DOI: 10.1542/peds.2011-0742
; originally published online August 28, 2011;
2011;128;e530
Pediatrics
and the Taiwan Infant Stool Color Card Study Group
Chiou
Shih, I-Hsien Lee, Wen-Chung Lee, Huey-Ling Chen, Hong-Yuan Hsu, Shu-Ti
Wu, Beng-Huat Lau, Tong-Chi Tsai, Yao-Jong Yang, An-Chyi Chen, Hsiang-Hung
Mao-Meng Tiao, Ming-Wei Lai, Hung-Chang Lee, Chieh-Chung Lin, Tzee-Chung
Yi-Chun Lin, Mei-Hwei Chang, Shu-Fen Liao, Jia-Feng Wu, Yen-Hsuan Ni,
2009
−
Decreasing Rate of Biliary Atresia in Taiwan: A Survey, 2004
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located on the World Wide Web at:
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of Pediatrics. All rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275.
Boulevard, Elk Grove Village, Illinois, 60007. Copyright © 2011 by the American Academy published, and trademarked by the American Academy of Pediatrics, 141 Northwest Point publication, it has been published continuously since 1948. PEDIATRICS is owned, PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly
2004 –2009
WHAT’S KNOWN ON THIS SUBJECT: Biliary atresia (BA) is the leading cause of liver death and liver transplantation in the pediatric age group. The pathogenesis of BA remains unclear, but epidemiological studies may enhance our understanding of the possible causes.
WHAT THIS STUDY ADDS: Decreasing rates of BA have been found in Taiwan since 2007, which may be related to
improvements in general socioeconomic status and possibly the popularity of rotavirus vaccination; this may shed light on possible preventive interventions for BA.
abstract
OBJECTIVES:The pathogenesis of biliary atresia (BA) is unclear, but epidemiological studies may help to elucidate possible causes. The goals of this study were to identify BA incidence changes in Taiwan in 2004 –2009 and to survey the factors that might influence incidence changes to elucidate the possible causes of BA.
METHODS:A Taiwan national registry system for BA has been estab-lished since 2004. By using data from the national registry system for BA, we identified BA incidence changes in 2004 –2009. We also evalu-ated the correlations between BA incidences and estimevalu-ated rotavirus vaccine coverage rates and between BA incidences and the gross do-mestic product.
RESULTS:A total of 185 patients with BA were identified in 2004 –2009 in Taiwan, whereas the number of live births was 1 221 189. Compared with the incidence of BA in 2004 –2006 (1.79 cases per 10 000 live births), the incidence of BA in 2007–2009 (1.23 cases per 10 000 live births) was decreased significantly (P⫽ .01). BA incidences were neg-atively correlated with the gross domestic product (P⫽ .02) and mar-ginally negatively correlated with rotavirus vaccine coverage rates (P⫽ .07).
