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International Journal of Environmental Research and Public Health logoLink to International Journal of Environmental Research and Public Health
. 2021 Sep 10;18(18):9566. doi: 10.3390/ijerph18189566

Tuberculosis Notification Trends and Treatment Outcomes in Penitentiary and Civilian Health Care Sectors in the WHO European Region

Andrei Dadu 1,*, Ana Ciobanu 2, Araksya Hovhannesyan 1, Natavan Alikhanova 3, Oleksandr Korotych 1, Elmira Gurbanova 4, Rafael Mehdiyev 3, Svetlana Doltu 5, Ogtay Gozalov 1, Sevim Ahmedov 6, Masoud Dara 1
Editor: Paul B Tchounwou
PMCID: PMC8466779  PMID: 34574488

Abstract

Setting: Tuberculosis (TB) morbidity in penitentiary sectors is one of the major barriers to ending TB in the World Health Organization (WHO) European Region. Objectives and design: a comparative analysis of TB notification rates during 2014–2018 and of treatment outcomes in the civilian and penitentiary sectors in the WHO European Region, with an assessment of risks of developing TB among people experience incarceration. Results: in the WHO European Region, incident TB rates in inmates were 4–24 times higher than in the civilian population. In 12 eastern Europe and central Asia (EECA) countries, inmates compared to civilians had higher relative risks of developing TB (RR = 25) than in the rest of the region (RR = 11), with the highest rates reported in inmates in Azerbaijan, Kazakhstan, Kyrgyzstan, Republic of Moldova, Russian Federation, and Ukraine. The average annual change in TB notification rates between 2014 and 2018 was −7.0% in the civilian sector and −10.9% in the penitentiary sector. A total of 15 countries achieved treatment success rates of over 85% for new penitentiary sector TB patients, the target for the WHO European Region. In 10 countries, there were no significant differences in treatment outcomes between civilian and penitentiary sectors. Conclusion: 42 out of 53 (79%) WHO European Region countries reported TB data for the selected time periods. Most countries in the region achieved a substantial decline in TB burden in prisons, which indicates the effectiveness of recent interventions in correctional institutions. Nevertheless, people who experience incarceration remain an at-risk population for acquiring infection, developing active disease and unfavourable treatment outcomes. Therefore, TB prevention and care practices in inmates need to be improved.

Keywords: tuberculosis, prisons, notification, outcomes, WHO European Region

1. Introduction

In 2019 in the world, 10 million people developed TB disease, and 1.4 million died from TB. Although WHO European Region carries only 3% of the global burden of tuberculosis (TB), it has one of the highest proportions of multidrug-resistant TB (MDR-TB). In 2019, an estimated 246,000 incident TB cases occurred in countries of the WHO European Region, equivalent to an average incidence of 26 cases per 100,000 population [1].

Over the last century, global control efforts have reduced the worldwide burden of tuberculosis (TB) [1]. Nevertheless, TB morbidity in the penitentiary sector (The term “penitentiary sector” includes jails, remand/detention/pre-trial centres and prisons) remain a significant barrier to ending TB in the World Health Organization (WHO) European Region by 2030 [1,2]. Worldwide, more than 10 million people are inmates, with around half located in Brazil, China, the Russian Federation and the United States of America [3,4]. According to the United Nations’ estimates of national population levels, the known prison population of the world increased by 3.7% between 2015 and 2018. In the WHO European Region, the most substantial increases in prison populations were observed in Turkey (an increase of 31%), Belarus (19%) and Italy (14%). However, prison populations decreased in Romania (a decrease of 22%), Ukraine (19%) and the Russian Federation (10%) during the same period [5].

TB prevention and care services in prisons are described as often being inadequate and poorly integrated with civilian services, and prison inmates consistently have higher risks of developing active TB and dying from TB than the general population, owing to poor conditions in prisons, such as overcrowding, inadequate ventilation, malnutrition, poor hygiene and poor health care [6,7,8,9,10,11,12]. Additionally, inmates often come from communities, which are at an increased risk of TB or HIV infections [2,8,13].

The objectives of this study were to describe the diversity of notification of incident TB cases (notification rate of incident TB cases—number of new and relapse tuberculosis cases registered and reported per 100,000 population [1]) and their trends in the civilian and penitentiary sectors between 2014 and 2018; the treatment outcomes in the penitentiary versus the civilian sectors, and to estimate the relative risks of developing active TB for prison inmates (inmates—includes people experience incarceration, detainees and convicts) in comparison to civilian population in the WHO European Region.

