Abstract
Background:
Despite a plethora of literature on barriers to addressing future fertility in childhood cancer survivors, the data are not representative of limited middle-income settings. Unique and context-specific factors may influence addressing future fertility care among childhood cancer survivors in Uganda. This study aimed to explore the experiences, attitudes, and perceptions of parents on their interactions with health providers about future fertility, as part of their child's cancer survivorship.
Methods:
Using grounded theory, semistructured interviews were conducted with parents of children diagnosed with cancer, <18 years of age, and not in the induction or consolidation phases of treatment. Transcripts were thematically analyzed.
Results:
A total of 20 participants were interviewed, with the majority identifying as female (n = 18). The global theme that arose was the importance of shared decision-making, and the key themes encompassing this were as follows: (1) importance of accurate information, (2) respect of autonomy, and (3) engagement and psychosocial support.
Conclusion:
In Uganda, parents of children with cancer value a multifaceted approach to satisfactory decision-making within the context of oncofertility.
Background
In sub-Saharan Africa, the incidence of childhood cancer varies between 50 cases per million person-years in the 0–14-year age group to 150 cases per million person-years in the 15–19-year age group. 1 In Uganda, the Kampala Cancer Registry estimated the childhood cancer incidence at 139 cases per 1 million children in the 0–19-year age group. 2 The 3-year survival rates, in Uganda, have improved over the past two decades, and vary between 86% and 30% for Hodgkin's disease and Wilms tumors respectively. 3 Data for the overall 5-year survival for all childhood cancers is lacking, but estimated to range between 20% and 40%, 4 for low–middle income settings. This is significantly lower than in high-income settings (80%–90%) 5 and this has been attributed to differences in early detection, access to efficient treatment modalities, toxic death, and supportive care. 6
These improved childhood cancer survivor rates have shifted the paradigm of the cancer care continuum toward integrating quality survivorship.7,8 Although there is a paucity of sub-Saharan Africa data, childhood cancer survivors are at risk of reproductive impairment in the long term. 9 These late reproductive effects include delayed puberty, premature ovarian failure, estrogen deficiency (females), testosterone deficiency (males), impaired spermatogenesis (males), sexual dysfunction, infertility, and pregnancy complications.9,10 Impairment of future fertility among childhood cancer survivors is associated with psychosocial dysfunction, lower quality-of-life scores, 11 and considerable psychosocial distress.12–15 Uniquely, female childhood cancer survivors have to face the historical societal burden placed on women to bear children. 16 This is exaggerated in the sub-Saharan African context, where they are at risk of ostracization, domestic violence, discrimination, and stigma.17–22
Oncofertility is a multidisciplinary field that integrates oncology care, fertility care, and psychological support. 23 This is aimed at assessing infertility risk, addressing ethical concerns, providing information to patients, parents, and carers regarding fertility preservation. 23 In addition, it involves screening for and management of long-term reproductive effects of cancer treatment. 23 Barriers to the realization of oncofertility in childhood cancer are complex. This is because children aged 0–17 years rely on their parents for decisions, support, and care since minors are unable to provide informed consent. 16 Therefore, parental or guardian perceptions are key to understanding the barriers to addressing future fertility in childhood cancer survivors.
There is no oncofertility program in Uganda. Much of this may be related to institutional, parental, and health provider barriers.24–26 Although largely unknown, unique and context-specific factors may influence addressing future fertility among childhood cancer survivors in Uganda. This study aimed to explore the experiences, attitudes, and perceptions of parents on their interactions with health providers about future fertility as part of their child's cancer survivorship.
Methods
Design
This qualitative study utilized grounded theory. Grounded theory methodology was used in an attempt to derive explanatory meaning from the data for a phenomenon that is “future fertility in oncology care in Uganda.”27,28 Using the interview data as the starting point enabled an inductive understanding of the concepts surrounding inadequate attention to future fertility among childhood cancer survivors, through the lens of the parents or guardians.27,29 This study was conducted as part of the Understanding Reproductive Health among Survivors of Pediatric and Young adult cancer (URHSPY) project, in Uganda.
