Journal of Immigrant and Minority Health

https://doi.org/10.1007/s10903-022-01366-0

ORIGINAL PAPER

Factors Associated with Development of Tuberculosis Disease Among

Refugees, Massachusetts, 2008–2018
Laura Smock1   · Thinh Nguyen1 · Kavita Gadani1 · Andrew Tibbs1 · Paul L. Geltman1,2 · John Bernardo1,3 ·
Jennifer Cochran1

Accepted: 6 April 2022

© The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature 2022

Abstract
Refugees and immigrants undergo tuberculosis screening prior to arrival in the United States. CDC Technical Instructions
for screening changed in 2007. Our goal was to quantify TB disease in refugees after 2007 and identify risks for disease.
Massachusetts refugee and tuberculosis databases were matched to identify refugees who arrived 2008–2017 and were diag-
nosed with tuberculosis infection or disease 2008–2018. Factors associated with disease were analyzed in SAS. Of 19,583
refugees, 4706 were diagnosed with infection at arrival and 60 with disease during the observation period. Lack of treatment
for infection was strongly associated (OR = 26.5, p = 0.0001) with diagnosis of disease; in a multivariate logistic regression
model, positive screening test (AOR = 12.5, p = 0.0001), class B1 status (AOR = 4.0, p = 0.0004), and < 2 years since arrival
(AOR = 60.0, p = 0.0001) were associated with disease. Providers should continue screening new arrivals, providing acces-
sible services, and treating infection to further reduce tuberculosis morbidity and mortality.

Keywords  Tuberculosis · Refugee

Introduction have been incorporated into a national strategy for eventual

Tuberculosis (TB) has been declining in Massachusetts and
the rest of the United States (US) [1], but there is still a
significant burden of TB around the globe, with 1.4 million
TB deaths worldwide in 2019 [2]. In Massachusetts from
2016 to 2020, there were 184 TB disease diagnoses per year
on average, and the Massachusetts Department of Public
Health (MDPH) is committed to reducing TB morbidity and
mortality in the state. TB in Massachusetts disproportion-
ately affects those who were born outside the US; in 2020,
88% of 200 TB patients diagnosed in Massachusetts were
born outside the US [3]. To further reduce the incidence of
TB in the US, overseas and domestic screening for TB and
treatment of latent TB infection (LTBI) are beneficial and
* Laura Smock
Laura.smock@mass.gov
1 Studies in China, South Korea, and the Philippines found
Massachusetts Department of Public Health, Division
of Global Populations and Infectious Disease Prevention,
305 South Street, Boston, MA 02130, USA
2
Boston University School of Medicine, Boston, MA, USA
3 US [8–10]. There has been a decline in TB disease among
Boston University Medical Center, Boston, MA, USA
TB elimination [4]. TB screening is required for refugees
and immigrants prior to arrival in the US. Overseas panel
physicians are appointed by the US government to conduct
medical examinations following Technical Instructions
written by the Centers for Disease Control and Prevention
(CDC) [5, 6]. These were modified in 2007 and implemented
internationally over the next 6 years. The updated Technical
Instructions required sputum cultures, in addition to smears,
in applicants with an abnormal chest radiograph, to promote
detection of smear-negative, culture-positive tuberculosis
[7]. Applicants diagnosed with TB with a positive culture
must complete TB treatment prior to travelling to the US.
Travel is permitted for several classifications of TB findings
without treatment, including abnormal chest radiograph with
negative sputum smears and cultures (class B1), positive
interferon gamma release assay (IGRA) or tuberculin skin
test (TST) with normal chest radiograph (class B2), or expo-
sure to TB (class B3) [7].
that culture-based screening among applicants for US immi-
grant visas was more sensitive than the earlier reliance on
smear alone, reducing the importation of TB disease into the

