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.

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.

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.

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.

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.

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.

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.

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.

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.

Changing Incidence of Uterine Cancer in Rural Egypt: Possible Impact of Nutritional and Epidemiologic Transitions.

PURPOSE: Uterine cancer is a top-ranking women's cancer worldwide, with wide incidence variations across countries and by rural and urban areas. Hormonal exposures and access to health care vary between rural and urban areas, globally. Egypt has an overall low incidence of uterine cancer but variable rural and urban lifestyles. Are there changes in the incidence of uterine cancer in rural and urban areas in middle-income countries such as Egypt? No previous studies have addressed this question from a well-characterized and validated population-based cancer registry resource in middle-income countries. The aim of this study was to explore the differences in clinical and demographic characteristics of uterine cancer over the period of 1999 to 2010 in rural and urban Gharbiah province, Egypt. METHODS: Data were abstracted for all 660 patients with uterine cancer included in the Gharbiah Population-based Cancer Registry. Clinical variables included tumor location, histopathologic diagnosis, stage, grade, and treatment. Demographic variables included age, rural or urban residence, parity, and occupation. Crude and age-adjusted incidence rates (IRs) and rate ratios by rural or urban residence were calculated. RESULTS: No significant differences were observed in most clinical and demographic characteristics between rural and urban patients. The age standardized IR (ASR) was 2.5 times higher in urban than in rural areas (6.9 and 2.8 per 100,000 in urban and rural areas, respectively). The rate ratio showed that the IR in urban areas was 2.46 times the rate in rural areas. CONCLUSION: This study showed that the disease IR in rural areas has increased in the past decade but is still low compared with the incidence in urban areas in Egypt, which did not show a significant increase in incidence. Nutritional transitions, obesity, and epidemiologic and lifestyle changes toward Westernization may have led to IRs increasing more in rural than in urban areas in Egypt. This pattern of increasing incidence in Egypt, which used to have a low incidence of uterine cancer, may appear in other middle-income countries that experience emerging nutritional and epidemiologic transitions. The rate of uterine cancer in urban areas in Gharbiah is almost similar to the corresponding rates globally. However, the rate in rural areas in this population has increased over the past decade but is still lower than the corresponding global rates. Future studies should examine the etiologic factors related to increasing rates in rural areas and quantify the improvement in rural case finding.

Changes in Uterine Cancer Incidence Rates in Egypt.

BACKGROUND: Uterine cancer is one of the top-ranking cancers in women with wide international variations in incidence rates. Developed countries have higher incidence rates than the developing countries. Egypt has significantly lower incidence of uterine cancer than other countries in the Middle East. This study aimed at verifying the incidence rate of uterine cancer and characterizing the demographic and clinical profiles of patients residing in the Gharbiah province in the Nile delta region of Egypt. METHODS: Data from 660 uterine cancer patients diagnosed during the period of 1999 to 2010 were abstracted from the Gharbiah Cancer Registry, the only population-based registry in Egypt. The data included age, marital status, number of children, residence, smoking, occupation, date and basis of diagnosis, tumor topography, morphology, stage and grade, and treatment. Crude rate, age-standardized rate (ASR), and age-specific rate were calculated and associated with demographic and clinical characteristics of patients. RESULTS: The study confirmed the low ASR of uterine cancer in Egypt, (4.1 per 100,000 (95% CI: 3.8-4.4)). The incidence rate increased significantly over the 12-year period. The crude rate (CR) was 1.95, 95% CI (1.64-2.25) in 1999-2002; 2.9, 95% CI (2.5-3.2) in 2003-2006; and 3.5, 95% CI (3.1-3.9) in 2007-2010. The rate ratio was 1.5, 95% CI (1.2-1.8) in 2003-2006 and 1.8, 95% CI (1.5-2.2) in 2007-2010 compared to 1999-2002. The majority of patients (83%) were postmenopausal with the highest age-specific rate in the 60-69-year age group (22.07 per 100,000 (95% CI: 19.3-25.2). The majority of patients were diagnosed at early stages (60% localized and 5% regional), had adenocarcinoma (68%), and resided in urban areas (54%). CONCLUSIONS: The study confirmed the low incidence rate of uterine cancer in the Gharbiah province of Egypt and significant increase in incidence in recent years. Future studies should focus on verifying the possible effect of hysterectomy on lowering the incidence, the factors related to the changes in rates between rural and urban areas, and the possible impact of nutritional and epidemiologic transitions on the increasing rates.

Clinical and epidemiologic variations of esophageal cancer in Tanzania.

