Each year, children from many countries around the world are adopted by families in the USA. Since 1999, over 230 000 children from other countries have been adopted by American families. International adoptions peaked in 2004 and have since decreased (Fig. 1). The majority of internationally adopted children had come from China, Russia, Guatemala, South Korea, and Ukraine. However, more recently, adoptions for China decreased, and Ethiopia has become the second leading country from which children are adopted by US families (Fig. 2) . Ratification of the Hague Convention (http://www.hcch.net), changes in adoption policies in China, increasing costs, and reported fraud associated with international adoption are reasons reported for the decline. Since 2003, international adoptees are older on average. Fewer young children (<1 year) have been available for adoption, and older children (1–2 years and 5–12 years) have increasingly been adopted (Fig. 3) . International adoptees share several common characteristics, including limited access to reliable healthcare and documented medical histories, challenging living conditions and settings (orphanages, families, and foster care), and diverse, often underdeveloped countries of origin. These predispose children to a number of medical problems and infections.
Prior to admission, the US Department of State requires that all children under consideration for adoption undergo a medical examination by a US designated physician in their country of origin. This examination is required to complete the visa application and is limited to screening for certain communicable diseases and evaluation for serious physical and mental disorders (http://www.cdc.gov/immigrantrefugeehealth). The Immigration and Nationality Act of 1996 stipulated that anyone seeking residence in the USA must show proof of vaccination with vaccines recommended by the Advisory Committee on Immunization Practices (ACIP). In 1997, this law was amended with a waiver that allows children younger than 10 years to receive these vaccines in the USA within 30 days of their arrival.
Infectious diseases are a primary concern when evaluating internationally adopted children, especially those from underdeveloped countries. Many children come from countries with a high prevalence of intestinal parasites and tuberculosis (TB) and where screening of pregnant mothers for hepatitis B, HIV, and syphilis is inconsistently performed [2–4]. Infections among international adoptees have resulted in a community outbreak of TB and prompted multistate investigations of measles [3–8]. These incidents reinforce the need to provide timely medical evaluations of internationally adopted children. While some medical issues are identified before adoption, other problems are missed or become apparent after adoption . A comprehensive evaluation of the child by a health practitioner knowledgeable in adoption medicine is essential. The focus of this review is to discuss the pre- and post-adoption evaluation for infectious diseases among internationally adopted children.
Prior to placement in the USA, all international adoptees must undergo medical evaluation in their home country. Medical records are meant to be available to parents and pediatricians for review. However, family histories and information relating to pregnancy, labor, postnatal, medical, and family histories are often unavailable due to the absence of the child's birth-parents. When records are available, pediatricians have to decipher and interpret medical terminology used in other countries. Perinatal encephalopathy and dysbacteriosis are frequently reported in records of children from Russia, but are rarely confirmed after adoption and evaluation in the USA . Occasionally, photographs and movie clips may be available and reveal features and stigmata of congenital and other infections. Laboratory tests performed in their home countries are sometimes available for review, that is, HIV antibody, hepatitis B surface antibody and antigen test, and syphilis (TRUST in China and Wasserman reaction/RW/WR in Russia). Laboratory results, if available, must be interpreted with caution as they may have been performed in laboratories which may not be reliable or may have been performed many months prior to adoption. Thus, a negative test result may not guarantee the absence of infection, and these tests along with others should be repeated on arrival in the USA (Table 1). Immunization records of international adoptees are also frequently missing or incomplete . When available, vaccine records are often confusing because the age at which immunizations were started and administered may differ from US immunization schedules. Another concern is the administration of lower potency vaccines to children who are frequently chronically ill and/or malnourished, making it difficult to assess whether the vaccine effectively induced protective immunity .
Parents need protection as well. They should seek advice before travel and receive recommended vaccines appropriate for the country of travel, and update missing vaccines [13,14]. Information on travel requirements and vaccines is available from the US Centers for Disease Control and Prevention (http://wwwnc.cdc.gov/travel/). Household members and close contacts of the adopted child should update and complete missing or delayed vaccines .
International adoptees should be evaluated within a few weeks of arrival in the USA. The evaluation and medical assessment should include a review of the available medical history (which may be inaccurate), a physical examination (vision, hearing, growth, and developmental screening), and a comprehensive laboratory screening based on previous exposure, infectious disease risks, nutritional status, and ethnicity [4,16]. While infectious disease-related issues are the most frequently identified problems, other undiagnosed metabolic, hematologic, and neurologic problems have also been identified . Commonly encountered infections and recommended screening tests for internationally adopted children are summarized in Table 1[17,18▪▪].
Hepatitis A virus (HAV) is prevalent in many of the countries where children of international adoption originate. In one study, anti-HAV antibodies were detected in 29% of 279 international adoptees. The rates were highest in children older than 2 years and those from Africa, Latin America, Eastern Europe, and Asia . Screening for anti-HAV antibodies at the initial visit distinguishes acute from past infection, susceptible children, and immune children (Table 1). Children susceptible to HAV should receive HAV vaccine if older than 1 year .