CONCLUSIONS:A significant decrease in BA incidence in Taiwan since 2007 has been noted and may be related to improvements in the gen-eral socioeconomic status and the popularity of rotavirus vaccination. Although more evidence is needed to establish a direct correlation, this phenomenon may shed light on possible causes of and preventive in-terventions for BA. Pediatrics 2011;128:e530–e536
AUTHORS:Yi-Chun Lin, MD,aMei-Hwei Chang, MD,a
Shu-Fen Liao, PhD,b,cJia-Feng Wu, MD, PhD,aYen-Hsuan Ni, MD,
PhD,aMao-Meng Tiao, MD,d,eMing-Wei Lai, MD,f
Hung-Chang Lee, MD,gChieh-Chung Lin, MD,hTzee-Chung Wu,
MD,i,jBeng-Huat Lau, MD,kTong-Chi Tsai, MD,lYao-Jong
Yang, MD, PhD,mAn-Chyi Chen, MD,nHsiang-Hung Shih,
MD,o,pI-Hsien Lee, MD,qWen-Chung Lee, MD, PhD,b,c
Huey-Ling Chen, MD, PhD,aHong-Yuan Hsu, MD, PhD,aShu-Ti
Chiou, MD, PhD,r,sand the Taiwan Infant Stool Color Card
Study Group
aDepartment of Pediatrics, National Taiwan University Hospital,
Taipei, Taiwan;bResearch Center for Genes, Environment, and
Human Health andcInstitute of Epidemiology and Preventive
Medicine, College of Public Health, National Taiwan University, Taipei, Taiwan;dDepartment of Pediatrics, Chang Gung
Memorial Hospital-Kaohsiung Medical Center, Kaohsiung, Taiwan;eDepartment of Pediatrics, College of Medicine, Chang
Gung University, Kaohsiung, Taiwan;fDepartment of Pediatrics,
Chang Gung Memorial Hospital, Taoyuan, Taiwan;gDepartment
of Pediatrics, Mackay Memorial Hospital, Taipei, Taiwan;
hDepartment of Pediatrics, Taichung Veterans General Hospital,
Taichung, Taiwan;iDepartment of Pediatrics, Taipei Veterans
General Hospital, Taipei, Taiwan;jDepartment of Medicine and sInstitute of Public Health, National Yang-Ming University, Taipei,
Taiwan;kDepartment of Pediatrics, Shin Kong Wu Ho-Su
Memorial Hospital, Taipei, Taiwan;lDepartment of Pediatrics, St
Joseph’s Hospital, Huwei, Taiwan;mDepartment of Pediatrics,
National Cheng Kung University Hospital, Tainan, Taiwan;
nDepartment of Pediatrics, China Medical University Hospital,
Taichung, Taiwan;oDepartment of Pediatrics, Kaohsiung Medical
University Hospital, Kaohsiung, Taiwan;pDepartment of
Pediatrics, Kaohsiung Municipal Hsiao-Kang Hospital, Kaohsiung, Taiwan;qDepartment of Pediatrics, Chi Mei Medical Center,
Tainan, Taiwan; andrBureau of Health Promotion, Department of
Health, Taipei, Taiwan
KEY WORDS
biliary atresia, incidence, epidemiology, rotavirus, gross domestic product
ABBREVIATIONS
BA—biliary atresia
GDP—gross domestic product
www.pediatrics.org/cgi/doi/10.1542/peds.2011-0742
doi:10.1542/peds.2011-0742
Accepted for publication May 13, 2011
Address correspondence to Mei-Hwei Chang, MD, Department of Pediatrics, National Taiwan University Hospital, No. 8, Chung-Shan S. Rd, Taipei, Taiwan. E-mail: [email protected]
PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).
Copyright © 2011 by the American Academy of Pediatrics
FINANCIAL DISCLOSURE:The authors have indicated they have no financial relationships relevant to this article to disclose.
Biliary atresia (BA) is the leading cause of death without liver transplan-tation in the pediatric age group.1–3
Immune-mediated ductal injury, in-flammatory triggers, and genetic fac-tors are thought to correlate with this disease.1,3 However, the exact
patho-genesis remains unclear. Data re-ported from different countries on the incidence of BA range from 0.42 cases per 10 000 live births in Croatia4to 3.2
cases per 10 000 live births in French Polynesia.4–22The estimated incidence
of BA in Taiwan was 1.46 cases per 10 000 live births in 1996 –2003, ac-cording to national health insurance data.20 However, the number of
pa-tients with confirmed diagnoses had never been well investigated in the whole of Taiwan before 2004, when a national stool color–screening and registry system was established.23By
using the data from the national BA registry system in Taiwan, we have the opportunity to investigate the exact changes in the incidence of BA in Tai-wan from 2004 to 2009 and to evaluate factors possibly correlated with the in-cidence changes, including rotavirus vaccine coverage rates and general socioeconomic status. This may have some implications regarding the pathogenesis of BA.
