To assess the awareness of tuberculosis (TB) risk, performance of TB screening and factors predicting TB screening among prescribers of tumor necrosis factor alpha (TNF-α) agents.

1. INT J TUBERC LUNG DIS 16(9):1168–1173
© 2012 The Union
http://dx.doi.org/10.5588/ijtld.12.0029
E-published ahead of print 12 July 2012
Tuberculosis screening in prescribers of anti-tumor necrosis
factor therapy in the European Union
M. Y. Smith,* B. Attig,† L. McNamee,* T. Eagle‡
* Abbott Laboratories, Abbott Park, Illinois, † Psyma International Inc, King of Prussia, Pennsylvania, ‡ Eagle Analytics
of California Inc., San Diego, California, USA
SUMMARY
SETTING: Physician offices and hospital-based settings gists in non-G5 countries. Factors predictive of TB
in 24 European Union countries. screening included rheumatology or gastroenterology
O B J E C T I V E S : To assess the awareness of tuberculosis specialty, higher awareness of TB reactivation as a risk,
(TB) risk, performance of TB screening and factors pre- greater adherence to TB testing guidelines, larger case-
dicting TB screening among prescribers of tumor necro- loads of patients with severe disease, practicing in a ma-
sis factor alpha (TNF-α) agents. jor industrialized country and greater number of anti-
M E T H O D S : A total of 915 prescribers (441 rheumatol- TNF agents for which risk-related information had been
ogists, 266 gastroenterologists and 208 dermatologists) received.
of anti-TNF agents participated in a 41-item survey be- C O N C L U S I O N S : Most physicians reported being aware
tween March and May 2010. Multivariate analyses were of the attendant risk for reactivation of latent TB infec-
conducted to identify predictors of TB screening. tion with anti-TNF treatments. Results suggest that dis-
R E S U LT S : Overall, ⩾88% of physicians identified TB tributing pertinent educational materials is an effective
reactivation as an adverse effect associated with anti- component of a risk minimization strategy to promote
TNF use. Self-reported TB screening ranged from 73% TB screening among anti-TNF prescribers.
of gastroenterologists in the five foremost industrial- K E Y W O R D S : tuberculosis; screening; anti-TNF agent;
ized economies (G5) countries to 92% of rheumatolo- adalimumab; risk minimization
AGENTS THAT BLOCK tumor necrosis factor-alpha addiction, human immunodeficiency virus infection);
(TNF-α) are highly effective for treating auto-immune 2) performing a tuberculin skin test or a TB blood test;
conditions such as rheumatoid arthritis, Crohn’s dis- and 3) ensuring that a chest radiograph is taken.10–18
ease and psoriasis.1 However, as TNF-α plays a key If LTBI is found, initiation of prophylactic treatment
role in host defense against mycobacterial infection, is recommended prior to initiation of anti-TNF ther-
patients receiving such treatment have increased sus- apy. Regardless of the results of TB screening, contin-
ceptibility to serious infections, including tuberculo- ued monitoring for development of active TB during
sis (TB).2–5 Specifically, latent Mycobacterium tuber- the course of anti-TNF treatment is recommended.19
culosis bacteria, which are contained by an effective When prescribers of anti-TNF-α agents have a low
immune response, may progress to active TB infec- clinical suspicion of TB infection, the risk of TB-
tion in the context of anti-TNF-α treatment.6 related morbidity and mortality is increased.2,20,21 To
Anti-TNF-α agents are associated with reactiva- raise awareness regarding this risk, product manu-
tion of latent TB infection (LTBI); such infection usu- facturers can employ a number of different risk mini-
ally occurs at extra-pulmonary sites.4,7–9 The likelihood mization tools, including product labeling and TB
of reactivating LTBI can be substantially reduced by screening brochures, patient alert cards and safety
screening patients for TB infection before and during monographs. In some instances, such educational ma-
anti-TNF treatment and by promptly initiating ap- terials may be distributed as part of a risk minimiza-
propriate prophylactic therapy if needed.2 tion commitment.
