Go 21 00140
Go 21 00140
Go 21 00140
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 6
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 as-
sociation (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.
JCO Global Oncol 9:e2100140. © 2023 by American Society of Clinical Oncology
Licensed under the Creative Commons Attribution 4.0 License
1
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Adejumo et al
medical practice for over 20 years, such referrals are near METHODS
to nonexistent in most developing countries. However, the This cross-sectional survey assessing willingness to undergo
recent findings from the largest case control studies in and pay for germline GT of patients with cancer is a com-
Nigeria, replicated in Cameroon and Uganda, showed that ponent of an ongoing study piloting the mainstreaming of
15% of women with breast cancer carried a susceptibility routine GT service into clinical practice in Nigeria. The re-
allele for inherited breast cancer.10,14 This provides the cruitment started in July 2018 at University College Hospital,
opportunity for leveraging on genetic-based precision Ibadan, Nigeria, and in August 2018, it was extended to
prevention in developing countries. Unfortunately, ac- Lagos University Teaching Hospital and Lagos State Uni-
cess to genetic counseling is a limiting factor. Also, versity Teaching Hospital, both in Lagos. At the three par-
testing for genetic mutations comes with responsibilities ticipating tertiary health institutions, patients with selected
on the part of the probands/consultands and relatives.15 cancers were informed of the availability of genetic coun-
In Nigeria, where basic initial genetic information is deficient, seling and testing (GCT) services at the clinics. Patients with
the prevalence of cancer as well as its genetic heritability breast, ovarian, endometrial, and prostate cancers including
continue unhindered in at-risk families because the patients first-degree relatives (FDRs) irrespective of family history of
and relatives do not have access to information on genetics any cancer, who were receiving genetic counseling for the
and genetic counseling. Moreover, as promising as genetics first time, participated in the study. They received genetic
and genetic counseling is, there is no evidence of integrated counseling at enrollment, by professionally trained nurse-
genetic counseling services in oncology care across Nigeria. genetic counselor, and informed consent was obtained.
Given that genetic approach to expanded carrier screening
Although this is predominantly breast cancer study, other
in health care setting is fairly new in most African settings,
cancers bring different flavors to the study in respect to the
little is known about how individuals perceive its use and if
specificity required in the provision of genetic counseling to
they are willing to pay for the service at all.16 To bridge this
cancers.
knowledge gap, the authors developed nurse genetic
counselors’ curriculum for training in genetic risk assess- In-depth genetic counseling (GC) was provided followed by an
ment and provide counseling service to patients with breast anonymous interviewer administered survey. The GC contents
cancer in three collaborating tertiary health institutions in include taking a personal and family history with pedigree
Nigeria. Also, we developed a study on how demographics, drawing; determining cancer mutation risk, educating about
knowledge, attitude, and practices may influence individ- genetics of hereditary breast cancer, GT methods, cost, and
uals’ willingness to pay for cancer genetics,13 especially in the meaning of the results; and discussing the benefits and
the developing countries17 to test price point toward inte- risks of GT, confidentiality issues, and importance of sharing
grating genetic services in Nigeria. the testing results with family members. A semistructured
questionnaire was, thereafter, administered on the partici-
Out-of-pocket cost implications on GT have been assessed
pants. Ethical approval was obtained from the appropriate
in other parts of the world.18 Not much is known across the
ethical committees of the teaching hospitals with the ethical
world, especially in an evolving genetic medicine envi-
approval numbers UI/EC/18/0251 and LREC/06/10/1225
ronment like Nigeria. Even in developed and more expe-
from Ibadan and Lagos, respectively.
rienced countries, cost has been established to be a barrier
to effective uptake of health services in general and genetic Sociodemographic data and family history of cancer were
services in particular.19-23 Willingness to pay for cancer captured for each participant, including family history of
genetic testing (CGT) is therefore a significant step toward cancer. Perception of causes of respondents’ cancer was
prevention as it encourages definite informed decision assessed by a response of yes/no to a list of causes. Will-
making on genetic cancer screening24 since Nigerian ingness of respondents to discuss cancer risk with their rel-
health care users have to pay for many other services out of atives was evaluated with four items. Likely benefits and
pocket. Generally, the Nigerian health care system has barriers to GT and testing service were explored. Willingness to
been described as not adequate in terms of accessibility, pay out of pocket for GT was evaluated with three items, which
affordability, and sustainability of essential and special care followed the exploration of their willingness to undergo the test.
