3. TABLE 1 Variations of Outcome According to Age at Kasai Operation in Reported Series
Age Threshold, Effect Follow-up and End No. of Origin of Study Year Study
Points Patients
Ͻ30 d, unfavorable Age at LT 92 St Louis Children’s Hospital (US) 2001 17
Ͻ30 d, favorable 4-y SNL 349 Multicenter study (Canada) 2007 16
Ͻ46 d, favorable 10-y SNL and 10-y OS 164 University Hospital Kremlin-Bicetre, Paris (France)
ˆ 1997 32
5-and 10-y SNL 472 Multicenter study (France) 1999 6
5-y and 10-y OS
4-y SNL 252 Multicenter study (France) 2006 11
Ͻ8 wk, favorable Clearance of jaundice 159 Chulalongkorn University, Bangkok (Thailand) 2005 33
Clearance of jaundice 50 King’s College, London (United Kingdom) 1989 34
Ͻ60 d, favorable 5-y and 10-y SNL 141 National Taiwan University Hospital, Taipei (Taiwan) 2006 35
5-y OS (ϭSNL) 904 Multicenter study (US) 1990 13
Actuarial OS 21 University of Oslo (Norway) 1993 36
Clearance of jaundice 62 Prince of Songkla University, Songkhla (Thailand) 2003 37
Clearance of jaundice 200 Tohoku University Hospital, Sendai (Japan) 1983 38
Bile flow 41 Childrens Hospital of Los Angeles (US) 1989 39
Ͻ2 mo, favorable 3-y OS (ϭSNL) 21 University of Colorado, Denver (US) 1980 40
10-y SNL 122 University Hospital Kremlin-Bicetre, Paris (France)
ˆ 1990 41
Ͻ7 wk, favorable 2-y SNL 36 University Hospital Munich (Germany) 2000 42
Ͻ10 wk, favorable SNL 266 University of Colorado, Denver (US) 1997 43
Ͻ10.5 wk, favorable 4-y SNL University of Colorado, Denver (US) 1979 44
Ͻ12 wk, favorable Clearance of jaundice 93 University of Hong Kong (Hong Kong) 1997 45
Ͻ90 d, favorable 20-y SNL 63 University Hospital Kremlin-Bicetre, Paris (France)
ˆ 2005 5
Clearance of jaundice 66 Indiana University School of Medicine, Indianapolis (US) 1989 46
Related (no defined 5-y SNL 1381 Multicenter study (Japan) 2003 47
threshold, younger age at Clearance of jaundice 108 University of Tubingen (Germany) 1998 9
surgery was observed in Actual SNL 47 Hospital of Porto Alegre (Brazil) 2002 48
groups with successful Actual SNL 49 Booth Hall Children’s Hospital, Blackley, Manchester (United Kingdom) 2000 49
Kasai operation) Clearance of jaundice 29 University of Alberta (Canada) 1996 50
No significant effect of age at 1-y SNL 75 Chulalongkorn University, Bangkok (Thailand) 2006 51
Kasai operation 2-y SNL 104 Multicenter study (US) 2007 12
5-y SNL 93 Multicenter study (United Kingdom) 2000 52
1-, 5-, 10-, and 20-y SNL 92 Hospital Infantil La Paz, Madrid (Spain) 2000 53
5-y OS 30 University of Bochum (Germany) 2005 54
5-y SNL 338 King’s College, London (United Kingdom) 1997 55
5-y OS (ϭSNL) 117 Juntendo University (Tokyo) 1993 56
3-y SNL 27 Ege University, Izmir (Turkey) 2004 57
OS (ϭSNL) 34 University of Michigan, Ann Arbor (US) 1991 58
Clearance of jaundice 81 University of Michigan, Ann Arbor (US) 2002 59
Clearance of jaundice 31 Emory University, Atlanta (US) 2001 60
Clearance of jaundice 35 Juntendo University, Tokyo (Japan) 1985 61
OS indicates overall survival.
examined: (1) the impact of age at Kasai operation on included. The diagnosis of BA was critically reassessed by
survival with native liver (SNL) in later childhood and the investigators of the study by consultation of the
adolescence; and (2) the expected benefits if the Kasai charts of every patient before inclusion in the study.
operation was performed earlier in every patient because Results of histologic examination of the biliary remnants
of a BA screening. were available in 584 (78%) patients. The median fol-
low-up in survivors was 7 years (range: 0.2–18.1 years).