2. Methods and Materials

This is a retrospective descriptive study analysing magnitude and time-series trends in the notification of new and relapse TB cases and TB treatment outcomes in the civilian and penitentiary sectors in the WHO European Region, based on data reported by WHO European Region Member States to The WHO global TB data collection system [14] between 2012 and 2018, inclusively.

2.1. Setting

The WHO European Region consists of 53 Member States covering a vast geographical region from the Atlantic to the Pacific oceans and from the Mediterranean to the Baltic Sea [15]. Our study focused on comparative analyses of TB indicators in eastern Europe and central Asia (EECA) countries as well as of those from the rest of the region. The EECA region is made up of 12 of the 15 countries, which were formerly part of the Soviet Union, excluding the Baltics, and which are located in the east of the WHO European Region.

2.2. Study Population and Design

Data were collected for new and relapse TB cases and their outcomes from the civilian and penitentiary sectors reported in WHO European Region countries. Three selection criteria were applied: (1) countries that provided at least one report on new and relapse TB cases in both the civilian and penitentiary sectors between 2014 and 2018; (2) countries that provided at least two data points on new and relapse TB cases in both civilian and penitentiary sectors between 2014 and 2019 for enabling analysis of the trend; (3) countries that reported outcomes for TB cases on first-line drug (FLD) treatment schemes in both the civilian and penitentiary sectors for at least one cohort between 2012 and 2016.

2.3. Data Variables and Sources

Data were obtained from 3 sources: (1) The WHO global TB data collection system [14] has an extended set of indicators for TB in European Region prisons, and data were extracted on: prison populations, the numbers of new and relapse TB cases in the civilian and penitentiary sectors for 2014 to 2018, and treatment outcomes for patients on FLD treatment schemes in the civilian and penitentiary sectors for 2012 to 2016; (2) total population estimates were extracted from World Population Prospects [16]; and (3) prison population estimates were taken from the World Prison Brief [17] for countries whose prison population data were missing from The WHO global TB data collection system.

2.4. Analysis and Statistics

For each country, we calculated annual notification rates per 100,000 population of new and relapse tuberculosis cases in civilian and penitentiary sectors separately. The Average Annual Percent Change (AAPC) was calculated by fitting a least-squares regression line to the natural logarithm of the rates, using the calendar year as a regressor variable.

As a measure of the effect of exposure to a prison setting on the risk of development of TB we computed the Relative Risk of TB in prison in reference to the civilian population and the corresponding confidence interval. Results were considered significant if the confidence interval did not include 1. The statistical analysis was performed using the online calculator VassarStats [18]. TB patients who were successfully treated or completed TB treatment were considered to have a favourable outcome; those who failed to complete treatment, were lost to follow-up or who died during the TB treatment were considered to have an unfavourable outcome, as per WHO standard definitions [19]. TB cases with no reported treatment outcomes were excluded from the analysis. We analysed the notification rate of incident TB cases and TB treatment outcomes (unfavourable versus favourable) for the civilian and penitentiary sectors.

3. Results

3.1. Notification Rate of Incident TB Cases and Relative Risks of Developing TB Disease in the Penitentiary Sector Compared with the Civilian Sector

Out of the 53 countries of the WHO European Region, 42, including 10 from the EECA region, reported the number of new and relapse TB cases in the civilian and penitentiary sectors at least once in the five-year period between 2014 and 2018. During this time, 11 (21%) countries did not provide any reports on TB in prisons (Table 1 and Figure 1).

Table 1.

Completeness of TB reporting for civilian and penitentiary sectors via The WHO global TB data collection system, WHO European Region countries.