Prior to initiation of anti-TNF treatment, it is rec- Despite its importance from a public health per-
ommended that multiple precautionary steps be taken spective, there has been little research on the aware-
to identify LTBI, including 1) taking a patient’s history ness of anti-TNF prescribers about the risk of TB or
to assess previous TB exposure and to identify social the extent to which they have adopted best practices
and medical risk factors (e.g., previous or active drug to reduce patients’ risk of TB reactivation.22 Our
Correspondence to: Meredith Smith, Abbott Laboratories, Bldg AP4Dept NJ44, 100 Abbott Park Road, Abbott Park, IL
60064, USA. Tel: (+1) 847 937 9464. Fax: (+1) 847 948 8050. e-mail: Meredith.Smith@abbott.com
Article submitted 11 January 2012. Final version accepted 13 March 2012.

2. Tuberculosis screening by anti-TNF prescribers 1169
study was designed to address this gap in the knowl- of safety issues associated with anti-TNF agents, ex-
edge base by assessing the awareness of TB infection perience prescribing them, types of testing conducted
risk and frequency of TB screening among anti-TNF to identify appropriate candidates for anti-TNF treat-
prescribers in European Union (EU) states. It also ment, whether anti-TNF agent risk-related educa-
sought to determine whether and to what extent peri- tional materials had been received from pharmaceuti-
odic TB re-testing was occurring and to identify fac- cal companies, and if so, what types. The survey was
tors predicting adherence to best-practice recommen- developed and pre-tested in English, and then trans-
dations for TB screening. lated into the main language of each participating
Our study focused on three anti-TNF agents on the country. The one exception was Belgium where French,
EU market: infliximab, etanercept and adalimumab. Dutch and German versions of the survey were avail-
The Summary of Product Characteristics (SmPC) for able and respondents were able to select their preferred
each of these three products states that prescribers language version. Respondents received financial com-
should screen patients for TB prior to prescribing and pensation (between US$50 and US$60 per interview
monitor them for TB throughout the duration of depending on the country) for survey participation.
anti-TNF treatment.23–25 We hypothesized that the
likelihood of conducting TB screening would be asso- Data analysis
ciated with the receipt of TB screening information Univariate and bivariate statistics were used to ana-
and related educational materials on anti-TNF agents. lyze study results. Responses to survey questions were
cross-tabulated by physician characteristics. For uni-
METHODS variate analyses, the χ2 test was used to compare the
frequency distribution of responses across physician
Study type and population groups. For between-group differences on values of
The study was a cross-sectional survey of rheuma- continuous variables, the Student’s t-test was used.
tologists, gastroenterologists and dermatologists in Significance levels were set at P < 0.05.
24 EU countries who prescribed anti-TNF-α agents. Multivariate logistic regression was used to ascer-
Countries were classified into two groups: the five tain the relative impact of each variable as a way to
foremost industrialized economies, or G5 countries differentiate physicians who performed TB testing
(Germany, France, Italy, Spain and the United King- from non-test performers. To assess TB screening per-
dom) versus the non-G5 countries.* The survey was formance, the dependent variable was defined as 1 =
conducted between 1 March and 31 May 2010. performs a TB history, uses either a purified protein
derivative (PPD) skin test or TB blood test, and con-
Sampling size and procedure ducts a chest X-ray for all patients to be prescribed
A random sample of anti-TNF-α prescribers by spe- any of the three anti-TNF agents (i.e., adalimumab,
cialty was generated within each of the participating etanercept or infliximab) vs. 2 = does not perform.
EU countries. The sampling frame was based on the Based on a literature review, 20 variables were iden-
top 10% of prescribers of adalimumab in the prior tified as potential predictors of TB testing.22 These
12 months (n = ~12 000, including 4338 rheumatol- variables included patient caseload characteristics,
ogists, 4511 gastroenterologists and 3151 dermatolo- physician training and practice setting characteristics,
gists). Sampling was stratified by specialty. physician awareness regarding TB risk, G5 status of
Both telephone and Internet-based methods were country where physician practiced, number of anti-
used for recruitment. Eligible physicians were 1) spe- TNF agents for which physician had received educa-
cialists or sub-specialists in rheumatology, gastro- tional materials and physician receipt of specific types
enterology or dermatology; 2) prescribers of adalim- of risk-related educational materials. After running the
umab for patients with rheumatic diseases, Crohn’s initial analysis with these 20 variables, seven proved
disease or psoriasis at some point within the past to be significant (P < 0.05 level) and were retained in
12 months; and 3) in Italy and Spain only, those who the final model: rheumatology specialty (yes/no), gas-
had been visited by a sponsor sales representative in troenterology specialty (yes, no), practices in a G5
the past year. Country-level response rates ranged from country (yes/no), is aware of TB as a risk associated
5.4% (Romania) to 35.73% (Spain).* with use of anti-TNF agents (yes/no), follows inter-
national, national or local guidelines for TB screening
Survey instrument (yes/no), percentage of patients with severe disease
The interview consisted of 41 questions and took ap- (i.e., rheumatoid arthritis, Crohn’s disease, psoriasis),
proximately 40 min to complete. Topics addressed and number of anti-TNF products for which safety
included demographic and clinical training charac- publications had been received.
