Vaccine completion and infectious diseases screening in a cohort of adult refugees following resettlement in the U.S.: 2013–2015

There has been an unprecedented rise in vaccine-preventable infections around the world, including in immigrant and refugee communities [1, 2]. The number of refugees being resettled in the U.S. was severely limited between 2017 and 2020, but it is expected to rise in the coming years due to anticipated changes in federal policy on refugee resettlement. Unlike most immigrant groups in the U.S., U.S.-bound refugees are not required to receive vaccinations prior to arrival [3]. Prior studies in refugees have demonstrated low rates of baseline immunity to vaccine-preventable infections, including measles, mumps, rubella (MMR), and viral hepatitis [4‐9]. To address this, the U.S. Centers for Disease Control and Prevention (CDC) and the U.S. Department of State developed a pre-departure vaccination program for U.S.-bound refugees, which has been growing in implementation since 2013 [10]. However, gaps in immunity may still persist, particularly in refugees resettled prior to or in the early years of this program. Although guidance from the CDC recommends vaccinating eligible refugees following resettlement [3], the proportion of refugees who complete post-resettlement vaccination, especially of multidose vaccines, is unknown.

Screening practices for HIV and hepatitis C virus (HCV) among refugees in the post-resettlement period are also unknown. Mandatory pre-departure HIV screening has not been conducted in U.S.-bound refugees since 2010 [11, 12]. Therefore, HIV screening is recommended for all refugees following resettlement [12], but these recommendations may not be consistently followed [13, 14]. Our objective was to determine the proportion of refugees who complete post-resettlement vaccination and HIV and HCV screening.

A total of 111 subjects met inclusion criteria for this study (Table 1). The mean age was 34 years (range: 19–76 years), and 41% were female. Countries of origin included Iraq (53%), Afghanistan (19%), Eritrea (11%), and Ethiopia (5%); the remainder (13%) were from other countries of origin (i.e., Sudan, Syria, the Democratic Republic of Congo, and Colombia). The median time between resettlement in the U.S. and initial assessment in the refugee clinic was 34 days (interquartile range: 15–44 days).

Aggregate baseline immunity to all of measles, mumps, rubella, hepatitis A, and hepatitis B was present in 27 (24%) subjects (Table 2). Of the remaining 84 subjects who were vaccine-eligible for MMR, hepatitis A, or hepatitis B, 42 (50%) were fully vaccinated within 1 year of resettlement date. Serologic immunity and vaccine completion varied by country of origin (Fig. 1). Twenty-eight subjects (25%) were non-immune to any of measles, mumps, or rubella. Of these 28 subjects, 20 (71%) completed the two-dose MMR vaccine series, 6 (21%) received one dose of the series, and 2 (8%) did not initiate the series within 1 year of resettlement. Seventy-eight subjects (70%) were non-immune to hepatitis B. Of these, 46 (59%) completed the three-dose vaccine series within 1 year, 26 (33%) had initiated but not completed the series, and 6 (8%) did not initiate the series within 1 year of resettlement. Nearly all subjects (96%) were vaccinated with Tdap after resettlement. Baseline immunity to varicella was present in 90% of subjects. Thirty-four subjects met criteria for the HPV vaccine series (i.e., age below 26 years), of whom 5 (15%) received at least one dose during the study period.

Among those who were vaccine-eligible, older age was associated with a lower odds of vaccine completion (for each year increase in age, OR: 0.96, 95%CI: 0.93–0.99). In particular, subjects older than 50 years-old had a much lower odds of vaccine completion compared to those younger than 50 years-old (OR 0.12, 95%CI: 0.02–0.47). A higher odds of vaccine completion was noted in subjects who were male (OR: 2.38, 95%CI: 1.02–5.71) and English speakers (OR: 3.70, 95%CI: 1.04–17.49). Country of origin was not associated with a difference in vaccine completion (Table 3).

Of the 78 subjects (70% of the cohort) completing HIV screening, two (3%) were diagnosed with HIV after confirmation with HIV RNA testing. Both were successfully linked to care at a local HIV clinic. One hundred and ten subjects (99% of the entire cohort) completed screening for HCV; two subjects (2%) were positive for HCV Ab, of whom one had detectable HCV RNA.

Among 111 resettled refugees, 84 (76%) were eligible for at least one of the following vaccines: MMR, hepatitis A, or hepatitis B. Although 93% of vaccine-eligible subjects initiated vaccination(s), only 50% completed vaccinations within 1 year of resettlement. This demonstrates that refugees who resettled in the U.S. during this time period (2013–2014) remain vulnerable to vaccine-preventable infections long after resettlement.

A plausible reason for incomplete immunization is patient acceptability to return to clinic for multi-dose vaccine series. This may be why the three-dose series for hepatitis B had a lower completion rate (59%) than hepatitis A (83%) or MMR (71%), both of which are two-dose series, and Tdap (96%), a one-dose series. One factor that may improve these rates in the U.S. is implementation of the CDC Overseas Vaccination Program for U.S.-bound Refugees, a program which initiates age-appropriate vaccinations at international asylum sites in the months prior to departure to the U.S. At the time of our study, this program was beginning to be implemented in six countries but has since expanded to all sites processing U.S.-bound refugees. Documentation of overseas vaccinations at these sites is available to health providers in the U.S. through the CDC Electronic Disease Notification system [18].