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foreign-born individuals in the US since 2007 [11, 12].
More specifically, this decline was most apparent among
persons within 1 year of arrival in the US [13]. The Cali-
fornia Department of Public Health compared state cohorts
of immigrants from Mexico, the Philippines, and Vietnam
who were evaluated for tuberculosis before and after the
2007 change in the Technical Instructions, and reported
a decline in the proportion of persons with suspected TB
within 6 months of arrival in the US [14]. They recom-
mended additional state and national surveillance to monitor
the effectiveness of the revised Technical Instructions and
recommended that future studies include the expanded list of
countries to which these new technical instructions applied
[14]. We examined data on refugees from all departure coun-
tries over a 10-year time frame. We hypothesized TB disease
among refugees was rare in Massachusetts in the 10 years
following the change in the CDC Technical Instructions. The
goal of the analysis was to quantify TB disease in Massa-
chusetts after the change in the CDC Technical Instructions,
and to identify risk factors for TB disease among refugees.
Methods
The MDPH Institutional Review Board reviewed and
approved this study. MDPH maintains TB and refugee health
data in the Massachusetts Virtual Epidemiologic Network
(MAVEN) database [15]. TB disease was reported to MDPH
by providers and laboratories. A report was confirmed as TB
disease if laboratory or clinical criteria were met in accord-
ance with the CDC case definition [16]. A report was defined
as LTBI if there was a positive IGRA or TST at the refu-
gee health assessment performed within 90 days of arrival
in Massachusetts, and TB disease was ruled out based on
clinical evaluation, laboratory findings where applicable,
and radiology.
Refugees were reported to MDPH by CDC through
the Electronic Disease Notification (EDN) system and by
refugee resettlement agencies. The Massachusetts refugee
health database includes persons eligible for refugee health
services, including refugee health assessment. States or
Replacement Designees provide health assessments for
refugees during the first 90 days of arrival, either through
health department clinics or contracts with private provid-
ers. All refugees should receive TB screening at the health
assessment after arrival in the US by TST or IGRA. This
screening test best captures TB infection at the time of entry
to the US, and if positive these tests were included in the
dataset. Refugees, Special Immigrant Visa-holders (eligi-
ble Iraqi and Afghan translators and interpreters who have
worked directly with the US Armed Forces or under Chief
of Mission) [17], asylees and their derivatives, Cuban and
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Journal of Immigrant and Minority Health
Haitian entrants, and certified victims of trafficking qualify
for refugee health assessment services.
Refugees, Special Immigrant Visa-holders, and derivative
asylees undergo overseas medical examination, including
TB screening, according to the CDC Technical Instructions.
Since asylees, Cuban and Haitian entrants, and certified
victims of trafficking are granted these types of humanitar-
ian immigration status after arrival in the US, they do not
undergo the overseas medical examination. In this analysis,
all populations eligible for state-supported refugee health
assessment are referred to as refugees. US Department of
State categorizations were used for world regions: Europe
and Eurasia, Sub-Saharan Africa, East Asia and Pacific,
Near East, South and Central Asia, and the Western Hemi-
sphere [18].
A match was performed between state refugee and TB
MAVEN data. All refugees who arrived in Massachusetts
between 2008 and 2017 were included in the match. The
match identified refugees who were diagnosed with LTBI
at arrival, or TB disease between 2008 and 2018. An addi-
tional year of observation (2018) was included for arrivals
from 2017 to detect incident TB disease in that year. Match-
ing was an iterative process based on combinations of the
following variables: last name, first name, gender, date of
birth, phonetic last name, phonetic first name, Soundex code,
Spelldex code and reverse name. Algorithms were used to
determine whether an individual in the TB database was
the same individual as in the refugee database. The algo-
rithms were: (1) last name, first name, date of birth, sex; (2)
four characters of last name starting at character three, first
two characters of first name, date of birth, sex; (3) Soun-
dex codes for last name, first name, date of birth, sex; (4)
Spelldex code for last name and first name, date of birth; (5)
reverse first name and last name, date of birth, sex; and (6)
last name, first name, year of birth. The matching algorithms
were run sequentially, with matched records removed from
subsequent algorithms. If a refugee matched according to
one of six algorithms, he/she was considered to be a match.
A line list was created including refugees who were identi-
fied through the match as having a TB disease diagnosis,
and each record was reviewed manually for confirmation.
Another dataset was created for records identified through
the match as refugee with a diagnosis of LTBI upon arrival.
SAS 9.3 was used to count the records in each dataset. The
LTBI dataset was used for part of the bivariate analysis, to
examine association of incomplete LTBI treatment with dis-
ease (Fig. 1; Table 3).
In individuals with TB disease, the possibility local
transmission was assessed by seeking genotyping matches
among Massachusetts cases in the TB Genotyping Informa-
tion Management System (TB GIMS), a dataset maintained
by CDC that includes genotyping results on all culture-con-
firmed TB cases.
Journal of Immigrant and Minority Health