PATIENTS AND METHODS
The charts of all children with BA or suspected BA Ethical Approval
treated in France since LT became available were re- This study received the agreement of French authorities
viewed by the investigators of the study, who visited the (Commission Nationale de l’Informatique et des Lib-
participating centers and analyzed the charts locally. All ertes, authorization 997085). The registry was strictly
´
45 pediatric centers (including medical, surgical, and LT confidential. Each family received an information letter
units) involved in the management of patients with BA indicating the aims and methods of the study and had
in France contributed to this survey; therefore, data the possibility to check or correct the data recorded for
collection was exhaustive. their child.
Inclusion criteria and registered data have been de-
scribed extensively for the French national outcome Statistical Analysis
study.11 In summary, all patients with BA who were Survival rates were estimated according to the Kaplan
living in France and born between 1986 and 2002 were Meier method. SNL ends at LT or at death (in patients
PEDIATRICS Volume 123, Number 5, May 2009 1281
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4. 200
180
160
Median age (minimum–maximum), d
140
120
100
80
60
40
20
0
1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002
Year
FIGURE 1
Age at Kasai operation from 1986 to 2002. No significant variation of age at Kasai operation was observed during the 17 years of the study.
who had not received a transplant). Results were ex- As described in the French national outcome study,
pressed as value with the SE of the mean. All statistical increased age at Kasai operation was independently, from
analyses were performed with StatView 5.0 (SAS Insti- other prognostic factors (such as polysplenia syndrome or
tute, Inc, Cary, NC). unfavorable anatomic patterns of the extrahepatic biliary
remnant), associated with a worse SNL outcome.11
RESULTS The comparison between patients who underwent
A total of 743 children were included. The detailed med- the Kasai operation before the age of 46 days versus
ical history of the patients has been reported in the patients who underwent the Kasai operation later and
French national outcome study.11 Briefly, a total of 695 patients without contraindications to surgery who did
(93.5%) children with BA underwent the Kasai opera- not undergo the Kasai operation (the main reason being
tion or a derived procedure, 48 (6.5%) children with BA delayed diagnosis in most of them), showed a 12.1%
did not undergo the Kasai operation. Median age at difference of 15-year SNL between the 2 groups (Fig 3).
Kasai operation was 60 days (range:12–180 days). No Consequently, the estimation of the possible benefits of
significant variation of the age at Kasai operation was early Kasai operation (performed before 46 days of life in
observed during the 17 years of the study (Fig 1). SNL all patients with BA) was calculated according to the
after the Kasai operation was 57.1% at 2 years of age following data: A ϭ number of new BA cases per year:
(SE: 1.9%; 363 patients alive with native liver), 37.9% 743/17 years ϭ 43.7 /year; B ϭ 15-year SNL for patients
at 5 years of age (SE: 2.0%; 177 patients alive with operated before 46 days of life: 34.9%; C ϭ 15-year SNL
native liver), 32.4% at 10 years of age (SE: 2.0%; 86 for patients operated after 45 days of life or patients
patients alive with native liver), and 28.5% at 15 years without contraindications to surgery who did not un-
of age (SE: 2.3%; 22 patients alive with native liver). dergo the Kasai operation: 22.8%; D ϭ ratio of patients
SNL decreased when age at Kasai operation increased with BA operated after 45 days of life or patients without
(P Ͻ .001) (Fig 2). The best results were obtained if the contraindications to surgery who did not undergo the
Kasai operation was performed before the age of 30 days, Kasai operation: 72.6%; E ϭ number of liver grafts per
and then decreased regularly with increased age at opera- patient who had received a transplant: 456 grafts in 386
tion. Nevertheless, patients operated after the age of 90 patients who received a transplant ϭ 1.18 graft per
days still had a 13% chance of surviving with their native patient who received a transplant.
liver until adolescence. The effect of age at Kasai operation The estimated savings of liver grafts in infancy and
lasted in late childhood and adolescence (Fig 2). childhood, if every patient with BA underwent the Kasai
1282 SERINET et al
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5. FIGURE 2
Variations of 2-, 5-, 10- and 15-year SNL according to age at Kasai operation. SNL significantly decreased when age at Kasai operation increased (P Ͻ .0001). a In this subgroup, the patient
with the longest follow-up underwent LT at the age of 14 years; therefore, the curve drops to zero without any consequence, however, to statistical results.
operation before 46 days of life, are 4.5 liver grafts per 2005: 476 pediatric LTs ϭ 79 LTs per year. Source:
year [ϭ A ϫ D ϫ (BϪC) ϫ E], which represents 5.7% of Agence de la Biomedecine, Paris, France).