The refugee health assessment is an important opportunity to ensure MMR immunity among refugee patients [1]. In this cohort, one in four subjects required MMR vaccination after resettlement. A prior study found a lower rate of MMR-eligible refugees (10%) from a sampling of asylum countries in East Africa and Southeast Asia [5]. That study found that 4% of MMR-eligible refugees did not receive a dose of the MMR vaccine during their initial encounter for the refugee health assessment, but they were unable to determine if vaccination was administered in subsequent encounters. Our study fills this research gap by looking at the post-resettlement period for a duration of 1 year. In our cohort, 8% of MMR-eligible subjects did not receive any doses of MMR vaccine within 1 year of resettlement, while 21% had received only one of the two-dose MMR vaccine series. This represents missed opportunities for the prevention of disease transmission, particularly in an era of frequent measles and mumps outbreaks.

Refugees in the U.S. frequently resettle from countries that lack nationwide hepatitis B vaccine programs, even though global hepatitis B vaccination coverage is improving [3]. Thirty percent of our cohort had baseline immunity against hepatitis B, which is comparable to a prior multi-center study of refugees [6]. We found that among those eligible for vaccination, only 59% completed the three-dose hepatitis B vaccine series within 1 year of arrival. This compares favorably to the general U.S. adult population which reports 25% vaccine coverage for hepatitis B [19]. However, this value is still too low given that individuals from hepatitis B-endemic countries remain at risk of incident infection even after resettlement in non-endemic countries [20].

Ten percent of subjects in this cohort were non-immune to varicella at the time of resettlement, which is consistent with previously published observations [7]. Varicella seroprevalence varies by age in different regions in the world; other studies have noted high varicella susceptibility in persons originating from tropical climates [21]. Varicella vaccination is not routinely available in many adult clinics (including ours at the time of this study) and therefore can be more challenging to provide for eligible adult patients. However, vaccination should be a priority since complications of varicella are more likely when primary infection occurs in adulthood [22].

Our study also evaluated the HPV vaccine series in eligible subjects. We found that among both men and women in our study cohort below the age of 26 years, only 15% had initiated the HPV vaccine series within 1 year of resettlement. Prior studies have noted marked disparities in HPV vaccination and cervical cancer screening among foreign-born persons in North America [23, 24]. A study of female Vietnamese-Americans found comparable rates of HPV vaccination and specifically noted an increased odds of vaccination among those who correctly recognized that HPV infection was not curable with medications [25]. This suggests room for improved counseling and education regarding the nature of HPV infection as a means to increase vaccination rates among foreign-born persons.

An important finding of this study was that only 70% of the cohort completed HIV screening, whereas 99% completed HCV screening. These data suggest a persistent stigma regarding HIV among refugee patients or a lack of perceived risk, despite an increased prevalence of risk factors for HIV and HCV infection among refugees, including exploitation during the migration process, exposure to sexual violence, and unregulated healthcare procedures [11]. HIV prevalence was 3% among those who underwent screening, which is comparable to a prior study of refugees resettling in Washington D.C. and higher than the general U.S. population [4]. Since 2010, refugees being resettled in the U.S. have not been required to undergo pre-departure HIV testing; HIV testing and counseling are therefore a crucial intervention in the refugee health assessment after arrival [11]. Our study reinforces the need to screen all refugees for both HIV and HCV in the current era of safe and effective therapies for both diseases to reduce the risk of long-term complications and transmission.

In a univariable analysis of predictors of vaccine completion among the vaccine-eligible, older age was associated with a lower odds of completing vaccination, particularly for those subjects greater than 50 years old. This may be related to decreased health literacy among older refugees or competing health issues for patients with more chronic conditions during follow-up visits. Subjects who were male and English speakers had greater odds of completing vaccination. This may be related to disparities in health literacy or challenges in navigating the healthcare system among refugees who are female and/ or non-English speakers [26, 27]. We do not believe that access to care or health insurance was a key determinant of these differences since all refugees in this cohort had insurance for the duration of this study and were seen in the same primary care network for other health needs.

These results should be interpreted within the limitations of study design. The seroprevalence estimates in this study may not reflect refugees who arrived in the U.S. after 2014, given the expansion of the Overseas Vaccination Program for U.S.-bound refugees and federal changes to refugee policies [10]. These data are from a single region in the U.S., serving refugees primarily from Iraq, Afghanistan, and East Africa. As compared to the rest of the state of Connecticut, and the remainder of the U.S., our study population under-sampled refugees originating from Southeast Asia, South Asia, Central/ South America, and Central Africa [28]. The sample size of this study population limited the precision of the point estimates and precluded a multivariable analysis. Therefore, the associations we found with vaccine completion may be subject to confounding. Although we could not capture vaccine administration in other healthcare settings, this was likely a rare occurrence because patients returned to the same primary care network for the rest of their healthcare needs. Further studies are needed to examine the reasons for incomplete vaccination and to develop approaches to improve vaccination among adult refugees. Reasons for incomplete vaccination in refugees, and effective approaches to improve vaccine completion, may be relevant to the general U.S. population more broadly [19].

In conclusion, almost all refugees eligible for vaccination with MMR, hepatitis A, and/ or hepatitis B initiated the recommended vaccination(s), but only 50% completed immunization within 1 year of their resettlement. Among those who completed HIV and HCV screening, 3% of refugees were newly diagnosed with HIV and 1% with chronic HCV. Refugee health providers must emphasize vaccinations and screening for chronic, treatable infections for their patients.