problems related to menopause.Thus, it is essential for health education programmes in Nigeria to increase awareness of age-related risk factors for breast cancer, notably older age at menopause, and commit more resources to ensure this knowledge translates into higher mammography uptake.

Table 1
shows descriptive data for the entire sample, and respondents with and those without prior mammography history.Only 52 women (9.6%) had a previous history of mammography screening.About 13% of respondents had a palpable lump and previous history of breast cancer.Just under 1 in 10 had a previous biopsy, and 4.4% had a positive family history of breast cancer (with around 4% having a first-degree relative with breast cancer).The average chronological age of the sample was just under 50 years, while the mean age at first confinement was around 23 years.Average age at menarche was just over 13 years, while the mean age at menopause was about 47 years.The average height and weight were 2.16 metres and 82.14 kg, respectively.

Sample Previous history of mammography No previous history of mammography P Mean ± SD Mean ± SD Mean ± SD
Independent t-tests were used to compare women with and without a mammography history on age-related risk factors, and also height and weight.Chi-square was used to compare groups on family history and the other nominal (i.e.categorical) variables.SD, Standard deviaion. Note:
Note: Independent t-tests were used to compare women with and without a mammography history on age-related risk factors, and also height and weight.Chi-square was used to compare groups on family history and the other nominal (i.e.categorical) variables.SD, Standard deviaion.

TABLE 2 :
Results of hierarchical logisic regression predicing mammography history from age-related risk factors and family history.