Increasing maternal racial and ethnic diversity in Taiwan has been observed since the 1970s because of the increas-ing numbers of brides from mainland China, Indonesia, and Vietnam. How-ever, the exact incidences of BA in China, Indonesia, and Vietnam are un-clear in the current literature. In this study, we investigated BA incidences among Taiwanese infants according to their maternal ethnic origins. This may help us understand genetic suscepti-bility in BA and shed light on the possi-ble risk factors for BA. Infectious causes, especially rotavirus, were pro-posed to be related to BA pathogenesis in previous studies.24–26 We
investi-gated the estimated rotavirus vaccine coverage rate in our infant population to determine whether rotavirus vac-cine coverage rates correlated with BA incidence changes. Racial and geo-graphic region differences in the inci-dences of BA may reflect the existence of predisposing genetic factors or socioeconomic status-related differ-ences in exposure to environmental factors.11,14,16 Therefore, we tried to
identify whether there was a correla-tion between socioeconomic status and the incidence of BA. Real gross do-mestic product (GDP) is the value of goods and services measured by using a constant set of prices, and it is the best measurement of the standard of living.27 We investigated the
correla-tion between general socioeconomic status according to real GDP and the incidence of BA, to determine whether general socioeconomic status changes influence the incidence of BA.
METHODS Subjects
All neonates who were born in Taiwan in 2004 –2009 and were diagnosed as having BA were included in this study. The patients were identified by the Taiwan Infant Stool Color Card Study Group. This national organization in-cludes the Taiwan Infant Stool Color Card Registry System and the Taiwan Biliary Atresia Study Group.23,28All
chil-dren living in Taiwan who were born in 2004 –2009 were the subjects screened for stool color and were reg-istered in the national registry system once the diagnosis of BA had been con-firmed through intraoperative cholan-giography.2 We designed an infant
stool color card with different stool color photographs, from normal stool to clay-colored stool, for Taiwanese in-fants. It is integrated into the child health booklet that is distributed to ev-ery neonate in Taiwan. It had been launched as a comprehensive national
screening and reporting system for BA for all neonates by 2004. There are 2 reporting systems for BA in Taiwan. The first system is the Taiwan Infant Stool Color Card Registry System. All physicians and families of infants are asked to check and to report the stool color when infants are brought to a clinic for the second dose of hepatitis B vaccine at 1 month of age or at any time after birth. The staff members of the registry center then follow up with the patients and list them on the na-tional BA profile if they are diagnosed eventually as having BA through intra-operative cholangiography. The sec-ond system involves the Taiwan Biliary Atresia Study Group. The members are pediatric gastroenterologists in 21 medical centers and hospitals where the Kasai operation can be performed. They are requested to report patients with newly diagnosed BA at least twice per year. In addition to the 2 reporting systems, the Taiwan Children Liver Foundation affords financial support for patients with newly diagnosed BA. This is an incentive to facilitate family reporting. This project was approved by the National Taiwan University Hos-pital institutional review board. Through these systems and networks, we are confident regarding the pro-files of patients with BA identified since 2004. All patients with BA in Taiwan are monitored by the Taiwan Infant Stool Color Card Study Group. With a good registry and follow-up system, we are able to analyze annual incidences accurately.
