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ARTICLE

Hepatitis B Virus Screening for Internationally

Adopted Children

Laura Patricia Stadler, MEd, MD, MSa,b, Adam G. Mezoff, MDc, Mary Allen Staat, MD, MPHa,b,d

aDepartment of Pediatrics,bDivision of Infectious Diseases, anddInternational Adoption Center, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio;cDivision

of Gastroenterology and Nutrition, Children’s Medical Center, Dayton, Ohio

The authors have indicated they have no financial relationships relevant to this article to disclose.

What’s Known on This Subject

Studies of internationally adopted children indicate that 2% to 5% have HBV. Horizontal transmission from adoptees to household members has been described and is of con-cern. The American Academy of Pediatrics recommends that providers screen interna-tionally adopted children for HBV.

What This Study Adds

To our knowledge, this is the first case of HBV infection in an international adoptee observed as a result of repeat serological testing (6 months later) after negative studies performed at the initial evaluation after arrival in the United States.

ABSTRACT

OBJECTIVES.The objectives of this study were to estimate the prevalence of hepatitis B virus protection, infection, and recovery among internationally adopted children and to examine the need for repeat testing 6 months after arrival in the United States.

METHODS.From November 1999 through October 2006, 1282 international adoptees were screened for hepatitis B virus, and results were examined with regard to age, gender, and birth country. The prevalence of hepatitis B virus protection, infection, and recovery was determined.

RESULTS.The prevalence of hepatitis B virus in internationally adopted children at our large international adoption center was 4%, including 1.1% with acute or chronic infection and 2.9% with resolved infection. Overall, 64% of internationally adopted children had evidence of hepatitis B virus immunization, with protective antibodies. We also report a case that highlights the need for repeat serological testing to detect hepatitis B virus infection or immunization in internationally adopted children who might have been infected or vaccinated just before adoption and thus not have serological evidence in initial testing.

CONCLUSIONS.These data reinforce the American Academy of Pediatrics recommenda-tions regarding hepatitis B virus screening and infection control measures for inter-national adoptees.Pediatrics2008;122:1223–1228

T

HE AMERICAN ACADEMY of Pediatrics Red Book1 recommends that health care

providers screen internationally adopted children (IAC) for infectious diseases, including hepatitis B virus (HBV), as part of a routine evaluation within the first few weeks after entry into the United States, to detect acute or chronic HBV disease. Specifically, HBV surface antigen (HBsAg), antibody to HBsAg (anti-HBs), and

an-tibody to HBV core antigen (anti-HBc) assays are recommended for the medical evaluation of IAC. In addition, consideration should be given to repeat testing 6 months later, to detect individuals who might have been newly infected and in the process of seroconversion during the initial evaluation.1The objectives of this study were to

estimate the prevalence of HBV infection among IAC and to examine the need for repeat testing 6 months after arrival.

METHODS

Between November 1999 and October 2006, 1282 IAC were evaluated at Cincinnati Children’s Hospital Medical Center (CCHMC) International Adoption Center. As part of a comprehensive evaluation, serological testing for anti-HBs, anti-HBc, and HBsAg was performed at the initial visit.

IAC were considered to be uninfected and unprotected if they tested HBsAg-negative, anti-HBs-negative, and anti-HBc-negative. IAC were considered to be protected (through vaccination) if they tested HBsAg-negative, HBs-positive, and HBc-negative. IAC were considered to be infected if they tested HBsAg-positive, anti-HBs-negative, and anti-HBc-positive. Chronic infection was defined by the persistence of a positive HBsAg result for

www.pediatrics.org/cgi/doi/10.1542/ peds.2007-2559

doi:10.1542/peds.2007-2559

Key Words

international adoption, hepatitis B, serological testing, vaccine-preventable disease

Abbreviations

HBV— hepatitis B virus

anti-HBs—antibody to hepatitis B virus surface antigen

anti-HBc—antibody to hepatitis B virus core antigen

HBsAg— hepatitis B virus surface antigen IAC—internationally adopted children CCHMC—Cincinnati Children’s Hospital Medical Center

CDC—Centers for Disease Control and Prevention

Accepted for publication Mar 3, 2008

Address correspondence to Mary Allen Staat, MD, MPH, International Adoption Center, Cincinnati Children’s Hospital Medical Center, 3333 Burnet Ave, MLC 7013, Cincinnati, OH 45229-3109. E-mail: mary.staat@cchmc.org

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⬎6 months. IAC were considered to have recovered from HBV infection if they tested HBsAg-negative, anti-HBs-positive, and anti-HBc-positive.

