Psychosomatics 42:337-343, August 2001
© 2001 The Academy of Psychosomatic Medicine
Psychiatric Disorders Before and After Living-Related Transplantation
Isao Fukunishi, M.D.,
Yasutoshi Sugawara, M.D.,
Tadatoshi Takayama, M.D.,
Masatoshi Makuuchi, M.D.,
Hideo Kawarasaki, M.D., and
Owen S. Surman, M.D.
Received November 16, 2001; revised March 2, 2001; accepted March 15, 2001. From the Tokyo Institute of Psychiatry, Tokyo Metropolitan Organization for Medical Research, the Second Department of Surgery, the Department of Pediatric Surgery, Faculty of Medicine, University of Tokyo, Tokyo 156, Japan; and the Massachusetts General Hospital, Harvard Medical School, Boston, MA. Address reprint requests to Dr. Fukunishi, Tokyo Institute of Psychiatry, 2–1–8 Kamikitazawa, Setagaya-ku, Tokyo 156, Japan. E-mail: fukunisi{at}prit.go.jp
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ABSTRACT
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The authors examined psychiatric disorders among two samples of patients who underwent living-related transplant (LRT) for kidney and liver failure. The postoperative prevalence of psychiatric disorders for adult transplant recipients was highest the first 3 months posttransplant. The incidence of psychiatric disorders in the adult recipients with living-related liver transplant (LRLT) was higher (54%, 22 of 41) than that of adult recipients with living-related kidney transplant (LRKT) (28%, 65 of 234). Twelve (80%) of the 15 adult LRLT recipients with adult child-to-parent donors exhibited paradoxical psychiatric syndrome (PPS). Among the 12 affected recipients, guilt-based psychiatric disorders of various types occurred despite successful operative outcome for both donor and recipient. The higher rate of psychiatric disorders among adult LRLT recipients was associated with the occurrence of PPS among recipients of an adult-child allograft. These results signal a new challenge for consultation psychiatrists working with transplant patients.
Key Words: Transplant
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INTRODUCTION
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In both the United States and in Europe the number of living related-liver transplants (LRLT) has been increasing rapidly. The total number of cases of LRLT during the 10 years from 1988 to 1998 was 562 in the United States1 and 1,047 in Europe.2 In 1999 alone, 173 recipients underwent LRLT in the United States. The principal reason for this increase in LRLT is the escalating demand for livers and insufficient availability of organs from brain-dead donors. More patients die while awaiting a cadaveric liver transplant (CLT).
Japan, too, has found an increased demand for CLT and LRLT. Despite this change and the current legality of cadaveric transplantation since 1998, Japanese society has not accepted in practice, the harvesting of organs from brain-dead donors. Patients with liver failure are therefore obliged to depend on LRLT. As in the United States and Europe, LRLT has been carried out mainly in children, but adult-to-adult LRLT is now widely accepted in Japan.
In contrast to LRLT, living-related kidney transplantation (LRKT) is in common practice around the world. Its popular acceptance derives from a briefer operative time and significantly lower morbidity relative to LRLT.
Several psychiatric follow-up studies are available for recipients and donors after transplantation.3–6 To our knowledge, there have to date been no studies of psychiatric findings among recipients and donors who underwent LRLT. On the basis of a 3-year follow-up study, the present study compares the perioperative incidence of psychiatric disorders for two groups of recipients and donors undergoing LRLT and LRKT.
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METHODS
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The subjects consisted of 1) 116 pairs of recipients and donors who underwent LRLT and 2) 325 pairs of recipients and donors who underwent LRKT. On the basis of the recipients' age, these pairs were divided into two sets for comparison: adult LRLT (over age 20) and pediatric LRLT (under age 20); adult LRKT and pediatric LRKT. All the donors for both LRLT and LRKT were over 20 years old. Mean age of recipients and donors was 18.7 (0–65) and 37.0 (20–61) in LRLT and 29.8 (0–62) and 48.4 (20–75) in LRKT, respectively. There were 52 males and 64 females who underwent LRLT and 114 males and 211 females undergoing LRKT.
The cause of liver failure in the subjects were the following: biliary atresia (n=70), primary biliary cirrhosis (n=16), fluminant hepatitis and others (n=4), primary sclerosing cholangitis (n=4), liver cirrhosis associated with hepatitis C virus (n=4), liver cirrhosis associated with liver cancer (n=3), Wilson's disease (n=3), Alagille syndrome (n=2), secondary biliary cirrhosis (n=2), liver cirrhosis associated with hepatitis B virus (n=1), drug-induced liver injury (n=1), familial amylodotic polyneuropathy (n=1), Byler syndrome (n=1), citrullinemia (n=1), and others (n=3).
