Objectives: This study sought to investigate immuno-suppressive medication adherence, therapeutic adherence, school performance, symptom exper-iences, and depression levels of patients having undergone liver transplant during childhood.

Materials and Methods: We performed a retro-spective, cross-sectional, case-controlled study to compare the depression levels of subjects with those of their healthy peers. Data were collected between June 23, 2014, and July 10, 2014 from 0- to 18-year-old patients having undergone a liver transplant between 1996 and 2014 (n = 27; the participant’s mean age, 17.59 y [SD = 4.29, min-max = 8-28 y]). The mean score for the immunosuppressant therapy adherence was 11.18.

To collect the data, the Demographic and Clinical Characteristics Form, Immunosuppressant Therapy Adherence Scale, Therapeutic Regimen Adherence Assessment Questionnaire, School Performance Assessment Questionnaire, Modified Transplant Symptom Occurrence and Symptom Distress Scale-58, and Beck Depression Inventory were used. To analyze the data, descriptive statistics (frequencies, mean, and standard deviation), Mann-Whitney U test, and ridit scoring were used.

Results: While the rate of adherence with clinical appointments was 55.5%, it was 33.3% with the diet (prescribed regime) and 44.4% with exercise. While 33.3% of the participants repeated a grade or were held back, 44.4% of them missed more than 20 school days. Of the symptoms, the recipients mostly experienced anxiety, restlessness, nervousness, fatigue, and difficulty in concentrating. The patients’ mean depression score was 7.77 when they were compared to their healthy peers, the difference was not statistically significant (P > .05).

Conclusions: In our study, the recipients' adherence with immunosuppressive therapy and clinical appointment was high. This study will provide data for the literature about pediatric liver transplant recipients’ adherence with diet and exercise, and physiological and psychological symptoms such as fatigue and anxiety.

Key words : Pediatric liver transplant, Nonadherence, School performance, Depression

Introduction

It is important to appropriately manage pediatric organ transplant recipients’ transition to adulthood, and to ensure their compliance with treatment. Adolescence is a transition between childhood and adulthood, from 11 to 21 years of age.¹ Adolescent organ transplant recipients have difficult experiences (eg, life risk related to organ disease, major complications related to organ transplant, frequent hospital visits, and complex drug using).^2,3 Studies conducted on the focus on health status (survival, rejection, and laboratory results) of children and adolescents having undergone organ transplant and their compliance with immunosuppressive therapy. The family, medical team, and social environment, take an important role in supporting physical and psychosocial compliance of patients who have undergone a liver transplant during childhood. Nurse members of a medical team should provide training and consultancy for the young patient, so that he can manage his health and postliver transplant compliance in the future.⁴

Posttransplant adherence includes taking medication regularly, having regular follow-ups and making lifestyle changes regarding high-risk behaviors (eg, smoking and alcohol consumption).⁵ Medication nonadherence in transplant patients is defined as taking a wrong drug or not taking the medicine at least once a month. Medication nonadherence is also defined as taking medication 2 or 2.5 times later than the time schedule at least once a month.⁶ Medication nonadherence is reported to be the most important cause of graft loss in adolescent transplant patients.^2,7,8 In their meta-analysis, Dew and associates⁹ investigated medical regimen adherence in pediatric organ transplant patients (0-18 y) and reported that studies generally cross-sectional. They also reported that of the 18 studies investigating liver transplant recipients’ (LTR) compliance, only 1 was conducted in Asia, 3 in Europe, and the other 14 in the United States. It has been emphasized that there are no studies on pediatric LTRs’ diet and exercise, and that there is only 1 study on the use of illicit drugs. Low socioeconomic status, separated parents, psychiatric disorders in the child, insufficient family support, and the increasing age of the child have been reported to increase nonadherence to the medical regimen.⁹ It also has been emphasized that young age is a risk factor for graft loss.² It is reported that appropriate age for adolescent patients to start taking their medication on their own is about 12 years.⁸ In the literature, it has been reported that 45% of the adolescent LTRs have their follow-ups regularly, and that living with an elderly parent or with a single parent adversely affects patients’ clinical compliance.¹⁰