All adopted children should be tested for hepatitis B virus (HBV) infection. In the 1990s, HBV surface antigen was detected in up to 5% of children of international adoption, especially those from Asia, Africa, central and Eastern Europe [2,3,10]. Since then, HBV vaccine use in infants has increased worldwide. However, administration of HBV vaccine at birth to prevent perinatal transmission remains suboptimal. Screening for HBV infection in international adoptees is recommended both to prevent HBV transmission to close contacts and to prevent consequences of chronic HBV infection. Children found to be chronically infected (Table 1) should undergo additional testing, and consultation with a pediatric infectious disease or liver specialist to assess if treatment is needed. Household contacts of children with acute or chronic HBV infection should also receive HBV vaccine and be counseled on practices to prevent transmission [20,21].
Similarly, testing for antibody to hepatitis C virus (HCV) is recommended for children adopted from countries where the prevalence of HCV is high (e.g. Russia, China, Eastern Europe, Africa, and Southeast Asia) . A previous study found that up to 1.3% of internationally adopted children had HCV infection . Detection of anti-HCV antibodies should be confirmed by nucleic acid testing for HCV RNA. All children with confirmed HCV infection require further consultation with a pediatric infectious disease or liver specialist. Re-testing for HCV in 6 months is recommended if initial screening results were negative. Transplacentally acquired HCV antibodies in young infants may remain detectable in serum up to 18 months of age and may not indicate infection .
All children must be screened for HIV infection prior to adoption (Table 1). Although adoptees frequently originate from countries with high rates of HIV infection, the incidence of HIV infection among international adoptees is low. In a study of international adoptees at 17 international adoption clinics, fewer than 1% of children had HIV infection . A history of failure to thrive, recurrent infections, developmental delay, opportunistic infection, and delayed dentition are suggestive of HIV infection, although malnutrition and/or prolonged stay in an orphanage may result in a similar clinical presentation. Some experts recommend that all children younger than 6 months be screened for HIV infection using HIV DNA PCR and that they be re-tested by HIV ELISA in 6 months if initial screening was negative. Since 2010, US immigration laws have permitted waivers for HIV-infected children. Consequently, adoptive parents in the USA are seeking and adopting children with known HIV infection, and these children may now constitute one of the largest sources of new pediatric HIV cases in the USA. Because of increasing global access to antiretroviral drugs, some international adoptees have access to and are on antiretroviral therapy. All children of international adoption with HIV infection need consultation with a pediatric infectious disease specialist for the management of their HIV infection.
Children are frequently adopted from countries where the prevalence of syphilis is high and perinatal screening is suboptimal. As such, congenital syphilis often remains undiagnosed. International adoptees are usually screened for syphilis in their home country and frequently treated if infected. However, up to 3% of international adoptees were diagnosed with congenital syphilis after their arrival in the USA [3,6,26]. Regardless of history and report of treatment, all children should be re-evaluated for syphilis with nontreponemal test, and if positive, confirmed by a treponemal serologic testing (Table 1). Children with a positive syphilis serologic test and confirmed syphilis infection need further evaluation (audiology, vision, neurologic, cerebrospinal fluid, long-bone radiographs, etc.) in conjunction with a pediatric infectious diseases specialist to assess the need for treatment.
Mycobacterium tuberculosis, along with other lesser known members of the Mycobacterium tuberculosis complex (M. bovis and M. africanum), is prevalent in countries where many international adoptees come from [26,27]. In spite of the widespread use of the bacille Calmette-Guérin (BCG) vaccine in these countries, drug-resistant M. tuberculosis and HIV circulate widely [12,28]. Among international adoptees screened, 5–19% were found to have a positive tuberculin skin test (TST) [3,27]. Whereas latent TB infection (LTBI) is most common in adopted children, active TB infection is not rare. An international adoptee was responsible for a community outbreak of TB in North Dakota . Screening for TB among international adoptees should be performed (Table 1) with TST or an interferon gamma release assay (for children >5 years), regardless of a history of BCG vaccination. Interpretation of the two screening methods is defined in the 2012 Red Book . Children found to have a positive TST or interferon gamma release assay should be carefully examined for symptoms and signs of TB, including a chest radiograph. Children assessed as LTBI should be treated with a course of isoniazid for 9 months. Children with active pulmonary or extra-pulmonary TB should be treated with multiple drug regimens. Every attempt should be made to obtain specimens (sputum, gastric aspirate, and lymph node) for mycobacterium culture and susceptibilities to help guide drug therapy. In the absence of culture information, drug therapy choices should be based on TB resistance patterns in the child's home country. Consultation with a pediatric infectious disease specialist is recommended and TB infections should be reported to the local health department.
