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PEDIATRICS Vol. 108 No. 3 September 2001, pp. 608-612
,,
From the * Department of Pediatrics, Columbia University,
College of Physicians & Surgeons, New York, New York; Objective. Internationally adopted
children are at increased risk of infections acquired in their country
of origin. Ongoing surveillance of this unique population is needed to
detect changing epidemiology and provide appropriate care.
Methods. We performed a retrospective cohort study of 504 children adopted from abroad and evaluated from 1997 to 1998 to
determine the prevalence of and factors associated with various
infectious diseases.
Results. The mean age of the study participants at medical
evaluation was 1.6 years; 71% were girls, and they were adopted from
16 countries, including China (48%), Russia (31%), Southeast Asia (8%), Eastern Europe (8%), and Latin America (5%). Overall, 75 (19%) of 404 children tested had tuberculin skin tests Conclusions. We demonstrated increased rates of latent
tuberculosis infection and G lamblia infection than
previously reported. Thus, ongoing surveillance of internationally
adopted children, international trends in infectious diseases, and
appropriate screening will ensure the long-term health of adopted
children as well as their families.
Department of
Pediatrics, Winthrop-University Hospital, Mineola, New York; and
Divisions of § Quarantine and Tuberculosis Elimination, Centers for
Disease Control and Prevention, Atlanta, Georgia.
ABSTRACT
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Abstract
Methods
Results
Discussion
Conclusion
References
10 mm, but
all had normal chest radiographs. BCG vaccination (odds ratio [OR]:
7.37; 95% confidence interval [CI]: 3.29, 17.16) and being Russian
born (OR: 2.90; 95% CI: 1.68, 5.00) were risk factors for latent
tuberculosis infection. Fourteen (2.8%) children had detectable
hepatitis B surface antigen, but no child had active hepatitis C, human
immunodeficiency virus, or syphilis. Giardia lamblia
antigen was detected in 87 (19%) of 461 tested children, and such
children were older (mean: 22 months vs 15.5 months) and more likely to
have been born in Eastern Europe (OR: 2.82; 95% CI: 1.70, 4.68).
The number of internationally adopted children in the
United States increased rapidly during the past decade. The Department of State estimates that from 1989 to 1994, an average of 7738 children
were adopted annually, whereas in 1997 and 1998, 12 743 and 15 774
children were adopted, respectively.1 In 1997 and 1998, most children were born in Russia, China, South Korea, Guatemala,
Romania, and Vietnam.1 More than half were younger than 1 year, and approximately 75% were girls. Most families lived in New
York, California, Pennsylvania, New Jersey, and Illinois.
Children who are adopted from abroad are at increased risk of
infections acquired in their country of origin.2,3 Screening for potential infections is performed on arrival to the
United States to provide appropriate treatment, to prevent transmission
of infections, and to alleviate parental anxiety.4-7 We
report the results of screening of a recent cohort of internationally adopted children for latent tuberculosis infection (LTBI), hepatitis B,
and other infectious diseases to assess the changing epidemiology of
infections among such children.
Study Design
A retrospective cohort study was performed. The outpatient
medical records of internationally adopted children were reviewed to
determine the prevalence of and factors associated with several infectious diseases. Institutional review board approval was obtained from the Centers for Disease Control and Prevention, Columbia University, and Winthrop-University Hospital.
Study Participants and Setting
The study participants included 504 children who were adopted
from abroad and examined from January 1997 to December 1998 at the
outpatient international adoption practice of one of the authors (J.A.)
in Mineola, New York. Families were either self-referred or referred by
their primary care physician.
Standardized Screening for Infectious Diseases
Children who are seen in this practice are evaluated according
to a standard medical protocol that includes a tuberculin skin test
(TST) performed by the Mantoux technique and chest radiograph if TST is
positive; serology for hepatitis B (surface antigen and antibody, core
antibody), hepatitis C, syphilis, and human immunodeficiency virus
(HIV); stool for ova and parasites, including antigen testing for
Giardia lamblia8; and culture for bacterial
pathogens. HIV testing was performed by the New York State assay for
newborn screening.9 Stool studies and serologic assays
other than that used for HIV testing were done in different
laboratories, depending on the child's health insurance.
Clinical Characteristics
Medical records were abstracted during 1999 and 2000. The
demographic data collected for study participants included country of
origin, age at adoption, age at first medical evaluation, and the
setting where the child lived before adoption (eg, orphanage, foster
care). Preadoption immunization records, including receipt of BCG and
hepatitis B, were reviewed, and the presence of a BCG scar was noted.