Children were included in the study if they were seen at the center and underwent complete HBV serological testing at the initial or 6-month follow-up visit. For children with negative serological results (for evidence of either immunization or infection), recommendations for administration of the HBV vaccine in accordance with the routine US schedule and repeat serological testing 6 months after arrival were given to both parents and primary care providers. Demographic data, includ-ing age, gender, and birth country, were included in the analysis. Countries from which ⬍10 children had emi-grated were grouped according to region, to provide anonymity. The study was approved by the CCHMC institutional review board.

RESULTS

Initial HBV serological results are shown in Fig 1. Of the 1282 IAC evaluated, 1214 (95%) had complete HBV serological testing performed at both the initial and fol-low-up visits. An additional 14 children had incomplete HBV testing performed at the initial visit but complete serological testing at the follow-up visit and thus were included in the total 1228 studied. Of the 14 IAC with complete repeat testing, 11 had positive anti-HBs results alone (reflecting immunization), 2 had positive anti-HBs and anti-HBc results (indicating past infection), and 1 had negative serological results. Of the 54 children not included in the study, 23 had incomplete testing at the initial visit without follow-up testing and 31 did not have testing performed.

Of 1228 children with available and interpretable se-rological results, 380 (31%) were uninfected and unpro-tected at the initial testing, with negative HBsAg, anti-HBs, and anti-HBc results. Of note, of those 380 children, 59% had documentation of HBV vaccination but had no serological evidence of immunization (9% had documentation of 1 dose, 18% had 2 doses, 29% had 3 doses, 2% had 4 doses, 0.3% had 5 doses, and 1% had 6 doses). Approximately 64% (789 children)

had evidence of immunization, with positive anti-HBs results. Another 50 (4%) had evidence of HBV infection; 14 (1.1%) had evidence of acute or chronic infection (positive HBsAg and HBc results and negative anti-HBs results), and 36 (2.9%) had evidence of recovery (negative HBsAg results and positive HBs and anti-HBc results).

Figure 2 presents results of repeat serological testing of IAC with initially negative serological results. Only 142 children (37%) with negative initial serological re-sults had repeat HBV testing completed. Of the IAC who had repeat testing, 47 (33%) still lacked positive anti-HBs findings, indicating no evidence of vaccination or infection. Of those 47 children, documentation from the children’s birth countries indicated that 18 children had no documented HBV vaccine doses, 6 had 1 documented dose, 7 had 2 documented doses, and 16 had 3 docu-mented doses, with a mean of 1.4 docudocu-mented doses. In the same group of children, 20 had documentation of receiving 1 HBV vaccine dose in the United States after their initial visit and 11 of receiving 2 doses (mean: 1 dose) but did not have protective antibodies when re-tested.

Another 91 children (64%) with initially negative serological results had positive anti-HBs results when repeat serological testing was performed. The range of doses of HBV vaccine given in the United States after the visit was 0 to 3, with an average of 1.3 doses. In addition, 3 children had evidence of recovery from HBV infection and 1 had evidence of acute infection.

Because we did not routinely repeat serological test-ing of IAC who had protective antibody levels at the initial visit, the majority of IAC with protective antibod-ies (88%) did not have repeat serological testing per-formed. Of the 95 (12%) with repeat serological results, 92 (96%) still had protective antibody levels (anti-HBs-positive only). Three children lacked evidence of serum antibodies in repeat serological testing.

Table 1 presents the country-specific demographic and serological results. The average age of children in the study was 26.5 months, and more than one half (56%) were female, with 92% of adoptees from China being

798 (65%) Protected 380 (31%)

Uninfected, Unprotected

14 (1.1%) Infected

36 (2.9%) Recovered 1228

IAC With Complete Serology

FIGURE 1

HBV serological results for IAC evaluated at CCHMC.

