Originally published as JCO Early Release 10.1200/JCO.2005.08.557 on September 19 2005

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Care-Related Distress: A Nationwide Study of Parents Who Lost Their Child to Cancer

From the Division of Clinical Cancer Epidemiology, Department of Oncology and Pathology; Childhood Cancer Research Unit, Department of Woman and Child Health; Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Karolinska Hospital, Stockholm; and Division of Clinical Cancer Epidemiology, Department of The Sahlgenska Academy, Gothenburg, Sweden

Address reprint requests to Ulrika Kreicbergs, RN, PhD, Clinical Cancer Epidemiology, Karolinska Institutet/Hospital Z5:U1, SE-171 76 Stockholm, Sweden; e-mail: Ulrika.Kreicbergs{at}onkpat.ki.se

	ABSTRACT

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PURPOSE: Palliative care is an important part of cancer treatment. However, little is known about how care-related factors affect bereaved intimates in a long-term perspective. We conducted a population-based, nationwide study addressing this issue, focusing on potential care-related stressors in parents losing a child to cancer.

METHODS: In 2001, we attempted to contact all parents in Sweden who had lost a child to cancer in 1992 to 1997. The parents were asked, through an anonymous postal questionnaire, about their experience of the care given and to what extent these experiences still affect them today.

RESULTS: Information was supplied by 449 (80%) of 561 eligible parents. Among 196 parents of children whose pain could not be relieved, 111 (57%) were still affected by it 4 to 9 years after bereavement. Among 138 parents reporting that the child had a difficult moment of death, 78 (57%) were still affected by it at follow-up. The probability of parents reporting that their child had a difficult moment of death was increased (relative risk = 1.4; 95% CI, 1.0 to 1.8) if staff were not present at the moment of death. Ten percent of the parents (25 of 251 parents) were not satisfied with the care given during the last month at a pediatric hematology/oncology center; the corresponding figure for care at other hospitals was 20% (33 of 168 parents; P = .0163).

CONCLUSION: Physical pain and the moment of death are two important issues to address in end-of-life care of children with cancer in trying to reduce long-term distress in bereaved parents.

	INTRODUCTION

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Palliative care is an important part of many diseases, including cancer. However, little is known on how the care itself and other factors during the palliative phase affect the bereaved intimates in a long-term perspective.

The loss of a child can be considered particularly stressful.¹ When the death is caused by a malignancy, the parents, in addition to suffering the loss, are usually exposed to the protracted physical and emotional suffering of the child.² When the disease is no longer curable, the parents may be particularly vulnerable, and the care given to the child may affect them even more. Children with cancer suffer from a number of symptoms during their last month of life,² and the communication with the child may also affect the child's well-being.³ A study of women who had lost their husband to cancer suggests that it was the late husband's psychological, rather than physical, symptoms that affected the spouse's long-term mental health the most.⁴ An investigation of women who had had a stillbirth showed that care-related factors affected the women's mental health 3 years after bereavement.⁵ Similarly, factors in the care of children with cancer may affect the surviving parents' risk of long-term psychological distress.

When prioritizing efforts to improve care, we may be helped by the bereaved intimates in identifying the factors that affect them the most in a long-term perspective. We conducted a population-based, nationwide study to determine to what extent certain care-related stressors resulted in long-term distress in bereaved parents who lost a child to cancer.

	METHODS

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We identified 368 children in Sweden who had been diagnosed with a malignancy before the age of 17 (from 1970 to l997) and who died before the age of 25 (from 1992 to 1997). The children were identified through the Swedish National Register of Causes of Death, which is linked with the Swedish National Register of Cancer. The children's parents were identified in the Swedish Population Register by their national registration number. A parent was defined as the guardian of the child at the time of the child's diagnosis. The parents were eligible for the study if they were born in one of the Nordic countries, had a nonconfidential phone number, and understood Swedish. We required permission of the child's former physician to contact the family; permission was given for all families.