a. Number of New and Relapse TB Cases, 2014–2018
Country Civilian Sector Penitentiary Sector Status
2014 2015 2016 2017 2018 2014 2015 2016 2017 2018
Albania 404 415 412 495 437 4 0 3 8 3 Y
Andorra 6 4 4 1 2 0 0 0 0 0 Y
Armenia a 1303 1151 1018 825 720 26 20 9 16 14 Y
Austria 619 0 Y
Azerbaijan a 5490 5228 4905 4975 4822 298 228 254 256 216 Y
Belarus a 3658 3090 2684 2253 107 121 97 106 Y
Belgium 851 916 967 896 35 12 19 20 Y
Bosnia and Herzegovina 1194 1091 666 2 4 0 Y
Bulgaria 1774 1599 1503 1392 1307 51 20 22 16 16 Y
Croatia 491 449 5 0 Y
Cyprus N
Czechia 458 489 497 474 16 19 14 25 22 Y
Denmark N
Estonia 230 197 180 168 140 6 9 8 3 5 Y
Finland N
France 4433 4610 4774 61 65 65 Y
Georgia a 3099 3070 2926 2539 2272 101 82 57 58 43 Y
Germany N
Greece N
Greenland N
Hungary 789 728 10 9 Y
Iceland 8 0 Y
Ireland 292 295 293 301 294 5 0 0 0 0 Y
Israel 356 278 5 2 Y
Italy N
Kazakhstan a 14,282 13,423 11,838 12,063 12,479 962 583 484 386 353 Y
Kyrgyzstan a 6233 6779 6810 6488 6198 157 248 216 199 140 Y
Latvia 685 664 609 522 53 33 32 21 Y
Lithuania 1424 1354 1312 1214 57 41 35 54 Y
Luxembourg 37 30 29 32 42 1 0 0 0 0 Y
Malta 45 32 50 42 0 0 0 0 Y
Monaco 0 0 0 0 Y
Montenegro 112 79 1 1 Y
Netherlands 798 845 863 757 784 16 5 14 19 7 Y
North Macedonia 280 278 260 206 214 4 4 3 10 3 Y
Norway N
Poland 6387 6065 5927 5365 5025 152 172 216 170 171 Y
Portugal 2198 2053 1833 1728 1812 53 61 39 32 44 Y
Republic of Moldova a 3937 3484 3398 3259 2933 121 124 173 99 89 Y
Romania 14,652 14,064 12,633 12,205 11,472 209 161 157 105 114 Y
Russian Federation a 91,025 89,218 82,797 76,344 70,967 11,315 10,372 9610 8166 7291 Y
San Marino 0 0 0 0 0 0 Y
Serbia 969 864 744 730 637 15 15 11 8 4 Y
Slovakia 299 291 264 210 21 17 17 18 Y
Slovenia 142 129 118 0 0 0 Y
Spain N
Sweden N
Switzerland 527 4 Y
Tajikistan a 5677 5804 5866 5794 5605 130 90 99 101 121 Y
Turkey 12,966 12,413 12,035 11,696 11,421 142 137 151 125 155 Y
Turkmenistan a N
Ukraine a 30,245 28,974 28,133 26,485 25,745 1456 1177 919 744 767 Y
United Kingdom 6581 5821 5766 5226 43 33 27 22 Y
Uzbekistan a N
b. Number of TB Patients Who Started on One of the FLD Treatment Schemes, 2012–2016
Country Civilian Sector Penitentiary Sector Status
2012 2013 2014 2015 2016 2012 2013 2014 2015 2016
Albania 405 470 402 409 406 2 2 4 0 3 Y
Andorra 9 0 6 4 4 0 5 0 0 0 Y
Armenia a 1341 1228 1202 896 861 9 23 26 14 8 Y
Austria N
Azerbaijan a 4341 3973 1389 1292 1270 275 321 234 183 194 Y
Belarus a 3298 2935 2648 2458 2076 127 99 58 67 47 Y
Belgium 855 856 833 895 955 30 22 34 10 18 Y
Bosnia and Herzegovina 1257 1194 1091 907 4 2 1 0 Y
Bulgaria 2136 1878 1744 1578 1488 44 25 45 20 22 Y
Croatia N
Cyprus 55 1 Y
Czechia 536 452 453 481 492 20 16 14 18 13 Y
Denmark N
Estonia 218 210 189 163 158 4 16 5 9 8 Y
Finland N
France N
Georgia a 3245 2994 2781 2780 2666 393 104 81 61 49 Y
Germany N
Greece N
Greenland N
Hungary 1161 1016 847 11 14 4 Y
Iceland N
Ireland 336 345 283 265 286 2 1 5 0 0 Y
Israel 506 295 317 261 3 10 5 2 Y
Italy N
Kazakhstan a 15,514 13,400 11,791 13,372 761 1056 682 634 Y
Kyrgyzstan a 5533 5610 5969 5910 125 121 170 162 Y
Latvia 823 764 631 609 560 49 40 44 33 32 Y
Lithuania 1428 1347 1238 1183 1126 31 45 44 36 26 Y
Luxembourg 37 1 Y
Malta 41 49 0 0 0 0 0 0 0 0 Y
Monaco 3 0 0 0 Y
Montenegro 107 119 112 79 0 0 1 1 Y
Netherlands 906 796 782 833 850 18 20 14 4 14 Y
North Macedonia 345 309 277 278 260 1 8 4 4 3 Y
Norway N
Poland 7057 6791 6369 6054 5904 204 220 131 142 195 Y
Portugal 2493 2336 2198 2053 1833 46 61 39 Y
Republic of Moldova a 4073 3747 3358 2903 2909 130 142 101 89 139 Y
Romania 16,313 15,048 14,321 13,747 12,304 112 140 204 161 155 Y
Russian Federation a 80,594 71,674 67,146 71,317 64,591 9072 11,627 9990 9107 8546 Y
San Marino 0 0 Y
Serbia 1171 1163 1032 868 722 26 21 13 14 11 Y
Slovakia 323 368 298 288 262 20 27 20 17 17 Y
Slovenia 138 139 142 129 0 0 0 0 Y
Spain N
Sweden N
Switzerland N
Tajikistan a 5664 5151 5047 5222 5254 147 112 102 76 70 Y
Turkey 13,409 13,047 12,791 12,219 11,851 126 123 142 143 166 Y
Turkmenistan a N
Ukraine a 29,346 28,016 21,270 23,015 21,618 1582 1710 1024 877 997 Y
United Kingdom 8106 7260 6469 5773 5649 35 33 43 29 26 Y
Uzbekistan a 13,783 349 Y

