Article
Reference
Prevalence of positive tuberculosis skin tests during 5 years of screening in a Swiss remand prison
RITTER, Catherine, ELGER, Bernice Simone
Abstract
Tuberculosis (TB) screening in prisons is recommended, but the appropriate methods remain controversial. Studies evaluating screening in remand prisons are scarce.
RITTER, Catherine, ELGER, Bernice Simone. Prevalence of positive tuberculosis skin tests during 5 years of screening in a Swiss remand prison. International Journal of Tuberculosis
& Lung Disease , 2012, vol. 16, no. 1, p. 65-9
DOI : 10.5588/ijtld.11.0159 PMID : 22236848
Available at:
http://archive-ouverte.unige.ch/unige:29138
Disclaimer: layout of this document may differ from the published version.
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Prevalence of positive tuberculosis skin tests during 5 years of screening in a Swiss remand prison
C. Ritter, B. S. Elger
University Centre of Legal Medicine of Geneva and Lausanne, Geneva, Switzerland
Correspondence to: Catherine Ritter, Centre Universitaire Romand de Médecine Légale, 9 av de Champel, 1211 Geneva 4, Switzerland. Tel: (+41) 22 757 31 12. Fax: (+41) 22 757 42 24. e-mail: catherine.ritter@unige.ch
Article submitted 11 March 2011. Final version accepted 19 July 2011.
B A C K G R O U N D : Tuberculosis (TB) screening in prisons is recommended, but the appropriate methods remain controversial. Studies evaluating screening in remand prisons are scarce.
M E T H O D : Between 1997 and 2001, voluntary screen- ing based on the tuberculin skin test (TST) was offered to all prisoners on entry into the largest remand prison in Switzerland. Prisoners with positive results underwent chest X-rays. We analysed this information collected in an anonymous database.
R E S U LT S : A total of 4890 prisoners entered the prison and were eligible for screening; 3779 (77.3%) had TST performed on average 9 days after arrival: 46.9% were
positive (induration ⩾ 10 mm). Positive TST rates were similar over the 5 years. Women were more likely to have a negative TST (60.4%) than men (47.7%; P <
0.001, Pearson’s χ2 16.5). Positive TSTs varied according to the prisoner’s country of origin (64% for sub-Saharan Africa, 57% for Eastern Europe, 56% for North Africa, 51% for Asia and 34% for North and West Europe).
C O N C L U S I O N : The percentage of TST-positive subjects was high, and most did not receive preventive treatment for latent TB. The usefulness of systematic TST for all prisoners on entry is limited, as diagnosis of TB disease usually remains the priority in prisons.
K E Y W O R D S : prison; screening; tuberculin skin test
TUBERCULOSIS (TB) is an important health threat in prisons worldwide.1–6 TB incidence in prisons clearly exceeds values reported among the general population.7,8 TB outbreaks,9,10 transmission of drug- resistant TB and TB transmission in the community by former inmates are of particular concern.11–13
It is therefore of considerable importance to imple- ment effi cient TB screening on entry. International rec- ommendations agree that the highest priority should be given to detecting TB disease.14,15 The US Centers for Disease Control and Prevention (CDC) recom- mend that, even in facilities with minimal TB risk (i.e., where no cases of infectious TB have been ob- served in the last year, and with an insignifi cant number of inmates with risk factors for TB), all newly arrived inmates should be evaluated for factors pre- disposing them to TB infection, or progression to TB disease if already infected.16 Those with risk factors such as human immunodefi ciency virus (HIV) posi- tivity, recent immigration from high TB prevalence countries, injecting drug use, diabetes, history of TB or close contact with TB cases, should undergo a tu- berculin skin test (TST), a QuantiFERON®-TB Gold (QFT-G) test (Cellestis, Carnegie, VIC, Australia) or a chest radiograph (CXR) within 7 days.
