Cancer Genetic Services in a Low- to Middle-Income Country: Cross-Sectional Survey Assessing Willingness to Undergo and Pay for Germline Genetic Testing

PURPOSE

Cancer genetic testing (CGT), a pathway to personalized medicine, is also being embraced in Nigeria. However, little is known about the influence of demographics and perceptions on individuals' willingness to access and pay for CGT. This study assessed patients' willingness to undergo CGT in southwest Nigeria as a catalyst for sustainable Cancer Risk Management Program.

METHODS

This was a cross-sectional study using semistructured questionnaire to interview 362 patients with cancer and 10 referred first-degree relatives between July 2018 and February 2020. Participants from three Nigerian teaching hospitals—University College Hospital, Ibadan, Lagos State University Teaching Hospital, Lagos, and Lagos University Teaching Hospital, Lagos, received genetic counseling and had subsequent CGT. Primary outcomes were willingness to undergo CGT in determining cancer risk and the willingness to pay for it. Ethical approval was from appropriate ethics committees of participating hospitals. Data were analyzed with SPSS version 22. Univariate comparison of categorical variables was performed by χ² test, multivariate analysis by logistic regression.

RESULTS

The participants from University College Hospital (56.2%), Lagos State University Teaching Hospital (26.3%), and Lagos University Teaching Hospital (17.5%) were mostly female (98.4%). Mean age was 48.8 years ± 11.79. Three hundred twenty-two (86.6%) patients and first-degree relatives were willing to take the test, of whom 231 (71.1%) were willing to pay for it. more than half (53.6%) of the participants were willing to pay between N10,000 and N30,000, which is less than $100 US dollars. Sociodemographic variables and willingness to test showed no association (P > .05). Education and ethnicity were found to be associated with their willingness to pay for CGT (P ≤ .05).

CONCLUSION

Learning clinically relevant details toward cancer prevention informs health-related decisions in patients and relatives, a motivator for willingness to pay for genetic testing in low- and middle-income countries. Increased awareness may influence outcomes of cancer risk management.

INTRODUCTION

Breast cancer has become the leading cancer affecting women globally, particularly in low-resource countries.^1,2 It is the most frequently diagnosed cancer in women, with 1.7 million new cases and 521,900 deaths in 2012 compared with 1.38 million new cases and 458,000 deaths in 2008,^3,4 representing 25% of all new cancer cases and 15% of all cancer deaths among females.^2,4,5

However, breast cancer outcomes had improved in many developed countries across the world in the past 2 decades, with incidence and mortality trends remaining relatively stable, even decreasing. On the contrary, these cannot be said about countries in Africa, Asia, Central America, and South America.^6-8 In Nigeria, breast cancer accounts for 34.2% of total cancer deaths⁹ and, like in other countries in sub-Saharan Africa, women present at younger age, with aggressive and advanced disease of very poor prognosis.¹⁰ Low- and middle-income countries account for more than 80% of breast cancer–related mortalities with inadequate awareness and low screening program in place.¹¹

In addition to proven methods of reducing the burden of breast cancer, genetic science has evolved and amassed massive knowledge of genes, genetic tests, and diagnostic tools for health care providers over the years.¹² Acceptance to test for genetic mutations is a behavior predictive of a giant step toward prevention.¹³ Although the use of genetic testing (GT) for screening of familial cancer risk has been available in global medical practice for over 20 years, such referrals are near to nonexistent in most developing countries. However, the recent findings from the largest case control studies in Nigeria, replicated in Cameroon and Uganda, showed that 15% of women with breast cancer carried a susceptibility allele for inherited breast cancer.^10,14 This provides the opportunity for leveraging on genetic-based precision prevention in developing countries. Unfortunately, access to genetic counseling is a limiting factor. Also, testing for genetic mutations comes with responsibilities on the part of the probands/consultands and relatives.¹⁵