Setting
The Uganda Cancer Institute (UCI) is the only tertiary cancer treatment facility in Uganda. It is the only center in Uganda with dedicated pediatric cancer care. The facility provides outpatient and inpatient clinical services. Annually, ∼600 children aged 0–17 years are diagnosed with cancer at the UCI with a 3-year survival rate ranging between 86% and 30% for Hodgkin disease and Wilms tumors, respectively. 3 Currently, there is no oncofertility program at the center, and subsequently, no fertility preservation options offered to childhood cancer patients.
Participants
Parents of children diagnosed with cancer were eligible if the affected child was <18 years of age and attending the outpatient pediatric oncology clinic. We excluded parents of children receiving induction or consolidation phases of treatment, parents <18 years of age, and parents who could not speak English or Luganda. Participants were approached in person and informed about the study by a bilingual (Luganda or English) research assistant. Participants were recruited through convenience sampling, with sample size determined by thematic saturation. 30 Thirty-six potential participants were approached, 28 agreed to participate and only 20 interviews were required to reach thematic saturation. All interviews were conducted in a private space within the UCI, and each interview had an average duration of 60 minutes.
Data collection
Interviews were conducted between November 1, 2021, and February 20, 2022. A semistructured interview guide was developed with input from all the authors, of which one was an expert in qualitative methodology (Supplementary Data). The interview guide was flexible to allow for in-filed improvisations. The interview guide was piloted, in September 2021, on 10 potential participants to gauge appropriateness, viability of the discussion and dialogue flow, build familiarity with the guide, and determine the interview time frame. Adjustments were made to the final guide before participant enrollment. The guide explored parents or guardians understanding of concepts related to the risk of cancer treatment-related infertility, child's future fertility, and decision-making. The interviewers were two female bilingual research assistants. Each face-to-face interview was attended by one participant and one interviewer.
Data analysis
The interviews were audio-recorded, and when appropriate translated into English by a professional service and transcribed verbatim into Microsoft Word® version 16.41. The transcripts were analyzed using NVivo 12. 31 Thematic analysis was used to develop a deep insight through systematic reflection that could help the emergence of meaningful categories from the collected complex rich codes. The principal investigator initially coded the data, which was then reviewed by the qualitative expert to ensure consistency. All the investigators met to discuss and review the emerging themes, and any differences in categorization were resolved through reviewing the data and arriving at a consensus. The principal investigator debriefed the supervisor and expert to provide a rigorous external check on the research process. All records were archived to provide an audit trail and baseline against which later data analysis and interpretations were tested to gauge adequacy.
Ethics
The study was reviewed and approved by the UCI and the University of Minnesota (UMN) Institutional Review Boards.
Results
Participants
A total of 20 participants were interviewed, with the majority identifying as female (16). The mean age was 35.6 years, most of the participants were married (15), and with at least a secondary-level education (15). The proportion of the related children with cancer was split male and female. The mean age at cancer diagnosis was 6.4 years and mean duration since diagnosis was 3.2 years. The cancer diagnoses were acute lymphoblastic leukemia (10), nephroblastoma (4), Burkitt lymphoma (1), astrocytoma (1), rhabdomyosarcoma (1), osteosarcoma (1), bladder carcinoma (1), and non-rhabdomyosarcoma (1) (Table 1).
Demographic Table (N = 20)
SD, standard deviation.
Themes
One global theme emerged from the face-to-face in-depth interview data: Shared decision-making. From this arose three major themes: importance of accurate information, respect of autonomy, and engagement and psychosocial support (Table 2).
Summary of Themes and Subthemes
Shared decision-making
This global theme defines how parents perceived their interactions with health workers and the aspects they valued in making decisions about their child's future fertility. The themes encompassing shared decision-making, and their exemplifying quotes are summarized in Tables 3–5.