The adequacy of a screening system depends on several factors: the prevalence of TB disease and in-
fection in the population screened, the prevalence of risk factors, the risk of transmission, practical issues related to the organisation of prison life and the re- sources of its medical department.
The present study presents TB screening data col- lected between 1997 and 2001 from the largest re- mand prison in Switzerland. The objective of our analysis was to explore the following questions:
1) What is the prevalence of latent TB infection (LTBI) and how many prisoners could be candidates for preventive treatment? 2) How many TB suspects could be identifi ed using TST and CXR? 3) How many detainees did not complete screening and why?
MATERIALS AND METHODS
The remand prison (for those awaiting trial) in the canton of Geneva was originally built for 270 prison- ers, but hosted 450–500 during the study period, with 2400 entries per year; the average length of stay was 60 days; three to fi ve inmates usually shared a cell. The medical staff comprised four full-time gen- eral practitioners and the equivalent of 12 full-time nurses. Nurses were present 24 h a day and oversaw all prisoners at entry.
Since 1992, the TST (0.1 ml of 2 tuberculin units of purifi ed protein derivative [PPD] RT23, Statens
S U M M A R Y
66 The International Journal of Tuberculosis and Lung Disease
Serum Institute, Copenhagen, Denmark) was used to screen prisoners and was offered to all detainees in the fi rst week of incarceration. Participation was voluntary. In case of refusal, CXR was offered. De- tainees with a positive TST (induration of ⩾10 mm, 5 mm in HIV-positive or immunosuppressed subjects or those with recent exposure to TB disease) under- went a CXR in the following 7 days. CXR could also be refused. Nurses interviewed prisoners systemati- cally at entry to detect symptoms of active TB, his- tory of prior TB and bacille Calmette-Guérin (BCG) vaccination status. CXRs were evaluated by a senior radiologist.
The study was approved by the President of the Central Ethics Commission of the University Hospi- tal of Geneva. The following data were entered into an unlinked anonymous computer fi le after release:
age, sex, country of origin, date of prison entry and release, history of prior BCG vaccination (if known), result of previous TST (if known), and dates and re- sults of TSTs and/or CXR. The results of sputum or culture analyses were kept in the prisoners’ medical records and were not available for analysis.
We used SPSS for Windows (version 13.0, Statisti- cal Package for the Social Sciences Inc, Chicago, IL, USA) to carry out statistical analyses; χ2 and Student’s t-tests were used to compare the different groups, with differences signifi cant at P ⩽ 0.05.
RESULTS
Population who underwent TST
Between 1 January 1997 and 17 January 2002, 4890 prisoners were incarcerated and were thus eli- gible for the screening process; 3779 (77.3%) under- went TST an average of 9 days (median, mean 16;
standard deviation [SD] ±38) after arrival.
No difference was found between women (2.5%) and men (2.9%; P = 0.71) regarding origin from countries with rates of multidrug-resistant TB (MDR- TB) of ⩾10%.17 Mean age (29.1 years) was higher among those who underwent TST than those who did not (28.0 years, P = 0.001). More women (83.2%) u nderwent TST than men (76.8%, P = 0.04). Prison- ers from some sub-Saharan African countries were underrepresented: <65% of those from Congo, Bur- kina Faso, Côte d’Ivoire and Sierra Leone underwent screening. Characteristics of prisoners eligible for screening are given in Table 1, and their region of ori- gin is shown in Table 2.
TST results
The TST results are known for only 3445 of the screen- ing participants. If we also take into account the 15 de- tainees who underwent TST shortly before entry, 1774 prisoners in total were TST-positive (36.3% of the 4890 prisoners eligible for screening and 46.9%
of the 3779 prisoners in the study pop ulation), while
Table 1 Characteristics of prisoners eligible for screening (n = 4890)
Characteristic n (%)
Mean age, years 29 [SD 10]
Range 13–83 Length of incarceration, days Median: 41
Mean: 87 [SD 133]
Sex
Women 370 (7.6)
Men 4250 (92.4)
SD = standard deviation.