Among the important issues of pediatric liver transplant recipients are difficulty in continuing their education and maintaining their school performance. In several studies, it has been indicated that recipients’ school performance are adversely affected because of an increase in absenteeism, grade repetition, hyperactivity, and learning disorders after undergoing a liver transplant.^11-13

In studies conducted to investigate pediatric patients having undergone liver transplant in Turkey, the most common indications observed in these patients are biliary atresia, Wilson's disease, cryptogenic liver disease, and familial intrahepatic cholestasis. It also has been reported that most of these children (80%-85%) underwent a living-donor liver transplant, and the most common complications they had were bile complications (eg, biliary leak, biliary atresia), infection, portal vein thrombosis, and hepatic artery thrombosis.^14-19 According to the results of several studies, in pediatric patients after a liver transplant, the mortality rate is 43.2%14; 1-year and 5-year survival rates were 89.3% and 83.5%,¹⁹ and acute rejection incidence was 39.3%.¹⁴ In addition, the growth of children was affected negatively after transplant.²⁰

In the literature, there are few studies on issues including psychosocial evaluations such as patients’ adherence to treatment, and symptoms and the level of depression they endure.^8-10 We should evaluate pediatric and adolescent patients from a psychosocial perspective because of its long-term effects on transplant results (eg, graft survival and morbidity).^2,21 In studies conducted in Turkey, the medical results of the patients have only been analyzed.^14-19 We have not been able to find studies in the literature investigating psychosocial factors (eg, patients’ adherence to medication, therapeutic adherence, school performance, symptom exper-iences, and depression level).

This study sought to comprehensively assess adherence to immunosuppressive medication and treatment, and school performance, symptom experience, and depression level after childhood liver transplant.

The research questions for patients having undergone pediatric liver transplant are as follows:

1. How do they adhere to their immunosuppressive medication regimen?
2. How do they adhere to their treatment (clinical appointment adherence, smoking, illicit drug use, alcohol consumption, dietary adherence and exercise adherence)?
3. How is their school performance (grade repetition, being held back in school, adversely affected school life, increase in school absence, and the number of days of absence per year)?
4. What is the level of symptom occurrence and symptom distress associated with adverse events of traditional and novel immunosuppressive drugs?
5. What is their level of depression, and is there a difference between them and their healthy counterparts of similar age and gender in terms of depression levels?

Materials and Methods

Design and setting
We performed a retrospective, cross-sectional, case-controlled study to compare the depression levels of pediatric liver transplant recipients with those of their healthy peers. We used self-report and parent-report by assessments to determine the outcomes of the study.

Sample
In the liver transplant unit where the study was performed, 43 patients aged between 0 and 18 years underwent a liver transplant between 1996 and 2014. Of these patients, 30 survived and are followed in the liver transplant outpatient clinic. The participation rate of the study was 90%, because 1 patient did not want to participate in the study and 2 patients could not be reached. The remaining 27 liver transplant patients comprised the study sample. The study protocol was approved by the University Non-Invasive Clinical Research Ethical Committee and was conducted in accordance with the Declaration of Helsinki. Written informed consent was obtained from all subjects or their parents. The purpose sample included those who (1) underwent a pediatric liver transplant (0-18 y); (2) could understand and write in Turkish. Those who (1) were mentally retarded, (2) were retransplanted or were on the retransplant waiting list, (3) were too ill to assess (eg, hospitalized for a serious condition) were excluded from the study.

Evaluation
To collect the data, the Demographic and Clinical Characteristics Form, Immunosuppressant Therapy Adherence Scale, Therapeutic Regimen Adherence Assessment Questionnaire, School Performance Assessment Questionnaire, the Modified Transplant Symptom Occurrence and Symptom Distress Scale – 58, and the Beck Depression Inventory were used.

Demographic and clinical characteristics form
The form consisted of 11 questions and was developed by the investigators of this study. It included questions about demographic data (age, gender, marital status, education level, occupation, living situation [with both parents, alternating with mother and father, with mother alone, with father alone]) and clinical data (liver disease cause, donor type, living donor relation, transplant time, and immunosuppressive therapy). Data on sociodemo-graphic characteristics were obtained from the patients and their relatives, and the clinical data were obtained from their medical records.

