Lessons learned, Summary, Challenges, and Recommendations.

In this final section, we summarize the different manuscripts included in his Supplement and outline the lessons learned. We also elaborate on the common educational challenges reported in the included articles and the possible recommendations for future global cancer education.

Experiential Learning in Career Development.

This manuscript demonstrates the learning experiences of graduate public health students through mentored field research in cancer epidemiology and cancer prevention over the past 13 years. The program has been funded through an R25 grant from the National Cancer Institute (NCI) since 2006 and has supported nearly 200 students from different universities in the USA. Included are data on student recruitment, selection, mentorship, and evaluation of research training in US minority settings as well as foreign countries. Examples of students' learning experiences and life-long skills that shaped students' careers are presented. The insights that fostered the experiential learning idea among key leaders at the NCI Cancer training branch have proven to be sound.

Developing and Maintaining a Global Research Training Infrastructure for Cancer Education.

This manuscript illustrates the 20-year process of establishing research sites that have been developed and maintained by the authors in collaboration with oncology colleagues at institutions in low- and middle-income countries. This infrastructure has been created for research training of US public health graduate students over the past 20 years for the Cancer Epidemiology Education in Special Populations (CEESP) Program funded by the US National Cancer Institute (R25 CA112383). We describe the history and resources that were utilized for developing and maintaining the research training infrastructure. We then define the elements needed for selecting and nurturing these global sites for education and research training of students. The elements include data and field resources, patient population, facilities for cancer management, laboratory resources, academic collaborators, and population parameters and cultural characteristics. These elements have also been essential in our US domestic training sites. We then emphasize the strengths and limitations of our global sites. Finally, we elaborate on our learning experience over the past 20 years. We believe that the material provided in this manuscript will serve as a useful toolkit for faculty, mentors, students, and trainees interested developing and/or utilizing research sites for cancer epidemiology and cancer prevention and control research training programs in global settings.

Global Aspects of the Cancer Epidemiology Education in Special Populations (CEESP) Program.

This manuscript provides a brief overview of the global aspects of the Cancer Epidemiology Education in Special Populations (CEESP) Program. The overview illustrates program history, aims, progress, evaluation, and dissemination. This manuscript sets the stage for the CEESP manuscripts included in this supplement that illustrate in the program infrastructure, mentoring, the student experiences, and unique features of students for achieving success. In this manuscript, we briefly outline some of the dissemination examples that resulted from utilizing the CEESP infrastructure, as outlined in some of the articles reporting on global research training sites from Egypt, Morocco, Oman, and Tanzania.

Using Key Informants to Evaluate Barriers to Education and Acceptability of the HPV Vaccine in Tanzania: Implications for Cancer Education.

Cervical cancer is the third most common cancer globally, with high mortality when left untreated. In sub-Saharan Africa, Tanzania shows higher incidence rates of cervical cancer at 59.1 per 100,000 compared with the global average of 13.1 per 100,000. The HPV vaccine has been shown to successfully reduce HPV infection and is recommended for school-age girls and boys in the USA. Understanding the acceptability of the HPV vaccine and the barriers to vaccination is important for ensuring that HPV vaccination programs are successful. In 2016, Tanzania began school-based HPV vaccination programs in cities and towns surrounding Dar es Salaam, the largest city in Tanzania. Successful implementation of HPV vaccination programs in Dar es Salaam relies on overcoming barriers to vaccination. This study focused on primary school teachers as key informants to assess these barriers. Participants were given a short survey and then asked to participate in focus group sessions. Overall, knowledge of HPV was low, with only 37% of participants having heard of the HPV and only 28.6% having heard of the HPV vaccine. Teachers had a very positive response to the HPV educational sessions. Of the teachers who completed the questionnaires, 100% of them were willing to speak with their school parents about the HPV vaccine and 99% would recommend this vaccine to parents. This study has significant implications for national cancer prevention vaccination programs, not only in Tanzania, but also in other countries starting HPV vaccination as teachers are potentially important advocates for immunization and other childhood health initiatives.

Mentoring in Global Cancer Research Training.

