Traumatic Stress Symptoms in Adolescent Organ Transplant Recipients
Lisa Libman Mintzer, PhD*; Margaret L. Stuber, MD‡; Debra Seacord, PhD‡; Marleen Castaneda, BA‡; Violet Mesrkhani, MA‡; and Dorie Glover, PhD‡
ABSTRACT. Objective. Symptoms of posttraumatic
stress disorder (PTSD) after life-threatening medical ill-ness have been found to predict poor outcome in prelim-inary studies of adults and children. However, these symptoms are rarely recognized in general medical or pediatric settings. Here we report on the first large inves-tigation to assess prevalence and correlates of self-re-ported symptoms of posttraumatic stress in a nonreferred sample of adolescent liver, heart, and kidney transplant recipients.
Methods. One hundred four adolescents, ages 12 to 20 years (mean: 15.7; SD: 2.1), completed and returned the University of California, Los Angeles, PTSD Index for the Diagnostic and Statistical Manual of Mental Disor-ders. All participants were at least 1 year post–initial transplant and were fluent speakers of English and/or Spanish.
Results. More than 16% of the adolescents met all symptom criteria for PTSD, and an additional 14.4% met 2 of 3 symptom-cluster criteria. Regression analysis indi-cated no effect of gender, ethnicity, age at interview, organ type, time since transplant, or age at transplant.
Conclusions. As has been found with other life-threatening pediatric conditions, solid organ transplan-tation can precipitate symptoms of posttraumatic stress. Symptoms are not predicted by what would be consid-ered objective factors increasing life threat, suggesting a greater salience of subjective appraisal of threat, as has been seen in studies of childhood cancer survivors. Pe-diatrics2005;115:1640–1644;transplant, psychological im-pact, PTSD, adolescents, Hispanic American.
ABBREVIATIONS. PTSD, posttraumatic stress disorder; UCLA, University of California, Los Angeles; DSM,Diagnostic Statistical Manual; OR, odds ratio.
I
mprovements in immunosuppression and surgi-cal innovations such as use of partial livers have radically changed the prognosis for pediatric solid organ transplant recipients over the past 2 de-cades and led to the creation of transplant centers across the United States. In 2003, the 3-year survival rate ranged from 95% to 97% for pediatric kidneyrecipients, 76% to 80% for liver transplant recipients, and 74% to 79% for heart transplant recipients.1
However, despite the improved survival, pediatric organ transplantation is not without risks and costs, both physical and psychological. The major surgical procedures leave large and permanent scars, and the daily immunosuppressive medications serve as a lifelong reminder of the brush with death.
The threat to life that is inherent in organ trans-plantation has raised the question of whether organ transplantation could be experienced by pediatric recipients as a traumatic event. Before the mid-1990s, it was believed that posttraumatic stress symptoms only occurred in response to extraordinary events such as war, child abuse or molestation, or exposure to natural disaster. However, over the past 10 years, there has been a growing body of literature demon-strating that a small but significant number of chil-dren and adolescents report posttraumatic stress re-sponses to medically life-threatening situations such as cancer and diabetes.2–6
Symptoms of posttraumatic stress disorder (PTSD) are categorized by theDiagnostic and Statistical Man-ual(DSM)of Mental Disorders, Version 4,7in 3
symp-tom clusters: reexperiencing, avoidance, and arousal. Reexperiencing symptoms include recurrent and dis-tressing recollections of the event, repeated distress-ing dreams of the event, actdistress-ing or feeldistress-ing as though the traumatic event were recurring (flashbacks), in-tense psychological distress at exposure to remind-ers, and physiologic reactivity to reminders. Avoid-ance symptoms consist not only of efforts to avoid thoughts or places associated with the traumatic event but also inability to recall important aspects of the event, diminished interest in activities, feelings of detachment from others, restricted range of affect, and a sense of foreshortened future. Increased arousal is characterized by difficulty falling or stay-ing asleep, irritability, difficulty concentratstay-ing, hy-pervigilance, and exaggerated startle response. Clearly, many of these symptoms are seen in other psychiatric conditions. The diagnosis is only made if the individual has (1) experienced, witnessed, or con-fronted an event involving actual or threatened death or serious injury to self or others, (2) reacted to the event with intense fear, helplessness, or horror, (3) experienced at least 1 reexperiencing symptom, 3 avoidance symptoms, and 2 increased arousal symp-toms for ⬎1 month, and (4) the symptoms cause clinically significant distress or functional impair-ment.