Table 2 Origin of prisoners eligible for screening (N = 4890)*
Origin
Women n (%)
Men n (%)
Total n North and Western Europe 96 (25.9) 1035 (22.9) 1131 Ex-Yugoslavia and
Eastern Europe (<5%) 48 (13.0) 928 (20.5) 976 Sub-Saharan Africa 31 (8.4) 837 (18.5) 868
Switzerland 88 (23.8) 619 (13.7) 707
North Africa 12 (3.2) 417 (9.2) 429 North (<1%) and
South America 62 (16.8) 250 (5.5) 312
Asia 18 (4.9) 269 (6.0) 287
Unknown 15 (4.1) 165 (3.7) 180
Total 370 (100) 4520 (100) 4890
*P < 0.01 (differences in origin between men and women using the χ2 test).
Table 3 TST results per year, 1997–2001
Year, results n (%) TST (%)
1997
TST-negative 250 (40.1) 51.9
TST-positive 232 (37.2) 48.1
482 (77.2) 100
No TST 142 (22.8)
Total 624 (100)
1998
TST-negative 364 (35.4) 46.0
TST-positive 427 (41.6) 54.0
791 (77.0) 100
No TST 236 (23.0)
Total 1027 (100)
1999
TST-negative 400 (35.1) 48.1
TST-positive 432 (37.9) 51.9
832 (73.0) 100
No TST 307 (27.0)
Total 1139 (100)
2000
TST-negative 367 (35.5) 51.8
TST-positive 341 (33.0) 48.2
708 (68.5) 100
No TST 326 (31.5)
Total 1034 (100)
2001
TST-negative 305 (28.6) 48.3
TST-positive 327 (30.7) 51.7
632 (59.3) 100
No TST 434 (40.7)
Total 1066 (100)
TST = tuberculin skin test.
1686 were TST-negative. The results were unknown for 334 subjects due to early release. A negative TST result was obtained in 60.4% of the women vs. 47.7%
of the men (P < 0.001, Pearson’s χ2 16.5). The vari- ability of positive TSTs over the years is not statisti- cally signifi cant (P = 0.111, χ2 test).
The TST diameter was known for 1469 subjects only (information lacking in the records): the mean induration was 13.8 mm (SD ±5.1, median 13 mm);
it was >20 mm for 5% of the participants. TST results per year during the period 1997–2001 are given in Ta- ble 3. Results by geographic region, absolute number and percentage of positive TSTs are given in Table 4.
Chest X-ray findings
In total, 1190 (67.1%) TST-positive detainees under- went CXR within a mean delay of 7.7 days (SD ±32, median 2); 584 TST-positive prisoners did not un- dergo CXR as required by the screening procedure instructions, 108 underwent CXR without prior TST, and the total number of CXRs performed was 1298.
CXR results were known for 909 cases: 823 were nor- mal and 86 abnormal; 26 showed abnormal fi ndings other than TB, mostly emphysema; 21 showed lesions compatible with previous TB, although active TB was not excluded; and 24 had lesions characteristic of TB sequelae. Seven CXRs showed specifi c TB lesions;
these prisoners had been diagnosed before arrival at the prison and they were already on anti-tuberculosis treatment. Eight more CXRs were abnormal: 4 showed specifi c TB lesions and 4 suspicion for TB. Five in- mates with abnormal CXR were from high TB preva- lence countries (Mali, Angola, Algeria, Ivory Coast).
None of the eight cases with abnormal CXR were from countries known for high MDR-TB prevalence.
The CXR results (n = 909) are shown in Table 5.
Screening drop-outs
Of the 1774 detainees with a positive TST, 1190 un- derwent CXR and 108 had a CXR without prior TST. A total of 3553 detainees (3445 + 108) under- went initial screening, while 2601 were fully screened (3553 − 952 TST-positive detainees without CXR re- sults, 53.1% of the initial eligible population of 4890).