This manuscript illustrates general concepts of mentoring in low- and middle-income countries (LMICs). The focus of this manuscript is on public health research based on our experiences with the Cancer Epidemiology Education in Special Populations (CEESP) Program which is further illustrated in this Supplement. While the CEESP Program provides research training in global and US minority settings, this manuscript is focused on the global aspects of the program. We describe the process of selecting students into the CEESP Program, the process of mentoring them, and the preparation of the mentoring sites. We emphasize the review of the CEESP mentors in LMICs and put forward recommendations for enhancing their mentoring skills and disseminating the experience to other US and global institutions interested in global cancer education.

Needs for Cancer Education In Oman Based on the Breast Cancer Screening Program.

Most breast cancers in Oman are diagnosed at advanced stages and therefore early detection is important. The Oman Cancer Association (OCA) initiated a mobile mammography program in 2009, but no studies have evaluated its impact. This study aimed at estimating the proportion and predictors of OCA-screened women who had repeated mammography (adherence) and the sensitivity and specificity of the program. Demographic, screening, diagnosis, and treatment data of 13,079 women screened in the OCA mammography clinic from 2009 to 2016, and medical records of all breast cancer patients seen at Royal and Sultan Qaboos University hospitals during the same period were retrieved. Logistic regression analysis was conducted to identify predictors of adherence. A total of 8278 screened women over age 42 years (median age of 50 ± 8 years) were included in the study. Only 18% of initially negative screened women were compliant with recommended subsequent screening. Predictors of adherence included age (50-69 years), family history of cancer, family history of breast cancer, and breast self-examination. The overall cancer detection rate was 4.1/1000 screened women. Positive predictive value of screening was 4.7% with a sensitivity rate of 53% and specificity of 92%. This study showed a low mammography adherence among previously screened women. The study revealed low sensitivity, high specificity, and an acceptable cancer detection rate. Future programs should focus on improving data collection of screened women, maintaining the linkage of databases of screening and treatment clinics, and developing guidelines for breast cancer screening in Oman. The recommendations based on the study results should be incorporated into future professional, patient, and public cancer education programs.

Field Research Experience of Medical Students: Learning and Translation from Global to Underserved US Settings.

While most medical schools in the USA provide opportunities for global health experiences, global health education is not included consistently or emphasized adequately in many medical school curricula. The City University of New York Medical School (CSOM) has a mission to educate and train students who are traditionally underrepresented in medicine to practice primary care in medically underserved communities in New York. This manuscript documents the experience of the CSOM in expanding global health education by introducing a new global health cancer training program, partnering with clinicians at the Ocean Road Cancer Institute (ORCI) in Tanzania. This manuscript illustrates the following points: (1) the CSOM curriculum that focuses on community health and social medicine; (2) the process by which students learn by developing research proposals for global cancer; (3) the field research experience and lessons learned; (4) learning about cancer and medicine in a developing country; and (5) lessons learned for translation from global to domestic underserved populations. We also suggest a checklist for future students interested in pursuing global cancer education and research, and recommendations for maximizing learning and career development of students interested in global cancer research and its application to underserved populations in the USA.

Quantifying the under-estimation of cervical Cancer in remote regions of Tanzania.

BACKGROUND: Cervical cancer is the most common cancer among women in Sub-Saharan countries, including Tanzania. While early detection and diagnosis are available in some parts of this large country, radiotherapy has been only available at the Ocean Road Cancer Institute (ORCI), in the capital city of Dar es Salaam and is just starting in a few regions. METHODS: The objective of this study was to compare the observed incidence of cervical cancer for the two remote regions of Mwanza in western Tanzania and Mbeya in southern Tanzania, based on their patients treated at the ORCI from 2011 to 2014. RESULTS: The number patients referred and treated at ORCI were (120 from Mwanza, and 171 from Mbeya, representing 24.6 and 32.8% of the patients histopathologically confirmed in the two sites, respectively. The results showed significant underestimation of cervical cancer in the two regions. The vast majority of patients who were histopathologically-confirmed in their local regions (73.92% from Mwanza and 65.1% from Mbeya), but did not receive the needed radiotherapy treatment at the ORCI. The estimated incidence for the two regions based on the number of patients treated at the ORCI were underestimated by 53.9% for Mwanza and 68.9% for Mbeya. CONCLUSIONS: Local establishment of radiotherapy treatment facilities in remote regions in Tanzania and similar other low-income countries is essential for providing effective treatment and improving survival of diagnosed cervical cancer patients. Linkage between the records of local remote hospitals and the main cancer treatment center in the capital city can also help support the emerging the population-based cancer registry at ORCI.