Table 1  Refugee arrivals and TB disease in Massachusetts 2008–

2018

Year Refugees Refugees with TB disease All TB

disease in
MA

2008 1517 4 261

2009 2216 3 244
2010 2202 7 222
2011 1811 7 196
2012 2269 5 215
2013 2021 9 201
2014 2165 8 199
2015 1927 9 192
2016 2432 7 190
2017 1023 1 210
2018 Not included in Not included in the dataset 200
the dataset
Total 19,583 60 2330

represented 96 different nationalities [19], including 26%

Fig. 1  Diagram of inclusion criteria for bivariate and multivariate
analyses
Bivariate analyses of risk factors were conducted to
examine associations with TB disease using SAS 9.3. Fac-
tors included sex, age group, world region of origin, whether
a medical exam was completed overseas prior to arrival,
TST result, IGRA result, class B TB classification, and
years since arrival. Treatment for LTBI was examined sepa-
rately with a different denominator. Crude odds ratios were
calculated, with 95% confidence intervals and p values to
determine statistical significance. The multivariate model
included any factors that were statistically significant in the
bivariate analysis, except for LTBI treatment, which had a
different denominator. Treatment for LTBI was not included
in the multivariate model. When analyzing data about LTBI
treatment, the dataset was restricted to include only those
refugees diagnosed with LTBI after either a positive IGRA
or TST at their refugee health assessment. For the other fac-
tors, the data were inclusive of all refugees.
Results
From 2008 to 2017, 19,583 refugees arrived in Massachu-
setts (Table 1). Refugees were 53.2% female and 46.8%
male; 39.3% were under age 20, 58.2% were age 20–64, and
2.4% were age 65 years and older; world region of origin
included 47.8% Near East and South Asia, 29.1% Africa,
9.7% East and Southeast Asia, 7.8% Latin America and
the Caribbean, and 5.5% Europe and Central Asia. Refu-
gees who arrived in Massachusetts during this time frame
from Iraq, 16% from Bhutan, 10% from Somalia, 8% from
Burma, 6% from the Democratic Republic of Congo, and
34% from other countries. Of the new arrivals, 89.2% had
undergone overseas medical screening prior to arrival by
panel physicians. (Table 2).
Sixty refugees were diagnosed with TB disease during
the observation period, and 4706 with latent TB infection at
refugee health assessment by 2018. The TB disease diagno-
ses were made following evaluation at TB clinics or other
facilities. Refugees comprised 2.6% of 2330 TB disease
diagnoses in Massachusetts during this time. Of all refu-
gees with TB disease, 35% were diagnosed clinically with
negative cultures; 42% of class B1 refugees with disease
had negative cultures overseas and were diagnosed clinically
with pulmonary TB in Massachusetts. The mean time from
arrival to diagnosis of TB disease was 514 days (median
288 days) (Fig. 2). Genotyping analysis indicated there was
only one case with possible local transmission. This geno-
typing match occurred between two family members and it
is unclear whether the transmission occurred overseas or in
Massachusetts.
The following factors were associated with development
of TB disease following arrival, in the bivariate analysis:
positive TST (OR = 9.0, 95% CI 3.4–25, p = 0.0001), posi-
tive IGRA (OR = 14.5, 95% CI 5.5–39, p = 0.0001), B1 clas-
sification by an overseas panel physician (OR = 6.7, 95%
CI 3.6–13, p = 0.0001), and less than 2 years since arrival
(OR = 42.2, 95% CI 24–74, p = 0.0001). Fifty of the 60 refu-
gees with TB disease had overseas medical screening prior
to entry to the US; of the 50 with overseas screening, 12
were class B1 with abnormal X-ray, negative sputum smears
and negative sputum cultures. There was an association

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 Journal of Immigrant and Minority Health

Table 2  Bivariate analysis of factors associated with TB disease among all refugees in Massachusetts 2008–2018
Risk factor Refugees with TB Total refugees % OR 95% CI P value
disease in MA