We found 561 bereaved parents who met the criteria, representing 323 children. Between August and October 2001, we sent these mothers and fathers an introductory letter explaining the objectives of the study and an invitation to participate. Afterwards, we telephoned the parents and asked for their oral informed consent before the questionnaire was sent out. To safeguard parental anonymity also vis-à-vis the researchers, the questionnaire was returned (without any name or code), and a card notifying the investigators that this had been done was returned separately. Ten days after the questionnaire was sent out, a combined thank you and reminder card was posted. An interviewer called the parents who had not returned his or her reply card. The study was approved by the Ethics Committee of the Karolinska Institutet.

The questionnaire was developed on the basis of literature studies, seven successive in-depth interviews with bereaved parents, and personal clinical experiences. A face-validity evaluation was performed with 15 separate bereaved parents to make sure that the questionnaire was understood correctly. The means of data collection were tested in a pilot study addressing 22 bereaved parents. Similar methods have been used in several previous investigations performed in our research group (Clinical Cancer Epidemiology).^4-7 The questionnaire included 129 questions with a total of 365 items concerning the child's medical and nursing care and the parents' mental health 4 to 9 years after the loss.

The present study focused on possible stressors experienced by bereaved parents during the entire care period of their child and whether the specific stressor still affected the parents at the time of the follow-up. The questionnaire posed the following questions: "Below are examples of experiences and memories that relatives of deceased persons may have. Are any of these in line with your experience? If so, does this affect you today?" The response categories were as follows: "Not relevant, not experienced," "Does not affect me at all today," "Affects me a little today," "Affects me moderately today," and "Affects me a lot today." Twelve possible stressors were enumerated. The questionnaire also addressed the parents' satisfaction with the care provided during the last month of their child's life. To compare fathers' and mothers' experiences and how these experiences affected them, ² tests were conducted.

For each outcome (eg, "My child had a difficult moment of death"), we calculated the percentage of parents in each category of the independent variable. When comparing the categories, we first calculated the relative risk as the ratio of the percentages, together with the 95% CI (using the Mantel-Haenszel formula for the variance). Multivariable logistic models were then constructed to determine the relative importance of the independent variables in explaining the variation in the outcome. We used SPSS (version 11; SPSS, Inc, Chicago, IL) for forward selection and backward elimination in which independent variables were added to or remained in the model with the proviso that P < .05.

The study was supported by grants from the Swedish Children's Cancer Foundation, the Stockholm County Council, the Swedish Research Council, and Capio's Research Foundation. The funding sources had no involvement in any part of the study.

	RESULTS

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Information was supplied by 449 (80%) of the 561 eligible parents, corresponding to 85% of the 531 parents who agreed to be included in the study. Of the 449 participating parents, 191 (43%) were fathers, and 251 (56%) were mothers (sex not stated by seven parents; Table 1).

Three of the studied stressors in the care of the children still affect approximately 10% of all participating parents a lot 4 to 9 years after the loss. Twelve percent of parents (53 of 431 parents) are still affected a lot by pain that could not be relieved, 10% (42 of 431 parents) are still affected by a difficult moment of death, and 8% (35 of 433 parents) are still affected by moments when their child's pain control was neglected. A few stressors still affected 7% of the parents a lot at follow-up; these stressors were insufficient contact with the health care service after the child's death (31 of 433 parents), negligent care of the child (30 of 434 parents), and lack of support by a close person (31 of 432 parents; Table 3).

Table 4 lists the results of a multivariable analysis from the 138 parents who provided information on "My child had a difficult moment of death" for different categories of certain independent variables. Relative risks (as a ratio of percentages) greater than 1.0% and 95% CIs not including 1.0 were obtained for city residential region, parents who have shared their worries with others (half or less), parents with anxiety the year before the child's diagnosis, and absence of staff at the moment of death. By forward selection, we obtained a final logistic regression model with five independent variables for reporting that "My child had a difficult moment of death." Factors making agreement with this statement more likely were city residential status, anxiety in the year before the child's diagnosis, not sharing worries with others, absence of depression in the year before the child's diagnosis, and absence of staff at the moment of death. The same final model was obtained by the procedure of backward elimination. The crude odds ratios listed in Table 4 were adjusted for the five independent variables in the final model; the odds ratios for the five variables in the final model were adjusted for the four other variables.

	DISCUSSION

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Our study shows that the two experiences that most frequently affect bereaved parents a lot 4 to 9 years after the loss of their child to cancer are pain that could not be relieved and a difficult moment of death. Parents of children cared for at pediatric hematology/oncology centers were half as likely to be dissatisfied with the care provided during the child's last month of life compared with parents of children cared for in other hospitals.