Short- and Long-Term Outcomes of Student Field Research Experiences in Special Populations.

Global health education and training of biomedical students in international and minority health research is expending through U.S. academic institutions. This study addresses the short- and long-term outcomes of an NCI-funded R25 short-term summer field research training program. This program is designed for MPH and Ph.D. students in cancer epidemiology and related disciplines, in international and minority settings (special populations) in a recent 7-year period. Positive short-term outcome of 73 students was measured as publishing a manuscript from the field research data and having a job in special populations. Positive long-term outcome was measured as having a post-doc position, being in a doctoral program, and/or employment in special populations at least 3 years from finishing the program. Significant factors associated with both short- and long-term success included resourcefulness of the student and compatibility of personalities and interests between the student and the on-campus and off-campus mentors. Short-term-success of students who conducted international filed research was associated with visits of the on-campus mentor to the field site. Short-term success was also associated with extent of mentorship in the field site and with long-term success. Future studies should investigate how field research sites could enhance careers of students, appropriateness of the sites for specific training competencies, and how to maximize the learning experience of students in international and minority research sites.

Barriers to Cervical Cancer Screening in Burkina Faso: Needs for Patient and Professional Education.

Cervical cancer is among the leading causes of cancer deaths for women in low-income African countries, such as Burkina Faso. Given that cervical cancer is a preventable disease through early detection and vaccination, this study aimed at understanding the barriers to cervical cancer early detection in Ouagadougou, the capital city of Burkina Faso. Women seeking screening and treatment for cervical cancer (n = 351) during the period of May-August 2014, at the Yalgado Ouedraogo University Hospital, were interviewed about their knowledge, attitudes, and practices toward cervical cancer. Interview questions elicited information about sociodemographic of participants, history of screening, knowledge of cervical cancer, and attitudes toward cervical screening. Scores were assigned to responses of questions and knowledge, and tertitles of distributions were used for comparison. A multivariate logistic regression was performed to predict cervical screening. Study participants were relatively young (37.5 ± 10.7 years) and predominately resident of urban areas (83.8 %), and over half had no or less than high school education. Over 90 % of participants had heard about cervical cancer, and about 55 % of them had intermediate-level knowledge of the disease, its screening, and/or risk factors. Knowledge level was lower among rural than urban residents. Predictors of screening included higher level of education (odds ratio (OR) = 2.2; 95 % confidence interval (CI) 1.48-3.23), older age (OR = 1.1; 95 % CI 1.06-1.12), higher socioeconomic standard (SES) (OR = 1.5; 95 % CI 1-2.37), urban residence (OR = 2.0; 95 % CI 1.19-3.25), encouragement for screening by a health care worker (1.98; 95 % CI 1.06-3.69), and employment (OR = 1.9; 95 % CI 1.13-3.11). Low awareness and socioeconomic barriers lead to underutilization of screening services of women. Motivation and education by healthcare workers are important factors for increasing screening rates. Organized patient and professional education programs in gynecologic services are warranted for improving screening in Burkina Faso and other low-resource countries in Africa.

Observed and expected incidence of cervical cancer in lusaka and the southern and Western provinces of Zambia, 2007 to 2012.