Data Collection and Statistical Analysis
A computerized form was used for medical record abstraction. All
data were entered into Microsoft Access 97 database (Microsoft Corporation, Redmond, WA). A descriptive analysis of patient
demographics and an analysis of the prevalence of infections were
performed with the use of Microsoft Access. Mean age was analyzed by
the Student's t test using Microsoft Excel 97. Relative
risk in the form of odds ratios (OR) and 95% confidence intervals (CI)
was computed by Epi Info, Version 6.0 (Centers for Disease Control and
Prevention, Atlanta, GA). To compare the weights of children of
different ages, weight was converted to z scores (the
difference between the child's observed weight value and median weight
value of the reference population divided by the standard deviation value of reference population) based on medians and standard deviation for US-born children as published by the World Health
Organization.10,11
Demographic Characteristics of Study Participants
The mean age of these 504 adoptees on arrival to the United States
was 1.4 years (range: 1 month to 11.2 years) and at initial medical
evaluation was 1.6 years (range: 1 month to 11.7 years; Table
1). Most (71%) were girls. The majority
of children lived in New York (85%), but a minority lived in New
Jersey (10%), Connecticut (3%), Pennsylvania (1%), and other states
(1%).
TABLE 1
METHODS
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References
RESULTS
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Results
Discussion
Conclusion
References
Country of Origin by Age and Gender for Internationally Adopted
Children, 1997-1998 (n = 504)
Children were born in 16 countries, although most were born in China (48%) and Russia (31%; Table 1). Overall, 95% of the children from Russia, 84% of the children from China, and 88% of the children from other countries had lived in orphanages. Thus, the majority (88%) of children had resided in an orphanage before adoption.
Latent Tuberculosis Infection
TSTs were performed in 404 study participants (80%), and mean age
at testing was 1.6 years (Table 2). Of
these 404 children, 242 (60%) had evidence of BCG immunization by
either vaccination record or scar; 220 (54%) children had a BCG scar, 83 (21%) had a vaccination record indicating BCG immunization, and 61 (15%) had both. The TSTs of 75 (19%) children were 10 mm read 48 to
72 hours after placement, and all had normal chest radiographs. It was
recommended that these children receive isoniazid therapy for treatment
of LTBI.
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Of the 75 children with TST 10 mm, 67 (89%) had evidence
of BCG immunization as determined by a scar and/or preadoption immunization records. The z scores of weight for age were
not significantly lower in children with LTBI compared with uninfected children (P = .146). Risk factors for LTBI as
determined by univariate analysis included Russian birth (OR: 2.90;
95% CI: 1.68, 5.00; P < .001) and BCG immunization
(OR: 7.37; 95% CI: 3.29, 17.16; P < .001).
Hepatitis B Virus Infection
In all, 499 adoptees (99%) were screened for hepatitis B. Fourteen (2.8%) children had serology positive for hepatitis B surface antigen (HBsAg), 11 of whom were hepatitis B core antibody positive and 5 of whom were hepatitis B e antigen positive. No adoptee had clinical hepatitis B defined as jaundice or icterus. These 14 children came from 4 countries: 8 (3.3%) of 240 children were from China, 4 (2.6%) of 154 children were from Russia, 1 (8.3%) of 12 children was from Romania, and 1 (5.3%) of 19 children was from Vietnam. Country of origin and age on arrival to the United States were not associated with being HBsAg positive (data not shown). All 14 children who initially were positive for HBsAg were determined to be chronic carriers of hepatitis B, defined as persistence of HBsAg for more than 6 months. There were no reported cases of intrafamilial spread of hepatitis B.
We next examined the relationship among hepatitis B immunization, hepatitis B, surface antibody (HBsAb), and hepatitis B infection. In all, 175 (35%) of 499 study participants who were screened for hepatitis B had detectable HBsAb (Table 3). Preadoption immunization records from the countries of origin were available for only 178 children and indicated that 96 (19%) of 499 children received hepatitis B vaccine: 42 of 96 received 3 doses, and 29 (69%) of these 42 had detectable HBsAb; 21 received 2 doses, and 14 (67%) had detectable HBsAb; and 33 received 1 dose, and 8 (24%) had detectable HBsAb. Not surprising, immunized children (1, 2, or 3 doses) were more likely to be HBsAb positive than nonimmunized children (OR: 2.55; 95% CI: 1.58, 4.14; P < .001), but country of origin did not predict antibody response (data not shown).