With regard to care-related stressors, factors that can be addressed in routine clinical care are particularly important. Our findings suggest that, by improving pain control and by reducing difficulties at the moment of death in children with cancer, the long-term distress in surviving parents may be reduced. There are, of course, stressors in the care of a dying child that cannot be eliminated, but it is reasonable to address the two aforementioned factors in clinical practice. In addition, many parents found the contact with the health care service after the death of the child insufficient, which is also an issue that can be addressed and improved.

Previous studies pertaining to factors in the care of children with cancer leading to long-term distress in bereaved parents are few in number. However, it has been reported that pain is a frequent problem in the care of children with cancer. Wolfe et al² reported, in a study of 103 parents, that nearly 80% of the children had pain during their last month of life and more than 50% of the children suffered a lot from the pain. Goldman and Chir⁸ studied 152 children with cancer and reported that 92% had pain during their last month of life and, in 7% of children, the pain remained unresolved. No association with parental distress caused by the child's suffering was discussed in these two reports. Whittam³ mentioned haunting memories of poor pain management in bereaved parents, but no specific data were presented. The International Society of Pediatric Oncology guidelines emphasize the need for professional pain control in pediatric palliative care to give the child the best possible quality of life.⁹ Moreover, not only is professional pain control beneficial for the child itself, it also affects the bereaved parents in a long-term perspective. With regard to the predictors we observed for reporting that the child had had unrelieved pain, it is understandable that a long duration of illness carries a higher probability of developing severe pain, and it is possible that parents with a high level of educational are more sensitive to unrelieved pain than other parents.

A stressor that also can be addressed in clinical care is "My child had a difficult moment of death," which still affects 57% of bereaved parents with such an experience 4 to 9 years after the loss. Parents reporting their child to have had a difficult moment of death were more likely to live in large cities, not have shared their worries with others, and have a history of anxiety, and staff were less likely to have been present at the moment of death. Whether anxiety-prone parents may have experienced the death more disturbingly or recalled the moment differently cannot be elucidated by our data. The factors related to parental distress seem to fall into the following two basic categories: attributes of the parents (such as antecedent anxiety and sharing of worries with others) and aspects of the care itself. The only common statistically significant predictor in the multivariable analyses on pain that could not be relieved and a difficult moment of death was absence of staff at the moment of death. In addition, a difficult moment of death was significantly more distressing for parents who did not have additional children after the diagnosis of the child who died (data not shown). To study these predictors and define the difficulties in detail are important issues for future studies.¹⁰

Another issue, which can be addressed relatively easily in clinical practice, is improving the health care service's contact with bereaved parents. Our data are supported by reports claiming that contact with caregivers after the child's death may be beneficial for the parents.^11,12 The International Society of Pediatric Oncology guidelines suggest 2 years of routine contact with bereaved families.⁹

The importance of a good social structure around the family with a terminally ill child has been acknowledged,¹³ and social support has been documented to reduce distress in other bereaved groups.^14,15 Although support from a close friend or relative may be difficult to address in routine clinical care, our data suggest that it may be valuable for clinicians in pediatric end-of-life care to assess the social support and, if it is insufficient, try to enhance it and to also provide avenues for sharing worries, such as with a psychologist.

In a study by Wolfe et al,² nearly 50% of the children with cancer were died in the hospital, and nearly half of these deaths occurred in the intensive care unit. The authors concluded that, although children with cancer often receive aggressive treatment at the end of life, they still suffer a great deal from more than one symptom. In contrast, in our study, only approximately 10% of the bereaved parents reported that their child died in the intensive care unit, and this was the place where the risk of a difficult moment of death of the child was the lowest. Thus, an intensive care unit may be appropriate when the terminal phase is associated with severe complications.

One strength of our study is the population-based setting, with a register covering nearly 100% of the eligible parents. Moreover, the questionnaire was anonymous, which presumably helps ensure honest answers. The 30 parents who did not agree to participate, the 59 parents who failed to return the questionnaire, and the 23 parents who could not be reached constitute a limitation of the study. Nevertheless, the investigation includes 80% of all eligible parents in Sweden who lost their child as a result of cancer during the period of 1992 to 1997. Importantly, our findings may not be generalized to other medical communities or other cultural settings without further evidence.

