Survivors of childhood cancer in Latin America: Role of foundations and peer groups in the lack of transition processes to adult long‐term follow‐up

Abstract Background Over the last decade, the population of childhood cancer survivors has rapidly increased in Latin America, opening a long chapter of challenges for healthcare providers in these countries to provide follow‐up and adult care. Aim In the process of exploring childhood cancer parent and patient engagement in resource‐limited settings, we highlight the challenges faced by Latin American survivors from El Salvador, Mexico, and Peru as they transitioned from receiving cancer treatment to life as a cancer survivors. Methods and Results Focus group discussions and interviews were performed as part of a larger qualitative study involving 10 low and middle‐income countries in four continents regarding patient and caregiver engagement in childhood cancer treatment. We present the results of the Latin‐American survivors and their experiences finishing treatment and life outside the pediatric oncology follow‐up system. Themes regarding a) losing eligibility for pediatric surveillance and care, b) the importance of peer survivors, and c) the need for giving back were part of their stories. Conclusion We suggest that given the lack of organized support from healthcare systems and providers for survivors' proper transition into adult‐centered care, foundations and non‐governmental organizations can provide transitional support, offer space for guidance/information, and work towards collaboration among systems for future integrated programs.


| INTRODUCTION
Incidence rates per million person-years for childhood cancer (0-14 years) in Latin America range from 128.1 in Argentina to 153.1 in Peru. 1 Current rates of survival lag behind high-income countries, for example, acute lymphoblastic leukemia (ALL) 5-year survival is 64.5% across Latin America compared to 89% in Western Europe. 2 This reflects significant progress made over the last few decades in improved access to care and increased resources for childhood cancer treatment. Strategies include twinning partnerships with high-income countries and galvanizing local nongovernmental organization (NGO) support (e.g., El Salvador), childhood cancer healthcare policy changes (e.g., Mexico), 3 international NGO projects (e.g., Sanofi Espoir Foundation "My Child Matters" award), 4

and the WHO Global Initiative for Childhood
Cancer focus country status (e.g., Peru). 5 In 2019, a study was conducted by the International Society of Paediatric Oncology (SIOP), Pediatric Oncology in Developing Countries Committee (PODC), Patient Family and Stakeholder Engagement Task Force (PFSE Task Force) to determine the extent of patient and caregiver engagement during treatment. Ten lowand middle-income countries (LMICs) participated from across 5/6 WHO regions. This paper reports on the results of three of these sites, Peru, El Salvador, and Mexico.
We highlight the challenges faced by Latin American survivors from these three countries as they transitioned from receiving cancer treatment to life as a cancer survivor. We argue that in Latin America, such a transition occurs without coordinated multidisciplinary support from healthcare services and providers; thus, former patients must navigate both their health and life reintegration beyond cancer treatment. Survivors are faced with the task to imagine and live a life as cancer survivors for which they are not necessarily prepared. They find ways to make sense of their new status in multiple ways. Here we address three themes from our respondent interviews.
Based on the survivors' testimonies and stories, we suggest leveraging and/or promoting the involvement of NGOs and childhood cancer foundations that can offer strategies to minimize the abrupt disruption in care as children/adolescents move from cancer treatment to survivor surveillance, adult healthcare and life beyond cancer treatment.

| Settings
The detailed methods of the larger study are available elsewhere. 6 In brief, in El Salvador, the local foundation Ayudame a Vivir (FAV), supporting psychosocial care and >50% of the cost of childhood cancer at the only pediatric hospital in the country, served as entry point to contact participants. In southwest Mexico, the local foundation, Canica, providing psychosocial support to families of children with cancer, contacted potential respondents. In Peru, two local pediatric oncologists (one on temporary leave) recruited survivors and parents from two hospitals to participate in the study. In El Salvador, a group of survivors function under the guidance of a psychologist from FAV and holds monthly meetings and visits to the pediatric oncology ward to talk with parents and children, many of them newly diagnosed. In Mexico, a group of survivors collaborates with Canica activities, participating in camps for children with cancer, and also started a theater play based on their treatment experiences. Some, but not all, the participants in this study are part of these groups. In Peru, there are no organized activities for survivors. The maximum age for admission in the hospital in El Salvador is <12 years old; in Mexico <16, Peru <15 in one hospital, and <18 in the second one.