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Gastrointestinal Tract Pathogens
Gastrointestinal (GI) pathogens were common among this cohort of internationally adopted children; 117 children had 1 or more pathogens noted. G lamblia antigen was detected in 87 (19%) of 461 children screened (Table 4). Being born in Eastern Europe, including Russia, Romania, Moldova, Bulgaria, and Hungary, was a risk factor for the acquisition of G lamblia (OR: 2.84; 95% CI: 1.70, 4.68; P < .0001). Children with detectable G lamblia antigen were older (mean age: 22 months) than children without this pathogen (mean age: 15.5 months; P < .001). The z scores of weight for age were not significantly different for children with G lamblia infection compared with uninfected children (P = .214). After treatment, the stools of 85 of 87 children were negative for G lamblia antigen; the 2 children who remained positive were retreated and cured.
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Stool microscopy often was abnormal: 455 (90%) of 504 study participants had 3 stool specimens tested for ova and parasites, and 32 children (7%) had 1 or more organisms identified. These included both pathogens and nonpathogens. Blastocystis hominis was found in 18 children, Dientamoeba fragilis was found in 10, Entamoeba coli was found in 7, Endolimax nana was found in 4, Hymenolepis nana was found in 3, and 1 child each had Ascaris lumbricoides, Chilomastix mesnili, and Entamoeba hartmanni. Stool cultures were positive for Campylobacter species in 5 children, for Shigella species in 3, and Salmonella species in 2. No children had Yersinia species isolated. Cryptosporidia species were identified by direct fluorescent antibody in 4 children.
Other Infectious Diseases
Hepatitis C serology was obtained in 496 (98%) of 504 study participants. Four were found to be hepatitis C antibody positive. Polymerase chain reaction testing for viral RNA was done in these 4 children, and none was positive. However, 2 children remained antibody positive after 1 year of age. Testing for syphilis was done in 478 (95%) of 504 adoptees ; 10 children had positive fluorescent treponemal antibodies and were rapid plasma reagin negative, and 1 child was rapid plasma reagin positive, but repeat testing was negative. Thus, no active cases of syphilis were diagnosed. Similarly, HIV serology was performed in 490 (97%) of 504 children , and 2 children had antibodies detected. However, because polymerase chain reaction DNA testing was negative, no cases of HIV infection were found.
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DISCUSSION |
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Since the 1980s, the unique medical needs of internationally adopted children have been recognized. Several previous investigators emphasized the importance of appropriate screening and treatment of infectious diseases such as TB, hepatitis B, syphilis, and GI pathogens.2,3,12,13 These earlier reports primarily examined children who were adopted from Korea and Romania. This study expands on these previous reports by examining the health status and needs of more recent adoptees. Many of the children in our study were born in China and Russia, as well as numerous other countries, which reflects the changing political, social, and economic conditions throughout the world.
Ongoing medical assessment of recently adopted cohorts of internationally adopted children is critical to address the potentially changing epidemiology of infectious diseases that are not always clinically apparent and to enhance targeted screening among this population. The outpatient international adoption practice studied had numerous advantages. This was a large cohort. Several countries of origin were well represented. The staff had frequent preadoption contact with agencies and parents. Screening and follow-up care were standardized and centralized. Furthermore, whereas some previous studies had relied on parental and physician questionnaires, in this study, medical records were reviewed. Overall, the screening algorithm used in this practice detected infectious diseases in 35% of participants; 75 children had LTBI, 117 had a GI tract pathogen (primarily G lamblia), and 14 were positive for HBsAg.
Early screening for TB is very important in internationally adopted children to offer appropriate intervention and care. Past rates of LTBI among adoptees have ranged from 0.6% to 5%.313-17 Thus, our rate of 19% is substantially higher than those previously reported. This may indicate a change in the epidemiology of TB among internationally adopted children and may be at least partially attributed to a change in the composition of countries of origin. Unlike previous reports, performed when most adoptees were born in Korea and Romania, our study participants were primarily from China and Russia. The association of LTBI with being Russian born is of particular concern given the rising rates of multidrug-resistant TB in Russia.18 Furthermore, 60% of the children in our study had received BCG and 88% had resided in orphanages. In contrast, of the 873 Korean adoptees previously described by Lange et al,15 none had received BCG and 90% had lived in foster care. Thus, a higher prevalence of BCG or more recent BCG use in our cohort also could account for our higher rate of positive TSTs. Although active TB is far less common than LTBI,3,13,15 a recent report described extensive transmission of TB to close contacts of a child adopted from the Marshall Islands.19 Although this child most likely did not have active TB at the time of adoption, administration of a TST on arrival to the United States and treatment for LTBI may have prevented the development of active disease. Future studies should continue to monitor rates of LTBI and assess the efficacy of isoniazid preventive therapy.