Some children in our study are represented by one parent (a mother or a father), and some are represented by two parents. When we analyze mothers and fathers separately, each child is represented by only one parent, and validity problems that may be caused by varying numbers of parents per children are eliminated. Regardless of whether we studied mothers and fathers together or mothers and fathers separately, "My child had pain that could not be relieved" and "My child had a difficult moment of death" were frequently reported stressors that affected a large proportion of the parents at follow-up. The finding that some stressors affect mothers more frequently may reflect the fact that mothers spend more time with the child.¹⁶ Nevertheless, for most of the stressors studied, the degree of affected parents at follow-up was not statistically different between mothers and fathers.

Although the overall aim of our study was to search for stressors and for means of improving the health care of children with cancer, the results also indicate that many parents did not encounter the stressors studied. Accordingly, more than two thirds of the parents did not find the moment of death difficult for the child, more than two thirds of parents did not find that the information about the severity of the disease was given inappropriately, and less than 5% of all parents were affected a lot at follow-up by the way this information was given. During the entire period of care, more than 50% of parents did not report having experienced negligence in the care of their child or poor behavior of staff. Nearly 80% of the participating parents did not find that they were informed too late about the fatal outcome. Similarly, two thirds of the parents had not experienced neglect of pain control.

The importance of experienced multidisciplinary staff to care for children with cancer has been acknowledged previously.¹⁷ In our study, the parents of children treated at pediatric hematology/oncology centers or at home were more satisfied with the care provided than parents whose children were treated at other hospitals; thus if possible, treatment in specialized units seems to be preferable. Although the families of children treated at home may have been a selected group with a presumed less final course of the disease and/or psychologically more stable, the satisfaction with care at home reported by many families should not be discounted (Table 2). Nevertheless, the majority of the parents reported satisfaction with the care during the child's last month, independent of the location of the terminal care.

A number of stressors occurring during the care of a child with terminal cancer cannot be eliminated or are difficult to address in routine clinical care. Good communication and honest information are probably of utmost importance, as when communicating about death with children aware of their imminent death.¹⁸ Our study suggests that improved pain control, improved care during the moment of death, and improved follow-up after the child's death are factors that may be rewarding to focus on in clinical practice to reduce long-term distress in bereaved parents. In other words, further improvement in the care of the sick child may also be beneficial for the parents in the long term.

As mentioned initially, although palliative care is an important part of many diseases, little is known on how the care itself affects bereaved intimates in a long-term perspective. Therefore, we encourage additional studies in this field, particularly because 99% of the bereaved parents found our investigation valuable and 68% were positively affected by the study, as reported recently.¹⁹

	Authors' Disclosures of Potential Conflicts of Interest

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The authors indicated no potential conflicts of interest.

	Acknowledgment

 
We thank the parents who made this study possible by bravely sharing their experiences with us. We also thank Ulla-Britt Rittvall for telephoning all the parents.

	NOTES

 
Supported by grants from the Swedish Children's Cancer Foundation, the Stockholm County Council, and the Capio's Research Foundation.

Presented in part at the 36th Annual Meeting of the International Society of Pediatric Oncology, Oslo, Norway, September 16-19, 2004, and the manuscript won the Schweisguth Prize 2004 for the best scientific article in pediatric oncology prepared by a trainee, as decided by the Scientific Committee of the International Society of Pediatric Oncology.

Authors' disclosures of potential conflicts of interest are found at the end of this article.

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9. Masera G, Spinetta JJ, Jankovic M, et al: Guidelines for assistance to terminally ill children with cancer: A report of the SIOP Working Committee on psychosocial issues in pediatric oncology. Med Pediatr Oncol 32:44-48, 1999[CrossRef][Medline]

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16. Kreicbergs U, Valdimarsdóttir U, Onelöv E, et al: Anxiety and depression in parents 4 to 9 years after the loss of a child owing to a malignancy: A population-based follow-up. Psychol Med 34:1431-1441, 2004[CrossRef][Medline]

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Submitted December 14, 2004; accepted June 3, 2005.

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