In Nigeria, where basic initial genetic information is deficient, the prevalence of cancer as well as its genetic heritability continue unhindered in at-risk families because the patients and relatives do not have access to information on genetics and genetic counseling. Moreover, as promising as genetics and genetic counseling is, there is no evidence of integrated genetic counseling services in oncology care across Nigeria. Given that genetic approach to expanded carrier screening in health care setting is fairly new in most African settings, little is known about how individuals perceive its use and if they are willing to pay for the service at all.¹⁶ To bridge this knowledge gap, the authors developed nurse genetic counselors' curriculum for training in genetic risk assessment and provide counseling service to patients with breast cancer in three collaborating tertiary health institutions in Nigeria. Also, we developed a study on how demographics, knowledge, attitude, and practices may influence individuals' willingness to pay for cancer genetics,¹³ especially in the developing countries¹⁷ to test price point toward integrating genetic services in Nigeria.

Out-of-pocket cost implications on GT have been assessed in other parts of the world.¹⁸ Not much is known across the world, especially in an evolving genetic medicine environment like Nigeria. Even in developed and more experienced countries, cost has been established to be a barrier to effective uptake of health services in general and genetic services in particular.^19-23 Willingness to pay for cancer genetic testing (CGT) is therefore a significant step toward prevention as it encourages definite informed decision making on genetic cancer screening²⁴ since Nigerian health care users have to pay for many other services out of pocket. Generally, the Nigerian health care system has been described as not adequate in terms of accessibility, affordability, and sustainability of essential and special care services, which include oncology care.^25-27 Women do not have access to cancer screenings as they do in much developed countries because of an array of factors, which include financing and no perceived need.^1,28

This study aimed to provide an insight from Nigeria in determining factors associated with intention and willingness to have genetic counseling and testing among patients with breast cancer and relatives. As part of plan to establish a routine and sustainable care, the study, also ascertained the willingness of the patients to pay for CGT.

METHODS

This cross-sectional survey assessing willingness to undergo and pay for germline GT of patients with cancer is a component of an ongoing study piloting the mainstreaming of routine GT service into clinical practice in Nigeria. The recruitment started in July 2018 at University College Hospital, Ibadan, Nigeria, and in August 2018, it was extended to Lagos University Teaching Hospital and Lagos State University Teaching Hospital, both in Lagos. At the three participating tertiary health institutions, patients with selected cancers were informed of the availability of genetic counseling and testing (GCT) services at the clinics. Patients with breast, ovarian, endometrial, and prostate cancers including first-degree relatives (FDRs) irrespective of family history of any cancer, who were receiving genetic counseling for the first time, participated in the study. They received genetic counseling at enrollment, by professionally trained nurse-genetic counselor, and informed consent was obtained.

Although this is predominantly breast cancer study, other cancers bring different flavors to the study in respect to the specificity required in the provision of genetic counseling to cancers.

In-depth genetic counseling (GC) was provided followed by an anonymous interviewer administered survey. The GC contents include taking a personal and family history with pedigree drawing; determining cancer mutation risk, educating about genetics of hereditary breast cancer, GT methods, cost, and the meaning of the results; and discussing the benefits and risks of GT, confidentiality issues, and importance of sharing the testing results with family members. A semistructured questionnaire was, thereafter, administered on the participants. Ethical approval was obtained from the appropriate ethical committees of the teaching hospitals with the ethical approval numbers UI/EC/18/0251 and LREC/06/10/1225 from Ibadan and Lagos, respectively.

Sociodemographic data and family history of cancer were captured for each participant, including family history of cancer. Perception of causes of respondents' cancer was assessed by a response of yes/no to a list of causes. Willingness of respondents to discuss cancer risk with their relatives was evaluated with four items. Likely benefits and barriers to GT and testing service were explored. Willingness to pay out of pocket for GT was evaluated with three items, which followed the exploration of their willingness to undergo the test. Participants were asked to indicate how much they were willing to pay out of pocket for GT service. Amount in naira with five choices offered were influenced by current practice by commercial laboratories in the United States, United Kingdom, and South Africa at the time of study using an equivalence of about $500 US dollars (USD) cutoff as the threshold limit of payment. Readiness to discuss the result of GT with relatives and the specific relatives to discuss it with were explored.