Preventive treatment
A total of 823 detainees were TST-positive with a normal CXR. By setting an upper age limit of either 25 or 35 years (according to the cantonal practice of the Geneva Centre for Tuberculosis Control at that time18), preventive treatment would be indicated for respectively 296 or 603 detainees. Only seven actu- ally received treatment, and their length of incarcera- tion allowed them to complete the 6-month regimen of daily isoniazid (INH).
Point prevalence
Eight prisoners were undergoing anti-tuberculosis treatment on entry. We detected four CXRs compati- ble with TB disease (typical lesions), and 25 others with lesions suspicious of TB. Taking into account the eight cases receiving TB treatment and the four new cases with typical lesions, the point prevalence of TB disease was estimated to lie between 12 and 37 per 4890, i.e., a point prevalence of between 245 and 757 per 100 000. Considering only the new cases, the point prevalence was estimated at between 82 (4 cases with specifi c lesions) and 593 (25 cases with suspicious CXR) per 100 000.
DISCUSSION
Prevalence of latent TB infection
We found a high prevalence of positive TSTs (46.9%) at entry to this Swiss remand prison. Comparative data in prisons are rare, ranging between 13% in New South Wales, Australia,19,20 18% in Italy,13 4.6–
32.8% in the United States,21 48% in Pakistan22 and 55.5% in Spain.23 Another study conducted in
Table 4 TST results in the study population by country*
or geographic region, 1997–2001
Geographic region
TST Negative
n (%)
Positive
n (%) Total Ex-Yugoslavia 280 (44.2) 353 (55.8) 633 Sub-Saharan Africa 196 (36.0) 348 (64.0) 544
Switzerland 286 (57.9) 208 (42.1) 494
France 257 (58.9) 179 (41.1) 436
North Africa 125 (43.6) 162 (56.4) 287 South America 104 (42.3) 142 (57.7) 246
Portugal 94 (58.8) 66 (41.3) 160
Asia 62 (49.2) 64 (50.8) 126
Italy 60 (60.0) 40 (40.0) 100
Spain 49 (58.3) 35 (41.7) 84
Eastern Europe 31 (43.1) 41 (56.9) 72 North and West Europe† 40 (65.6) 21 (34.4) 61 Former Soviet Union 26 (46.4) 30 (53.6) 56 North America 8 (61.5) 5 (38.5) 13
Unknown 68 (51.1) 65 (48.9) 133
Total 1686 (48.9) 1759 (51.1) 3445
*Highly represented countries, i.e., Switzerland, France, Portugal, Italy and Spain.
† Excluding Switzerland, France, Portugal, Italy and Spain.
Table 5 CXR results (n = 909)
n (%) No CXR report or no CXR performed 3984 (81.5)
Normal CXR 823 (16.8)
Abnormal CXR, other than TB 26 (0.5) TB confirmed and already undergoing
treatment at entry 7 (0.1)*
TB sequelae (previous, inactive TB lesions) 24 (0.5) Specific TB lesion, previously unknown 4 (0.1) Lesions suspicious for TB, previously unknown 4 (0.1) Lesions of unknown origin, possibly previous
TB, active disease not excluded 21 (0.4)
Total 4890 (100)
*In one more patient undergoing anti-tuberculosis treatment at entry, CXRs had been taken previously at the hospital and were not repeated at entry.
CXR = chest X-ray; TB = tuberculosis.
68 The International Journal of Tuberculosis and Lung Disease
1994 (n = 201) in the same setting in Switzerland showed 35% positive TSTs,18 but comparisons were limited by methodological differences between the two studies.