−: not reported; EECA: east European central Asia; N: excluded from the analysis; TB: tuberculosis; Y: included in the analysis; WHO: World Health Organization a EECA country.

Figure 1.

Figure 1

Countries/states selected for case analysis based on the availability of TB reporting forms. TB: tuberculosis; WHO: World Health Organization.

Table 2 shows the notification rate of incident TB cases (The notification rate of incident TB cases is the number of new and relapse tuberculosis cases reported per 100,000 population [1]) and percentage annual changes in notification rate of incident TB cases in the civilian and penitentiary sectors during 2014–2018 for the countries included in this study. In the penitentiary sectors of seven countries, all of which are in the EECA region, incident TB rates of more than 1000 per 100,000 population were reported: Azerbaijan, Kazakhstan, Kyrgyzstan, the Republic of Moldova, the Russian Federation, Tajikistan and Ukraine (Table 2 and Figure 2).

Table 2.

Notification rate of incident TB cases and year-to-year percentage changes in TB notification rates, WHO European Region, 2014–2018.

a. Civilian Sector
Country Notification Rate of Incident TB Cases per 100,000 Population Annual Change in Notification Rate of Incident TB Cases (%)
2014 2015 2016 2017 2018 2014–2015 2015–2016 2016–2017 2017–2018 Average
Albania 13.9 14.2 14.1 16.9 15.2 2.6 −0.8 18.2 −10.8 2.3
Andorra 7.6 5.1 5.2 1.3 2.6 −39.0 0.9 −138.2 69.3 −23.5
Armenia a 44.9 39.5 34.9 28.2 24.4 −12.8 −12.5 −21.2 −14.4 −14.1
Azerbaijan a 57.9 54.5 50.5 50.7 48.6 −6.1 −7.5 0.4 −4.4 −4.3
Belarus a 38.7 32.7 28.5 23.9 −16.8 −14.0 −17.3 −14.8
Belgium 7.6 8.1 8.5 7.8 7.8 6.7 4.8 −8.3 −0.5 0.7
Bosnia and Herzegovina 33.5 30.8 20.1 −8.4 −12.0
Bulgaria 24.6 22.3 21.1 19.7 18.1 −9.8 −5.5 −7.0 −8.4 −7.4
Croatia 11.5 10.7 −3.9
Czech Republic 4.3 4.6 4.7 4.5 3.9 6.5 1.6 −4.8 −14.2 −2.7
Estonia 17.5 15.0 13.7 12.9 10.6 −15.3 −8.8 −6.7 −19.3 −11.8
France 6.9 7.1 7.4 7.3 3.5 3.1 −1.3 1.8
Georgia a 77.8 77.9 74.7 65.1 56.9 0.1 −4.1 −13.8 −13.4 −7.5
Hungary 8.1 7.5 6.1 −6.9
Ireland 6.2 6.3 6.2 6.3 6.1 0.7 −1.3 1.8 −3.6 −0.6
Israel 4.5 3.5 −26.3 −26.3
Kazakhstan a 81.9 75.8 66.0 66.4 68.2 −7.7 −13.9 0.6 2.8 −4.5
Kyrgyzstan a 108.1 115.7 114.5 107.5 120.8 6.8 −1.1 −6.3 11.7 2.8
Latvia 34.1 33.4 31.0 26.8 −2.0 −7.5 −14.4 −7.7