| Post-cancer treatment standard care
Information about common practices for childhood cancer end of treatment in our Mexican site was not available, however, for the two other countries, it is as follows: In El Salvador, patients who finish treatment receive 10-years of follow-up or until they reach 18 years of age with their pediatric treating team. Monthly check-up appointments are programmed initially and gradually distanced depending on the child's diagnosis and age, and sometimes particular treatment circumstances. Children who reach the age limit for hospital admission (12 years) during treatment, are not affected by this rule and receive treatment until completion and through follow-up. Telemedicine follow-up with calls and test results were initiated this year, especially for those without detected medical conditions or who had reached the last years of long-term follow-up. At the time of discharge when after-treatment follow-up ends, all survivors are advised to register in the national social security health system. Survivors with conditions that require treatment by other specialists are referred to the adult care system. Currently, there's no integrated system in place; the protocol for follow-up and referral is not formalized, and there's no follow-up to determine how the survivors proceed once discharged from the pediatric system.
In one of the hospitals in Peru, follow-up occurs for at least 5 years, and the same teenager-treatment team continues followup even after the survivors reach the hospital admission age limit (18 years). In the second hospital, after-treatment follow-up continues until the children reach the hospital admission age limit (15), then they have to move to adult services for treatment or follow-up.

| Participants, data collection, and analysis
An El Salvadorean pediatric oncology psychologist/medical anthropologist and a Colombian medical anthropologist conducted all research. Appropriate permission to conduct the studies was arranged according to local practice in each country. In-depth interviews and focus-group discussions were conducted with adolescents and young adults who had finished cancer treatment at least 5 years prior.   For example, Erika was 10 when she was diagnosed with acute lymphoblastic leukemia (ALL). She and her parents moved from their hometown (a 24-h bus ride) to a small rented apartment close to the hospital in Lima, Peru's capital city during her 2 years treatment. After she was able to return home following completion of her treatment, Erika felt that she could continue with her life with reasonable normality: … then everything finished: the chemotherapy, the pills, the whole treatment ended. It was a success. In this sense, some respondents reflected that when they had finished treatment, they did not have questions about their future or the long-term treatment consequences, they were too young for such worries, both during and after treatment. It was only after they entered young adulthood that questions about their treatment and late effects arose as their lifestyles and interests changed due to pending adulthood. The following quotations serve as an example of worries of a young adult cancer survivor: There are things that I did not ask at the moment because I was not interested, maybe now I'm inter- We found that, in general, and given the absence of a referral system that supports the transition from childhood care to adult services, survivors in this study trusted their pediatric oncologists as their primary source of follow-up medical consultation. This was the case both for minor issues after ending their cancer treatment as well as for the follow-up period, which supposed that they did not use adult healthcare services. Furthermore, survivors reported that they consulted their trusted pediatric oncologist for random ailments and not necessarily for post-treatment medical conditions requiring a specific follow-up. Ivan, a survivor of ALL, mentioned: Here it is important to note that many survivors have developed a good relationship with their pediatric oncologists during treatment, which was an essential pre-condition for further off-treatment contact with healthcare providers. This situation raises questions about what happens to survivors who, for reasons beyond the scope of this research, are not able to establish meaningful relationships with their pediatric oncology healthcare team or adult healthcare providers. However, this is not an experience that is equally easy for all.

| Importance of peer survivors
Ana told us that even now, after more than 15 years of having finished treatment, her mother cannot understand why Ana likes to remember her experiences. Ana recognizes that at the beginning it was difficult to tell her story, but now she feels it is a healing and strengthening experience.  This shared experience creates a sense of belonging among childhood cancer survivors.
We also found that gathering with other survivors is an opportunity to compare their questions about long-term consequences of treatment and determine whether small ailments or discomforts are shared by others or if they are individual experiences. For example, Lina has checked with her friends about little physical annoyances, from gastric burning to joint-cracking, or mouth blisters, and concluded that everything must be related to long-term effects of treatment that not only she has experienced.  pediatric oncologist as their top option (e.g., compared to a GP), but it must be noted that in this country, survivors are followed by a pediatric oncologist for 10 years after treatment. 11 Sadak et al. found that survivors in the United States mentioned wanting to be seen consistently by one of their existing oncologists during their transition to adult care or in other words, "someone that goes on that journey with you" (p. 10). 12 In this regard, a survey among pediatric oncologists in the United States showed that perceived patients' attachment to providers was the most frequently reported barrier for transfer to adult care. 13 It's been reported that even where a system is in place, survivors' preferences and personal attachment to their physicians play a role in their use of adult health care and engagement with the followup process. 7 This reflects survivor statements in this study who relied on their pediatric oncologists for healthcare advice despite being discharged from care since they had no survivorship surveillance program to rely on and did not want to initiate care from an adult health care provider with no knowledge of their cancer experience.

| Importance of peer survivors
Once again, there have been few recent studies on the experience of childhood cancer survivors relying on peer (other cancer survivors) support. In the United States, Liptak et al. found that a group of adolescent and young adult survivors of a brain tumor, who participated in a social support group (focus on recreation, art, and communication), felt that being with other survivors with a similar medical history was helpful. 14 They described an atmosphere of acceptance and understanding in the group that was lacking in their day-to-day lives.
Some survivors also mentioned reflecting on their experiences as having fewer devastating consequences than other survivors. These findings support the experiences of the survivors in this study who described the importance of peer interactions with other survivors.

