Prostate Cancer Awareness Among Women: A Mixed-methods Systematic Review

Background: With the burden of prostate cancer, it has become imperative to exploit cost-effective ways to tackle this menace. Women have demonstrated their ability to recognize early cancer signs and it is therefore relevant to include women in strategies to improve the early detection of prostate cancer. This systematic review seeks to gather evidence from studies that investigated women’s knowledge about; (1) the signs and symptoms, (2) causes and risk factors, and (3) the screening modalities of prostate cancer. Findings from the review will better position women in the ght against the late detection of prostate cancer. Methods: The convergent segregated approach to the conduct of mixed-methods systematic reviews was employed. Five databases namely; MEDLINE (EBSCOhost), CINAHL (EBSCOhost), PsycINFO (EBSCOhost), Web of Science, and EMBASE (Ovid) were searched from January 1999 to December 2019 for studies conducted with a focus on the knowledge of women on the signs and symptoms; the causes and risk factors; and the screening modalities of prostate cancer. Results: Of 2201 titles and abstracts screened, 22 full-text papers were retrieved and reviewed, and 7 were included: 3 quantitative, 1 qualitative, and 3 mixed-methods studies. Both quantitative and qualitative ndings indicate that women have moderate knowledge of the signs and symptoms; and the causes and risk factors of prostate cancer. However, women recorded poor knowledge about prostate cancer screening modalities or tools. Conclusions: Moderate knowledge of women on the signs and symptoms, and the causes and risk factors of prostate cancer were associated with education. These ndings provide vital information for the prevention and control of prostate cancer and encourage policy-makers to incorporate health promotion and awareness campaigns in health policies to improve knowledge and awareness of prostate cancer globally. knowledge scores. 24% of prostate cancer asymptomatic; 65%, 67%, in passing urine, dysuria, and frequently pass urine symptoms. identifying tools applicable to prostate cancer screening. 5. 46%, 61%, and 38% of women respectively selected prostate-specic antigen (PSA), digital rectal examination (DRE), and x-ray as prostate cancer screening tools. health-seeking of and strong of a to this of were familiar with the the asymptomatic of early-stage fair urinary frequency, diculty in urinating, and dysuria from one of the qualitative indicate urinary frequency, diculty in urinating, glandular enlargement of the and erectile and of PCa