Data Sources for Live Births, Maternal Ethnic Origins, and GDP
We used data from the Department of Statistics, Ministry of the Interior, Tai-wan, to calculate BA incidences ac-cording to different maternal ethnic origins and data from the Directorate-General of Budget, Accounting, and Statistics, Executive Yuan, Taiwan, to
Rotavirus Vaccine Coverage Rate
The rotavirus vaccine was introduced to Taiwan in late 2006, as a self-paid vaccine. There are 2 commercial rota-virus vaccines available in Taiwan. One is pentavalent, bovine-human, reas-sortant vaccine (RotaTeq [Merck, Whitehouse Station, NJ]; cover sero-type: G1,G2,G3,G4,P1A[8]; a complete course requires 3 doses), and the other is monovalent, live, attenuated vaccine from human rotavirus strain G1P[8] (Rotarix [GlaxoSmithKline Bio-logicals, Rixensart, Belgium]; cover se-rotype: G1; heterotypic protection of G2, G3, G4, and G9; a complete course requires 2 doses). Both vaccines were designed to target the capsid glyco-protein VP7 and VP4 of group A rotavi-rus, which is the common cause of gastroenteritis in infants. Previous ar-ticles on the link between rotavirus and BA in humans presented data on rotavirus C,24 whereas the common
problem of gastroenteritis in infants is caused mainly by rotavirus A. Because rotavirus group A and group C share some common capsid proteins, vacci-nations against rotavirus group A may provide partial protection against ro-tavirus group C. The data on estimated annual rotavirus vaccine doses are from the Centers of Disease Control in Taiwan. The estimated numbers of per-sons who received vaccines in each year are adjusted by the total doses required for a complete course for dif-ferent vaccines. The estimated number of persons who received vaccine was calculated as one-third of total taTeq doses plus one-half of total Ro-tarix doses. The vaccine coverage rate was defined as the estimated number of persons who received vaccine di-vided by the annual number of live births in Taiwan.
Statistical Analyses
Poisson regression was applied to examine the annual changes in BA in-cidence rates and to test the associ-ation between BA incidence rates and estimated rotavirus vaccine cov-erage rates and GDP. All analyses were performed by using SAS 9.1 (SAS Institute, Inc, Cary, NC).
RESULTS
Changes in BA Incidences
There were 185 patients born in Tai-wan in 2004 –2009 for whom BA was diagnosed through intraoperative cholangiography and other diseases were ruled out on the basis of histo-pathologic results and clinical courses. They were monitored by 21 hospitals and the Taiwan Infant Stool Color Card Study Group. The inci-dence of BA in Taiwan in 2007–2009 was 1.23 cases per 10 000 live births, which was 69% of the incidence in 2004 –2006, when the incidence was 1.79 cases per 10 000 live births (P⫽ .01) (Table 1).
Maternal Ethnic Origins
We divided the annual live births in Taiwan and patients with BA into 3 groups according to maternal ethnic origins (Table 2). Among the 185 pa-tients with BA, maternal ethnic origins were verified for 184 patients. All of the
184 patients’ fathers were Taiwanese; 167 patients were born to Taiwanese mothers (incidence: 1.54 cases per 10 000 live births from Taiwanese mothers), 11 patients were born to mothers from China (incidence: 1.82 cases per 10 000 live births from moth-ers from China), and 6 patients were born to mothers from Southeast Asia, including Indonesia and Vietnam (inci-dence: 0.80 cases per 10 000 live births from mothers from Southeast Asia). There were no significant differences between different maternal ethnic ori-gins (P⫽ .11 for Taiwan vs China and .59 for Taiwan vs Southeast Asia, re-spectively, from Poisson regression analyses). Compared with the inci-dence in 2004 –2006, the inciinci-dence of BA among infants from Taiwanese mothers decreased markedly in 2007– 2009 (P⫽ .01; odds ratio: 1.5 [95% con-fidence interval: 1.10 –2.05]). No inci-dence changes with time were found for BA among infants from mothers from Mainland China, Indonesia, or Vietnam. With longitudinal comparison from 2004 to 2009, P⫽ .88 in Mainland China and P⫽ .86 in Southeast Asia, respectively.