Immunosuppressant therapy adherence scale
The Immunosuppressant Therapy Adherence Scale (ITAS) is the first and only valid, reliable, and accessible scale developed in the United States in 2005 by Chisholm and associates to assess Immunosuppressant Therapy (IST) adherence of patients having undergone organ transplant.²² While the factor analysis of the original ITAS was performed with combined and nomological validity methods, its reliability was tested with the Cronbach's alpha reliability coefficient and item-total score correlations. After the analysis was complete, the analysis revealed the scale was reliable and valid.²² Turkish reliability and validity study of the scale was conducted by Bayhan and Karayurt (personal communication). The validity of the Turkish version of the scale was established using language, content, structure, and combined validity methods, and its reliability was tested with internal consistency reliability coefficients and item analysis. The analysis of the scale showed that the scale was a reliable and valid measurement tool (personal communication).

The ITAS includes 4 items that question and organ transplant patients’ adherence to immuno-suppressant therapy in 3 months preceding administration of the questionnaire. The items of the scale are rated on a 4-point Likert-type scale. The frequency of failing in adherence is scored from 3 to 1. Three points refers to 0% nonadherence, 2 points to 0% to 20%, 1 point to 21% to 50%, and 0 points to > 50%. Scores obtained from each item are summed and then IST adherence is assessed. The possible scores from the scale ranged from 0 to 12. Higher scores indicate higher adherence rates.²²

School performance assessment questionnaire
The questionnaire which comprises 5 questions was developed by the researchers through a literature review to assess school performance.^11-13 The questions are as follows: class repetition (yes/no, if yes, which year), being held back (yes/no, if yes, how many years), adversely affected school life (yes/no), an increase in absence (yes/no), and the number of days absent per year.

Therapeutic regimen assessment questionnaire
Because of the lack of instruments to assess adherence to the therapeutic regimen, the question-naire was developed by investigators to assess therapeutic adherence status of participants.^7,9,10 The questionnaire included 6 questions: (adherence/-nonadherence), smoking (yes/no; the number of cigarettes a day), illicit drug use (yes/no; frequency), alcohol consumption (yes/no; amount; frequency), dietary adherence (5 answering categories ranging from never following my diet, to following it every day), and exercise adherence (5 answering categories ranging from never to daily).

Modified transplant symptom occurrence and symptom distress scale – 58-MTSOSD-58.
The validity of the Modified Transplant Symptom Occurrence and Symptom Distress Scale (MTSOSD-59) was well established in Dobbels study.²³ The MTSOSD-59 included 59 items related to symptoms associated with the adverse events of traditional and novel immunosuppressive drugs and assesses the patient’s appraisal of symptoms associated with the adverse events of immunosuppressive drugs. Turkish validity and reliability study of MTSOSD-59 was performed by Ordin and associates in 2013.²⁴ Content validity was evaluated using the Content validity index (Content validity index = 1.0). After the content validity of the Turkish version of the instrument was established, it was called MTSOSD-58 because it included 58 items. The Turkish version of the scale was found to have a good construct validity. The reliability of the scale was tested with the split half method and was found to be good in symptom occurrence (0.919) and symptom distress (0.920) dimensions.²⁴ We determined the most frequently occurring and most distressing adverse effects using ridit analysis.

Each symptom of the scale is scored in view of symptom occurrence (SO) and symptom distress (SD). Symptom occurrence is assessed on a 5-point rating scale ranging from 0 (never occurring) to 4 (always occurring), and symptom distress is also assessed on a 5-point rating scale ranging from 0 (not at all distressing) to 4 (extremely distressing).^23,24

Beck depression inventory
Beck Depression Inventory (BDI) was developed by Beck in 1961,²⁵ and is a reliable and valid instrument used in diverse populations, including transplant recipients.²⁴ The Beck Depression Inventory was adapted into Turkish in 1998 by Hisli²⁶ and shown to have acceptable reliability and validity. A score of 17 or higher is suggestive of the presence of a depressive disorder. In our study, Cronbach α coefficients were 0.90 for the healthy control participants and 0.89 for the transplant recipients, indicating excellent reliability.