1 (0.7%) Acutely Infected 142

Uninfected, Unprotected

47 (33%) Uninfected, Unprotected

91 (64%) Protected

3 (2%) Recovered FIGURE 2

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female. The average age of IAC with HBV infection was 56.3 months. Approximately 64% of IAC (789 children) had evidence of protective antibodies resulting from HBV immunization. The overall prevalence of HBV in-fection (at initial and repeat screening) among the 1228 IAC with available serological results was 4%, including 1.1% with acute or chronic infection and 2.9% with resolved infection. There were 36 children with evidence of recovery and 14 children with acute or chronic infec-tion, as shown according to birth country in Table 1.

Among the 14 adoptees with acute or chronic infec-tion, 4 of the families knew about the HBV diagnosis (from medical chart review) before adoption. All of those parents had confirmed receipt of HBV vaccine or verification of HBV immunity. For the remaining 10 adoptees with HBV infection, the parents had no knowl-edge of the diagnosis; only 1 parent had received HBV vaccine in preparation for travel and arrival of the child. Of particular interest, 1 adoptee with negative sero-logical results at the initial visit had evidence of acute HBV infection (positive HBsAg results) when repeat test-ing was performed 6 months later. This case is presented below.

CASE REPORT

A 23-month-old girl was evaluated after arriving from Vyshny Volocheck, Russia, with her adopted parents and an unrelated adopted brother from the same orphanage. The laboratory testing performed at 1 year of age indicated negative HBsAg results. There was no documentation re-garding maternal HBV status. The initial assessment of the girl at the CCHMC International Adoption Center at 23 months of age indicated height and head circumference measurements of⬍5th percentile and weight of 5th

per-centile. The child had no evidence of hepatosplenomegaly. Serological testing indicated negative results for all HBV markers. Hepatitis C and HIV serological tests also were nonreactive. The girl’s brother had protective levels of anti-HBs, consistent with vaccination.

At an evaluation 6 months later, the child was in good health and had received HBV vaccine 2 and 4 months after her initial assessment. Her examination results were unremarkable, with no icterus or hepatospleno-megaly being noted. Repeat serological testing for HBV yielded positive results for HBsAg and anti-HBc. HBV e antigen and anti-HBV e antibody assay results were negative. Testing for hepatitis A and D yielded negative results, and a repeat serological test for hepatitis C was nonreactive. The patient’s liver function test results were elevated (alanine aminotransferase: 740 U/L; reference range: 0 – 45 U/L; aspartate aminotransfer-ase: 630 U/L; reference range: 0 – 65 U/L).

The patient’s HBV genotype (D1) was determined with polymerase chain reaction and restriction fragment length polymorphism assays by Focus Diagnostics (Cypress, CA). After the diagnosis of HBV infection was made, the parents were tested, demonstrated no evidence of infection or pro-tection, and thus were appropriately vaccinated. The child’s HBsAg assay yielded positive results 6 months after the initial testing, confirming the diagnosis of chronic HBV infection. Her liver function test results had normalized by 3 years of age. The child cleared HBsAg at 4 years of age and developed anti-HBs at 52 months of age, demonstrat-ing recovery from HBV infection.

DISCUSSION

The existing literature varies greatly with regard to the prevalence of HBV among IAC, likely reflecting

differ-TABLE 1 Demographic Characteristics and Prevalence of HBV Protection and Infection According to Birth Country Countries and Regions Total,n

(%)

Female,n

(%)

Overall Age, Mean (Range), mo

HBV Protection,

n(%)a

HBV Infection,

n(%)

Age of HBV-Infected Children, Mean

(Range), mo

Russia 406 (33) 181 (45) 29 (6–201) 275 (68) 8 (2) 55 (13–157)

China 278 (23) 256 (92) 21 (6–168) 173 (62) 16 (6) 42 (11–168)

Guatemala 217 (18) 98 (45) 17 (4–136) 170 (78) 4 (2) 5 (4–6)

South Korea 65 (5) 25 (38) 12 (4–65) 40 (62) 4 (6) 11 (6–16)

Kazakhstan 64 (5) 31 (48) 30 (7–174) 40 (63) 2 (3) 95 (41–150)