Total 60 19,583 0.3%

Sex*
 Male 34 9151 0.4 Ref
 Female 26 10,420 0.2 0.87 0.52–1.5 0.5944
Age group**
 < 5 years 1 1700 0.1 0.15 0.02–1.1 0.0598
 5–14 years 3 3953 0.1 0.19 0.06–0.63 0.0063
 15–19 years 6 2064 0.3 0.73 0.3–1.8 0.4823
 20–24 years 10 2346 0.4 1.1 0.52–2.2 0.8577
 25–44 years 27 6768 0.4 Ref
 45–64 years 11 2271 0.5 1.2 0.6–2.5 0.5867
 > 65 years 2 476 0.4 1.1 0.25–4.4 0.9435
World region of origin***
 Africa 25 5695 0.4 Ref
 Near East and South Asia 27 9360 0.3 0.66 0.38–1.1 0.1296
 East and Southeast Asia 5 1898 0.3 0.40 (combined due to 0.18–0.89 0.0254
 Europe and Central Asia 0 1085 0.0 small numbers)
 Latin America and the Caribbean 3 1529 0.2
Overseas medical exam
 Yes 50 17,466 0.3 Ref
 No 10 2117 0.5 1.7 0.84–3.3 0.1434
Skin test at entry
 Negative 5 7450 0.1 Ref
 Positive 18 2966 0.6 9.0 3.4–25 0.0001
IGRA at entry
 Negative 5 6140 0.1 Ref
 Positive 20 1708 1.2 15 5.5–39 0.0001
Class B TB classification ****
 No TB classification (including those 46 18,549 0.2 Ref
with no overseas exam)
 B1 (abnormal X-ray, negative smears 12 730 1.6 6.7 3.6–13 0.0001
and cultures, no overseas treatment)
 B2 (positive TST/IGRA) 2 289 0.7 2.8 0.68–12 0.16
Years since arrival
 Less than 2 years 42 1064 3.9 42 24–74 0.0001
 At least 2 years 18 18,518 0.1 Ref

*Twelve people had gender other or unknown

**Five people had unknown age
***Sixteen people did not have world region of origin documented
****Fifteen people had B3 classification, and none developed disease

between lack of overseas medical exam and development of
TB disease, but the association was not statistically signifi-
cant (OR = 1.7, 95% CI 0.84–3.3, p = 0.1434).
Of the 4706 refugees with a diagnosis of LTBI within
90 days of arrival in Massachusetts, lack of complete LTBI
treatment was strongly associated with development of TB
disease (OR = 26.5, 95% CI 8.3–85, p = 0.0001) (Table 3).
LTBI treatment completion was documented for three (5%)
refugees prior to the diagnosis of TB disease: Two were
prescribed isoniazid daily for 9 months, one developed iso-
niazid-resistant disease and the other developed pan-suscep-
tible pulmonary TB. The third was prescribed rifampin for
4 months and developed pan-susceptible TB. For each of
these individuals 3 to 4 years passed from completion of

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Journal of Immigrant and Minority Health

Fig. 2  Histogram of days from

arrival to diagnosis with TB
disease

Table 3  Bivariate analysis of Risk factor Refugees with Refugees % OR 95% CI P value

factors associated with TB TB disease with LTBI
disease, among refugees with
latent TB infection following LTBI treatment after entry
arrival in Massachusetts,
 Complete LTBI treatment 3 2744 0.1 Ref
2008–2018
 Never started OR incomplete 57 2022 2.8 27 8.3–85 0.0001
LTBI treatment

LTBI treatment to confirmation of TB disease. Genotyp- Discussion

ing of these three isolates provided no evidence for acquisi-
tion of reinfection TB by local transmission following LTBI After CDC Technical Instructions for immigrant and refu-
treatment. gee overseas TB screening were changed in 2007, refugees
Positive screening test, class B1 status, and less than 2 comprised only 2.6% of all TB disease diagnoses in Mas-
years since arrival were statistically significant in the bivari- sachusetts. Statistically significant risks associated with
ate analysis and were included in a multivariate model. In TB disease included positive screening test, class B1 sta-
a multivariate logistic regression model, positive screen- tus overseas, and recent arrival. There was an association
ing test (IGRA or TST) (AOR = 12.5, 95% CI 6.0–26, between lack of overseas medical exam and development of
p = 0.0001), class B1 status (AOR = 4.0, 95% CI 1.9–8.7, TB disease, but it was not statistically significant. Perhaps
p = 0.0004), and less than 2 years since arrival (AOR = 60.0, with larger numbers of arrivals in this category, the results
95% CI 31–116, p = 0.0001) were associated with develop- would reach statistical significance. Lack of complete treat-
ment of TB disease (Table 4). ment for LTBI was strongly associated with disease but was
not included in the multivariate model. Complete treatment
for LTBI among refugees should be prioritized by their pro-
viders and health departments. Approximately 80% of TB
disease in the United States is thought to be a result of pro-
gression over time from untreated LTBI [20].
Table 4  Multivariate analysis of factors associated with TB disease
among all refugees in Massachusetts 2008–2018 A recent CDC study found that post-arrival evaluation of
class B1 arrivals (including both refugees and immigrants)
Risk factor N % AOR 95% CI P value
is highly effective at identifying and treating LTBI and TB
Positive screening test 37 1 13 6.0–26 0.0001 disease, but strategies are needed to improve evaluation
Class B1 status 12 2 4.0 1.9–8.7 0.0004 and LTBI treatment rates [21]. Our analysis identified a
 < 2 years since arrival 42 4 60 31–116 0.0001 lower proportion of culture-negative TB disease diagnosed