We used the Beck Depression Inventory, a 21-item self-report scale, to assess presence and severity of depressive symptoms. Each item is scored on a 4-point scale ranging from 0 (absent) to 3 (severe). The total score ranges from 0 to 63. Higher scores indicate more severe depression.²⁵

Data collection
Between June 23 and July 10, 2014, all eligible patients were contacted by phone before a scheduled outpatient clinic visit. Data were collected using the face-to-face and telephone interview techniques. In a silent and separate room of the outpatient clinic, the researcher explained the study to the patient and the parent(s) together, and asked for informed consent from both parties. Total time needed to complete all the questionnaires ranged from 25 to 40 minutes, depending on the age and intellectual capacity of the patient or the parent(s). The data also were collected from the families of patients who were under the age of 18. The data also were collected from healthy LTRs of similar age and gender to make comparisons. Healthy subjects completed the Beck Depression Inventory scale too.

Data analyses
Statistical analyses were performed with SPSS software (SPSS: An IBM Company, version 16.0, IBM Corporation, Armonk, NY, USA). Descriptive statistics (frequencies, mean, and standard deviation) are presented as appropriate for all of the measurements described. The patients’ BDI scores were compared to those of healthy peers using the Mann-Whitney U test.

For the MTSOSD-58, the ridit analysis was used. A ridit analysis represents the relative probability to an identified distribution. The use of ridits implies the selection of a reference distribution and so the ridit of a (sub)sample will always be compared with the ridit of a chosen reference group. The reference group was determined by calculating the frequency distribution across all items and patients. The frequency distribution of all patients within 1 item was compared to this overall frequency distribution. A ridit, ranging from 0 to 1, was obtained. This method was used to determine the most frequently occurring and the most distressing adverse events.^27,28

Results

The mean age of the participants was 17.59 (SD = 4.29, min-max = 8-28 y). Of the patients, 77.7% (n = 21) were adolescents (11-21 y). The mean age for undergoing liver transplant was 10.4 years (SD = 4.44, min-max = 1-17 y). Mean time after transplant was 7.5 years (SD = 3.73, min-max = 3-17 y). Of the patients, 88.9% (n = 24) lived with their families; while 44.4% of the patients and their families had an income lower than their expenses and 55.6% of them had an income equal to their expenses. Other demographic and clinical characteristics are presented in Table 1. Because 13 of the patients participating in the study were ≤ 18 years old, the interviews were held with their parents (10 mothers, 3 fathers). The mean age of the parents was 40.62 years (SD = 6.29, min-max = 30-51 y). Of the parents, 53.84% were not to work and 84.62% were primary school graduates.

Immunosuppressant therapy adherence
The mean age of the patients for taking medication on their own was 13.25 years (SD = 1.88, min-max = 10-18 y). Patients took a mean number of 1.55 tablets (SD = 0.64) a day, usually at 2 different times for immunosuppression or comorbid conditions. The maximum possible scores from the ITAS and each subscale were 12 and 3. In our study, the mean total score obtained from the ITAS was 11.18 (SD = 1.18, min-max = 8-12) and the mean score for the frequency of forgetting to take medication (item 1) was 2.81 (SD = 0.48, n = 4). The mean score for the frequency of taking medication later than scheduled time (item 2) was 2.37 (SD = 0.88, n = 12). The patients stated that they never quit taking medicine because of adverse effects (item 3) or external factors (eg, health reports, pharmacy) (item 4) (mean = 3.00, SD = .00).

Therapeutic regimen adherence
Of the sample, 15 complied (55.55%) with clinical controls regularly, 3 (11.11% [a 15-year-old girl, a 21-year-old man, and a 22-year-old man]) smoked cigarettes (10 cigarettes a day), 1 drank alcohol (3.70%) (a 15-year-old girl, usually beer, and less than once a month). None of the participants took illicit drugs. While 9 of the patients (33.33%) complied with their diet plan, 12 exercised regularly (44.44%).