services, which include oncology care.25-27 Women do not Participants were asked to indicate how much they were
have access to cancer screenings as they do in much willing to pay out of pocket for GT service. Amount in naira with
developed countries because of an array of factors, which five choices offered were influenced by current practice by
include financing and no perceived need.1,28 commercial laboratories in the United States, United Kingdom,
and South Africa at the time of study using an equivalence of
This study aimed to provide an insight from Nigeria in
about $500 US dollars (USD) cutoff as the threshold limit of
determining factors associated with intention and willing-
payment. Readiness to discuss the result of GT with relatives
ness to have genetic counseling and testing among patients
and the specific relatives to discuss it with were explored.
with breast cancer and relatives. As part of plan to establish
a routine and sustainable care, the study, also ascertained Data were analyzed using SPSS version 22. Univariate
the willingness of the patients to pay for CGT. comparison of all categorical variables was performed by χ2
TABLE 1. Sociodemographic Characteristics of Study Respondents TABLE 1. Sociodemographic Characteristics of Study Respondents
Characteristic No. (%) (Continued)
Age, years Characteristic No. (%)
TABLE 3. Discussion of Cancer With Respondents’ Relatives more than a third (40.9%) could not attribute any reason for
Discussion of Cancer With Relatives No. (%) developing their cancer (Table 2). Respondents with cancer
Discussed with siblings reported that they discussed their cancer with their siblings
Yes, all of the siblings 268 (72.0) (72.0%) and all their children (64.2%). However, one fifth of
the respondents discussed with both parents (20.4%), while
Yes, some of the siblings 50 (13.4)
11.0%, 18.3%, and 45.2% of the respondents did not discuss
No, not all 41 (11.0)
their cancer at all with any of their close relatives (Table 3).
Not applicablea 13 (3.5)
Of the 322 participants willing to test, 231 (71.1%) were
Discussed with children
willing to pay for the test (Fig 1). Slightly more than half
Yes, all of the children 239 (64.2) (53.6%) of the respondents agreed to pay between N10,000
Yes, some of the children 20 (5.4) and N30,000, which is below $100 USD, while more than a
No, not all 68 (18.3) third (34.6%) were willing to pay N5,000 or less, which is less
Not applicable a
45 (12.1) 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
Discussed with parents
(28.2%) of the respondents who were willing to test were not
Yes, both parents 76 (20.4)
ready to pay for the test. Of these, 78 (85.7%) revealed their
Yes, one of the parents 71 (19.1) reason to be lack of fund. Some of them added that they even
No, not all 168 (45.2) had no money for treatment, while seven (7.7%) insisted that
Not applicablea 57 (15.3) the test should be free. Few other respondents (5.5%)
Discussed with other relatives provided no reason for not willing to pay for GT.
Yes, all of the other relatives 159 (42.7) The findings showed that 322 (86.6%) patients and FDR
No, not all 141 (37.9) were willing to undergo the test (Fig 1). Of the 10 respon-
dents who were not willing to take the test, five (50.0%)
Not applicablea 72 (19.4)
declared that they do not want to know if they carry
a
Includes first-degree relatives and those who have no sibling, mutations or not, five (50.0%) stated that they do not want
children, and both parents. to be seen as bringing bad news to the family, while all the
10 (100.0%) submitted that they would be worried if they
(98.4%) were female. The respondents were of diverse test positive.
ethnicity, and educational qualification ranged from ele-
Willingness to discuss cancer GT results with members of
mentary to postgraduate, with a mean monthly income of
their family was explored among the respondents who were
N60,545.69 87 6 N87,611.91 (Table 1).
willing to test. Of the 319 (99.1%) who were willing to
One fifth (20.7%) of the respondents reported positive family discuss the test results, top five relatives with whom they are
history of cancer, while there were a variety of perceived causes willing to discuss their genetic test results were sisters in
of the cancer by the respondents, of which stress (12.7%), 239 (74.9%), daughters in 226 (70.8%), brothers in 198
heredity/family history (11.3%), unhealthy diet (9.7%), and (62.1%), sons in 197 (61.7%), spouses in 121 (37.9%),
previous history of breast cancer (9.7%) were top four, and and mothers in 93 (29.2%; Table 5).