13

clinically after arrival among refugees, compared to the
CDC’s national dataset of class B1 immigrants and refu-
gees. The CDC study found 53% of class B1 arrivals with
TB disease nationally were diagnosed with culture nega-
tive TB disease after arrival. This analysis identified 35%
of all refugees with TB disease were diagnosed clinically
with negative cultures in Massachusetts. Of refugees with
class B1 status overseas, who were diagnosed with TB dis-
ease in Massachusetts, 42% were diagnosed clinically with
pulmonary TB. In Massachusetts and nationally [21], class
B1 refugees are more likely than class B1 immigrants to
undergo timely evaluation after arrival. Refugees have sup-
port from case managers in all states, as well as community
health workers in Massachusetts, to facilitate attendance at
TB clinic appointments.
Shorter time since arrival in the US was associated with
development of disease in this analysis. Another study
reviewed records from 2001 to 2008, and found nonimmi-
grant visitors (students, temporary workers, exchange visi-
tors, tourists, and business travelers) to the US contributed
substantially to the burden of TB among foreign-born indi-
viduals, specifically within the first year of their arrival and
from countries with a high burden of TB [22]. TB may have
a shorter incubation period than previously thought [23];
new arrivals to the US may have been recently infected prior
to departing their home countries. At this time only immi-
grants and refugees are required to undergo pre-departure
TB screening; non-immigrant arrivals to the US, such as
students and temporary workers, are not required to undergo
the overseas medical process. Therefore, US public health
programs and primary care providers should prioritize TB
education, TB screening, and LTBI treatment for recent
arrivals from regions of high TB risk.
The analysis has several limitations. While we observed
that refugees made up a very small proportion of all TB
disease diagnoses in the state after the 2007 change to the
CDC Technical Instructions, we cannot show causality;
other factors may have contributed to infrequent diagnosis
of TB among refugees during this time period. The data-
set did not include data on TB among refugees prior to the
change in the CDC Technical Instructions, so we are unable
to draw conclusions about a decline after the change, only
that TB diagnoses were rare after the change. Refugees who
arrived at the beginning of the period of observation (2008)
had more opportunity to develop TB than those who arrived
in 2017. It is possible that some people may have developed
TB after 2018 and were not included in the dataset.
Some refugees may have moved out of Massachusetts
before 2018. We are unable to track movement out of state,
and it is possible some refugees who originally resettled
in Massachusetts may have been later diagnosed with TB
in another state. If any refugees were diagnosed with TB
disease outside of Massachusetts, they would be missing
13
Journal of Immigrant and Minority Health
from this analysis, and the percentage of refugees with TB
presented here may be low. We are unable to assess whether
refugees are more or less likely to move out of the state
soon after arrival, and we are unable to assess differences
between refugees who move out of the state compared to
those who stay.
This analysis differs from previous publications because
it includes 10 years of data on refugees from all departure
countries. The findings add to the body of evidence that
importation of TB to the US among immigrants and refugees
was low after adoption of a culture-based screening algo-
rithm by CDC for immigrants and refugees in 2007. Health
departments should continue screening all refugees, evalu-
ating class B1 arrivals, providing outreach and community
education, and treating LTBI to further reduce the incidence
of TB disease. Health departments should support refugees
to ensure completion of LTBI treatment. Complete treatment
for LTBI among refugees is important to prevent future TB
disease diagnoses. Primary care providers should also screen
for, and ensure treatment of, LTBI among new arrivals to the
US to further reduce TB morbidity and mortality.
Acknowledgements  This paper is dedicated to the memory of Vernard
Green of the Centers for Disease Control and Prevention, who provided
initial and ongoing encouragement to the authors. The project was sup-
ported by a grant from the Centers for Disease Control and Prevention,
Epidemiology and Laboratory Capacity for Prevention and Control of
Emerging Infectious Diseases (ELC) Cooperative Agreement, CK19-
1904, section K. Thank you to the Massachusetts refugee health assess-
ment sites, resettlement agencies, TB clinics and community health
workers who screened, treated, and supported refugees with TB.
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