School performance
Approximately, 9 of the participants (33.33%) had either repeated a grade or had been held back at least 1 school year, with 55.5 currently in primary school grade (0%). Absences from school increased in 22 of the sample after transplant (81.48%), and 12 of them missed more than 20 school days (44.4%). One of the recipients dropped out of school because of infection risk and continued his education through distance education. Another recipient repeated the same grade twice, because of increased absences and thus dropped out of school.

Symptom experience
Based on the ridit analysis, the most frequently occurring and most distressing adverse effect from the patient’s point of view is shown in Figure 1. The 3 symptoms experienced by the patients most were anxiety, restlessness, and nervousness for symptom occurrence, and fatigue, symptom distress, and difficulty in concentrating for symptom distress.

Depression
Mean depression score of liver transplant recipients on the BDI was 7.77 (SD = 6.81, min-max = 0-18), with 24 of the patients (88.81%) showing no depressive symptoms; and 3 of the patients (11.12%) experiencing depressive symptoms. The mean BDI scores of the healthy LTRs having age and gender distribution similar to that of the case group LTRs was 7.42 (SD = 5.64, min-max = 0-20) (P > .05). The com-parison revealed that there was no significant difference between the 2 groups (U = 347.500; P = .950).

Discussion

The mean age of the patients for taking medication on their own was 13.25 years in our study, it was 12 years in a study conducted in the United States.⁸ This difference may be due to the fact that the mean age of the participants was higher in our study, and that parents in Turkish society display protective behaviors more and thus do not want share medicine-taking responsibility with their children. In this study, patients’ adherence to immunosuppressant treatment was high, and nonadherence was due to forgetting to take medication or taking medication later than the scheduled time. (Similar to our study, the IST) adherence rate (87.1%) in Dew and associates’⁹ meta-analysis was high (ITAS mean, 11)¹⁸. “Imuno-suppressant thereapy” adherence is important in terms of prolongation of graft survival time, and reduction in morbidity and rejection.²⁹ In the literature, it is recommended that patients' self-report assessment of IST adherence should be performed in conjunction with clinical assessments.⁹ The IST adherence scale used in our study is a valid and reliable measurement tool, and is implemented quite easily in clinical settings. Thus, it is recommended that it should be routinely implemented in conjunction with clinical records to objectively assess patients’ IST adherence.

While more than half of the patients had their controls regularly in our study, the rate was 45% in Berquist and associates’ study.¹⁰

While more than half of the patients had to come regularly their clinical follow-ups in our study, the rate was 45% in Berquist and associates’ study.¹⁰

In a meta-analysis, the highest rate of nonadherence to clinical controls was observed among LTRs.⁹ It is reported that regular clinical follow-ups reduce the possibility of rejection, and the frequency and duration of hospitalizations.²⁹ In the literature, while the tobacco use rate was determined as 0.7% in pediatric liver, kidney, heart, and lung transplant patients, the alcohol and illicit drug use rate was 0.6%.⁹ The high tobacco use rate in this present study can be explained by the high proportion of adolescents in the study sample (78%).

Smoking poses a cancer risk to LTRs.³⁰ Detailed questioning of smoking habit in adolescent LTRs and providing them with training and counseling about the hazards of smoking by nurses and other health professionals are important in terms of reducing morbidity and mortality.³⁰ Approximately half of the patients in our study exercised regularly, and one-third of them complied with their diet plan. In the literature, the rate of diet and exercise adherence among pediatric kidney, heart, and lung transplant patients was reported to be 94.6%.⁹ Conversely, we have not found any study results on liver transplant patients. All LTRs are at risk of deterioration in glucose metabolism, increased serum lipid levels, high blood pressure, deterioration of renal functions, and cancer due to the immunosuppressive drugs they have to take.² Diet and exercise are important in reducing these problems in pediatric and adolescent organ transplant recipients with a long life expectancy. Therefore, it is recommended that patients' adherence to diet/exercise programs should be assessed through the self-report method, and that they should be informed about the issue. In the literature, it is suggested that interventions in modifiable risk factors (eg, the psychological state should be performed to enhance therapeutic adherence of pediatric recipients aged between 0 and 18 y).⁹