teristics, patient caseload characteristics, awareness The logistic regression was performed using Proc
Logistic Statistical Analysis Software, version 9.2 (SAS
* A list of the participating countries and responses by G5 status Institute Inc, Cary, NC, USA) on a Windows XP 64 bit
can be obtained from the corresponding author. OS PC (Microsoft, Redwoods, WA, USA). Bootstrap

3. 1170 The International Journal of Tuberculosis and Lung Disease
Table 1 Physician characteristics by specialty and by G5 vs. non-G5 country status for 2010 survey
Rheumatologists Gastroenterologists Dermatologists
G5 Non-G5 G5 Non-G5 G5 Non-G5
(n = 229) (n = 212) (n = 173) (n = 93) (n = 138) (n = 70)
Characteristic % % % % % %
Practice setting
Hospital 81 88 92 90 78 76
Office 19 12 8 10 22 24
Mean number of years in practice 16 19 16 18 14 16
% time in direct patient care 84 75 82 75 82 75
Age, years
⩽39 29 19 32 16 49 29
40–49 39 33 38 44 29 28
50–59 26 36 27 32 21 33
⩾60 5 11 3 8 1 10
Sex
Male 64 51 80 85 58 54
Female 36 49 20 15 42 46
Time prescribing biologics, years
<1 3 13 22 17 30 33
1–3 11 25 57 60 57 56
>3 86 62 21 23 13 11
Patients of total caseload with indication for anti-TNF 25 26 21 19 14 15
TNF = tumor necrosis factor.
re-sampling was performed on the final model using and non-G5 countries alike, 95% of rheumatologists
an SAS macro available on the SAS web site called recognized TB reactivation as a risk. Similarly, a high
%JackBoot. Iterations (n = 500) of the classic boot- percentage of gastroenterologists (95% in non-G5
strap were run using the Proc Logistic module in SAS and 88% in G5 countries) and dermatologists (94%
(results available upon request to corresponding au- in non-G5 and 90% in G5 countries) reported recog-
thor). Model parameters were stable over repeated re- nizing TB reactivation as a risk.
sampling of our data. Estimates were bias-corrected.
All estimates were considered statistically significant Percentage reporting following guidelines
at the P < 0.05 level. for TB screening
Prescribers were also asked whether they followed
RESULTS any TB screening guidelines (e.g., international, na-
tional and/or local guidelines) prior to prescribing an
Physician characteristics anti-TNF agent: 92% of rheumatologists in non-G5
A total of 915 physicians participated in the sur-
vey (441 rheumatologists, 266 gastroenterologists and
208 dermatologists). The majority of the respondents
had practices located in a hospital setting as opposed
to an office (Table 1). Respondents had practiced for
a mean of 14 years (range 2–40); the majority were
male and aged >40 years. Most rheumatologists had
prescribed anti-TNF agents for >3 years (G5 coun-
tries, 86%; non-G5 countries, 62%). The majority
of the G5 and non-G5 gastroenterologists had pre-
scribed anti-TNF agents for 1–3 years (respectively
57% and 60%). Compared to the other specialty
groups, a higher proportion of dermatologists had
been prescribing biologics for <1 year (30%, G5;
33%, non-G5).