Background
Prostate cancer (PCa) is the most common non-skin cancer occurring in men and is accountable for 3.8% of all mortality caused by cancer in men (1,2). According to the GLOBOCAN, 2018 database, it is estimated that it is the fth primary cause of cancer death in men globally. It further reported that the highest mortality rate is found in the Caribbean and Southern African men worldwide (1,3). A recent study by Yeboah-Asiamah et al. reported that PCa was the second most common cancer in areas such as Australia, the United States, and New Zealand (4). Though fewer than 30% of all incidence of PCa are from developing countries, these countries have previously been estimated to have the highest mortality from PCa due to late diagnosis (5,6). Although sub-Saharan Africa (SSA) has a low rate of the disease, the incidence is projected to increase if screening is encouraged (7). Hence, PCa remains a vital public health concern in both developed and developing countries.
The Centers for Disease Control and Prevention (CDC) in North America, organized a workshop with the motive to explore strategies to control and prevent the disease based on the increasing incidence and mortality rate of PCa (8). To address mortality rates related to the disease, participants recommended strategies to improve PCa awareness (8). Also, as documented by many studies, PCa incidence is a direct re ection of the rate at which high-risk groups screen for the disease (4,9). In Europe, early screening was attributed to a 20% reduction in PCa mortality rate (10). Although there is evidence suggesting a reduction in PCa mortality due to early screening, a United States (US) study did not highlight a reduction in mortality (11). The prostate-speci c antigen (PSA) test and the digital rectal examination (DRE) are useful screening tools, although initial controversies were surrounding the use of these tools (12). Because of overlap in PSA levels in men with prostatitis, benign prostatic hyperplasia, and PCa, it was assumed that PCa cannot be screened using the PSA test (13). Catalona et al. demonstrated that PSA could be utilized as a screening tool for PCa and it has widely been adopted (14). DRE is the only procedure whereby physicians can examine part of the prostate gland (15). The ndings are only based on the physician impression, hence poor inter-rater reliability and also a limitation to the palpable region of the prostate gland (15). However, DRE sometimes detects PCa in men with PSA, 4.0 ng/mL (16). Regardless of the controversial nature of screening and the potential for early screening to reduce mortality, studies support the need to encourage screening (4,12).
Women have essential characteristics that make them better managers of family health as compared to men. Therefore, it is not surprising that there is evidence positioning women as individuals who make adequate observations about the health of their partners (9,17). In promoting the early detection of PCa, women have been documented to observe the slightest symptoms presented by their partners and push them to seek medical attention (9,18). In a study conducted by Blanchard et al., it was recommended that efforts must be made to actively involve women in improving the timely detection of PCa through the closure of knowledge-gaps (19).
Also, men admit seeking out their wives' opinions as sources of health information (20). In the context of the early detection of PCa, women can play various roles such as information seekers, advocates, health advisors, and support persons (21). Therefore, there is the need to gather current evidence about women's knowledge of PCa as the ndings will be vital in equipping women to contribute towards the early detection of the disease.
In light of the availability of limited evidence addressing the awareness of women on prostate cancer, this review will seek to combine quantitative and qualitative data to increase the validity of ndings through data triangulation as recommended by Caruth and supported by Lizarondo et al. (22,23). Thus, this review seeks to map out current evidence regarding women's awareness of PCa under the scopes of; 1) signs and symptoms, 2) risk factors and causes, and 3) screening guidelines.

Methodology
The Joanna Briggs Institute (JBI) reviewer's manual for the conduct of mixed-methods critical appraisal and synthesis formed the backbone of the study (23). With guidance from the JBI manual, a protocol was developed to guide the review process according to the convergent segregated approach (23

Inclusion criteria
We considered studies that were published in English and peer-reviewed journals between January 1999 and December 2019. Included studies were selected from primary research of any methodology; and explored awareness on signs and symptoms, causes and risk factors, and screening of prostate cancer. Studies that were conducted among women regardless of the geographical location were included. Studies that were mainly conducted in men were excluded in addition to studies not published in the English language.

Information sources and search strategy
An initial explorative search in PubMed founded search terms in preparation for comprehensive electronic search. The selected search terms were combined with Boolean operators for a comprehensive electronic search in MEDLINE (EBSCOhost), CINAHL (EBSCOhost), PsycINFO (EBSCOhost), Web of Science, and EMBASE (Ovid) as "(prostate cancer ) AND (awareness OR knowledge) AND (signs OR symptoms) AND (risk factors OR causes) AND (screening) AND (women)". The search strategy (Appendix 1), so developed, was utilized by the rst (EW) and second (KBM) reviewers to independently conduct a literature search as outlined in the review protocol (24).