Supporting Quotes for the Importance of Accurate Information
Supporting Quotes for Respect of Autonomy
Supporting Quotes for Engagement and Psychosocial Support
Importance of accurate information
This was a recurring theme throughout the in-depth interview. Parents considered this the cornerstone to understanding cancer treatment-related reproductive failure, so as to make informed decisions regarding their child's future fertility. Four subthemes further define this theme (Table 3).
Thorough medical explanation
Nearly all the parents were satisfied with receiving detailed information about the cancer diagnosis and the treatment process in a language they understood. They were informed about the immediate side effects of the treatment. They felt that all their questions were answered, and this helped them build confidence in the care their child received.
Inadequate information about future fertility
Despite the thorough explanation regarding cancer treatment and immediate expectations, participants were not satisfied with the limited information provided regarding the children's future fertility. Most of the parents reported having no prior knowledge about any impact of cancer or treatment on reproductive health. Parents needed more information and were curious about the impact of cancer on fertility. In addition, they were worried about the myths and misconceptions among fellow parents such as “all cancer treatment causes infertility.” To them, knowing would not result in refusal of treatment but rather prepare them and their children for the future.
Afraid to ask
A few participants, more so those who had some knowledge on the impact of cancer treatment on future fertility, were afraid to raise concerns about the fertility impact of cancer treatment. They were worried about being misunderstood by the health workers and being labeled “arrogant.” They thought this impression could affect the treatment or care their children received. These participants felt this greatly limited their discussion with the doctors.
The right information to the right audience
Although information about future fertility was important to all participants, some of the parents recommended that considerations be made regarding the different attitudes, perceptions, and the value placed on the child's future fertility with respect to cancer. They reported that these varying attitudes could be influenced by religion, educational level, and socioeconomic status. In addition, they reported that misperceived information could result in treatment abandonment for some parents. They cautioned the doctor to adapt the information to the parents, especially to those of a lower education background.
Timing of information matters
Although parents wanted more information and honesty about future fertility, there were varying views on the best time to receive this information. Majority of the parents wanted the information regarding future fertility concerns, given at enrollment before the child started treatment. They wanted this so that they would make an informed decision and know what to expect. However, some of the parents wanted future fertility discussed after treatment had been initiated, and when the child was somewhat better. The felt they would be in a better position to receive this information.
Fertility preservation options
Nearly all parents were curious and open to any efforts to prevent any potential fertility decline in their children. Some inquired about storage of gametes and use of alternative treatments that are less toxic to fertility. They were saddened by the fact that no options were made available to them at the start of treatment.
Respect of autonomy
Nearly all parents who requested honesty and clarity from the health workers wanted their right of self-determination to be respected. They wanted to be given all the facts about their child's future fertility so that they could make informed choices. They echoed the fact that this did not mean abdicating the duty to their child's care but respect for their right to make an informed decision (Table 4).
Child's assent and participation
A few of the parents especially those with teenagers felt their children should be involved in the future fertility discussion. Some parents were worried about how to approach the discussion about future reproduction with their children. They felt the doctors were more skilled to engage the children about this topic. Other parents valued the opinions of their children about reproduction despite their age. All in all, they requested the information be made understandable to the affected children, so that their participation would be meaningful.
Engagement and psychosocial support
A major theme that arose was the value parents placed on engagement and psychosocial support. This aided them in making decisions and coping with the reproductive expectations of cancer treatment. Participants appreciated that the health workers were constantly involved with them, answering their questions, showing compassion, reassurance, and encouragement. Nonetheless, some parents still found the engagement with the health workers inadequate (Table 5).
Encouragement and reassurance
Parents felt comforted and more hopeful following interactions with health workers. The health workers offered compassion, love, counseling, and psychological support to the children and parents throughout their care. Parents reported that their interaction with nurses made them feel less afraid and more optimistic about the treatment process and the child's future fertility.