Awareness of TB reactivation as an adverse event Figure 1 Percentage of rheumatologists, gastroenterologists
associated with the use of anti-TNF agents and dermatologists who reported identifying TB as an adverse
event associated with anti-TNF agents: G5 vs. non-G5 EU mem-
Across all three specialties, physicians reported rec- ber countries, 2010. TB = tuberculosis; G5 = the five foremost
ognizing TB reactivation as an adverse event associ- industrialized economies; TNF = tumor necrosis factor; EU =
ated with anti-TNF agents as a class (Figure 1). In G5 European Union.

4. Tuberculosis screening by anti-TNF prescribers 1171
Figure 3 Percentage of rheumatologists, gastroenterologists
and dermatologists who reported ever re-testing their anti-TNF
agent patients for latent TB in G5 vs. non-G5 EU member coun-
tries, 2010. TB = tuberculosis; G5 = the five foremost industri-
alized economies; TNF = tumor necrosis factor; EU = European
Union.
Figure 2 Percentage of rheumatologists, gastroenterologists
and dermatologists who reported following guidelines for TB
testing of their patients prior to prescribing anti-TNF agents: countries. Physicians who reported being aware of
G5 vs. non-G5 EU member countries, 2010. TB = tuberculosis; risks for TB associated with the use of anti-TNF
G5 = the five foremost industrialized economies; TNF = tumor
agents were approximately twice as likely to screen
necrosis factor; EU = European Union.
as physicians who were not; similarly, those who re-
ported adherence to TB screening guidelines (either
countries and 85% in G5 countries reported that local or international) were 2.3 times more likely to
they did follow TB screening guidelines; 80% of gas- screen for TB than those who did not. Furthermore,
troenterologists in non-G5 countries reported that other significant predictors of TB screening included
they followed TB screening guidelines vs. 73% in G5 higher proportion of patient caseload with severe dis-
countries, while a similar percentage of dermatolo- ease (OR 1.02), and greater number of anti-TNF
gists in both G5 and non-G5 countries (76%) stated agents for which the physician received risk-related
that they followed TB screening guidelines when pre- educational materials (OR 1.32).
scribing anti-TNF agents (Figure 2).
TB re-testing
Predictors of TB screening Physicians were asked whether they ever re-tested pa-
Results of the logistic regression model showed that tients for TB following initiation of anti-TNF treat-
rheumatology and gastroenterology specialty status ment. Differences emerged by specialty and by G5 vs.
had odds ratios (ORs) of respectively 1.7 and 2.4, in- non-G5 country status (Figure 3). The lowest level of
dicating that individuals in these specialties were sig- re-testing was reported by dermatologists in non-G5
nificantly more likely than dermatologists to report countries (30%). Rheumatologists in G5 countries
conducting TB screening (Table 2). The G5/non-G5 were less likely to re-test for TB than their counter-
country status variable had an OR of 2.2, indicating parts in non-G5 countries (41% vs. 50%, P < 0.05),
that G5 physicians were significantly more likely to while the percentage of gastroenterologists in G5
screen for TB as compared to physicians in non-G5 countries who reported conducting TB re-testing
(33%) did not differ appreciably from that reported
by their counterparts in non-G5 countries (31%).
Table 2 Results of logistic regression for predictors of TB
screening by rheumatologists, gastroenterologists and Among those who reported conducting TB re-
dermatologists (n = 915) in select EU member countries, 2010 testing, the average time to re-testing ranged from
12 months (dermatologists in non-G5 countries) to
Point estimate
Predictors of OR (95%CI) 27.3 months (gastroenterologists in non-G5 coun-
tries). Specifically, the average wait time for G5 and
Rheumatologist (yes /no) 1.73 (1.16–2.60)
Gastroenterologist (yes /no) 2.41 (1.52–3.82) non-G5 rheumatologists before TB re-testing was ap-
Practicing in a G5 country (yes /no) 2.19 (1.56–3.08) proximately the same (respectively 25.6 months, 95%
Aware of risks of TB associated with use of confidence interval [CI] 1–12 vs. 25.3 months, 95%CI
anti-TNF agent 1.97 (1.10–3.53)
Follow any guidelines for TB testing (yes /no) 2.25 (1.51–3.33) 1–60). The mean wait time for gastroenterologists dif-
% of patients with severe disease (rheumatoid fered between G5 and non-G5 countries (18.8 months,
arthritis, Crohn’s disease, psoriasis) 1.02 (1.01–1.03) 95%CI 1–24 vs. 27.3 months, 95%CI 1–60). In con-
Number of anti-TNF agents for which they
had received safety publications 1.32 (1.15–1.54) trast, dermatologists reported the shortest mean in-
terval between TB re-testing in both G5 and non-G5
TB = tuberculosis; EU = European Union; G5 = the five foremost industrial-
ized economies; OR = odds ratio; CI = confidence interval; TNF = tumor countries (respectively 13.6 months, 95%CI 2–60 vs.
necrosis factor. 12.4 months, 95%CI 3–24).