The cause of renal failure in the subjects were the following: 4 diabetic nephropathy and 321 nondiabetic nephropathy, including chronic glomrulonephritis (n=159), IgA glomrulonephritis (n=55), lupus nephritis (n=23), nephrosclerosis, polycystic kidney, membranous progressive nephropathy, Alport syndrome, hypoplastic kidney, and others.
Donors for patients undergoing transplantation were the recipients' parents (n=80), children (n=15), brothers/sisters (n=7), spouses (n=4), grandparents (n=2), and others (n=8) in LRLT and recipients' parents (n=233), spouses (n=43), brothers/sisters (n=40), grandparents (n=1), and others (n=8) in LRKT.
After obtaining informed consent from each of the pairs, all the recipients were interviewed by a psychiatrist and a psychologist. Interviews were conducted on four occasions: just prior to, 3 months after, 1 year after, and 3 years after transplantation.
Likewise, donors were interviewed by the same psychiatrist and psychologist on two occasions: just before and 1 month after transplantation. In Japan, transplant recipients remain in hospital for 3 months postoperatively vs. 1 month for the donor.
Diagnoses of psychiatric disorders were made based on DSM-IV diagnostic criteria.7 Postoperative outcome data were obtained for liver function, kidney function, allograft rejection, major complications, and length of hospitalization.
Regarding major medical complications, vascular (hepatic arterial thrombosis, portal vein thrombosis, and hepatic venous stenosis) and biliary (bile duct stenosis and bile leakage) complications were seen in 32 (27.6%) of 116 LRLT recipients, and acute and chronic rejection responses were seen in 22 (19.0%) and 1 (0.8%) of 116 LRLT recipients. Eight (6.9%) recipients died. None of 116 LRLT donors exhibited major complications. Regarding LRKT, 38 (11.7%) of 325 recipients exhibited major complications including pulmonary infections and 12 (3.7%) died. None of 325 LRKT donors exhibited major complications.
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RESULTS
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Prevalence Rate of Psychiatric Disorders Pre- and Post-LRT (3-year follow-up)
Table 1 presents the prevalence rates of psychiatric disorders in the recipients at the four time points considered; just before LRT, 3 months after LRT, 1 year after LRT, and 3 years after LRT and in their donors at the two time points considered; just before LRT and 1 month after LRT. Table 2 shows the DSM-IV diagnoses for the recipients and their donors.
Comparisons of Prevalence Rate of Psychiatric Disorders Between Adult and Pediatric Transplantation (LRLT and LRKT)
Adult vs. Pediatric LRLT. Among the recipients, the prevalence rates of psychiatric disorders were significantly higher for adult recipients than for pediatric recipients at the four evaluation times considered, just before LRLT (df=1,  2=8.3, P=0.004), 3 months after LRLT (df=1, 2=42.0, P=0.00001),and 1 year after LRLT (df=1, 2=5.6, P=0.02).
For donors, the prevalence rates of psychiatric disorders were significantly higher for donors for adult recipients than for donors for pediatric recipients only in the evaluation performed 1 month after LRLT (df=1, 2=7.6, P=0.006).
Adult vs. Pediatric LRKT. For recipients, the prevalence rates of psychiatric disorders were significantly higher for adult recipients than for pediatric recipients only 3 months after LRLT (df=1, 2=26.2, P=0.00001).
For donors, there were no significant differences in the prevalence rates of psychiatric disorders between donors for adult recipients and donors for pediatric recipients who underwent LRKT.
Comparisons of Prevalence Rate of Psychiatric Disorders Between LRLT and LRKT
Adult LRLT vs. Adult LRKT. For the recipients, the prevalence rates of psychiatric disorders were significantly higher for adult LRLT recipients than for adult LRKT recipients at the two times studied, just before transplant (df=1, 2=5.9, P=0.01) and 3 months after transplant (df=1, 2=10.8, P=0.001). When we compared the prevalence rate of psychiatric disorders again after the exclusion of recipients with pre- and postoperative delirium, the above two significant differences were eliminated. During the 3-month period after transplant, however, the prevalence rates of psychiatric disorders were still significantly higher for adult LRLT recipients than for adult LRKT recipients [15 (36.6%) of 41 adult LRLT recipients and 47 (20.1%) of 234 adult LRKT recipients; df=1, 2=5.4, P=0.02]. On the contrary, just before transplant, the prevalence rates of psychiatric disorders were still higher for adult LRKT recipients than for adult LRLT recipients [0 of 39 adult LRLT recipients and 5 (2.1%) of 234 adult LRKT recipients] although the differences did not reach statistical significance (df=1, 2=0.8, P=0.36).