| Giving back
Survivors in this study noted their need to give back by visiting children on treatment for cancer, entering into a health care profession, or volunteering. This is a topic that has not been well investigated and certainly not in low-or middle-income countries. Yet, Molinaro and Fletcher in a study of Canadian childhood cancer survivors found that the survivors had experienced post-traumatic growth by giving "back to the pediatric cancer community" (p. 272). 15 The survivors described giving back to organizations that had supported them during treatment and also sharing their experiences with others receiving treatment to encourage them to remain positive. The Latin American survivors in this study reported that giving back was a way to have a purposeful life, which can also be viewed as a positive achievement, particularly in light of the expected late effects of childhood cancer treatment and increased risk of a second malignancy.

| Survivorship guidelines
Working groups from Europe and North America have developed clinical practice guidelines for long-term follow-up of childhood cancer survivors. 16 These guidelines are built under the underlying premise that actual follow-up is possible and in place. Unfortunately, the literature indicates that this is generally true only in high-income countries where structured long-term follow-up for survivors and not necessarily for those who reach adult age is provided, as noted in a study of 15 high-income countries and three middle-income countries, 17 and a survey in the United States that showed that the largest pediatric cancer programs were the ones that offered better established transition to adult care. 12 Similarly, the need for programs and guidelines for survivors' transition from pediatric to adult health care in high-income countries has been recognized. 18 However, major structural challenges for the implementation of such transition processes involve the wide differences between available resources and hospital systems in place, healthcare systems in each country, and childhood cancer policies, among many others. 19 Even in rich-resource settings there is a lack of well-established follow-up and support systems for childhood cancer survivors. 20 In a contrasting experience, in Chile, childhood cancer treatment is provided almost entirely under a national program that secures treatment in the major public hospitals and supports rehabilitation and psychosocial needs through the participation of NGOs. This centralized model that sets childhood cancer as a top priority of a national health policy is the basis for a structured and coordinated collaboration that established a comprehensive national follow-up program with guidelines encompassing, medical, nursing, psychological, social work, occupational therapy, and education areas. 21 In limited-resource settings, the lack of well-coordinated services within healthcare systems in these countries may delay putting in place an effective transition and follow-up program. Thus, the role of childhood cancer organizations (e.g., NGOs) is essential, since they have shown to be instrumental in providing a safe and familiar environment to launch initiatives for survivors' psychosocial care and other possibilities for a well-organized follow-up program. As mentioned above, these organizations offer peer survivors a space to feel supported and to strengthen a sense of belonging after finishing treatment. In general, the involvement of civil society through organized work of NGOs in the improvement of quality care and outcomes in childhood cancer treatment is not only necessary but has been proven to be highly effective. 22

| LIMITATIONS
We did not collect data about institutional protocols for transitioning, or possible adult-pediatric clinic contacts, although we have indications that these services are fairly disconnected.
We have to consider that changes may have been introduced in the hospitals over time (from the time our respondents received treatment and the time they have been interviewed as survivors) regarding how the end of treatment and end of follow-up are conducted, and how the patients and their families were informed, or the resources or contacts made available to them. However, apart from meetings supported by NGOs and hospital visits, the survivors in this study were not aware of programs or systems to address their care. We cannot generalize our findings across each country or all of Latin America, due to our small sample.

| CONCLUSION
The survivor stories in this study teach us that even if the healthcare systems in these countries are not ready to implement follow-up and transition programs for childhood cancer survivors, there are resources, mainly the NGOs and the survivors themselves who can initiate supportive systems in the direction of formal future strategies. Initiatives mobilized at a basic level, as presented above, address what many survivors want and need to do as part of their after-treatment life. That is, survivors giving to and receiving peer support from fellow survivors, which is not only beneficial but also crucial for their well-being. These initiatives can then be leveraged to create long-term programs that are inclusive of the specific survivor needs in each setting and to eventually reach a level of multi-institutional programs. Institutional coordination between existing NGO foundations and hospitals is possible and should be encouraged as a next step in the process of building a robust program. 23 Most survivors of childhood cancer in Latin America will eventually adapt and cope, but we do not know how well since we have no published data. Our interviews with survivors in Mexico, El Salvador, and Peru have shown that they experience a new level of unexpected challenges, although many have found ways to cope through giving back and peer-to-peer support. Therefore, it appears that a follow-up program is essential, and aligns with the right of the survivors to receive transitional support from pediatric oncology programs before

DATA AVAILABILITY STATEMENT
Research data are not shared.

ETHICAL STATEMENT
Appropriate permission to conduct the studies was arranged according to local practice in each country. Permission to conduct the study was granted by two relevant hospitals, one in Peru and one in El Salvador, and by the Mexican NGO, because the children had been treated in multiple hospitals. Participants subsequently gave explicit oral consent for participation in the research before the start of the interview. All names used in this article are pseudonyms.