Ukraine 36 (3) 13 (36) 59 (15–173) 14 (39) 3 (8) 40 (32–49)

Romania 24 (2) 10 (42) 39 (11–94) 13 (54) 1 (2) 75

Bulgaria 27 (2) 13 (48) 47 (21–164) 7 (26) 3 (11) 109 (43–150)

Other Eastern Europeb 12 (1) 8 (67) 19 (3–40) 6 (50) 0 (0) NA

Vietnam 24 (2) 15 (63) 22 (3–98) 8 (33) 0 (0) NA

India 23 (2) 15 (65) 31 (5–130) 19 (83) 0 (0) NA

Other Asia and Pacific Rimc 19 (2) 9 (47) 31 (3–152) 9 (47) 1 (5) 90

Ethiopia 12 (1) 6 (50) 69 (22–109) 4 (33) 2 (17) 65 (22–108)

Other Latin America and Caribbean regiond

12 (1) 5 (42) 55 (4–190) 7 (58) 1 (8) 190

Other Africae 9 (1) 6 (67) 72 (6–188) 4 (44) 5 (56) 77 (13–188)

Overall 1228 (100) 691 (56) 27 (3–201) 789 (64) 50 (4) 56 (4–190)

NA indicates not applicable.

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ences in geographic origins and the more-recent use of preadoptive screening. In a review of preadoptive med-ical charts for 43 children from Russia and Eastern Eu-rope, Albers et al2found that 2% of children had chronic

HBV infection. Other researchers detected that 3% to 5% of Chinese and Korean children were infected with HBV,2,3whereas Hershow et al4found prevalence rates

of 2.8% to 7% in Korean and Indian immigrant orphans in the 1970s and 1980s. Both Jenista and Chapman5and

Johnson et al6detected HBV infection in as many as 23%

to 53% of children from Romania. Hostetter et al7found

that 5 (2%) of 293 adoptees, mostly from Korea, Central and South America, India, and Haiti, had acute HBV infection, 2% had recovered from infection, and 9 (3%) had evidence of chronic infection. Of the 5% of adoptees who were HBsAg-positive, Asian ethnicity and receipt of blood transfusion before entry into the United States were associated risk factors.

Some studies performed incomplete serological test-ing (such as testtest-ing for HBsAg and anti-HBc alone3or

HBsAg and anti-HBs alone8), whereas our series used a

complete hepatitis panel as recommended,9,10which

al-lowed us to describe each outcome of infection (acute, chronic, or recovered) and to verify immunization. Our data indicated that 64% of children had evidence of immunization at the initial testing, whereas Saiman et al11found that only 35% of adoptees in their series had

protective anti-HBs. In that study, 53% of those with documentation of HBV vaccination in their birth coun-try had anti-HBs.

In our study, 16 of 380 IAC with no detectable anti-HBs at the first visit had documentation of 3 doses of HBV vaccine. This lack of antibodies may represent vac-cine nonresponders, waning immunity, or inaccurate documentation from the children’s birth countries. It is concerning that, of 47 children with repeat serological results indicating a lack of protective antibodies, 42 had documented vaccination (either in the birth country or in the United States). The Centers for Disease Control and Prevention (CDC)Pink Book12indicates that 16% to

40% of infants who have received 1 dose of HBV vaccine have protective anti-HBs levels (ⱖ10 mIU/mL). Protec-tion rates increase with addiProtec-tional doses; 80% to 95% of infants who have received 2 doses have protective anti-HBs, and 98% to 100% of infants who have received 3 doses have protective anti-HBs. It is not clear why the children in our study continued to lack antibodies.

Another interesting finding is that 18 children with initially negative anti-HBs results had not received any doses of vaccine in the United States when retested 6 months later, despite our recommendations. The Inter-national Adoption Center recommends that, if a child has no vaccination documentation and no anti-HBs at the initial testing, then the whole HBV series (3 doses) should be administered. If the child has no anti-HBs and has documentation of 2 or 3 doses of vaccine, then our recommendation is to administer 1 dose of vaccine and to recheck serological results at the 6-month visit. It is not clear why these children did not receive the recom-mended doses of vaccine. Possible reasons may be that the children did not visit their primary care provider, the

perceived risk of HBV was low, or, if multiple vaccines were needed, the HBV vaccine was postponed.