For the donors, the prevalence rates of psychiatric disorders were significantly higher for donors for adult recipients who underwent LRLT than for donors for adult recipients who underwent LRKT only at the evaluation 1 month after transplant (df=1, 2=13.0, P=0.0003).
Pediatric LRLT vs. Pediatric LRKT. For the recipients, there were no significant differences in the prevalence rates of psychiatric disorders between pediatric recipients who underwent LRLT and pediatric recipients who underwent LRKT.
For the donors also, there were no significant differences of the prevalence rates of psychiatric disorders between donors for pediatric recipients who underwent LRLT and donors for pediatric recipients who underwent LRKT.
Comparison of Prevalence Rates of Psychiatric Disorders Between Recipients and Their Donors
There was no significant difference in the prevalence rates of psychiatric disorders between adult recipients and their donors who underwent LRLT. As for adult recipients and donors who underwent LRKT, pediatric recipients and donors who underwent LRLT, and pediatric recipients and donors who underwent LRKT, the same results were obtained and no significant differences were revealed.
After transplant, we could not directly compare the prevalence rates of psychiatric disorders between recipients and their donors because the time when psychiatric interviews were administered were different (3 months after transplant in recipients and 1 month after transplant in donors).
Comparison of Prevalence Rate of Psychiatric Disorders Among Just-Before, 3-Month, 1-Year, and 3-Year After Transplant in Recipients
In adult recipients who underwent LRLT, the prevalence rate of psychiatric disorders 3 months after LRLT was the highest of all four time periods considered. In adult recipients who underwent LRKT, the prevalence rate of psychiatric disorders was highest 3 months after LRKT.
In pediatric LRLT and LRKT, all prevalence rates were less than 5% and no significant differences were found.
Relationship Between Postoperative Medical Dataand Psychiatric Disorders
There were no significant relationships of psychiatric disorders to postoperative medical data (liver function, kidney function, allograft rejection, major complications, and length of hospitalization).
Paradoxical Psychiatric Syndrome (PPS)
Among the 22 of 41 (54%) adult LRLT recipients and 65 of 234 (28%) adult LRKT recipients with psychiatric disorders, PPS was seen in 14 (34%) and 12 (5%), respectively.
Among the 41 adult-to-adult LRLT cases, 15 donors were adult children (10 sons, 5 daughters) of the recipient. Twelve (80%) of 15 exhibited PPS. (We will refer to these cases as Adult Child-to-Adult LRLT) There were no such adult child-to-adult cases among the LRKT cases.
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DISCUSSION
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Consultation liaison psychiatrists have reported on the incidence of psychiatric disorders among donors and recipients undergoing organ transplantation. However to our knowledge there are no reported data on the incidence of psychiatric disorders for those undergoing LRLT. We investigated the incidence of psychiatric disorders in living-related transplantation and focused on the following four variables: 1) recipient age (adult, over age 20; pediatric, under age 20), 2) transplanted organ (LRLT or LRKT), 3) recipient or donor status, and 4) time course (pre- or posttransplantation).
The highest incidence of psychiatric disorders occurred among adult LRT recipients during the 3-month period after transplantation. This finding was evident in both adult LRLT and adult LRKT. Psychiatric disorders were most prevalent among the adult LRLT recipients (54% of cases). One reason for this observed high prevalence rate is that postoperative delirium tends to be manifested in the recipients more frequently just after LRT. After the exclusion of cases with postoperative delirium, we recalculated the prevalence rate of psychiatric disorders 3 months after transplantation. As a result, the prevalence rate was approximately 37% in adult LRLT recipients and 20% in adult LRKT recipients. In both, total prevalence rate and prevalence rate (exclusion cases with postoperative delirium) 3 months after transplantation, we found that there were significant differences of the prevalence rate between adult LRLT and LRKT recipients. This result suggests that significant differences of the prevalence rate between adult LRLT and LRKT recipients are not related to the presence or absence of postoperative delirium.