From the *Division of Child and Adolescent Psychiatry, Department of Psychiatry and Biobehavioral Science, Neuropsychiatric Institute, Univer-sity of California, Los Angeles, California; and ‡Behavioral Sciences Depart-ment, La Rabida Children’s Hospital, Chicago, Illinois.
Accepted for publication Jan 20, 2005. doi:10.1542/peds.2004-0118 No conflict of interest declared.
Reprint requests to (M.L.S.) 760 Westwood Plaza, UCLA Neuropsychiatric Institute, Los Angeles, CA 90024-1759. E-mail: mstuber@mednet.ucla. edu
To date, there are only 3 published studies that examine traumatic stress symptoms in pediatric or-gan transplant recipients. Two included only liver transplant recipients, and all 3 looked at very small samples. Shemesh et al8reported on a pilot study of
19 pediatric liver transplant recipients referred for nonadherence to medical regimens. Six of 19 patients met criteria for PTSD. Three of these 6 patients (and none of the others) were considered significantly nonadherent by the panel of clinicians. Treatment of the posttraumatic stress symptoms resulted in im-provements in the adherence. Walker et al9studied
18 liver transplant recipients between 7 and 16 years old and found that they reported significantly more symptoms of posttraumatic stress than a comparison group of children who had a chronic life-threatening illness or had undergone a routine surgical opera-tion. Wallace et al10 evaluated 64 renal transplant
recipients, 6 to 21 years of age, with self-report mea-sures and art-based assessments. They found that 36% of the study population had symptoms consis-tent with depression and/or posttraumatic stress.
Studies of adult organ transplant recipients have also suggested that transplantation might be experi-enced as a traumatic event. In a study of 158 adult heart transplant recipients and 142 family caregivers, 10.5% of the recipients and 7.7% of the caregivers met full criteria for PTSD. An additional 5% of the recipients and 11% of the caregivers were considered to be probable cases of PTSD.11
Here we report on the first large investigation to assess symptoms of posttraumatic stress in a nonre-ferred sample of pediatric liver, heart, and kidney transplant recipients. Building on the studies dis-cussed above, the specific objectives of this descrip-tive study were to (1) assess prevalence of self-re-ported PTSD symptoms in adolescent kidney, heart, and liver transplant recipients, (2) compare the prev-alence of PTSD symptoms in liver, heart, and kidney transplant recipients, and (3) examine the relation-ship of specific demographic and medical variables to the severity of PTSD symptoms reported.
Hypotheses to be investigated included the follow-ing:
1. Adolescent organ transplant recipients would re-port a prevalence of posttraumatic stress symp-toms equal to or greater than that reported by adult transplant recipients and other pediatric populations.
2. Severity of posttraumatic stress symptoms would be positively related to the actual risk of mortality. That is, kidney transplant recipients would report fewer symptoms than liver transplant recipients, who would report fewer traumatic stress symp-toms than heart transplant recipients.
3. Adolescents with a more acute onset of organ failure and more complicated medical course (thus, more exposure to traumatic events) would report more posttraumatic stress symptoms than those with chronic conditions and fewer medical complications.
METHODS Inclusion/Exclusion Criteria
The sample comprised adolescents between 12 and 20 years of age who had received a liver, kidney, or heart transplant at University of California, Los Angeles (UCLA) Center for the Health Sciences between 1980 and 1999. Inclusion required that participants be at least 1 year post–initial transplant and be fluent speakers of English and/or Spanish. Adolescents were excluded from participation if they could not understand verbal questions worded at a seventh-grade level or were unavailable to participate in a 1-hour in-person or telephone interview. Although most of the adolescents were continuing to receive their posttransplant medical care from UCLA, this was not a prerequisite of their participation.
Subject Recruitment
A list of 282 patients who conformed to the age and postsur-gical interval criteria was generated from a comprehensive list of all pediatric heart, liver, or kidney transplants performed at UCLA between 1980 and 1999. This list was reviewed by members of the transplant teams, who excluded 53 recipients who had died and 22 who should not be contacted about the study for other reasons (including living in another country, unsuccessful transplant sur-gery, and significant developmental delay or learning disorder). Invitations to participate in the study were mailed to the remain-ing 207 eligible adolescents (and their caregivers, when the poten-tial participants were under the age of 18). Forty-seven adolescents could not be located and were thus considered lost to follow-up. Of the remaining 160 adolescents, 49 refused participation and 111 agreed to participate in the study (69% response rate). Seven subjects had incomplete data sets, yielding a total analyzable sample of 104 adolescents.