Need more engagement
Participants felt the matter of future fertility was very complex in children with cancer. They felt this topic was not given enough time throughout the discussions with the health workers. They requested for more discussions about this with health workers beyond enrollment. In addition, they wanted their children followed up for any of the long-term effects and appropriate remedies recommended.
Insufficient doctor-to-patient ratio
Parents understood that the health workers were very busy as the number of patients often outnumbered the number of health workers. They believed this limited the interaction time they received, and the level of explanation about reproductive expectations with cancer. Among these participants, some recommended that nurses be trained to counsel the parents. They thought this would offload some of this burden from doctors, and in turn nurses would offer them more time to discuss complex issues such as long-term effects of treatment.
Partner support
A few of the mothers felt decisions about future fertility were complex, and that they needed the child's father to be involved. These women did not want to be blamed for anything that could go wrong with the child's future fertility. They requested the health workers to engage and encourage men to be involved in the affected child's care. For example the child's father should come along for the appointments.
Discussion
This study conceptualizes what parents consider important in making decisions regarding their child's future fertility, when faced with cancer. The global theme encompassing the data, was the value parents placed on shared decision-making between themselves and the health workers. Understanding shared decision-making in context of the future fertility discussion, in children with cancer, is important to Uganda. This is supported by the increasing incidence of childhood cancer and improving rates of childhood cancer survival.3,32 We identified themes and subthemes that provide a framework for engaging parents of children with cancer, when faced with decisions regarding long term reproductive outcomes after treatment.
Since the majority of these parents reported lack of prior knowledge on the reproductive impact of cancer treatment, they valued accurate and timely information about their child's reproductive health and future fertility. Similar views on the importance of provider information, content, and timing of fertility-related discussions are shared by adolescents with cancer and their parents in high-resource settings. 33 The parents wanted this information straight from the provider, and as they stated, “not part of gossip from peers.” A similar perception of inadequate information and negative attitude toward the associated misinformation from peers is reported in other settings.34,35 In addition, parents acknowledged that limited knowledge and access to fertility preservation options were a barrier to shared decision-making, as reported in high-income settings. 33
Parents in this study were keen on adolescent participation in the decision-making process. Although few valued adolescent joint participation and input in the discussion process, as echoed by adolescents in other settings,35,36 many were concerned about their inability to explain the implications of treatment to their children. Fear of emotional burden, lack of fertility-related knowledge and trust in the health provider, as reported by others, 37 were major drivers of this perspective. In addition, parents wanted the information appropriately adapted to their child's age and information needs. Similar attitudes to adolescent information needs, have been reported in other settings. 37
This study helps to correct the perception that Ugandan parents are likely to decline treatment if they are aware of all toxicity, including impact on fertility. Rather, as this study shows, they want complete information to make the best decision for their child. Nonetheless, parents in this study were split on when to have the future fertility discussion. Some opted for at the start, and others preferring at the end of treatment. This underscored their limited knowledge on reproductive risks, and the availability and temporality of any remedies in regard to their child's future fertility. One unique limitation to the information exchange between parents and health care providers in this study population was their fear to ask questions about their child's future fertility. This, they thought, would be misinterpreted as imposing behavior, and subsequently limiting their child's care.
Parents appreciated the commitment of the doctors to provide information about the cancer diagnosis, the cancer treatment journey, and immediate side effects of the treatment. However, parents needed health workers to respect their right to determine what is best for the child. This conflict between patient autonomy and medical care values, as perceived by the health care provider, is a common cause of ethical dilemmas in oncofertility. 38
Parents in this study appreciated the value of encouragement, psychosocial support, and counseling provided by the health workers to help them cope with the anxieties of an uncertain cancer prognosis and reproductive future for their children. This is need for oncofertility counseling, and psychosocial support is shared by adolescents and young adults in other settings.34,39 In addition, parents in this study wanted continued engagement with the health providers about treatment-related effects and long-term effects, especially fertility. Similarly, parents in a high-resource setting valued continued engagement as the shock of the initial diagnosis blocked their ability to comprehend any information about future fertility at enrollment. 37
One of the limitations to proper and continued engagement in the context of future fertility was the insufficient doctor-to-patient ratio. Parents proposed that the nurses be trained to take up the task, so as to ease the burden placed on the doctors.