Data were analyzed using SPSS version 22. Univariate comparison of all categorical variables was performed by χ² test and multivariate analysis. Expected outcomes include perceived causes of cancer, perceived benefits of GCT, willingness to discuss their cancer and genetic counseling and risk assessment with relatives, willingness to undergo GT, and pay for the test.

RESULTS

A total of 372 respondents participated in the study between July 2018 and February 2020. Most (97.3%) had at least one cancer, while the remaining 2.7% were FDRs with strong family history of cancer. Respondents from University College Hospital were 56.2%, while 26.3% and 17.5% were from Lagos State University Teaching Hospital and Lagos University Teaching Hospital, respectively. Mean age of respondents was 48.8 years ± 11.79 and most (98.4%) were female. The respondents were of diverse ethnicity, and educational qualification ranged from elementary to postgraduate, with a mean monthly income of N60,545.69 87 ± N87,611.91 (Table 1).

TABLE 1.

Sociodemographic Characteristics of Study Respondents

One fifth (20.7%) of the respondents reported positive family history of cancer, while there were a variety of perceived causes of the cancer by the respondents, of which stress (12.7%), heredity/family history (11.3%), unhealthy diet (9.7%), and previous history of breast cancer (9.7%) were top four, and more than a third (40.9%) could not attribute any reason for developing their cancer (Table 2). Respondents with cancer reported that they discussed their cancer with their siblings (72.0%) and all their children (64.2%). However, one fifth of the respondents discussed with both parents (20.4%), while 11.0%, 18.3%, and 45.2% of the respondents did not discuss their cancer at all with any of their close relatives (Table 3).

TABLE 2.

Respondents' Perceived Causes of Personal Cancer Risk

TABLE 3.

Discussion of Cancer With Respondents' Relatives

Of the 322 participants willing to test, 231 (71.1%) were willing to pay for the test (Fig 1). Slightly more than half (53.6%) of the respondents agreed to pay between N10,000 and N30,000, which is below $100 USD, while more than a third (34.6%) were willing to pay N5,000 or less, which is less than $15 USD, and only two (0.9%) were willing to pay up to N150,000, which is about $400 USD (Table 4). However, 91 (28.2%) of the respondents who were willing to test were not ready to pay for the test. Of these, 78 (85.7%) revealed their reason to be lack of fund. Some of them added that they even had no money for treatment, while seven (7.7%) insisted that the test should be free. Few other respondents (5.5%) provided no reason for not willing to pay for GT.

FIG 1.

Respondents’ willingness to undergo cancer genetic test and pay for the test. CGT, cancer genetic testing.

TABLE 4.

Respondents’ Disclosure of How Much They Are Willing to Pay for Genetic Testing

The findings showed that 322 (86.6%) patients and FDR were willing to undergo the test (Fig 1). Of the 10 respondents who were not willing to take the test, five (50.0%) declared that they do not want to know if they carry mutations or not, five (50.0%) stated that they do not want to be seen as bringing bad news to the family, while all the 10 (100.0%) submitted that they would be worried if they test positive.

Willingness to discuss cancer GT results with members of their family was explored among the respondents who were willing to test. Of the 319 (99.1%) who were willing to discuss the test results, top five relatives with whom they are willing to discuss their genetic test results were sisters in 239 (74.9%), daughters in 226 (70.8%), brothers in 198 (62.1%), sons in 197 (61.7%), spouses in 121 (37.9%), and mothers in 93 (29.2%; Table 5).

TABLE 5.

Respondents' Willingness to Discuss Genetic Test Result With Relatives

Benefits of cancer genetics and risk assessment in relatives were perceived by most patients (66.1%) to help with cancer prevention and 52.2% as early detection of cancer (Table 6), while most (65.9%) viewed cost as the major barrier to GT (Table 7).

TABLE 6.

Respondents' Perceived Benefits of Cancer Genetics and Risk Assessment

TABLE 7.