The proportion of live births from Tai-wanese mothers among the total live births in Taiwan increased from 86.75% in 2004 to 91.31% in 2009, whereas the proportion of live births BA Cases Live Births per 10 000 Live Births (95% Confidence Interval)
2004 40 216 419 1.85 1.00 2005 35 205 854 1.70 0.92 (0.58–1.44) 2006 37 204 459 1.81 0.98 (0.63–1.53) 2007 23 204 414 1.13 0.61 (0.36–1.02) 2008 22 198 733 1.11 0.60 (0.36–1.01) 2009 28 191 310 1.46 0.79 (0.49–1.28) 2004–2006a 112 626 732 1.79 1.00 2007–2009a 73 594 457 1.23 0.69 (0.51–0.92) 2004–2009 185 1 221 189 1.51 —
The number of BA cases was determined from data from the Taiwan Stool Color Card Study Group, and the diagnosis was confirmed through intraoperative cholangiography. The data on live births were from the Department of Statistics, Ministry of the Interior, Taiwan.
aPoisson regression was used to test the difference in annual incidences of BA. The overall incidence in 2007–2009 was
from mothers from Mainland China decreased slightly, from 5.18% in 2004 to 4.64% in 2009, and the pro-portion of live births from mothers from Indonesia and Vietnam de-creased from 8.07% in 2004 to 4.05% in 2009. Analysis of the annual inci-dences of BA among infants with different maternal ethnic origins showed similar trends in incidence reduction with time for total BA in Taiwan and BA among infants born to Taiwanese mothers.
Rotavirus Vaccine Coverage
The estimated numbers of persons who received rotavirus vaccination have been increasing since Novem-ber 2006, when rotavirus vaccines were introduced into Taiwan. The es-timated numbers of persons who re-ceived rotavirus vaccination were 12 324 in 2006, 47 057 in 2007, 60 241 in 2008, and 96 447 in 2009. As the number of children who received ro-tavirus vaccination increased, the number of patients with BA de-creased, from 112 patients in 2004 – 2006 to 73 patients in 2007–2009 (Fig 1). We found a marginally significant
correlation between the decrease in the incidence of BA and the increase in the coverage rate for rotavirus vacci-nation (P⫽ .07).
Gross Domestic Product
A significant negative correlation was found between annual real GDP and BA incidence changes in 2004 – 2009 (P ⫽ .02). The Poisson model indicated the following: incidence rate ⫽ exp(⫺6.0425 ⫺ [2.2531 ⫻ real GDP]) (Fig 2).
DISCUSSION
According to the published literature, BA is more common among Asian and French Polynesian people,10,21but the
estimated incidence in Asia is available only for Japan and Taiwan.18,20Through
the use of a well-established BA regis-try system and a national BA study group in Taiwan, the data obtained since 2004 are the first national data with well-defined cases. Therefore, the advantages of this study include the reliable sources of data, which were obtained from a region with well-defined cases, well-well-defined annual live birth numbers, and well-defined ma-ternal ethnic origins, which have not been investigated previously for BA in Taiwan.
In our study, the Taiwan Infant Stool Color Card Study Group clearly defined cases as BA only when the diagnoses were confirmed through intraopera-tive cholangiography and other dis-eases were excluded on the basis of clinical courses and liver histopatho-logic evaluations. Therefore, overesti-mation of the incidence of BA could be excluded. Because of the active promo-tion of the use of infant stool color cards and education for family mem-bers and physicians, underestimation
TABLE 2 Incidences of BA According to Maternal Ethnic Origins in Taiwan in 2004 –2009 Infants Born to
Taiwanese Mothers
Infants Born to Mothers From Mainland China
Infants Born to Mothers From Indonesia or
Vietnam Incidence of BA, No. of cases per
10 000 live births (n/N) 2004 1.92 (36/187 753) 1.78 (2/11 206) 1.15 (2/17 460) 2005a 1.67 (30/179 345) 2.99 (3/10 022) 0.61 (1/16 487) 2006 1.94 (35/180 556) 0.96 (1/10 423) 0.74 (1/13 480) 2004–2006a 1.84 (101/547 654) 1.90 (6/31 651) 0.84 (4/47 427) 2007 1.04 (19/183 509) 3.95 (4/10 117) 0.00 (0/10 788) 2008 1.17 (21/179 647) 0.00 (0/9843) 1.08 (1/9252) 2009 1.49 (26/174 698) 1.13 (1/8871) 1.29 (1/7741) 2007–2009 1.23 (66/537 854) 1.73 (5/28 831) 0.72 (2/27 781) 2004–2009a 1.54 (167/1 085 508) 1.82 (11/60 482) 0.80 (6/75 208) Pb .01 .88 .86
Risk ratio (95% confidence interval)
1.50 (1.10–2.05) 1.09 (0.33–3.58) 1.17(0.21–6.40)
There were 185 patients with BA in Taiwan in 2004 –2009, and 184 patients’ maternal ethnic origins were identifiable.