´
all pediatric LTs performed annually in France (2000 –
DISCUSSION
Although numerous reports have shown that late per-
formance of the Kasai operation worsens its results (Ta-
1.0
ble 1), the real impact of age at the time of Kasai oper-
0.8
ation has remained controversial.15 To establish the
potential benefits of mass screening for BA, 2 main
0.6
issues remained unclear: (1) does the prognosis of the
Kasai operation progressively decrease when age at sur-
SNL
0.4 gery increases, and what happens to children operated in
12.1% the first month of life? and (2) Does the better short-
0.2 term prognosis observed after early Kasai operations
persist or fade in late childhood and adolescence?
0.0 In the present large series, we found that the earlier
the Kasai operation, the better its results. Especially in
0.0 2.5 5.0 7.5 10.0 12.5 15.0 17.5 20.0
Age, y
the subgroup of 59 patients operated on in the first
month of life, the outcome was better than in the chil-
FIGURE 3
Comparison of the 15-year SNL between patients with BA having undergone a Kasai
dren operated on later in life. These findings correlate
operation before and after 45 days of life. The comparison of the 2 groups showed a with data from the Canadian national study, in which 21
12.1% difference of the 15-year SNL. patients with BA operated on before the age of 1 month
PEDIATRICS Volume 123, Number 5, May 2009 1283
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6. had a better SNL than 291 patients operated on when transplant are not well known but are undoubtedly less
older.16 These results contrast with a previous study fo- than those of a transplanted child. In a scenario where
cusing on the results of the Kasai operation performed in the annual charges of a patient with BA who has not
the first month of life17: the outcome seemed worse in received a transplant would be 10 000 Euros, the total
the 9 of 92 patients who underwent the Kasai operation savings for the 4.5 yearly economized pediatric LTs in
in the first month of life, suggesting that early diagnosis France would amount to ϳ500 000 Euros per year. In
might have been related to a different pathogenesis of the United States, the same savings of 5.7% of all pedi-
the disease, associated with a worse prognosis. Notewor- atric LTs would represent 32.7 LTs per year (4016 pedi-
thy, in the detailed analysis of prognostic factors of Kasai atric LTs were performed in the United States between
operation in the French series, classical factors of poor 2000 and 2006 [ie, 574 pediatric LTs per year (www.
prognosis such as polysplenia syndrome, or unfavorable unos.org)]). The estimated first-year charge for a LT is
anatomy of the extrahepatic biliary remnant, were ϳ450 000 dollars, and the estimated annual follow-up
found to be independent of age at surgery by multivar- charges are ϳ30 000 dollars.24 In a scenario where the
iate analysis.6,11 charges of a patient with BA who has not received a
Whether the benefit of an early Kasai operation transplant would be 15 000 dollars, the total financial
would last in late childhood and adolescence remained savings would amount to ϳ18 million dollars per year.
uncertain. It has been shown that most of the patients Therefore, BA screening programs seem to be a cost-
with BA alive with their native livers at the ages of 10 effective investment for society.