Perceived Barriers to Cancer Genetics and Risk Assessment

Bivariate analysis of the sociodemographic variables and willingness to test for genetic mutations showed no association between age, marital status of the respondents, their religion, ethnicity, educational status, and family history of cancer. However, an association was found between respondents' educational status, ethnicity, and their willingness to pay for genetic test. Other variables were not statistically significant in influencing the respondents' decision to pay for GT services (Table 8).

TABLE 8.

Association Between Sociodemographic Characteristics, Willingness to Have Genetic Testing, and Pay for the Test

DISCUSSION

This study has generated data and insight into the perceptions and acceptance of genetic counseling and testing in cancer care among patients with cancer in a subsect of Nigerian population. The data also revealed the influence of social, cultural, and economic premise of the awareness and perceptions of cancer genetics and hereditary predispositions in a resource-constraint setting.

Patients with cancer and first-degree relatives in the study were found to represent the major ethnic diversities of Nigeria, and a large proportion had at least a secondary school education, which made the interaction relatively easy. Nevertheless, despite the views of possible causes of individual cancer among the patients, not all could attribute their cancer to any cause.

The proportion of respondents who linked their cancer to familial risk was not substantial with the proportion of those with family history of cancer. Such views on the basis of knowledge and beliefs may have an implication for understanding the possible influence of genetics and its influence on prevention for others in their families. Also, there was a mention of spirituality as a cause of their cancer by a few respondents, which was a factor established in previous studies.^29,30 This reported low level of spiritual view of cancer causality may not be unrelated to the increased awareness about cancer in this setting, although late presentations still occur.³¹

Respondents indicate willingness to discuss their cancer diagnosis with their siblings and their children in their totality or part. This shows an illustration of general value of considering a patient or first-degree relative's interests as an individual encased in a cultural environment that has impression on his/her overall being.^32,33 Many of the respondents were not willing to disclose to their parents, which is not uncommon in patients with cancer as telling loved ones about their diagnosis has been adjudged to be one of the most difficult aspects of having cancer, which leads to delay in telling those they perceived to be vulnerable and concealed their emotions from relatives to protect them.^34,35 However, evidence has shown that talking about cancer helps people reorganize their thoughts and feelings and make sense of their experience³⁴ and may provide a specific-tailored support for them.³⁶

The results of willingness to test for genetic mutations among a large proportion (86.6%) of patients with cancer and FDR in this study show a significant factor toward acceptance of the test in this part of the world. Studies have found factors associated with increased acceptance and willingness, which includes risk perception and family experience^37,38 and good knowledge of genetics.³⁹ These factors, however, were not directly significant in deciding whether to have genetic test or not in this study. To encourage testing for the most at risk, women are currently advised to test for the BRCA1/2 gene mutation if a family member has tested positive for it, or if a close relative has been diagnosed with cancer.⁴⁰ The perceived benefits of genetic counseling and testing service for risk assessment were mostly favorable and this could be a contributory factor to their willingness to test for genetic mutations.

Most of the participants showed a readiness to discuss with at least a close member of the family, especially mothers, brothers, sisters, daughters, sons, and spouses. This becomes important for the uptake of GT⁴¹ and its role or implication in preventing and detecting cancer early as it is the responsibility of the proband, who is the first to be tested, to inform the relatives of the genetic test results.⁴² The postulation that male relatives are less likely to be informed of genetic test results⁴² is also seen in this study, and it has been documented that probands are more likely to share genetic test results with their children, female relatives, and relatives who they perceived had a favorable opinion about learning the results.^43-47

Therefore, supporting probands/consultands to communicate their test results and risk information with their relatives is key to obtaining the full benefits of genetic services.⁴⁸ Although there is a dearth of data about the reaction of relatives with whom genetic test results are shared, evidence has shown that open, positive family relationships increase the likelihood of disclosure of test results, while emotional distance, family conflict, and loss of contact decrease the likelihood of disclosure.^49-51