In Uganda, and in similar limited-resource settings, male involvement in maternal and child health is low. This is influenced by contextual and culturally-defined gender roles.40,41 This study echoes male partner absence and acknowledges the value of a partner's psychosocial support in the decision-making process, regarding childhood cancer care.
Overall, the parents in this study echoed the importance of shared decision-making. They considered it a key to navigating complex issues surrounding future fertility and the urgency of potentially lifesaving cancer treatment children. Similar attitudes to shared decision-making have been reported by others.26,32 Furthermore, parents in this setting value adequate provider driven information, access to fertility preservation options, adolescent participation, sustained engagement, and psychosocial support, as pivotal elements in the decision-making process. Efforts to develop a childhood oncofertility program in Uganda should be centered around addressing the aspects of shared decision-making.
Limitations
Several limitations could have affected the external validity of this study. First, the study represents the experiences and perspectives of a subset of parents with a demographic skewed toward women. There is a limited description of the related children with cancer such as the treatment phase at the time of the interview. This would have added an extra layer of granularity to the context of the study. Perspectives on future fertility-related decision-making can vary in a larger sample even within a similar setting, and thus, this study may not fully reflect the diversity of Ugandan parents and their perception and attitudes toward oncofertility.
Conclusion
Parents of children with cancer in limited-resource settings, share a multifaceted understanding of the important elements to the future fertility-related decision-making process. Providing adequate information about the impact of cancer on fertility constitutes the backbone of a satisfactory decision-making process.
As the Uganda cancer control programme is yet to establish an oncofertility aspect, an opportunity exists to address these barriers and reinforce the facilitators to decision-making during the future fertility discussion. An implementation study on a comprehensive childhood cancer survivorship program inclusive of fertility preservation is needed. Additional research can explore the experience and perspectives of adolescents and health workers in the future fertility decision-making process.
Data Sharing Statement
All individual participant data, protocol, analysis plan, and code book are available to anyone who wishes to use the data to achieve the aims stated in the study protocol. The data are available upon request to the corresponding author for a duration of 5 years from publication.
Footnotes
Acknowledgments
We would like to acknowledge the team at the Fogarty North Pacific Global Health (NPGH) consortium for their tireless mentorship efforts toward the research team. The team at Global Health Uganda for the astute project management skills, and the UCI for ensuring a conducive environment within which to carry out the study.
Authors' Contributions
A.K.: Conceptualization, methodology, validation, funding acquisition, project administration, investigation, formal analysis, data curation, data visualization, and writing the original article draft. D.Z.: Methodology, validation, project administration, supervision, and article review. S.X.: Methodology, validation, project administration, formal analysis, data curation, and article review. V.G-L.: Supervision, data curation, resources, and article review and editing. J.K.B.: Methodology, validation, project administration, supervision, and article review. H.W.: Methodology, validation, validation, funding acquisition project administration, supervision, and article review. R.G.: Methodology, validation, validation, funding acquisition, project administration, supervision, and article review.
Author Disclosure Statement
The authors declare that they have no competing interests.
Funding Information
This study was funded by the NPGH research fellow training consortium, under the Fogarty International Centre and the National Institutes of Health (Grant No. D43 TW009345) and supported by the National Institutes of Health's National Centre for Advancing Translational Sciences (Grant No. UL1 TR002494). The funding organizations did not have any role in the design of the study or writing of the article. V.G-L. receives funding from the NICHD under grant number Z1A HD008985.
References
Supplementary Material
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