100
86%
90 Yes
No
80 72% No response
Respondents (%)
70
60
50
FIG 1. Respondents’ will- 40
ingness to undergo cancer 28%
30
genetic test and pay for
the test. CGT, cancer ge- 20
11%
netic testing. 10
3%
0
Willingness Willingness
to Undergo to Pay for
CGT CGT
TABLE 4. Respondents’ Disclosure of How Much They Are Willing to TABLE 6. Respondents’ Perceived Benefits of Cancer Genetics and
Pay for Genetic Testing Risk Assessment
How Much Respondents Are Willing to Pay n = 231, No. (%) Perceived Barriers No. (%)
N10,000-N30,000 124 (53.6) Motivates self-examination 180 (48.4)
N40,000-N60,000 7 (3.0) Helps family and children 157 (42.2)
N70,000-N90,000 8 (3.5) Reduces concern about cancer 177 (47.2)
N100,000-N120,000 3 (1.3) Reduces uncertainty 148 (39.8)
N130,000-N150,000 2 (0.9) Provides sense of control 147 (39.5)
Other (≤ N5,000) 85 (36.8) Helps plan for the future 170 (45.7)
Not willing to disclose 2 (0.9) Helps make important life decisions 156 (41.9)
Helps with cancer prevention 246 (66.1)
Early cancer detection 194 (52.2)
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 DISCUSSION
(Table 6), while most (65.9%) viewed cost as the major This study has generated data and insight into the per-
barrier to GT (Table 7). ceptions and acceptance of genetic counseling and testing
Bivariate analysis of the sociodemographic variables and in cancer care among patients with cancer in a subsect of
willingness to test for genetic mutations showed no asso- Nigerian population. The data also revealed the influence of
ciation between age, marital status of the respondents, their social, cultural, and economic premise of the awareness
religion, ethnicity, educational status, and family history of and perceptions of cancer genetics and hereditary pre-
cancer. However, an association was found between re- dispositions in a resource-constraint setting.
spondents’ educational status, ethnicity, and their will- Patients with cancer and first-degree relatives in the study
ingness to pay for genetic test. Other variables were not were found to represent the major ethnic diversities of
statistically significant in influencing the respondents’ de- Nigeria, and a large proportion had at least a secondary
cision to pay for GT services (Table 8). 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.
TABLE 5. Respondents’ Willingness to Discuss Genetic Test Result
With Relatives The proportion of respondents who linked their cancer to
Willingness to Discuss With Relatives No. (%) familial risk was not substantial with the proportion of those
Willing to discuss genetic test result with with family history of cancer. Such views on the basis of
relatives (n = 322)
TABLE 7. Perceived Barriers to Cancer Genetics and Risk Assessment
Yes 319 (99.1)
Perceived Barriers No. (%)
No 3 (0.9)
Cost 245 (65.9)
Which relative would you like to discuss
the test result with? n = 319 Access to the testing center 171 (46.0)
TABLE 8. Association Between Sociodemographic Characteristics, Willingness to Have Genetic Testing, and Pay for the Test
Willingness to Have Willingness to Pay
Socio-Demographic Characteristic Genetic Testing, No. (%) P for Genetic Testing, No. (%) P
Age, years
≤ 40 75 (23.3) .624 81 (26.4) .128
41-50 113 (35.1) 73 (31.6)
51-60 86 (26.7) 64 (27.7)
60+ 48 (14.9) 33 (14.3)
Marital status
Single 23 (7.2) .633 16 (7.0) .625
Married 241 (75.3) 175 (76.1)
Separated/divorced 17 (5.3) 13 (5.7)
Widowed 39 (12.2) 26 (11.3)
Religion
Christianity 261 (81.8) .800 183 (80.3) .238
Islamic 58 (18.2) 45 (19.7)
Ethnicity
Yoruba 213 (66.8) .535 161 (71.2) .044
Ibo 63 (19.7) 37 (16.4)
Hausa 2 (0.6) 1 (0.4)
Others 41 (12.9) 27 (11.9)
Highest level of education
Elementary 60 (19.2) .832 49 (21.9) .019
Secondary 86 (27.6) 65 (28.9)
Diploma/NCE 63 (20.2) 36 (16.0)
BSc 80 (25.6) 54 (24.0)
MSc 17 (5.4) 16 (7.1)
PhD 6 (1.9) 5 (2.2)
History of cancer in the family
Yes 70 (21.7) .256 44 (19.1) .307
No 252 (78.3) 186 (80.9)
Occupation
Employed 114 (36.1) .946 113 (46.1) .500
Self-employed 163 (51.6) 78 (31.8)
Unemployed 18 (5.7) 54 (22.0)
Retiree 21 (6.6) 86 (46.5)
Monthly income
, N30,000 113 (46.1) .706 59 (31.9) .706
N30,000-N99,000 78 (31.8) 40 (21.6)
Above N99,000 54 (22.0) 81 (26.4)
knowledge and beliefs may have an implication for un- of cancer causality may not be unrelated to the increased
derstanding the possible influence of genetics and its awareness about cancer in this setting, although late
influence on prevention for others in their families. Also, presentations still occur.31
there was a mention of spirituality as a cause of their cancer Respondents indicate willingness to discuss their cancer
by a few respondents, which was a factor established in diagnosis with their siblings and their children in their to-
previous studies.29,30 This reported low level of spiritual view tality or part. This shows an illustration of general value of
considering a patient or first-degree relative’s interests as out of pocket for it. This may not be unconnected with their
an individual encased in a cultural environment that has perception of benefits of genetic test and this singular factor
impression on his/her overall being.32,33 Many of the re- has been shown in other studies to positively influence
spondents were not willing to disclose to their parents, willingness to pay for genetic tests.13,18,48 The result did not
which is not uncommon in patients with cancer as telling find any association between age, marital status, level of