Numerous authors have recommended that internationally adopted children be screened for hepatitis B. Comparison of our results with previously published results highlights international differences in the epidemiology of hepatitis B infection. The highest rate of hepatitis B infection has been described in Romanian children (20%),12 whereas Chinese and Korean children had rates between 3% and 6%.14,16 Intrafamilial spread of hepatitis B from adopted children also has been documented,20-22 which further emphasizes the importance of screening children on arrival to the United States. Of note, most of these instances of intrafamilial spread were reported before the 1990s, when coverage for hepatitis B was somewhat lower in the American-born population than it is today.
There is no consensus about reimmunizing adopted children with hepatitis B vaccine.23,24 However, some experts recommend reimmunizing all internationally adopted children, regardless of antibody status or vaccination history, because of concerns about long-term immunity; use of outdated, poorly stored, or biologically impotent vaccines; potential suboptimal response to vaccines in malnourished children; and inaccurate or poorly documented vaccination records from the countries of origin. Our data corroborated these concerns, as 45% of children who received at least 1 dose of hepatitis B vaccine before adoption were negative for HBsAb, including 33% of those who had received 3 doses. However, more research is needed to evaluate and expand on these findings before definitive conclusions and recommendations can be made.
In general, screening for G lamblia among international
adoptees has proved to be fruitful. Previous studies demonstrated that
7% of adoptees from China,17 18% of adoptees from Romania,12 and 9% of 279 adoptees from various countries harbored G lamblia.3 However, previous studies
have reported no G lamblia infection among Korean
adoptees.14 G lamblia infection was very common
in our study participants, as 19% had G lamblia antigen
detected. We also found that rates in specific countries were higher
than previously published. Adoptees from China had twice the rate of
infection with G lamblia previously noted
15% versus
7%17and adoptees from Romania had 3 times the infection
rate previously reported50% versus 18%.12 Likewise,
extremely high rates were found in children from Eastern Europe,
particularly Bulgarian (67%), Romanian (50%), and Moldovan children
(36%). It is probable that the higher rate of G lamblia infection noted in our study reflects, in part, use of the G
lamblia antigen rather than microscopy. The children who harbored
G lamblia also were noted to be older than uninfected
children, which may suggest longer exposure to pathogens in their
country of origin before adoption. Although GI parasites were frequent
in our study population, bacterial pathogens were rare.
Experts have recommended that internationally adopted children be screened for syphilis, HIV, and hepatitis C. However, the prevalence of these infections has been very low, with the exception of Romanian-born children.25 Like our study, large cohort reviews have detected rare exposure to HIV and hepatitis C, as demonstrated by positive serologic tests. Rare reports of active syphilis have been found.12,14,16,17 It is likely that screening for HIV and treatment of syphilis occur in the countries of origin, limiting these diseases in children who are adopted. However, rates of HIV and syphilis are rising dramatically in countries in Eastern Europe as a result of changes in social, political, and economic conditions in the former Soviet Union.26,27 Thus, it is critical to continue to study the prevalence of HIV, syphilis, and hepatitis C among internationally adopted children to provide US pediatricians with updated guidelines for appropriate screening.
There are several limitations to this study. Only 178 (35%)
preadoption immunization records were available, and these may not be
accurate. Furthermore, lack of these records is not definitive proof of
lack of past immunizations, which may lead to misclassification of
preadoption immunization status. Laboratory tests were performed in
different laboratories using different assays. Birth dates often are
estimated, especially when children are abandoned. Some children were
seen only once at this international adoption practice, and subsequent
TSTs could not be included in this study. Finally, no standard exists
for the diagnosis of LTBI, and some of the TSTs 10 mm could have been
due to recent BCG immunization.
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CONCLUSION |
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Internationally adopted children continue to be at high risk for numerous infectious diseases. Judicious use of screening tests and appropriate treatment are critical to ensure the health of this unique population. Assessing the children's health also is important to prevent the transmission of infectious diseases to their adoptive families and to profile changing patterns of infectious diseases in other countries that may have an impact on the United States. The number of internationally adopted children has more than doubled in a decade, and the countries of origin also have changed. Thus, periodic surveys of large cohorts of internationally adopted children are important to monitor changing epidemiologic trends. To reach these goals, the American Academy of Pediatrics should periodically update clinical practice recommendations used by the physicians who care for children who are adopted from abroad.