Those who indicated their refusal to participate via postcards included with the invitation letter were not contacted again. Transplant recipients who expressed interest in the study and those who had not declined after a 2-week period were contacted by telephone. Trained members of the research team described the study to the adolescent and parent and assessed their interest in participating. In accordance with the UCLA Institutional Review Board, informed consent was obtained from participants ⱖ18 years of age and from parents of participants⬍18; assent was obtained from all participants⬍18 years of age. Adolescents who agreed to participate were interviewed by trained research assis-tants using standardized instruments. Attempts were made to schedule in-person interviews before or after scheduled visits to UCLA outpatient transplant clinics for patient and family conve-nience. When participants did not have an upcoming appoint-ment, telephone interviews were arranged. In those cases, adoles-cents were first mailed the questionnaires in a sealed envelope and instructed not to open them until the time of the interview. Parents were asked not to open the envelopes (which were addressed to the adolescents) and not to listen in while the adolescent was on the phone doing the interview. Both in person and by telephone, the interviewer read a portion of the questions (demographic form and open-ended questions) to the adolescent and recorded the participant’s answers. Adolescents filled out the remaining ques-tionnaires with the assistance of the interviewer when needed. Participants received 2 movie passes as compensation for their time and participation.
Assessment of PTSD Symptoms
The UCLA PTSD Index for the DSM12was completed by each adolescent transplant recipient. The UCLA PTSD Index for the DSM is a well-established, 22-item self-report instrument used to measure symptoms of PTSD in adolescents ages 12–20. The cur-rent version is designed to correspond to the items and symptom clusters used in the diagnostic criteria for PTSD as defined by the DSM.7
Okla-homa City Federal Building,19and pediatric liver transplant.8The reaction index for this study was translated and back-translated by native Mexican Spanish speakers for consistency to the intent of the original wording of the measure. Six of the 104 adolescents preferred to complete the measure in Spanish. These adolescents were interviewed in Spanish by native speakers using the Spanish version of the measure.
The PTSD Index assesses 7 avoidance, 5 hyperarousal, and 5 reexperiencing symptoms. Each item is rated in frequency expe-rienced in the last month: 0 indicates “none”; 1, “a little” (twice a month); 2, “some” (twice a week); 3, “much” (3 times per week); or 4, “most of the time.” Participants who endorsed a minimum of 1 reexperiencing item, 2 avoidance items, and 3 hyperarousal items at a severity level of at least 3 (“much”) per item were classified as “full PTSD likely.” Participants who met criteria for 2 of 3 symptom clusters were classified as “partial PTSD likely.” A continuous measure of severity of each posttraumatic stress symp-tom cluster was obtained by summing severity ratings for each item (0 – 4).
Potential Predictors of PTSD
Demographic variables included gender, ethnicity, age at inter-view, age at transplant (before or after the age of 6), time since transplant, and type of transplant (heart, liver, or kidney). Data for the illness-related variables were collected by chart review. Spe-cific aspects of each child’s transplant and illness-related medical histories were coded into categories based on onset and course. Although the general distinctions among the categories remain consistent across services, slight variations in the definition were permitted to accurately represent the nature of the diseases of each particular organ system. Acute onset was characterized as the sudden onset of life-threatening illness, with time between diag-nosis and transplant typically being brief (⬍3 days for liver,⬍3 months for heart, and immediate need for dialysis for kidney). Chronic onset was characterized by an illness that progresses over time, a condition that may have been present from birth, and a time between diagnosis and transplant of usually⬎1 year.
A chart review was also used to measure severity of the sub-ject’s medical condition over the 2 years before the date of inter-view for this study. The severity rating was mild or moderate to severe and was based on specific factors: (1) number of hospital days; (2) number of intensive care unit days; (3) retransplantation (yes/no); and (4) return to dialysis (yes/no).
Data Analysis
Descriptive data are reported for prevalence of PTSD symp-toms. Univariate analysis of variance was used to examine sever-ity of symptoms as a function of individual demographic and illness-related variables. Binary (full PTSD likely versus none) logistic-regression analysis with backward elimination was used to identify predictors of PTSD status from the potential demo-graphic and illness-related variables. To examine the reliability of variables to predict groups meeting 2 or 3 symptom criteria or none, analyses were repeated with a more liberal criteria (PTSD-symptomatic versus none) and with linear regression for a 3-level outcome: “full PTSD likely” (met all symptom criteria), “partial PTSD likely” (met 2 symptom cluster criteria), or “no symptoms.” Exploratory analyses were also undertaken to examine the rela-tionships between predictor variables and the severity of each symptom cluster.