Selection of studies
The rst and second reviewers, being guided by the developed review protocol, singularly screened and compared the titles and abstracts of the literature search outcomes to a developed standard (Appendix 2). Studies that successfully passed the initial stage of screening were subjected to the independent full-text reading by EW and KBM before consideration for data extraction. Lastly, hand-searching and snowballing on references of selected articles were done to nd eligible studies in the grey area. There were no disagreements between EW and KBM. Hence, the third reviewer (ABBM) assessed the studies before data extraction was conducted by the lead author according to the JBI data extraction tools outlined in the review protocol (24). The characteristic of studies that successfully went through the data extraction, the key ndings that were extracted, and a summary of the study selection process are detailed respectively (Table 1, Table 2, and Fig. 1).  1. Generally, the knowledge score of women on the symptoms of prostate cancer was appreciable. 2. Women who knew about the existence of prostate cancer in their families had higher knowledge scores. 3. 24% of women responded prostate cancer is asymptomatic; whilst 65%, 67%, and 63% respectively noted the di culty in passing urine, dysuria, and the need to frequently pass urine as symptoms. 4. Women found it di cult in identifying tools applicable to prostate cancer screening. 5. 46%, 61%, and 38% of women respectively selected prostate-speci c antigen (PSA), digital rectal examination (DRE), and x-ray as prostate cancer screening tools.  4. Most women did not know the location of the prostate gland in addition to the available screening tools. Nevertheless, the PSA was mentioned. 5. Some women perceived colonoscopy as a prostate cancer screening tool. 6. Risk factors that attracted much attention from women included; poor diet (high red meat and fatty food consumption) and inadequate physical activity. 7. Other risk factors that did not attract much attention included; increased age (where age greater or equal to 45 years was tagged the highest risk), stressful lifestyle, family history of the disease, being of African decency, poor screening habit, cigarette smoking and poor access to quality healthcare. 8. Women erroneously perceived a man's sexuality and regularity of sexual intercourse as risk factors. 1. 100 women each from 7 countries were involved in the study. 2. 28% of female respondents spontaneously included prostate cancer in their list of available cancers whilst 69%, who didn't initially list prostate cancer, agreed to the existence of the disease when asked a closed-ended question. 3. Women in the United Kingdom (40%), United States (20%), France (23%), Germany (24%), Italy (21%), Spain (26%), and Sweden (39%) were spontaneously aware of prostate cancer. When prompted, additional respective 58%, 76%, 70%, 75%, 76%, 69% and 61% of women recognized the existence of prostate cancer. 4. Women in Spain (36%), the United States (35%), Italy (23%), Sweden (22%), the United Kingdom (17%), France (17%), and Germany (9%) recognized PSA as a prostate cancer screening tool. 5. 20% of women in the United States, 14% in France, 8% in Spain, 6% in the United Kingdom, 6% in Germany, 5% in Italy, and 2% in Sweden recognized DRE as a prostate cancer screening tool. 6. Mistakenly, 37% of women in Spain, 22% in Italy, 17% in France, 13% in the United Kingdom, 10% in Germany, 11% in Sweden, and 5% in the United States recognized the use of urine as a prostate cancer screening sample. 7. The inability of women to recognize at least a prostate cancer screening tool followed the trend: Germany (71%), Sweden (60%), the United Kingdom (56%), the United States (53%), France (52%), Italy (44%) and Spain (41%).

Quality assessment
As described in the review protocol (24), the methodological quality assessment tool (Appendix 3) was adopted and modi ed for this review (25). The tool appraised the studies' quality based on the studies sample representativeness, response rate, reliability, and validity of the data collection tool. The tool was modi ed to suit the results from the included studies. A score was calculated, and the quality of the studies was classi ed as weak (0-33.9%), moderate (34-66.9%), or strong (67-100%). Eligible records were subjected to independent quality assessment by EW and KBM. Methodological quality outcomes were not grounds for exclusion.

Synthesis and integration of ndings
The review ndings were subjected to the convergent segregated approach to synthesis and integration according to the developed review protocol (24). A narrative synthesis was separately performed for qualitative and quantitative ndings. The results were nally integrated.

Results
Conducting the review, according to the developed protocol, yielded 2200 studies results. A detailed citation screening led to an additional study, which increased the total studies to 2201. Regarding the summary of the study selection process (Fig. 1), 1672 studies were obtained after 529 duplicates were removed from the pool of data. Post-titles and abstracts review excluded 1650 studies leaving 22 studies. The 22 studies were further reduced to 7 after a full-text reading resulted in the exclusion of 15 studies.

Characteristics of included studies
The data extracted from the seven (7) studies are detailed ( Table 1). The publication years ranged from 2003 to 2018 with 5 studies having been conducted in the United States. One of the studies was a multicenter study that involved multinationals (26). The study with the highest female participants (4040 women) was conducted in Spain (27). Webb et al. recruited the lowest sample size, 14 women (28). A total of 5634 women were involved in the 7 studies. Two studies were solely conducted in women, three included other diseases, and two did not disclose study duration.