aThe maternal ethnic origin of 1 patient born in 2005 was not identifiable.
bPoisson regression was applied to test the BA incidence changes with time between 2004 –2006 and 2007–2009 for
different maternal ethnic origins. A significant decrease in the incidence of BA was noted for infants born to Taiwanese mothers (P⫽ .01).
FIGURE 1
Trend of association between estimated rotavirus vaccination coverage rates and BA incidences in 2004 –2009 (P⫽ .07). The Poisson regression was as follows: incidence of BA ⫽ exp(⫺8.670 ⫺ [0.076 ⫻ vaccination coverage rate]).
of patient numbers was less possible during this period.
A previous study showed seasonal changes in BA rates.18However, annual
incidence reductions had not been re-ported previously. The findings provide support for theories that BA may be influenced by environmental exposure during pregnancy or in the perinatal period, racial composition changes in a region, or socioeconomic status changes. We also noted that, although there has been an obviously decreased incidence of BA in Taiwan since 2007, the incidence increased again in 2009, to 1.46 cases per 10 000 live births. There also may be a natural cycle and fluctuation. Therefore, the study will be continued to determine incidence changes and correlations with rotavi-rus vaccine coverage and socioeco-nomic status.
The association between BA and race was reported in 1974 by Shim et al,5on
the basis of 20 cases. Those authors found wide variations in the incidence of BA among Chinese (3 cases per 10 000 live births), Filipino (2 cases per 10 000 live births), and white (0.6 cases per 10 000 live births) groups. In 1997, Yoon et al11 reported a higher
inci-dence among nonwhite infants (0.96 cases per 10 000 live births) than among white infants (0.44 cases per
10 000 live births). In 2004, Caton et al16
reported that infants of black mothers were at higher risk for BA, with a risk ratio of 1.94, compared with infants of white mothers. In our study, the inci-dence among patients with mothers from Indonesia or Vietnam (0.8 cases per 10 000 live births) was one-half that among patients with Taiwanese mothers (1.54 cases per 10 000 live births). However, many fewer infants were born of mothers from Indonesia or Vietnam, compared with Taiwanese mothers, during the study period. Therefore, the BA incidence among in-fants in Taiwan was truly decreasing rather than reflecting changes in ma-ternal population composition. Viruses have been detected in liver specimens from infants with BA, with inconsistent results (eg, rotavirus, re-ovirus, Epstein-Barr virus, cytomegalo-virus, and human herpesvirus).25,26,29
An established animal model of virus infection in BA is rhesus rotavirus30,31;
infection of murine neonates leads to obstructive cholangiopathy. Bondoc et al32 reported that maternal
vaccina-tion against rhesus rotavirus could prevent the rotavirus-induced murine model of BA in newborn mouse pups, and Turowski et al33reported that oral
vaccination with RotaTeq or Rotarix prevented most rhesus
rotavirus-tion effects on BA in humans is cur-rently lacking. Clustering of the dis-ease and incidence changes with time may help to elucidate whether infec-tious causes play an important role in direct ductal injury or postinfec-tious autoimmune-related ductal in-jury.26,34,35 Although rotavirus
vacci-nation is started at 2 months of age, which exceeds the average age of on-set of BA, herd immunity might decrease rotavirus infection during pregnancy or in the perinatal period. Rotavirus vacci-nation was introduced in Taiwan in No-vember 2006, when the reduction in BA incidence was first noted. A marginally significant negative correlation was found between the incidence of BA and the rotavirus vaccine coverage rate in 2006 –2009 (P⫽ .07). A longer observa-tion period is needed for the develop-ment of rotavirus herd immunity, which may provide stronger evidence. Addi-tional study of the yearly incidences of rotavirus diseases among infants and pregnant women, rotavirus immunity among pregnant women, and breast-feeding rates also may shed light on pre-ventive interventions.