RESULTS
Adolescents who participated in the study did not differ significantly from those who refused partici-pation on any of the following variables: gender, ethnicity, type of transplant, age at transplant, and current age. Information on severity of medical com-plications and medical diagnosis was not available for those who refused participation because we could not obtain the required consent for medical chart reviews. Sample characteristics are described in Table 1.
Prevalence of Symptoms
Table 2 displays the rates and characteristics of PTSD symptoms. As shown, 30.7% of the sample was PTSD-symptomatic: 16.3% met all symptom criteria for PTSD (full PTSD likely), and an additional 14.4% met 2 of 3 symptom-cluster criteria (partial PTSD likely). Of the total sample, 49% (n⫽51) met criteria for the avoidance symptom cluster, 38.5% (n ⫽ 40) met reexperiencing symptom cluster criteria, and 25% (n⫽26) met the arousal symptom-cluster crite-ria.
Predictors of PTSD
Univariate analysis of variance showed no effect of any demographic or illness-related variable on total symptom severity. Logistic regression analysis with backward elimination was then used to examine a predictor model from all demographic and illness-related variables. One subject was missing medical complication ratings; thus, all regression analyses were based on data from 103 participants. Results indicated no effect of any demographic (gender, eth-nicity, age at interview) or illness-related (organ type, time since transplant, age at transplant) vari-ables except a 2-variable model consisting of illness onset (acute versus chronic) and medical complica-tions in the past year (mild versus moderate/severe).
TABLE 1. Sample Characteristics
N 104
Gender, female, % (n) 41.3 (43) Ethnicity, % (n)
Caucasian 42.3 (44)
Hispanic 34.6 (36)
Black 8.6 (9)
Asian 4.8 (5)
Other 9.6 (10)
Type of transplant, % (n)
Liver 50 (52)
Kidney 37.5 (39)
Heart 12.5 (13)
⬎1 Transplant
Yes 44.2% (46)
Age at interview, y, range; mean (SD) 12.1–20.0; 15.57 (2.1) Time since transplant, y, range; mean
(SD)
1.0–14.5; 7.30 (7.3)
Age at transplant, y, range; mean (SD)
1.2–18.3; 8.34 (4.8)
TABLE 2. Prevalence of Symptoms
Diagnostic Category Met Criteria, % (n)*
Symptom Number, Mean (SD)
Symptom Severity, Mean (SD)
No symptoms 69.2 (72) 4.99 (2.9) 8.97 (5.2)
Partial PTSD likely 14.4 (15) 9.60 (2.4) 22.67 (5.5)
Full PTSD likely 16.3 (17) 11.35 (2.1) 33.11 (6.7)
When in a regression model together, these variables were significant predictors of PTSD status (full PTSD likely versus none). This model also held when re-gressed on symptomatic (full and partial) PTSD com-pared with no symptoms (Table 3). Exploratory anal-ysis of each symptom cluster revealed that although medical complications remained a significant predic-tor of the severity of all 3 symptom clusters, illness onset (acute versus chronic) was only a significant predictor of reexperiencing but not of avoidance or arousal severity.
DISCUSSION
This study of 104 adolescent solid organ transplant recipients confirmed and extended some of the pre-vious findings from pilot studies of posttraumatic stress symptoms in children experiencing medical life threat. Although the majority of the adolescents did not report clinically significant levels of posttrau-matic stress symptoms, a large subset reported symptoms that were frequent and severe enough to be clinically distressing or to cause impairment in function. The number of organ transplant recipients who reported symptoms consistent with a diagnosis of PTSD was, as hypothesized, comparable to those reported by adult heart transplant recipients,11
young adult survivors of childhood cancer,20parents
of childhood cancer survivors,2mothers of pediatric
organ transplant recipients,21and parents of children
with injuries or recently diagnosed diabetes or can-cer.3They were equal to4or significantly higher than
the symptoms reported by childhood cancer survi-vors.6,22 Clearly, despite the excellent prognosis,
these survivors continue to experience intrusive re-minders, hyperarousal, and avoidance consistent with the experience of a traumatic event.
However, contrary to our hypothesis, the type of transplant, with the corresponding difference in prognosis, did not predict the presence of significant PTSD symptoms. That is, although dialysis offers a life-saving alternative for kidney transplant recipi-ents in case of rejection, the kidney transplant recip-ients did not report significantly fewer symptoms in response to the transplant experience than the heart or liver transplant recipients, which seems to reflect the greater salience of subjective appraisal of threat, compared with the “objective data” of statistical re-ports. In fact, it was the adolescents with mild, rather than moderate or severe complications of the trans-plant, who were more likely to report symptoms of posttraumatic stress. These findings are consistent with findings from the study of childhood cancer survivors, in which the majority of the variance was accounted for by the individuals’ trait anxiety and their perception of life threat, not by more objective measures of severity of illness or complications.6
Ad-ditional study is needed to determine if these are also salient elements of the medical experience for pedi-atric transplant recipients.