Quality of included studies
According to the scoring scheme of the quality assessment tool (Appendix 3), two studies (27,28) were evaluated as moderate-quality whilst ve studies were evaluated as strong quality. None of the studies were excluded based on methodological quality assessment outcomes. There was no disagreement between EW and KBM.

Review ndings
Study ndings, presented in Table 2, were heterogeneous. Quantitative studies indicate that women knew about the existence of PCa. In exploring qualitative evidence, women exhibited knowledge of PCa. Therefore, both arms of the review are supportive of each other.
Women had moderate knowledge about the signs and symptoms of PCa drawing from quantitative ndings. The asymptomatic nature of early staged PCa; and women moderately knew urinary symptoms such as urinary frequency, di culty in urinating, and dysuria. Qualitative studies indicate that women were aware of signs and symptoms such as urinary frequency, di culty in urinating, glandular enlargement of the prostate, and erectile dysfunction. Hence, quantitative and qualitative ndings revealed that women moderately knew the urinary symptoms of PCa.
Quantitative studies indicate an average score of women on knowledge of risk factors of PCa. Risk factors women knew were increasing age, presence of a rst-degree relative, being genetically linked to Africa, and excessive truncal obesity. Qualitative evidence recognized all risk factors documented by the quantitative ndings except truncal obesity. Also, identi ed risk factors included poor diet, inadequate exercise, stressful lifestyle, poor screening habits, cigarette smoking, and poor access to quality healthcare. Women wrongly reported sexual orientation and frequent sexual activity as risk factors. Therefore, qualitative ndings con rm the quantitative claim that women have shared knowledge about the risk factors of PCa.
Quantitative studies indicate that women had poor knowledge about PCa screening. Although it was reported that women knew about PSA and DRE, knowledge scores were signi cantly low. Also, women poorly recognized urine as a screening sample, PSA as an exclusive diagnostic tool, and failed to identify more than one screening tool. Qualitative studies respectively reported PSA and blood as a screening tool and sample. Colonoscopy was wrongly reported as a PCa screening tool. Conclusively, both arms of the review reported women knew about PSA and had poor knowledge about PCa screening.

Discussion
The heterogeneity of the study ndings warranted the synthesis as a narrative (23,29). The convergent segregated approach was employed according to the recommendation of the JBI reviewer's manual (23).
Generally, from the quantitative evidence, women knew about prostate cancer (19,26,30,31). The knowledge of women was found to have increased with educational and nancial status (19); and disease familiarity (19,31). The awareness of women about the existence of PCa increased when the disease was mentioned compared to an initial request for women to list cancers (26). Qualitative evidence showed that women were aware of PCa (18,30). They appreciated and speci cally requested for PCa education partly because they could not tell the location of the prostate gland (18). Thus, quantitative and qualitative evidence indicates that women know about PCa. Women's awareness could be due to their role in family health management and the possible health-seeking behavior of educated and nancially strong women. As persons are faced with the experiences of a health condition, they will seek to make sense of this illness by acquiring knowledge (32), experiences, and beliefs; hence this theory might explain the improved awareness of women who were familiar with the disease.
Most of the quantitative studies indicate that women are aware of the asymptomatic nature of early-stage PCa (19,30,31). Symptoms that women had a fair knowledge about included urinary frequency, di culty in urinating, and dysuria (31). Findings from one of the qualitative studies indicate that women fairly recognized urinary frequency, di culty in urinating, glandular enlargement of the prostate, and erectile dysfunction as signs and symptoms of PCa (18). Being familiar with the disease may explain the awareness of women of the urinary symptoms associated with PCa.
According to Okoro and colleagues' quantitative study, although knowledge of PCa was not adequate, women knew associated risk factors such as being a rst-degree relative, being a man of African descent, and excessive truncal obesity (30). Blanchard et al. also documented women's recognition of increasing age as a PCa risk factor (19). One of the qualitative studies indicates women knew increasing age could increase a man's chance for PCa development (18,28). Other causes and risk factors women identi ed included poor diet, inadequate exercise, stressful lifestyle, family history of the disease, being of African descent, poor screening habits, cigarette smoking, and poor access to quality healthcare (18). Erroneously, one study reported that women perceived sexual orientation and frequent sexual activity as risk factors (18). Both quantitative and qualitative ndings documented women knew increasing age, family history, and African descent as PCa risk factors.
Quantitatively, women's responses to queries about PCa screening was poor (26,31). Some women were unable to recognize at least a PCa screening tool whilst others mistakenly recognized urine as a suitable sample for PCa screening (26). According to Okoro et al. the majority of women exclusively tagged PSA elevation as a basis for PCa diagnosis (30). This, therefore, calls for extensive education because benign prostatic hyperplasia, prostatitis, and PCa usually present with elevated PSA (13). Evidence from qualitative ndings indicated women knew physical examination must augment blood analysis (28). Also, women mentioned PSA and colonoscopy as screening tools (18). The results from included qualitative studies con rmed that women had poor knowledge about PCa screening. The mention of colonoscopy as a screening tool further supports a lack of adequate knowledge about PCa screening.
This critical appraisal and synthesis revealed over the 20 years of study search, only four studies out of the seven included studies investigated all the outcomes of interest. Two studies did not investigate women's awareness of the signs and symptoms (27,28) and the causes and risk factors (27, 31) of PCa. Therefore, although quantitative and qualitative ndings were supportive of each other, studies investigating the causes and risk factors, as well as the signs and symptoms of PCa, were lacking.