AIM: To estimate the incidence of esophageal cancer (EC) in Kilimanjaro in comparison to other regions in Tanzania. METHODS: We also examined the clinical, epidemiologic, and geographic distribution of the 1332 EC patients diagnosed and/or treated at Ocean Road Cancer Institute (ORCI) during the period 2006-2013. Medical records were used to abstract patient information on age, sex, residence, smoking status, alcohol consumption, tumor site, histopathologic type of tumor, date and place of diagnosis, and type and date of treatment at ORCI. Regional variation of EC patients was investigated at the level of the 26 administrative regions of Tanzania. Total, age- and sex-specific incidence rates were calculated. RESULTS: Male patients 55 years and older had higher incidence of EC than female and younger patients. Of histopathologically-confirmed cases, squamous-cell carcinoma represented 90.9% of histopathologic types of tumors. The administrative regions in the central and eastern parts of Tanzania had higher incidence rates than western regions, specifically administrative regions of Kilimanjaro, Dar es Salaam, and Tanga had the highest rates. CONCLUSION: Further research should focus on investigating possible etiologic factors for EC in regions with high incidence in Tanzania.

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.

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.

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.

Trends in Breast Cancer Incidence Rates by Age and Stage at Diagnosis in Gharbiah, Egypt, over 10 Years (1999-2008).

Background. This study was undertaken to evaluate trends in breast cancer incidence in Egypt from 1999 to 2008 and to make projections for breast cancer occurrence for the years 2009-2015. Patients and Methods. We utilized joinpoint regression and average annual percent change (AAPC) measures with 95% confidence intervals (CI) to describe the trends in breast cancer incidence rates from the Gharbiah Cancer Registry by age and stage at diagnosis and to estimate expected breast cancer caseloads for 2009-2015. Results. From 1999 to 2008, the AAPC in breast cancer incidence rates in Gharbiah significantly increased among women 50 years and older and among localized tumors (AAPC %, 95% CI, 3.1% to 8.0%). Our results predict a significant increase in breast cancer caseloads from 2009 to 2015 among women aged 30-39 (AAPC %, 95% CI, 0.9% to 1.1%) and among women aged 40-49 years (AAPC %, 95% CI, 1.0% to 2.6%). Conclusion. These results have important implications for allocating limited resources, managing treatment needs, and exploring the consequences of prior interventions and/or changing risk factors in Egypt and other developing countries at the same stages of demographic and health transitions.

Characterizing inflammatory breast cancer among Arab Americans in the California, Detroit and New Jersey Surveillance, Epidemiology and End Results (SEER) registries (1988-2008).

INTRODUCTION: Inflammatory breast cancer (IBC) is characterized by an apparent geographical distribution in incidence, being more common in North Africa than other parts of the world. Despite the rapid growth of immigrants to the United States from Arab nations, little is known about disease patterns among Arab Americans because a racial category is rarely considered for this group. The aim of this study was to advance our understanding of the burden of IBC in Arab ethnic populations by describing the proportion of IBC among different racial groups, including Arab Americans from the Detroit, New Jersey and California Surveillance, Epidemiology and End Results (SEER) registries. METHODS: We utilized a validated Arab surname algorithm to identify women of Arab descent from the SEER registries. Differences in the proportion of IBC out of all breast cancer and IBC characteristics by race and menopausal status were evaluated using chi-square tests for categorical variables, t-tests and ANOVA tests for continuous variables, and log-rank tests for survival data. We modeled the association between race and IBC among all women with breast cancer using hierarchical logistic regression models, adjusting for individual and census tract-level variables. RESULTS: Statistically significant differences in the proportion of IBC out of all breast cancers by race were evident. In a hierarchical model, adjusting for age, estrogen and progesterone receptor, human epidermal growth receptor 2, registry and census-tract level education, Arab-Americans (OR=1.5, 95% CI=1.2,1.9), Hispanics (OR=1.2, 95% CI=1.1,1.3), Non-Hispanic Blacks (OR=1.3, 95% CI=1.2, 1.4), and American Indians/Alaskans (OR=1.9, 95% CI=1.1, 3.4) had increased odds of IBC, while Asians (OR=0.6, 95% CI=0.6, 0.7) had decreased odds of IBC as compared to Non-Hispanic Whites. CONCLUSIONS: IBC may be more common among certain minority groups, including Arab American women. Understanding the descriptive epidemiology of IBC by race may generate hypotheses about risk factors for this aggressive disease. Future research should focus on etiologic factors that may explain these differences.