loved ones about their diagnosis has been adjudged to be education, monthly income, or family history of cancer and
one of the most difficult aspects of having cancer, which the respondents’ willingness to pay for genetic test, contrary
leads to delay in telling those they perceived to be vul- to a Canadian study in which these factors are impactful in
nerable and concealed their emotions from relatives to the readiness to pay for the test.24
protect them.34,35 However, evidence has shown that
The subject of how much money respondents were willing to
talking about cancer helps people reorganize their thoughts
pay also deserves committed attention. Half of the respon-
and feelings and make sense of their experience34 and may
dents were not ready to pay more than N30,000, that is,
provide a specific-tailored support for them.36
about $100 USD, which is way below $250 USD, the cost of
The results of willingness to test for genetic mutations among a the current test kit used in this study. These results suggest
large proportion (86.6%) of patients with cancer and FDR in that individuals of medium socioeconomic status are willing
this study show a significant factor toward acceptance of the to pay a moderate cost for GT as payments for most health
test in this part of the world. Studies have found factors as- services in Nigeria are out of pocket.49 Interestingly, fewer
sociated with increased acceptance and willingness, which respondents (2.2%) were more willing to pay between
includes risk perception and family experience37,38 and good N100,000 and N150,000 ($270 USD-$400 USD) for GT out
knowledge of genetics.39 These factors, however, were not of pocket. Although this may mean a possibility for consid-
directly significant in deciding whether to have genetic test or eration of acceptability of GT among a few higher-income
not in this study. To encourage testing for the most at risk, populations, cost was implicated by most respondents in this
women are currently advised to test for the BRCA1/2 gene study to be the major barrier toward genetic counseling and
mutation if a family member has tested positive for it, or if a testing services, as also found in previous studies.50-53 This
close relative has been diagnosed with cancer.40 The perceived willingness recorded is very significant, considering the role of
benefits of genetic counseling and testing service for risk as- decreasing socioeconomic status in health care financing.54
sessment were mostly favorable and this could be a contrib-
Perception of causes of cancer in probands as well as of
utory factor to their willingness to test for genetic mutations.
benefits of genetic counseling and testing will awaken their
Most of the participants showed a readiness to discuss with at interest and intention to test for deleterious mutations, which
least a close member of the family, especially mothers, affects their care and prevention in their loved ones. Cost is a
brothers, sisters, daughters, sons, and spouses. This becomes major factor in accessing genetic services and needs a
important for the uptake of GT41 and its role or implication in holistic approach to overcome the challenges in the highly
preventing and detecting cancer early as it is the responsibility burdened health care systems of low- to middle-income
of the proband, who is the first to be tested, to inform the countries like Nigeria and to reach the underserved pop-
relatives of the genetic test results.42 The postulation that male ulations. Culturally informed interventions and research are
relatives are less likely to be informed of genetic test results42 is needed to support families in facilitating effective risk
also seen in this study, and it has been documented that communication critical to the uptake of genetic services and
probands are more likely to share genetic test results with their the preventive impact.
children, female relatives, and relatives who they perceived
In conclusion, with the recognition of the fact that 5%-10%
had a favorable opinion about learning the results.43-47
of all cancers are hereditary, there is a growing need to
Therefore, supporting probands/consultands to commu- improve access to GC and GT, before and after cancer
nicate their test results and risk information with their diagnosis. This publication identifies opportunities to le-
relatives is key to obtaining the full benefits of genetic verage on an insight from Nigeria in determining factors
services.48 Although there is a dearth of data about the associated with intention to test and willingness to have
reaction of relatives with whom genetic test results are genetic counseling and testing among patients with cancer
shared, evidence has shown that open, positive family and relatives. Willingness to pay for CGT identified could
relationships increase the likelihood of disclosure of test lead to a reform in health systems financing and exploration
results, while emotional distance, family conflict, and loss of of other strategies for best practices in cancer care and
contact decrease the likelihood of disclosure.49-51 control. The study has shown that probands have a pivotal
The study examined the willingness to pay for genetic test role to play in communicating cancer risk information to
among the respondents and found that although such a test family members, which promises to improve uptake of
is relatively new in Nigeria, most of them were willing to pay genetic services and the cancer control outlook.