Comparable data among the general population are scarce. One study, based on contact tracing, con- ducted in the same canton as the present study, showed that the prevalence of positive TSTs in prison (42%) was higher than among the general exposed popula- tion: 30% of Swiss and 40% of foreign-born persons were TST-positive (36% of all tested persons).24
Previously BCG-vaccinated persons are signifi cantly more likely be TST-positive than non-vaccinated per- sons.25 Nonetheless, the high percentage of positive TST results in the current study could not be explained by vaccination, as we observed a discrepancy between positive TST results and origin from a country with routine BCG vaccination. Information on BCG vacci- nation was therefore considered invalid in our study.
The greater number of negative TST results in women could be partially explained by geographic origin, as more females than males were of Swiss ori- gin (23.8% vs. 13.7%). Most TST-positive prisoners were young and, among those who underwent CXR, most were normal. A large number of prisoners ful- fi lled the criteria for LTBI; however, only a small percentage received preventive treatment. This could be explained by the widespread opinion among health staff that it is useless to start treatment if it is interrupted by the prisoner’s release. As the average length of incarceration was 2 months, most detainees would not complete INH treatment while in prison.
In addition, obtaining blood for monthly liver en- zyme testing in a great number of detainees receiving INH was found to overstrain the available time of the health care staff. Instead, staff preferred to inform detainees about diagnostic fi ndings and recommend a post-release visit to the Geneva Centre for Tubercu- losis Control, free of charge, to those remaining in Switzerland.
Estimated TB disease incidence
Our study was limited by the high number of refusals and incomplete screening. This may have affected the representativeness of our results, in particular of TB incidence estimates. Furthermore, our study analysed data from an irreversibly anonymous database. We were therefore unable to check the medical records to confi rm TB disease. During the study period one to two cases of TB disease were diagnosed in the prison (Jean-Paul Janssens, personal communication, Ge- neva Centre for Tuberculosis Control). From these numbers, we estimated TB incidence to be 42–
84/100 000 prison entries, which indicates, according to the CDC, that this is not a minimal risk prison.16
The risk of TB disease going undetected was high, as we found an underrepresentation of prisoners from several countries in sub-Saharan Africa where
TB incidence is known to have been >300/100 000 in the past 10 years;3,26 less than 65% of the prisoners from sub-Saharan Africa participated in screening.
Difficulties with the screening system
The sensitivity of the TST for TB disease ranges from 75% to 90%.16 Furthermore, in our sample, HIV sta- tus and the prevalence of other pathologies that could cause anergy were unknown.
The high proportion of detainees who did not un- dergo CXR despite a positive TST was disturbing, particularly in a Swiss prison with a well-organised health service. Nonetheless, in the light of the com- plex organisation of prisons, the frequent short stays and sudden and unannounced departures, it was probably diffi cult to obtain dramatically improved rates of full screening. TST screening has been in- creasingly abandoned in public institutions in Swit- zerland as it is not cost-effective: few cases of active TB were detected, few LTBI cases were treated and screening was time-consuming.27 In addition, as shown by our study, among those who underwent neither TST nor CXR, a signifi cantly higher percent- age were from countries with a high incidence of TB and/or MDR-TB.
Based on the principle of equivalence of care in the prison setting,28 and following the changes made in the screening strategy at the Swiss borders, TST screening of prisoners has also been abandoned in the study setting, leaving symptom screening the only method available for screening for TB disease (the prior objective of the screening process in that set- ting). The TST is still used to detect LTBI in contact tracing, and the interferon-gamma release assay is used to confi rm positive TSTs in case of a history of a previous positive TST or BCG vaccination.29
Prisoners who left prison rapidly (after 1–3 days on average) and did not show symptoms at entry were not screened. Other reasons that rendered screening less than optimal were refusals by detain- ees, organisational problems and, possibly, low staff motivation to conduct screening.11,30 The delay be- tween TST and CXRs could also have been short- ened; however, this is a diffi cult decision in a remand prison, even one categorised as a ‘non-minimal risk facility’, to determine available staff resources to be dedicated to TB screening when there are multiple important and more visible health problems and pre- vention tasks.