OBJECTIVES: Cervical cancer is increasing but underestimated in developing countries. We calculated the observed and expected incidence of cervical cancer in Lusaka and Southern and Western provinces of Zambia. METHODS/MATERIALS: Data for 2007 to 2012 were obtained for the 3 provinces. Data included age, residence, year of diagnosis, marital status, occupation, human immunodeficiency virus (HIV), stage, radiotherapy, and chemotherapy. Expected incidence in Southern and Western provinces was calculated based on observed incidence for Lusaka province, adjusting for HIV. RESULTS: Crude and age-standardized incidence rates (ASRs) in Lusaka were 2 to 4 times higher than incidence in the other 2 provinces. Lusaka had a rate of 54.1 per 10(5) and ASR of 82.1 per 10(5) in the age group of 15 to 49 years. The Southern province had a rate of 17.1 per 10(5) and ASR of 25.5 per 10(5); the Western province had a rate of 12.3 per 10(5) and ASR rate of 17.2 per 10(5). The observed cervical cancer incidence rates in the Southern and Western provinces were lower than the rate in Lusaka, possibly because of the uncertainty of underreporting/underdiagnosis or actual lower risk for reasons yet unclear. The HIV seroprevalence rates in patients from the 3 provinces were 46% to 93% higher than seroprevalence in the respective general populations. CONCLUSIONS: Cervical cancer is significantly underestimated in Zambia, and HIV has a significant role in pathogenesis. Future studies should establish methods for case ascertainment and better utilization of hospital- and population-based registries in Zambia and other similar developing countries.

Most women diagnosed with cervical cancer by a visual screening program in Tanzania completed treatment: evidence from a retrospective cohort study.

BACKGROUND: Visual inspection with acetic acid (VIA) to identify and treat pre-cancerous lesions is effective for cervical cancer prevention. Screening programs also facilitate screening and diagnosis of invasive cancers that must be referred for radiation therapy or chemotherapy. This study compared characteristics of women diagnosed with invasive cervical cancer by a VIA screening program who did and did not follow up for treatment and who did and did not complete treatment at the Ocean Road Cancer Institute (ORCI), Dar es Salaam, Tanzania. METHODS: We conducted a retrospective cohort study of ORCI screening referrals from the period November 2002 to June 2011. Women referred for treatment of invasive disease (n = 980) were identified from an existing database of all women attending the screening clinic during this period (n = 20,131) and matched to a dataset of all cervical cancer patients attending ORCI in this period (n = 8,240). Treatment information was abstracted from patient records of women who followed up. Records of a random sample (n = 333) of unscreened patients were reviewed for disease stage. RESULTS: Of the 980 women referred women, 829 (84.6%) sought treatment. Most of those women (82.8%) completed their prescribed radiation. Lower disease stage, having a skilled occupation, residence in Dar es Salaam, and younger age were independently associated with loss to follow-up. Higher disease stage, residence in Dar es Salaam, older age, and later year of first treatment appointment were independently associated with incomplete treatment among those who followed up. Significantly more screened women had stage 1 disease (14.0%) than unscreened women (7.8%). CONCLUSIONS: Most women referred from the screening clinic completed treatment for their cancer at ORCI. Some of those lost to follow-up may have sought treatment elsewhere. In most cases, the screening clinic appears to facilitate diagnosis and treatment, rather than screening, for women with invasive cervical cancer.

The future of the cancer prevention workforce: why health literacy, advocacy, and stakeholder collaborations matter.

In considering the role of the cancer prevention workforce in meeting the nation's future health care needs, it is vital to address the considerable gaps in information, communication, training, professional development, roles, and levels of collaboration among diverse disciplines, stakeholders, and constituencies. As part of an October 2009 symposium at The University of Texas MD Anderson Cancer Center entitled "Future Directions in Cancer Prevention and Control: Workforce Implications for Training, Practice, and Policy," the Health Policy and Advocacy Working Group was convened to discuss barriers to closing these gaps. Three major themes emerged from the group's deliberations and are discussed here: (1) the role of critical health literacy and evidence-based collaborations in cancer prevention education, research, and practice; (2) the implications of health advocacy for policy development and clinical and public health practice; and (3) culturally and linguistically appropriate cancer prevention programs and information within advocacy/workforce collaborations. Mechanisms for addressing these gaps are presented.

Cancer prevention health services research: an emerging field.