5. 1172 The International Journal of Tuberculosis and Lung Disease
DISCUSSION These wide differences in monitoring practices may
reflect the fact that there is no EU or international
Our survey of TB risk awareness and screening is consensus recommendation on whether or how often
the first to be reported for EU prescribers of anti- to conduct TB re-testing.19
TNF-agents. Our study results provide a snapshot of This study had several limitations. First, TB screen-
physicians’ awareness of latent TB reactivation risk ing performance was based on physician self-report.
and reported TB screening practices for patients A number of factors, including social desirability and
with chronic inflammatory diseases being considered deficits in recall, may have affected the accuracy of
for anti-TNF treatment. The vast majority of physi- these responses. Second, we limited recruitment to
cian respondents reported being aware of the risk of high-volume prescribers of anti-TNF agents. This ap-
reactivation of LTBI in patients taking anti-TNF proach increased sampling efficiency but may have
agents. Most physicians reported utilizing guidelines introduced some selection bias. Third, we did not de-
—typically national guidelines—for conducting TB termine whether prescribers who reported not per-
screening tests prior to prescribing anti-TNF agents. forming TB re-testing had referred their anti-TNF pa-
Consistent with this, reported rates of TB screening tients to pulmonary specialists for such testing.
ranged from 73% (gastroenterologists in G5 coun-
tries) to 92% (rheumatologists in non-G5 countries).
CONCLUSION
Study results revealed room for improvement in
clinical practice across EU countries. About one in Receipt of anti-TNF safety information was associ-
every 10 anti-TNF prescribers reported not follow- ated with higher prescriber awareness of the risk of
ing any guideline for pre-treatment TB screening, and LTBI with anti-TNF agents as well as an increased
between 8% and 27% of physicians reported not likelihood of performing TB screening. These findings
screening their patients for TB.11,26 suggest that the provision of pertinent educational ma-
We found that rheumatologists and gastroenterol- terials can be an effective component of a risk mini-
ogists were at least twice as likely as dermatologists mization strategy to promote TB screening among
to screen potential anti-TNF users for LTBI; likewise, anti-TNF prescribers. Physicians who prescribe anti-
physicians in G5 countries were twice as likely to TNFs, particularly those in non-G5 countries, may
screen for TB as those in non-G5 countries. Physi- benefit from additional interventions that prompt and
cians who reported being aware of the risk of TB re- support them to conduct TB screening and monitor-
activation in patients on anti-TNF agents were ap- ing.30–34 To improve the effectiveness of risk minimi-
proximately twice as likely to screen patients as those zation efforts in this area, further studies are needed
who were unaware of or did not adhere to any guide- to understand and overcome barriers that constrain
lines. This finding underscores the value of providing knowledge transfer and behavior change in prescrib-
TB risk-related educational materials to prescribers. ers of anti-TNF agents.
The positive linear relationship between the number
of anti-TNF agents for which physicians had received Acknowledgements
safety-related educational materials and the likeli- The authors thank R Hoffman, B Paperiello and S Williamson for
hood of TB screening supports the learning concept input in the survey design and study implementation, and C Hof-
that the repeated receipt of reinforcing information mann for editorial assistance. Funding for this study was provided
from multiple sources can promote desired behav- by Abbott Laboratories. MS and LM are full-time employees of Ab-
bott Laboratories. BA of Psyma International Inc (King of Prussia,
ioral change among physicians.
PA, USA) and TE were paid as consultants by Abbott Laboratories.