Acknowledgement
Funding was provided by a research grant from the University of Geneva.
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TB screening in a Swiss remand prison i
C O N T E X T E : Les directives recommandent le dépistage de la tuberculose (TB) dans les prisons, mais les mé- thodes appropriées font toujours l’objet de controverse.
Les études évaluant le dépistage dans les prisons de dé- tention préventive sont rares.
M É T H O D E : Entre 1997 et 2001, un dépistage volontaire basé sur les tests cutanés tuberculiniques (TST) a été pro- posé à tous les prisonniers lors de leur admission dans la plus grande prison de détention préventive en Suisse. On a prévu qu’un cliché thoracique serait pratiqué chez les prisonniers dont les résultats seraient positifs. Nous avons analysé les informations recueillies dans une base de données anonymes.
R É S U LTAT S : Il y a eu 4890 prisonniers admis et éligibles pour le dépistage. Le test TST a été pratiqué chez 3779 (77,3%) en moyenne 9 jours après leur admission ;
46,9% étaient positifs (induration ⩾ 10 mm). Les taux de positivité du TST ont été similaires au cours des 5 an- nées. Le TST a plus tendance à être négatif chez les femmes (60,4%) que chez les hommes (47,7% ; P <
0,001 ; χ2 de Pearson 16,5). La positivité du TST varie en fonction de l’origine des prisonniers (64% pour l’Afrique sub-saharienne, 57% pour l’Europe de l’Est, 56% pour l’Afrique du Nord, 51% pour l’Asie et 34%
pour l’Europe du Nord et de l’Ouest).
C O N C L U S I O N : Le pourcentage de TST positif est élevé, et chez la plupart on n’a pas offert de traitement préven- tif pour une TB latente. L’utilité d’un TST systématique chez l’ensemble des prisonniers lors de l’admission est li- mitée, puisque le diagnostic de la maladie TB reste habi- tuellement la priorité dans les prisons.
M A R C O D E R E F E R E N C I A : Las normas existentes reco- miendan la detección sistemática de la tuberculosis (TB) en las prisiones, pero el método más apropiado de apli- carla sigue siendo fuente de controversia. Los estudios que evalúan esta práctica son escasos.
M É T O D O : Entre 1997 y el 2001 se ofreció la detección voluntaria de la TB mediante la prueba cutánea de la tu- berculina (TST) a todos los reclusos en el momento de su entrada a la más grande cárcel transitoria en Suiza.
En las personas con resultado positivo, se programó una radiografía de tórax. Esta información se recogió en una base de datos anónima y luego se analizó.
R E S U LTA D O S : Ingresaron a la prisión 4890 personas que cumplían con los criterios de aplicación de la prueba de detección. Se practicó la prueba TST a 3779 de ellos (77,3%), en promedio 9 días después de su ingreso. En 46,9% de los casos el resultado fue positivo (diámetro de induración de ⩾10 mm). El índice de positividad de
la prueba permaneció estable durante los 5 años del es- tudio. Las mujeres exhibieron mayor probabilidad de presentar un resultado negativo de la prueba TST que los hombres (60,4% contra 47,7%; P < 0,001; prueba χ2 de Pearson 16,5). La positividad de la prueba TST varió en función del origen (64% en las personas prove- nientes de África subsahariana, 57% en las personas de Europa del este, 56% de África del norte, 51% de Asia y 34% de Europa del norte y occidental).
C O N C L U S I Ó N : El porcentaje de resultados positivos a la prueba TST fue alto y en la mayoría de los casos no se administró el tratamiento preventivo de la infección TB latente. La utilidad de la detección sistemática de la TB a todos los reclusos en el momento de su ingreso me- diante la prueba TST es escasa, pues el diagnóstico de la TB activa sigue siendo la prioridad en la mayoría de los establecimientos penitenciarios.
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