years and 20 years5 had undergone the Kasai operation Despite repeated attempts to sensitize medical staff to
before the age of 90 days. The recent national Canadian check the color of stools in the first month of life, the age
study showed that the benefit of an early Kasai opera- at Kasai operation did not decrease in France during the
tion, in the first month of life, is maintained until late 17 years of the study, with a stable median age at Kasai
childhood and adolescence.16 Our data confirm these operation of 60 days. Recently, a special mention has
findings in a larger series, and show that whatever the been added in the French individual health booklet of
follow-up in childhood, survival rate with native liver each infant, to inform the parents to check the color of
increased when age at surgery decreased (Fig 2). To the stools of their infants, and another information cam-
evaluate the potential benefits of a realistic mass screen- paign to parents and health professionals is currently
ing, we compared the children operated before 46 days underway.25 It is too early to evaluate the benefits of
to the rest of the patients without contraindications to these actions. In other countries, several screening
surgery. The threshold of 45 days was chosen, because in methods have been proposed.15 Currently, the most sim-
many countries the first visit with the pediatrician is at ple and effective method seems to be the stool color card,
the end of the first month of life, and in case of suspected introduced by Matsui and Dodoriki26 in Japan, and also
cholestasis, the diagnosis of BA seems realistic in the used in Argentina27 and Taiwan.28 Systematic checking
next 2 weeks. This comparison showed a 12.1% differ- of stool color before the end of the first month of life is
ence of 15-year SNL (34.9% vs 22.8%) between the 2 a sensitive method to detect cholestasis. The costs of such
groups. From our data, a rough estimation showed that a screening program are limited, and are most likely
if the Kasai operation was performed before 46 days in inferior to the savings obtained by the spared LTs; this
every patient, 4.5 pediatric LTs could be spared each was evaluated in Switzerland by a financial simulation
year, representing 5.7% of all pediatric LTs performed within a project for the executive MBA in management
annually in France. of technology at the Swiss Federal Institute of Technol-
What would be the impact of such a pediatric LT- ogy, Lausanne and the University of Lausanne, Switzer-
saving policy? Reducing the need for scarce pediatric land (P. Minder, MBA Launch plan for BA screening
liver grafts would shorten the transplantation waiting card, unpublished data, November 2007). A national
list and reduce the need for living related donors, whose pilot study of such BA screening is under way in Swit-
risks cannot be neglected (the morbidity rate of left zerland.
lobectomy is estimated at 10%).18,19 The very long-term At the other end of the spectrum, our data also show
adverse effects of prolonged immunosuppression are that late Kasai operations (performed after the age of 3
still incompletely known, but impaired renal function months) still can help avoid some LTs in infancy and
(that may lead to chronic renal failure), dyslipidemia, childhood: 15-year SNL was 13.4% in this subgroup of
diabetes, and increased risk of malignancy are cer- patients. Therefore, as already emphasized by other
tain.20 Delaying transplantation after infancy and avoid- studies, the Kasai operation should not be systematically
ing Epstein-Barr virus primary infection in an immuno- denied after 3 months.29–31 Nevertheless, a precise pre-
suppressed child might reduce the risk of posttransplant operative checkup is necessary to detect patients with
lymphoproliferative disease.21 Today, the results of LT in advanced liver disease (presenting with signs such as
adults are close to those in pediatric patients,22 especially ascites, impaired synthetic functions, reversed portal
with diseases that do not recur after LT, such as BA. flow and/or arterial diastolic flow) and orient them to
Reducing pediatric LTs would also lead to significant primary LT.
financial savings. In France, the estimated first-year cost
for LT is 100 000 Euros, and the estimated annual fol- CONCLUSIONS
low-up charges are 20 000 Euros.23 The costs of fol- Increased age at surgery had a progressive and sustained
low-up of a patient with BA who has not received a deleterious effect on the results of the Kasai operation
1284 SERINET et al
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7. until adolescence. These findings indicate a rational basis 5. Lykavieris P, Chardot C, Sokhn M, Gauthier F, Valayer J,
for BA screening to reduce the need for LT in childhood. Bernard O. Outcome in adulthood of biliary atresia: a study of
63 patients who survived for over 20 years with their native
liver. Hepatology. 2005;41(2):366 –371
ACKNOWLEDGMENTS 6. Chardot C, Carton M, Spire-Bendelac N, Le Pommelet C, Gol-
This study was supported by PHRC National 2002 grant mard JL, Auvert B. Prognosis of biliary atresia in the era of liver
AOM 02007. The study sponsor had no influence on the transplantation: French national study from 1986 to 1996.
study design; the collection, analysis, or interpretation of Hepatology. 1999;30(3):606 – 611
7. Wildhaber B, Coran AG, Drongowski RA, et al. The Kasai
data; the writing of the report; or the decision to submit
portoenterostomy for biliary atresia: a review of 27-year
the article for publication. experience with 81 patients. J Pediatr Surg. 2003;38(10):
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centers who participated in our study: Amiens: C. Lena- 8. Shteyer E, Ramm GA, Xu C, White FV, Shepherd RW. Out-
erts and J. P. Canarelli; Angers: J. L. Ginies and L. Cou- come after portoenterostomy in biliary atresia: pivotal role of
pris; Besancon: E. Plouvier and D. Aubert; Bondy: J.