Recommendations For Practice
From the review ndings, it is recommended that PCa control programs should also focus on educating women. Clinicians and public health practitioners should include women in prostate cancer health promotion. Women should be encouraged to attend PCa clinics with their male signi cant others suffering from the disease and the effect of this strategy in reducing PCa mortality rate investigated.

Recommendations For Research
Further studies are recommended to investigate the knowledge of women living in low and middle-income countries (LMIC) about PCa. Such studies should focus extensively on the knowledge of women on PCa screening. Also, it is recommended for research to develop and pilot a PCa educational intervention model, applicable to women to reduce the burden of the disease. This tool should be cultural-speci c for easy acceptance and recognition. Also, current evidence on the willingness of women to offer social support to men with PCa should be investigated.

Study Limitations
The various restrictions that were imposed on the literature search included a search range from January 1999 to December 2019, a search into only 5 databases, and the outright exclusion of non-English publications.
Other limitations were the exclusion of studies conducted in women who received education on prostate cancer, healthcare professionals, healthcare students, and college/university students, and further exclusion of studies that involved (LGBTQ) participants.

Declarations
Ethics approval and consent to participate Ethical permission was not required since the study did not involve the enrollment of humans or animals as study subjects.

Consent for publication
None.

Availability of Data and Materials
Data and other pieces information are available at; https://doi.org/10.17605/OSF.IO/BR456

Competing Interests
None.

Funding
None.

Authors' Contributions
EW is credited with the conception of the review, the coordination of the systematic review, the development of the search strategy, the search and selection of studies to be included in the review, the extraction and management of quantitative and qualitative data, the assessment of methodological quality, the ltering of all reference materials, the integration and interpretation of the data, the drafting of the manuscript and is the principal reviewer. KBM is credited with the conception of the review, the review of the search strategy, the search and selection of studies to be included in the review, the extraction and management of quantitative and qualitative data, the assessment of methodological quality, the integration and interpretation of the data and the review of the manuscript. ABBM is credited with the review of the search strategy, the assessment of the studies before data extraction, and the review of the manuscript. VB is credited with the review of the manuscript, the coordination of the systematic review, and the co-supervisor of the review. FO is credited with the conception of the review, the review of the manuscript, and the overall supervision of the review. All authors have reviewed and accepted the nal manuscript of the review for publication.