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FOOTNOTES |
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Received for publication Nov 17, 2000; accepted Jan 22, 2001.
Address correspondence to Lisa Saiman, MD, MPH, Division of Infectious Diseases, Department of Pediatrics, Columbia University, College of Physicians & Surgeons, 650 West 165th St, New York, NY 10032. E-mail: ls5{at}columbia.edu
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ABBREVIATIONS |
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LTBI, latent tuberculosis infection; TST, tuberculin skin test; HIV, human immunodeficiency virus; BCG, bacille Calmette Guérin; OR, odds ratio; CI, confidence interval; HBsAg, hepatitis B surface antigen; HBsAb, hepatitis B surface antibody; GI, gastrointestinal.
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REFERENCES |
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This article has been cited by other articles:
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  I. Trehan, J. K. Meinzen-Derr, L. Jamison, and M. A. Staat Tuberculosis Screening in Internationally Adopted Children: The Need for Initial and Repeat Testing Pediatrics, July 1, 2008; 122(1): e7 - e14. [Abstract] [Full Text] [PDF]
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 D. Harmon TB Infection and Malnutrition Are Prevalent Among Internationally Adopted Children AAP Grand Rounds, February 1, 2008; 19(2): 14 - 15. [Full Text] [PDF]
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A. M. Mandalakas, H. L. Kirchner, S. Iverson, M. Chesney, M. J. Spencer, A. Sidler, and D. Johnson Predictors of Mycobacterium tuberculosis Infection in International Adoptees Pediatrics, September 1, 2007; 120(3): e610 - e616. [Abstract] [Full Text] [PDF]
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 R. Long MD and J. Boffa MIH Why internationally adopted children should be screened for tuberculosis Can. Med. Assoc. J., July 17, 2007; 177(2): 172 - 173. [Full Text] [PDF]
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 U. Sethuraman and D. Kamat Management of Child With Fever After International Travel Clinical Pediatrics, April 1, 2007; 46(3): 222 - 227. [PDF]
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 T. S. Murray, M. E. Groth, C. Weitzman, and M. Cappello Epidemiology and Management of Infectious Diseases in International Adoptees Clin. Microbiol. Rev., July 1, 2005; 18(3): 510 - 520. [Abstract] [Full Text] [PDF]
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 K. EKDAHL and Y. ANDERSSON IMPORTED GIARDIASIS: IMPACT OF INTERNATIONAL TRAVEL, IMMIGRATION, AND ADOPTION Am J Trop Med Hyg, June 1, 2005; 72(6): 825 - 830. [Abstract] [Full Text] [PDF]
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L. Miller, W. Chan, K. Comfort, and L. Tirella Health of Children Adopted From Guatemala: Comparison of Orphanage and Foster Care Pediatrics, June 1, 2005; 115(6): e710 - e717. [Abstract] [Full Text] [PDF]
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Pediatric Tuberculosis Collaborative Group Targeted Tuberculin Skin Testing and Treatment of Latent Tuberculosis Infection in Children and Adolescents Pediatrics, October 1, 2004; 114(4/S2): 1175 - 1201. [Abstract] [Full Text] [PDF]
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L. J. Nelson, E. Schneider, C. D. Wells, and M. Moore Epidemiology of Childhood Tuberculosis in the United States, 1993-2001: The Need for Continued Vigilance Pediatrics, August 1, 2004; 114(2): 333 - 341. [Abstract] [Full Text] [PDF]
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 F.-X. Weill, M. Demartin, D. Tande, E. Espie, I. Rakotoarivony, and P. A. D. Grimont SHV-12-Like Extended-Spectrum-{beta}-Lactamase-Producing Strains of Salmonella enterica Serotypes Babelsberg and Enteritidis Isolated in France among Infants Adopted from Mali J. Clin. Microbiol., June 1, 2004; 42(6): 2432 - 2437. [Abstract] [Full Text] [PDF]
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 L. H. Chen, E. D. Barnett, and M. E. Wilson Preventing Infectious Diseases during and after International Adoption Ann Intern Med, September 2, 2003; 139(5_Part_1): 371 - 378. [Abstract] [Full Text] [PDF]
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 Infectious Diseases of Internationally Adopted Kids Journal Watch Infectious Diseases, October 4, 2001; 2001(1004): 6 - 6. [Full Text]
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