AFFILIATIONS Data analysis and interpretation: Toyin I.G. Aniagwu, Olutosin A. Awolude,
1
Department of Nursing, College of Medicine, University of Ibadan, Babatunde Adedokun, Makayla Kochheiser Anthonia Sowunmi, Dezheng
Nigeria Huo, Olufunmilayo I. Olopade
2
School of Occupational Health Nursing, University College Hospital, Manuscript writing: All authors
Ibadan, Nigeria Final approval of manuscript: All authors
3
Department of Obstetrics and Gynaecology, University College Hospital, Accountable for all aspects of the work: All authors
Ibadan, Oyo, Nigeria
4
Center for Clinical Cancer Genetics & Global Health, Department of AUTHORS’ DISCLOSURES OF POTENTIAL CONFLICTS OF
Medicine, The University of Chicago, Chicago, IL INTEREST
5
Lagos State University Teaching Hospital, Lagos, Nigeria
6
The following represents disclosure information provided by authors of
Center for Population and Reproductive Health, College of Medicine,
this manuscript. All relationships are considered compensated unless
University of Ibadan, Ibadan, Oyo, Nigeria
7
otherwise noted. Relationships are self-held unless noted. I = Immediate
Department of Public Health Sciences, The University of Chicago,
Family Member, Inst = My Institution. Relationships may not relate to the
Chicago, IL
subject matter of this manuscript. For more information about ASCO’s
conflict of interest policy, please refer to www.asco.org/rwc or ascopubs.
CORRESPONDING AUTHOR org/go/authors/author-center.
Toyin I.G. Aniagwu, MPH, School of Occupational Health Nursing, Open Payments is a public database containing information reported by
Nursing Education Department, University College Hospital, Ibadan, companies about payments made to US-licensed physicians (Open
Nigeria; e-mail: [email protected]. Payments).
Babatunde Adedokun
PRIOR PRESENTATION Employment: Amgen
Presented in part at the African Organization for Research and Training in Stock and Other Ownership Interests: Amgen
Cancer (AORTIC), Maputo, Mozambique, November 6, 2019.
Olufunmilayo I. Olopade
Employment: CancerIQ (I)
SUPPORT Leadership: CancerIQ
Supported by NIH grants from Susan G. Komen for the Cure (O.I.O.) and Stock and Other Ownership Interests: CancerIQ, Tempus, 54gene,
Breast Cancer Research Foundation (O.I.O.). The study is partially HealthWell Solutions
funded by R01CA228198-03S1 (D.H.) and Color Genomics Foundation. Research Funding: Novartis (Inst), Roche/Genentech (Inst), Cepheid
(Inst), Color Genomics (Inst), Ayala Pharmaceuticals (Inst)
AUTHOR CONTRIBUTIONS Other Relationship: Tempus, Color Genomics, Roche/Genentech
Uncompensated Relationships: Healthy Life for All Foundation
Conception and design: Prisca O. Adejumo, Toyin I.G. Aniagwu, Olutosin
Open Payments Link: https://openpaymentsdata.cms.gov/physician/
A. Awolude, Babatunde Adedokun, Makayla Kochheiser Anthonia
olopade
Sowunmi, Oladosu Ojengbede, Olufunmilayo I. Olopade
Financial support: Oladosu Ojengbede, Dezheng Huo, Olufunmilayo I. No other potential conflicts of interest were reported.
Olopade
Administrative support: Toyin I.G. Aniagwu, Olutosin A. Awolude, Makayla
Kochheiser Anthonia Sowunmi, Olufunmilayo I. Olopade
ACKNOWLEDGMENT
Provision of study materials or patients: Olutosin A. Awolude, Abiodun The authors would like to acknowledge Stella Odedina for her
Popoola, Oladosu Ojengbede contributions with data collection and in the review of the manuscript.
Collection and assembly of data: Prisca O. Adejumo, Toyin I.G. Aniagwu,
Olutosin A. Awolude, Makayla Kochheiser Anthonia Sowunmi, Abiodun
Popoola, Olufunmilayo I. Olopade
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