In October 2009, The University of Texas MD Anderson Cancer Center hosted a symposium, "Future Directions in Cancer Prevention and Control: Workforce Implications for Training, Practice, and Policy." This article summarizes discussions and an Internet and literature review by the symposium's Health Services Infrastructure Working Group. We agree on the need for the recognition of Cancer Prevention Health Services Research (CP-HSR) as a unified research field. With advances in cancer screening and increased emphasis on preventive services under healthcare reform, there is a growing need for investigators with both cancer prevention and HSR expertise to consider the comparative effectiveness of cancer screening methods, the cost-effectiveness of early detection technologies, and the accessibility of preventive care for individuals at risk of cancer. Defining CP-HSR as a field will provide investigators with credibility and will serve to draw more researchers to the field. Increasing funding to train individuals in CP-HSR will be important to help meet the anticipated demand for investigators with this specialized multidisciplinary expertise.

Career development needs assessment in cancer prevention and control: focus on research in minority and international settings.

This study was conducted as a needs assessment to inform the development of an educational program designed to provide mentorship and skills supporting careers in cancer research, with a focus on domestic minority populations and international settings. The objectives were to determine: (1) the level of interest among trainees in careers in cancer research and (2) preferences and constraints constituted by potential components, features, and duration of the proposed extramural training program. The target populations were participants and directors of federal training programs in cancer research, specifically (1) trainees in the NCI-K01, K07, and K08 programs, as well as the Department of Defense (DoD) Breast and Prostate Control Programs and (2) PIs of NCI R25 training programs and federally designated Comprehensive Cancer Centers. We developed, piloted, and administered electronically a survey to elicit perspectives of trainees' career development needs and preferences. Response rates from each training group exceeded 65%, with the exception of the K08 trainees (49%). The proportion of cancer research trainees who are interested in careers that include research on US minority groups was 70% of K01 trainees, 72% of K07 trainees, 45% of K08 trainees, and 75% of DoD trainees. A substantial percent of these trainees indicated their plans also include cancer research in international settings: 60% of K01s; 50% of K07s, 42% of K08s, and 87% of DoD trainees. Trainees identified substantial interest in a program that would provide the following: mentoring, manuscript writing skills, collaborative research in special populations, financial support, and focused modular courses. This study offers encouraging evidence of interest which focused in extramural education to augment skills facilitating cancer-related research in special populations.

Genetic variations of the PI3K-AKT-mTOR pathway and clinical outcome in muscle invasive and metastatic bladder cancer patients.

The phosphoinositide-3 kinase (PI3K)-AKT- mammalian target of rapamycin (mTOR) pathway is an important cellular pathway controlling cell growth, tumorigenesis, cell invasion and drug response. We hypothesized that genetic variations in the PI3K-AKT-mTOR pathway may affect the survival in muscle invasive and metastatic bladder cancer (MiM-BC) patients. We conducted a follow-up study of 319 MiM-BC patients to systematically evaluate 289 single-nucleotide polymorphisms (SNPs) of 20 genes in the PI3K-AKT-mTOR pathway as predicators of survival. In multivariate Cox regression, AKT2 rs3730050, PIK3R1 rs10515074 and RAPTOR rs9906827 were significantly associated with survival. In combined analysis, we found a cumulative effect of these three SNPs on survival. With the increasing number of unfavorable genotypes, there was a significant trend of higher risk of death in multivariate Cox regression (P for trend <0.001) and shorter median survival time in Kaplan-Meier estimates (P log rank <0.001). This is the first study to evaluate the role of germ line genetic variations in the PI3K-AKT-mTOR pathway genes as predictors of MiM-BC clinical outcomes. These findings warrant further replication in independent populations and may provide information on disease management and development of target therapies.

Research training of students in minority and international settings: lessons learned from cancer epidemiology education in special populations.

This article describes the development and evaluation of an NCI-sponsored short-term summer cancer research education program. The study questions examined: the feasibility of conducting a cancer education program in special populations at multiple US and international field sites for masters students; the merit and worth that students and faculty attribute to the program; and students' scholarly and cancer-related career outcomes. Developing a new curriculum, increasing the pool of mentors, utilizing and increasing the number of field sites, and program dissemination were also evaluated. Evidence of the program's success included students' completion of field experiences at multiple sites and their subsequent 70% project-related publication rate, with 79% of trainees reporting themselves as likely to pursue future cancer-related careers. Evaluation-guided future plans for the program include implementing faculty development to further enhance the program outcomes.