The prevalence of acute or chronic HBV infection in our study (1.1%) was slightly lower than that seen in other studies,2,11,13 although the prevalence of patients

with evidence of recovery (2.6%) was comparable. In our study, 29% of the adoptive parents knew that their child had acute or chronic HBV infection before adop-tion. Therefore, the prevalence of unsuspected HBV in-fection was⬍1%, a lower risk than in previous studies. This is likely attributable to routine preadoptive labora-tory testing in the child’s birth county identifying HBV status, as well as education that might influence deci-sions about adopting an affected child.

In our patient population, children with evidence of HBV infection emigrated from countries defined by the CDC as having intermediate or high prevalence of chronic HBV.14 High-prevalence (8%) countries and

regions include Africa, Southeast Asia (including China), Korea, Indonesia, Philippines, Haiti, and the Dominican Republic. Intermediate-prevalence (2%-7%) countries and regions include South Central and Southwest Asia, Israel, Japan, Eastern and Southern Europe, Russia, most areas surrounding the Amazon River basin, Hon-duras, and Guatemala. Given that 100% of children infected with HBV emigrated from these countries, the screening recommendations by the American Academy of Pediatrics1and the CDC15seem appropriate.

An issue of concern is how to interpret the findings for the 298 children ⬍12 months of age who had positive anti-HBs results in the initial testing. In our series, 1 child had negative anti-HBs results in repeat testing. That child had 3 doses of HBV vaccine documented in China and was 9 months of age when initially evaluated. It is possible the initial serological results reflected maternal antibodies and the child did not actually receive the documented doses of HBV vaccine, the vaccine was given but not of adequate quality, or the child was a nonresponder. Given this find-ing, at our center we now recommend, in addition to our general recommendations, that adoptees with initial test-ing performed before 12 months of age have repeat testtest-ing performed after 12 months of age.

Two children ⬎1 year of age had initial serological results that were positive for anti-HBs alone but repeat testing yielded negative results for all serological mark-ers. A 22-month-old child with no documentation in Russia received 1 dose of HBV vaccine after his initial visit and had negative anti-HBs results 3 months later. In addition, a 24-month-old child with 3 doses of vaccine documented in Russia had no protective antibodies 15 months after the last dose. The lack of serum anti-HBs in repeat testing may be reflective of an immunologic nadir (ie, the child has antibodies but levels are below the numerical cutoff value; however, the child would likely be protected if exposed). There are data on children with anti-HBs levels of⬍10 mIU who showed evidence of an anamnestic response after a booster dose of HBV vaccine was given,16,17and it is possible that these children would

be protected if challenged with HBV.

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a result of repeat serological testing (6 months later) after negative studies performed at the initial evaluation after arrival in the United States. Because this child had no high-risk exposures after emigrating and her adoptive sibling and parents had no evidence of acute or chronic HBV infection, it is likely that she acquired HBV in Russia near the time of her adoption.

The patient’s isolate (D1 genotype) was epidemiolog-ically linked to her birth country in southeastern Rus-sia,18 an area in which the incidence of HBV infection

doubled in the late 1990s. Other studies confirmed the D1 serotype in Russia,19,20 as well as the Middle East,

Eastern Europe,21India,22Kazakhstan, and Iran.23

HBV has a long incubation period, and negative se-rological results at our patient’s initial evaluation might have reflected infection just before emigration, because she likely was in the process of mounting an immune response. The recommendations to repeat HBV serolog-ical testing 6 months after the initial assessment are warranted, given the clinical, virological, and serological course of acute HBV infection. In acute infection, HBsAg is usually present 4 to 22 weeks after infection, whereas individuals with chronic infection have HBsAg persisting forⱖ6 months. Because the “window of opportunity” to detect HBsAg is limited, it is of utmost importance to obtain complete serological results (anti-HBs, HBsAg, and anti-HBc) to determine adoptees’ HBV status. In our case, it is likely that our patient acquired HBV through horizontal transmission, as suggested by reports from disease-endemic areas.4,24

Horizontal transmission from IAC to household mem-bers has been described25,26and is of additional concern.