In the literature, it has been noted that pediatric LTRs’ school performance is affected most by the adverse effects of the posttransplant period.^12,29 In 2 studies conducted in the United States and Canada, the rate of grade repetition and being held back in school in pediatric LTRs with 5-year survival was determined as 18%, and the rate for being absent from school for more than 20 days was 17%¹¹ whereas the rates in pediatric LTRs with 10-year survival were 20% and 10%.¹² In another study, the grade repetition rate in pediatric LTRs was 20%, and the rate of those who missed more than 20 school days was 18%.¹³ In our study, the grade repetition rate among LTRs was higher than in aforementioned studies, and nearly half of the patients were determined to be absent from school for more than 20 days.

One of the factors leading to adversely affected school performance is the fear of infection risk. Another one is fatigue. In Turkey, recipients usually have fatigue because the majority of liver transplant centers are located in major cities, and thus posttransplant patients and their families have to make long-distance trips because of frequent follow-up visits, which leads to fatigue in recipients. In our sample, primary school students’ repeating a grade or being held back could be due the fact that they experienced these problems of early posttransplant period more. Similar to our study, Gilmour and associates13 reported that absenteeism was more common during the first 18 months posttransplant. Immunosuppressive medication use after a liver transplant, the presence of cytomegalovirus infections, and the severity of liver disease before transplant affect children's cognitive functions.^2,13 In our sample, 48 of the patients (15%) underwent transplant because of metabolic diseases (7 primary hyperoxaluria, 4 Wilson’s disease, 1 of tyrosinemia, 1 Crigler–Najjar type 1). According to the results of another study, cognitive structure and intelligence level (IQ < 70) of children having undergone a liver transplant were lower than were those of healthy children. The same study also determined that the neurologic status of children who underwent a liver transplant because of a genetic metabolic disorder was even worse.³¹ Therefore, some liver transplant patients should continue their education in special education centers. Health professionals should evaluate recipients who repeat a grade, have excessive absences or drop out of school in terms of their special education needs and should refer them to special education centers.

There is a gap in the literature related to the symptoms of pediatric and adolescent LTRs. In a study of adolescent kidney transplant patients (median age, 15 y), the most prevalent symptoms were increased appetite, fatigue, headache, pimples, trembling hands, increased thirst, lack of energy, mood swings, flatulence, and warts on the hands or feet.⁷ That these symptoms were different from the symptoms observed in our patients can be explained by the use of different immunosuppressants in the liver transplant. In our study, the patients experienced all the psychological symptoms included in the MTSOSD-58. The presence of many psychological symptoms in our study is probably because of the fact that most patients were adolescents. Determination, prevention, and appropriate management of these symptoms can enhance adherence to IST.

Psychological state and depression level of pediatric and adolescent organ transplant patients are important factors affecting their compliance with medical regimen.^1,9,32 Our search for studies investigating the depression level in liver transplant patients after transplant demonstrated a gap in the literature. On the other hand, a study of kidney transplant patients demonstrated no depression in 82.6% of the patients,⁷ which is similar to the rate (88%) determined in this present study. That there was no difference between the depression level of the case group patients and that of their healthy peers is a positive outcome. This outcome of the present study provides new data to the literature.

Limitations
The study was conducted with a small sample in only 1 center is its limitation. In addition, because the study has a retrospective, cross-sectional design, it is subject to the limitations of this design.

Conclusions

This present study provides new data to the literature about pediatric patients’ posttransplant compliance with diet and exercise, symptom experiences, and depression levels. The participants’ adherence to IST and clinical appointments was found to be high. The participants’ school performance was excessively affected, especially during the early posttransplant period. Nurses specialized in transplant play an important part in the psychosocial assessment of patients and providing support for them. In Turkey, where the number of organ transplant centers and patients is on the increase, there is a need to train certified nurses specialized in the field of transplant and to employ them in these centers. It is recommended risk factors affecting study variables be investigated in larger samples with longitudinal prospective studies in the future.

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