Intestinal parasite infections are common among internationally adopted children. Up to 27% of international adoptees have one or more pathogen(s) detected after arrival in the USA. The most common parasite, Giardia lamblia, has been identified in 19% of children [3,29▪▪]. Entamoeba histolytica, Dientamoeba fragilis, Ascaris lumbricoides, Trichuris trichura, Strongyloides stercoralis, and other parasites have also been detected [2,3,29▪▪,30]. The prevalence of parasites in adoptees varies by country, with higher rates among older children and in children adopted from Ukraine, Ethiopia, and Russia [23,29▪▪]. Reversible effects of chronic parasite infection (i.e. growth delay, anemia, and impaired cognition) are frequently present in international adoptees. Gastrointestinal symptoms such as diarrhea may be absent or underappreciated because of language barriers and young age . All international adoptees should be screened on arrival with at least three stool specimens tested for ova and parasites, collected 2–3 days apart [29▪▪]. Additional stool testing for Giardia by immunoassay increases detection rates . Treatment of Giardia and some parasites is recommended, and is particularly important if the child is symptomatic or malnourished. Recommended drugs for the treatment of parasites are summarized in the 2012 Red Book . Repeat testing of stool for ova and parasites should be performed after treatment. Occasionally, children have a negative stool examination, but have peripheral eosinophilia. Further evaluation for parasites that have a tissue phase during their life cycle (Ascaris, Strongyloides, and Toxocara), and other less common causes of eosinophilia, should be performed (Table 1). In children with eosinophilia in whom evaluation for parasites is negative, empiric treatment with albendazole may be considered .
IMMUNIZATION AND VACCINE-PREVENTABLE DISEASES
The completeness of adoptee immunization records varies by country. Records from South Korea are usually adequate. However, a significant proportion of records are incomplete, and when available are questionable [2,10]. In earlier studies, 37–65% of international adoptees had no documentation or deficient vaccination records [11,34]. Moreover, among those with vaccine records, only 53–70% had protective antibodies to previous vaccinations [30,35]. For adoptees presenting with vaccine records, providers have to decide what vaccines to administer. Several options exist, including disregarding previous vaccinations and beginning immunizations appropriate for the child's age, or verification of the vaccine records by measuring antibodies to vaccines previously administered, followed by selective immunization if antibodies are low or absent (Table 1). Most experts re-immunize children younger than 1 year and malnourished children and reserve antibody testing for older children . Measuring antibody levels in older children has been reported to be cost-effective in assessing the need for further immunization . However, in a recent study, children who had completed their primary vaccine series (≥3 documented doses of vaccine) in their home country, protective immunity was documented against diphtheria (85%), tetanus (95%), hepatitis B (77%), Haemophilus influenzae type b (67%), and polio (93%). This rate was significantly higher than among those with fewer doses . To minimize unnecessary serologic testing and/or vaccination for international adoptees with documented and completed primary vaccine series it is reasonable to accept vaccine records from their home country and complete immunizations with vaccines appropriate for the child's age. Children with deficient, delayed, or questionable immunization records should re-start and complete immunizations with vaccines appropriate for their age. Immunization recommendations are summarized in the 2012 Red Book and the ACIP 2012 policy statement on Recommended Childhood and Adolescent Immunization [15,37].
Because children are adopted from many different countries, uncommon infections unique to those regions have been identified in children of international adoption. These include Chagas disease, malaria, yaws, measles, scabies, lice, and leprosy [26,38,39]. Identification, screening, and treatment of some uncommon infections can be found in reference texts [40,41]. Other medical problems should be addressed or referred to pediatric subspecialist as needed.
The evaluation of children of international adoption can be complex. Because infections and immunization issues are common among international adoptees, infectious disease specialists and pediatricians serve vitally important roles in working with the family to identify the child's healthcare needs. A comprehensive evaluation of the child (medical history, physical examination, and appropriate laboratory testing) is crucial for the early identification and treatment of medical problems, including infections. Screening for infections and evaluation of previous immunizations are central to the diagnosis and medical management of these children.
The author thanks C. Stockmann and Drs J. Christenson and A. Pavia for their critical review of the manuscript. Funding: National Institute of Allergy and Infectious Diseases [grant number U01A1082482] and the Centers for Disease Control Prevention [U18-IP000303–01].
This project was further supported by the University of Utah, Department of Pediatrics through the Children's Health Research Center and the Pediatric Clinical and Translational Research Scholars Program, the H. A. and Edna Benning Presidential Endowment, and the Primary Children's Medical Center Foundation.
Conflicts of interest
There are no conflicts of interest.
REFERENCES AND RECOMMENDED READING
Papers of particular interest, published within the annual period of review, have been highlighted as:
- ▪ of special interest
- ▪▪ of outstanding interest
Additional references related to this topic can also be found in the Current World Literature section in this issue (p. 155).
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