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Gaudelus and C. Grapin; Bordeaux: T. Lamireau and P. J Pediatr Gastroenterol Nutr. 2006;42(1):93–99
Vergnes; Brest: L. de Parscau and B. Fenoll; Caen: J. F. 9. Schweizer P, Lunzmann K. Extrahepatic bile duct atresia: how
Duhamel and T. Petit; Clermont-Ferrand: M. Meyer and efficient is the hepatoporto-enterostomy? Eur J Pediatr Surg.
T. Scheye; Colmar: D. Meyer Gast and S. Geiss; Dijon: 1998;8(3):150 –154
F. Huet and E. Sapin; Grenoble: J. P. Chouraqui and J. F. 10. Duche M, Fabre M, Kretzschmar B, Serinet MO, Gauthier F,
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Dyon; Le Havre: B. Le Luyer and M. Menard; Lille: F. Chardot C. Prognostic value of portal pressure at the time of
Kasai operation in patients with biliary atresia. J Pediatr Gas-
Gottrand, M. Bonnevalle, R. Sfeir, and R. Besson; Limo-
troenterol Nutr. 2006;43(5):640 – 645
ges: L. De Lumley and J. L. Alain; Lyon Debrousse: P.
11. Serinet MO, Broue P, Jacquemin E, et al. Management of
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Alessandrini; Marseille Timone: J. Sarles, B. Roquelaure, 12. Shneider BL, Brown MB, Haber B, et al. A multicenter study
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OUR PIGS, OUR FOOD, OUR HEALTH
“The late Tom Anderson, the family doctor in this little farm town in north-
western Indiana, at first was puzzled, then frightened. MRSA (methicillin-
resistant Staphylococcus aureus) sometimes arouses terrifying headlines as a
‘superbug’ or ‘flesh-eating bacteria.’ The best-known strain is found in hos-
pitals, where it has been seen regularly since the 1990s, but more recently
different strains also have been passed among high school and college ath-
letes. The federal Centers for Disease Control and Prevention reported that by
2005, MRSA was killing more than 18 000 Americans a year, more than
AIDS. Dr Anderson at first couldn’t figure out why he was seeing patient after
patient with MRSA in a small Indiana town. And then he began to wonder
about all the hog farms outside of town. Could the pigs be incubating and
spreading the disease? One of the first clues that pigs could infect people with
MRSA came in the Netherlands in 2004, when a young woman tested
positive for a new strain of MRSA, called ST398. The family lived on a farm,
so public health authorities swept in—and found that 3 family members, 3
co-workers and 8 of 10 pigs tested all carried MRSA. Since then, that strain
of MRSA has spread rapidly through the Netherlands— especially in swine-
producing areas. A small Dutch study found pig farmers there were 760 times
more likely than the general population to carry MRSA (without necessarily
showing symptoms), and Scientific American reports that this strain of MRSA
has turned up in 12% of Dutch retail pork samples. Now this same strain of
MRSA has also been found in the United States. A new study by Tara Smith,
a University of Iowa epidemiologist, found that 45% of pig farmers she
sampled carried MRSA, as did 49% of the hogs tested. The study was small,
and much more investigation is necessary.”
Kristof ND. New York Times. March 12, 2009
Noted by JFL, MD
1286 SERINET et al
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9. Impact of Age at Kasai Operation on Its Results in Late Childhood and
Adolescence: A Rational Basis for Biliary Atresia Screening
Marie-Odile Serinet, Barbara E. Wildhaber, Pierre Broué, Alain Lachaux, Jacques
Sarles, Emmanuel Jacquemin, Frédéric Gauthier and Christophe Chardot
Pediatrics 2009;123;1280-1286
DOI: 10.1542/peds.2008-1949
Updated Information including high-resolution figures, can be found at:
& Services http://www.pediatrics.org/cgi/content/full/123/5/1280
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