The CDC and other experts have recommended that HBsAg screening be done in adopted or fostered orphans or unaccompanied minors from countries where HBV infection is endemic27–29and, if the child is

HBsAg-posi-tive, then family members should be vaccinated.1,4,30In

addition, the Advisory Committee on Immunization Practices recommends that HBV vaccine be given to adults who anticipate international travel to countries with high or intermediate prevalence of chronic HBV infection.30Unfortunately, our patient’s parents did not

receive HBV immunization before international travel and thus were not protected. Of 5 sets of parents who knew they were adopting a child with HBV, all con-firmed receipt of or received vaccination as recom-mended by the American Academy of Pediatrics1and the

Advisory Committee on Immunization Practices.30 For

the 9 children with ultimate diagnoses of chronic HBV infection (unknown at the time of adoption), only 1 of the parents had been vaccinated before adoption. In addition to reminding primary care providers to evaluate IAC with HBV serological testing 6 months after arrival in the United States, this case emphasizes the need for adoptive parents to confirm immunity or to obtain HBV vaccination before traveling to disease-endemic areas for adoption.

CONCLUSIONS

Approximately 2% to 5% of IAC are infected with HBV. This case reinforces the need for HBV serological testing

to be repeated 6 months after the initial testing. In addition, given the potential risk of HBV infection for families adopting children from disease-endemic areas, families should be counseled to seek immunization or to verify immunity to HBV before adoption and travel.

ACKNOWLEDGMENTS

Salary support to Dr Stadler during this research was pro-vided by Molecular Epidemiology Child Environmental Health NIEHS training grant 5-T32-ES010957-08, through the Department of Environmental Health, Division of Bio-statistics and Epidemiology, University of Cincinnati Col-lege of Medicine.

We thank Jen Andriga, Marina Bischoff, Tyler Brown-ing, Dee Daniels, RN, CPNP, Vanessa Florian, Kristen Frommier, Emilie Grube, Rotimi Okunade, and Elizabeth Roberts for their assistance with this study. We are in-debted to all of the wonderful children and their families who participated in this study, helping to improve the health of IAC in the future.

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IN DRUG CASE, JUSTICES WEIGH RIGHT TO SUE

“For nearly a century, Americans have been able to sue drug companies for deaths or injuries caused by medicines. Now the pharmaceutical industry and other big businesses are hoping the Supreme Court will sharply curb that right. In a case called Wyeth v. Levine, which the court will hear next week, a Vermont guitarist named Diana Levine lost an arm to gangrene caused by an improperly administered nausea drug. A Vermont jury awarded her $6.7 million in damages from Wyeth, accepting her argument that the drug maker should have put stronger warnings on the label. In its appeal of the verdict, the drug maker says the drug’s label was approved by the Food and Drug Administration, and it argues the federal regulator’s judgment should trump state law on issues of product safety. Many lawsuits are based on state consumer-safety regulations that often are stronger than federal standards. ‘This case is worth tens of billions to the pharmaceutical industry,’ said Ms Levine’s lawyer.’

Shelling Out: Payments in some major drug-related lawsuits:

Merck,Vioxx, Has agreed to more than $4 billion in settlements

Wyeth,Diet pills, About $20 billion in fen-phen-related costs

Lilly,Zyprexa, Settlements top $1.3 billion

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Munday A and Wang SS.Wall Street Journal. October 27, 2008

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DOI: 10.1542/peds.2007-2559

2008;122;1223

Pediatrics

Laura Patricia Stadler, Adam G. Mezoff and Mary Allen Staat

Hepatitis B Virus Screening for Internationally Adopted Children

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DOI: 10.1542/peds.2007-2559

2008;122;1223

Pediatrics

Laura Patricia Stadler, Adam G. Mezoff and Mary Allen Staat

Hepatitis B Virus Screening for Internationally Adopted Children

http://pediatrics.aappublications.org/content/122/6/1223

located on the World Wide Web at:

The online version of this article, along with updated information and services, is

by the American Academy of Pediatrics. All rights reserved. Print ISSN: 1073-0397.

Figure

FIGURE 2
TABLE 1Demographic Characteristics and Prevalence of HBV Protection and Infection According to Birth Country

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