As shown in Table 2, psychiatric disorders other than delirium were 1) mood disorders, especially major depression and dysthymic disorder; 2) adjustment disorders; 3) somatoform disorder, for example somatization disorder; 4) anxiety disorders, most notably, posttraumatic stress disorder; and 5) brief psychotic disorder unassociated with immunosuppressant toxicity. C-L psychiatrists have been especially observant about toxic psychosis from immunosuppressant medications.8–11 Our research leads us to focus more on psychodynamic features of the LRLT experience.
Recently we encountered recipients and donors with psychiatric disorders manifested in a paradoxical form that occurs despite successful transplantation, without tissue rejection or other medical complication.12–15 We called this disorder paradoxical psychiatric syndrome (PPS). Prior studies12–14 have demonstrated that this syndrome is frequently seen in adult recipients, especially those receiving LRT. These recipients had strong guilt feelings toward their donors, and they could not verbalize their inner feelings.12–14 They tended to display avoidant coping behaviors and to suppress their conflicts. PPS symptoms are seen not only in recipients but can also be seen in the donors of LRT.15 Manifestations of PPS include major depression, somatization disorder, adjustment disorder, and conversion disorder.12–15
The word syndrome implies a cluster of symptoms. By PPS we refer to mixed psychiatric symptomatology associated with prominent conflicts (e.g., guilt regarding the risk taken by the donor).
Diagnostic criteria for PPS consists of the following four elements. When all four elements exist, psychiatric symptoms were judged as PPS.
- Prominent conflicts associated with transplantation (for example, guilt regarding the donor's welfare)
- Situational reaction such as depression, anxiety, conversion, somatization, and adjustment disorder, and/or psychosis.
- The reaction occurs as a late complication after liver transplantation (within the first year after transplant).
- Favorable medical status of donor and recipient, without tissue rejection or other major medical complication.
In the present study, 22 (54%) of 41 adult LRLT recipients and 65 (28%) of 234 adult LRKT recipients exhibited psychiatric disorders. After excluding instances of delirium and toxic psychosis, the incidence of psychiatric disorders was 14 (34%) in adult LRLT recipients and 44 (19%) in adult LRKT recipients. Among these, PPS was seen in 14 (34%) of the adult LRLT recipients and 12 (5%) of the adult LRKT recipients.
Fifteen adult LRLT recipients received an adult child-to-parent partial liver allograft. There was no parallel occurrence among those undergoing LRKT. Of the 14 adult LRLT recipients who experienced PPS, 12 had an adult child donor. The remaining two recipients had a spousal and a sibling donor. Of the 15 adults who had an adult-to-child donor, 12 (80%) exhibited PPS. Thus, adult partial liver recipients tend to exhibit PPS in the 3 months after transplantation. This result suggests that a higher rate of psychiatric disorders among adult LRLT recipients was associated with the occurrence of PPS among recipients of an adult-to-child allograft.
Among pediatric recipients, the incidence of psychiatric disorders was relatively low. Previous reports have shown that school maladjustment sometimes occurs after LRKT transplant in children.16 In the present study, data on school maladjustment were limited because we did not obtain school records or teacher interviews.
For donors, incidence of psychiatric disorders including major depression and somatization was less than 10%. It was difficult to predict adverse psychological outcome among donors even after careful preoperative psychiatric assessment.
Several methodological limitations of this study should be noted. First, because postoperative delirium may depend on somatic conditions after transplant, we cannot draw a definite conclusion from comparisons of the incidence rate of psychiatric disorders, including cognitive disorders such as delirium. Second, there is no literature on the reliability and validity of the diagnosis of PPS, although several studies have documented the clinical characteristics of PPS.12–15 Third, the concept of PPS was introduced in Japan, and the prevalence and incidence rate of PPS in a sample of American recipients and donors who have undergone LRT should be examined to rule out PPS as a culture-bound syndrome.
In summary, we found a relatively high incidence of postoperative psychiatric disorders among recipients who underwent LRLT. Most notable was the occurrence of PPS with a varied presentation of guilt-driven symptomatology despite satisfactory surgical outcome for both donor and recipient. This was particularly likely to occur when the donor was an adult child of the recipient. Postoperative PPS occurred in half of the cases in this category. We alert consultation psychiatrists to the risk of postoperative psychiatric disorder particularly in the 3 months after adult child-to-adult LRLT.
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ABSTRACT
INTRODUCTION