A significant predictor of physician TB screening
was G5 country status. LTBI is much more prevalent
in non-G5 areas. TB incidence has increased in Europe References
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7. Tuberculosis screening by anti-TNF prescribers i
RÉSUMÉ
C O N T E X T E : Des bureaux des médecins et des contextes les rhumatologues dans les pays non-G5. Des facteurs
hospitaliers dans 24 pays de l’Union Européenne. prédictifs du dépistage de la TB comportent une spécialité
O B J E C T I F S : Evaluer le degré de prise de conscience du de rhumatologie ou de gastroentérologie, une meilleure
risque de tuberculose (TB), les performances du dépi- conscience du risque que représente la réactivation de la
stage de la TB et les facteurs qui permettent le dépistage TB, une meilleure adhésion aux directives des tests pour
de la TB chez les prescripteurs des agents facteur de né- la TB, une charge plus importante de patients atteints
crose tumorale-alpha (TNF-α). d’une maladie grave, le fait de pratiquer dans un pays
M É T H O D E S : En total, 915 prescripteurs (441 rhumato- avec une large industrialisation et un nombre plus grand
logues, 266 gastroentérologues et 208 dermatologues) d’agents anti-TNF pour lesquels des informations liées
d’agents anti-TNF ont participé à une enquête compor- au risque avaient été reçues.
tant 41 données entre mars et mai 2010. On a mené des C O N C L U S I O N S : La plupart des médecins ont signalé
analyses multivariées pour identifier les facteurs prédic- être conscients du risque qui accompagne les traitements
tifs du dépistage de la tuberculose (TB). anti-TNF en matière de réactivation d’une infection TB
R É S U LTAT S : La réactivation de la TB a été identifiée latente. Les résultats suggèrent que la distribution de
par ⩾88% des médecins comme effet indésirable associé documents éducatifs pertinents est une composante effi-
à l’utilisation des anti-TNF. Le dépistage auto-rapporté ciente de la stratégie de minimisation du risque visant à
de la TB a été de 73% chez les gastroentérologues dans promouvoir le dépistage de la TB par les prescripteurs
les cinq pays les plus industrialisés (G5) et de 92% chez de médicaments anti-TNF.
RESUMEN
MARCO DE REFERENCIA: Se realizó un estudio en me- rólogos de los cinco países más industrializados (G5) y
dios hospitalarios y en consultorios médicos de 24 países 92% por los reumatólogos de los demás países. Los fac-
de la Unión Europea. tores que predijeron la práctica de la detección siste-
O B J E T I V O S : Evaluar el conocimiento del riesgo de apa- mática de la TB fueron la especialidad en reumatología
rición de tuberculosis (TB), la práctica de la detección de o gastroenterología, un mejor conocimiento del riesgo
esta enfermedad y los factores asociados con la realiza- de reactivación de la TB, un mayor cumplimiento de las
ción de la investigación sistemática, por parte de quienes directrices sobre las pruebas diagnósticas de la TB, la
recetan medicamentos antagonistas del factor de necro- atención a un mayor número de pacientes con enferme-
sis tumoral alfa (TNF α). dad grave, la práctica en un país industrializado y la uti-
M É T O D O S : Participaron en el estudio 915 médicos que lización de una mayor cantidad de medicamentos con
recetan medicamentos anti-TNF (441 reumatólogos, efecto anti-TNF, sobre los cuales se había recibido in-
266 gastroenterólogos y 208 dermatólogos), los cuales formación relacionada con los riesgos.
respondieron a un cuestionario con 41 elementos entre C O N C L U S I Ó N : La mayoría de los médicos afirmó po-
marzo y mayo del 2010. Mediante análisis multifacto- seer conocimientos sobre el riesgo probable de reacti-
riales se definieron los factores que permiten predecir la vación de una infección tuberculosa latente con la ad-
práctica de la detección sistemática de la TB por parte ministración de tratamientos antagonistas del TNF.
de estos profesionales. Estos resultados indican que la distribución de material
R E S U LTA D O S : En las tres especialidades, 88% y más de didáctico pertinente, constituye un componente eficaz
los médicos reconocieron la reactivación de la TB como de una estrategia de disminución de riesgos, tendente a
una de las reacciones adversas asociadas con el uso de fomentar la detección sistemática de la TB por parte de
los medicamentos anti-TNF. La autonotificación de la los médicos que recetan medicamentos anti-TNF.
detección osciló entre 73% por parte de los gastroente-