As hypothesized, adolescents with an acute onset of the illness that precipitated the need for the trans-plant were more likely to report symptoms of post-traumatic stress. This is consistent with clinical ob-servations that previously healthy children with abrupt organ failure experience organ transplants as more intrusive and life changing than those who have organ transplants as a result of congenital or chronic illnesses. In practical terms, children in the acute situation were less healthy and had to take more medications after the transplant than they had in their usual life before the transplant, whereas in the more chronic cases children felt better and took fewer medications after the transplant. Moreover, this difference in response seems to be long-lasting, because this is seen in children who are varied num-bers of months and years posttransplant. Although this finding will have to be replicated, it could be useful in identifying children and families at risk for psychological problems.
There are some obvious limitations to this study. The adolescents studied had received their trans-plants at varying ages and in different years. The specific techniques and immunosuppressant medica-tions used in transplantation changed between 1980 and 1999, and children of different ages understand the experience of the transplant differently depend-ing on their developmental levels. However, it is somewhat surprising that no significant independent impact on outcome was found for the age and time variables, “time since transplant” or “age at time of transplant.”
Another limitation is the lack of a well-established Spanish-language version of the PTSD Reaction In-dex. The version we used was translated and back-translated specifically for this study. It has subse-quently been used by other research groups but has not undergone formal validity testing. However, given the large number of pediatric organ transplant recipients who are primarily Spanish speaking at this center, it seemed important to include them in this study. Larger studies will allow additional explora-tion of language as a variable in PTSD.
The use of hospitalizations, intensive care unit stays, or retransplantation as a proxy for medical complications is a rough approximation and may not be a valid measure of this variable. A study is now ongoing to investigate the utility of this type of as-sessment using prospective data with a larger trans-plant population.
Clinical Implications
Identification of children who have responded to medical procedures such as organ transplantation with posttraumatic stress is not purely of academic interest. There is a growing body of literature that suggests that PTSD can have “a cascading negative effect on children’s development and functioning.”23
A study of 59 traumatized children and adolescents found that there was substantial clinical impairment and distress for both those who met criteria for all 3
TABLE 3. Logistic-Regression Analyses Predicting Full PTSD Likely (n⫽103)
Predictors of PTSD Symptoms  Wald P OR Acute vs chronic onset 1.21 5.30 .02 3.36 Medical complications in the past year* 1.80 4.78 .03 6.08
symptom clusters and those who met the criteria for only 2.24 In a recent study of young adults who are
survivors of childhood cancers, posttraumatic stress was related not only to poor psychological adjust-ment but also to significantly lower function in areas such as school, work, and personal relationships.25
Additional research will be needed to establish the relationship of posttraumatic stress symptoms to ac-ademic and social functioning in organ transplant recipients. However, there are already provocative data to suggest a relationship between nonadherence to medications and posttraumatic stress in pediatric liver transplant recipients.8 Although replication is
needed, this would represent an important insight into a significant clinical problem.
This study demonstrates how difficult it is to pre-dict which child or adolescent will respond to solid organ transplantation with posttraumatic stress symptoms. Studies of childhood cancer suggest that the child’s appraisal of threat to their life bears little or no relationship to the appraisal of prognosis by the physician.6Current clinical efforts are under way
to prevent the development of posttraumatic stress responses in medical settings through “trauma-aware” care, which focuses on decreasing the help-lessness and fear that transforms a stressful proce-dure or event into a traumatic one. Much of this involves education and support for parents, who generally serve as the indicator for children of the degree of danger.6Studies of mothers of bone
mar-row transplant patients and cancer survivors dem-onstrate the consistently higher percentage of moth-ers who report symptoms consistent with a diagnosis of PTSD.2,26As in so much of pediatric care, effective
interventions to treat or prevent PTSD must start with the families.
ACKNOWLEDGMENT
This research is part of a larger study sponsored by a grant from the Maternal and Child Health Bureau (Title V, Social Secu-rity Act), Health Resources and Services Administration, Depart-ment of Health and Human Services (R40 MC00120).
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DOI: 10.1542/peds.2004-0118
2005;115;1640
Pediatrics
Mesrkhani and Dorie Glover
Lisa Libman Mintzer, Margaret L. Stuber, Debra Seacord, Marleen Castaneda, Violet
Traumatic Stress Symptoms in Adolescent Organ Transplant Recipients
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