The study examined the willingness to pay for genetic test among the respondents and found that although such a test is relatively new in Nigeria, most of them were willing to pay out of pocket for it. This may not be unconnected with their perception of benefits of genetic test and this singular factor has been shown in other studies to positively influence willingness to pay for genetic tests.^13,18,48 The result did not find any association between age, marital status, level of education, monthly income, or family history of cancer and the respondents' willingness to pay for genetic test, contrary to a Canadian study in which these factors are impactful in the readiness to pay for the test.²⁴

The subject of how much money respondents were willing to pay also deserves committed attention. Half of the respondents were not ready to pay more than N30,000, that is, about $100 USD, which is way below $250 USD, the cost of the current test kit used in this study. These results suggest that individuals of medium socioeconomic status are willing to pay a moderate cost for GT as payments for most health services in Nigeria are out of pocket.⁴⁹ Interestingly, fewer respondents (2.2%) were more willing to pay between N100,000 and N150,000 ($270 USD-$400 USD) for GT out of pocket. Although this may mean a possibility for consideration of acceptability of GT among a few higher-income populations, cost was implicated by most respondents in this study to be the major barrier toward genetic counseling and testing services, as also found in previous studies.^50-53 This willingness recorded is very significant, considering the role of decreasing socioeconomic status in health care financing.⁵⁴

Perception of causes of cancer in probands as well as of benefits of genetic counseling and testing will awaken their interest and intention to test for deleterious mutations, which affects their care and prevention in their loved ones. Cost is a major factor in accessing genetic services and needs a holistic approach to overcome the challenges in the highly burdened health care systems of low- to middle-income countries like Nigeria and to reach the underserved populations. Culturally informed interventions and research are needed to support families in facilitating effective risk communication critical to the uptake of genetic services and the preventive impact.

In conclusion, with the recognition of the fact that 5%-10% of all cancers are hereditary, there is a growing need to improve access to GC and GT, before and after cancer diagnosis. This publication identifies opportunities to leverage on an insight from Nigeria in determining factors associated with intention to test and willingness to have genetic counseling and testing among patients with cancer and relatives. Willingness to pay for CGT identified could lead to a reform in health systems financing and exploration of other strategies for best practices in cancer care and control. The study has shown that probands have a pivotal role to play in communicating cancer risk information to family members, which promises to improve uptake of genetic services and the cancer control outlook.

AUTHOR CONTRIBUTIONS

Conception and design: Prisca O. Adejumo, Toyin I.G. Aniagwu, Olutosin A. Awolude, Babatunde Adedokun, Makayla Kochheiser Anthonia Sowunmi, Oladosu Ojengbede, Olufunmilayo I. Olopade

Financial support: Oladosu Ojengbede, Dezheng Huo, Olufunmilayo I. Olopade

Administrative support: Toyin I.G. Aniagwu, Olutosin A. Awolude, Makayla Kochheiser Anthonia Sowunmi, Olufunmilayo I. Olopade

Provision of study materials or patients: Olutosin A. Awolude, Abiodun Popoola, Oladosu Ojengbede

Collection and assembly of data: Prisca O. Adejumo, Toyin I.G. Aniagwu, Olutosin A. Awolude, Makayla Kochheiser Anthonia Sowunmi, Abiodun Popoola, Olufunmilayo I. Olopade

Data analysis and interpretation: Toyin I.G. Aniagwu, Olutosin A. Awolude, Babatunde Adedokun, Makayla Kochheiser Anthonia Sowunmi, Dezheng Huo, Olufunmilayo I. Olopade

Manuscript writing: All authors

Final approval of manuscript: All authors

Accountable for all aspects of the work: All authors

AUTHORS' DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

The following represents disclosure information provided by authors of this manuscript. All relationships are considered compensated unless otherwise noted. Relationships are self-held unless noted. I = Immediate Family Member, Inst = My Institution. Relationships may not relate to the subject matter of this manuscript. For more information about ASCO's conflict of interest policy, please refer to www.asco.org/rwc or ascopubs.org/go/authors/author-center.

Open Payments is a public database containing information reported by companies about payments made to US-licensed physicians (Open Payments).