Economists use real GDP as the best indicator of general socioeconomic status. We identified a significant nega-tive correlation between BA incidences and real GDP. The phenomenon showed that improvements in general socioeco-nomic status may correlate with de-creasing BA rates. Improving socioeco-nomic status reflects better knowledge regarding disease, better health care, more-complete public health policy, and possibly less pathogen exposure during pregnancy and in the perinatal period, but more direct evidence is needed to explain the phenomenon.
CONCLUSIONS
In our study, the incidence of BA in Tai-wan in 2004 –2009 was 1.51 cases per FIGURE 2
Negative association between GDP and BA incidences in 2004 –2009 (P⫽ .02). The Poisson regression was as follows: incidence of BA⫽ exp(⫺6.0425 ⫺ [2.253 ⫻ real GDP]).
10 000 live births, which was 1.5 to 2 times higher than rates in Western coun-tries, except French Polynesia. We no-ticed that the incidence of BA in 2007– 2009 had obviously decreased, which had never been noted before. A contrib-uting effect of maternal population com-position changes on the reduction in BA incidences with time was carefully ex-cluded. The incidence changes with time more possibly might be attributable to general socioeconomic status improve-ment. Herd immunity to rotavirus proba-bly plays some role in the BA incidence reduction, but more-powerful evidence is needed, which may shed light on dis-ease prevention.
ACKNOWLEDGMENTS
This work was supported by grants from the Bureau of Health Promotion, Department of Health, Taiwan (project 9804004A).
The members of the Taiwan Infant Stool Color Card Study Group are, in addition to the authors of this arti-cle, Pi-Feng Chang (Far Eastern Me-morial Hospital), Ju-Bei Yen (Chang Gung Memorial Hospital, Chiayi, Tai-wan), Chia-Hsiang Chu (Buddhist Tzu Chi General Hospital, Hualien, Tai-wan), Ching-Chung Tsai (E-DA Hospi-tal, Kaohsiung, Taiwan), Lung-Huang Lin (Cathay General Hospital), Shan-Ming Chen (Chung Shan Medical
Uni-versity Hospital), Chih-Cheng Chen (PingTung Christian Hospital, Ping-Tung, Taiwan), and Te-Kuei Hsieh (Hsin-Chu General Hospital, Depart-ment of Health, Executive Yuan). We are sincerely grateful to the Bureau of Health Promotion, Department of Health, Taiwan, for assistance and sup-port, to Dr Wei-Ju Su, from the Centers of Disease Control, Department of Health, Taiwan, for assistance in col-lection of the data on estimated annual rotavirus vaccine doses, and to Chia-Chi Chia-Chi, for collection of the data from the Taiwan Infant Stool Color Card Study Group.
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DOI: 10.1542/peds.2011-0742
; originally published online August 28, 2011;
2011;128;e530
Pediatrics
and the Taiwan Infant Stool Color Card Study Group
Chiou
Shih, I-Hsien Lee, Wen-Chung Lee, Huey-Ling Chen, Hong-Yuan Hsu, Shu-Ti
Wu, Beng-Huat Lau, Tong-Chi Tsai, Yao-Jong Yang, An-Chyi Chen, Hsiang-Hung
Mao-Meng Tiao, Ming-Wei Lai, Hung-Chang Lee, Chieh-Chung Lin, Tzee-Chung
Yi-Chun Lin, Mei-Hwei Chang, Shu-Fen Liao, Jia-Feng Wu, Yen-Hsuan Ni,
2009
−
Decreasing Rate of Biliary Atresia in Taiwan: A Survey, 2004
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