Lithuania 48.2 46.3 45.2 42.1 36.4 −4.1 −2.4 −7.2 −14.6 −6.8
Luxembourg 6.7 5.3 5.0 5.5 7.0 −22.8 −5.0 8.5 23.7 1.1
Malta 10.6 7.5 11.7 9.8 12.5 −34.6 44.2 −17.8 25.0 4.3
Monaco 0.0 0.0 0.0 0.0
Montenegro 17.9 12.6 −35.0 −35.0
Netherlands 4.7 5.0 5.1 4.5 4.6 5.4 1.8 −13.4 3.4 −0.7
North Macedonia 13.5 13.4 12.5 9.9 10.3 −0.8 −6.8 −23.4 3.8 −6.6
Poland 16.7 15.9 15.5 14.1 13.3 −5.1 −2.2 −9.8 −5.9 −5.6
Portugal 20.5 19.7 17.7 16.8 17.7 −3.8 −10.8 −5.7 5.5 −3.6
Republic of Moldova a 96.9 85.8 83.9 80.6 72.5 −12.1 −2.3 −4.0 −10.6 −7.0
Romania 73.5 70.9 64.0 62.1 58.9 −3.6 −10.2 −3.0 −5.3 −5.4
Russian Federation a 63.6 62.3 57.8 53.2 48.9 −2.1 −7.5 −8.2 −8.5 −6.4
San Marino 0.0 0.0 0.0 0.0 0.0 0.0
Serbia 10.9 9.8 8.4 8.3 7.2 −11.1 −14.6 −1.6 −13.8 −9.7
Slovakia 5.5 5.4 4.9 3.9 4.7 −2.8 −9.8 −22.9 20.1 −3.8
Slovenia 6.9 6.2 5.7 −9.8 −9.1 −9.0
Tajikistan a 68.0 68.0 67.2 65.0 61.7 0.0 −1.1 −3.3 −5.3 −2.4
Turkey 16.9 15.9 15.2 14.5 13.9 −5.9 −4.6 −4.4 −4.3 −4.7
Ukraine a 67.5 65.0 63.4 60.0 58.3 −3.8 −2.4 −5.6 −2.9 −3.6
United Kingdom 10.1 8.9 8.8 7.9 7.1 −12.9 −1.5 −10.4 −11.0 −8.6
EECA 67.2 64.3 60.2 56.4 53.1 −4.4 −6.6 −6.6 −6.0 −5.7
Non-EECA 17.2 14.9 14.0 13.6 12.7 −14.6 −5.8 −3.4 −6.8 −7.4
All Countries 38.8 34.9 32.6 31.2 29.1 −10.6 −6.7 −4.4 −7.2 −7.0
b. Penitentiary Sector
Country Notification Rate of Incident TB Cases per 100,000 Population Annual Change in Notification Rate of Incident TB Cases (%)
2014 2015 2016 2017 2018 2014–2015 2015–2016 2016–2017 2017–2018 Average
Albania 76.9 0.0 49.2 147.7 56.8 −100.0 109.9 −95.5 −7.3
Andorra 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
Armenia a 662.8 509.8 184.7 328.3 395.9 −26.2 −101.5 57.5 18.7 −12.1
Azerbaijan a 1580.0 1115.8 1217.6 1266.5 1117.9 −34.8 8.7 3.9 −12.5 −8.3
Belarus a 359.3 344.1 275.8 301.4 −4.4 −22.1 8.9 −5.7
Belgium 297.4 109.3 161.4 188.3 160.1 −100.1 39.0 15.4 −16.3 −14.3
Bosnia and Herzegovina 65.7 119.2 0.0 59.5 −100.0
Bulgaria 597.9 261.8 277.7 220.3 229.3 −82.6 5.9 −23.2 4.0 −21.3
Croatia 114.9 0.0 −100.0
Czech Republic 85.8 91.1 62.3 112.8 102.0 6.0 −38.0 59.4 −10.1 4.4
Estonia 181.8 296.6 281.6 107.1 200.0 49.0 −5.2 −96.6 62.4 2.4
France 91.3 97.8 95.2 96.7 6.9 −2.7 1.6 1.9
Georgia a 973.8 844.0 610.7 625.0 473.4 −14.3 −32.4 2.3 −27.8 −16.5
Hungary 47.6 47.4 92.0 17.9
Ireland 37.3 0.0 0.0 0.0 0.0 −100.0 0.0 0.0 −100.0
Israel 24.1 9.9 −89.0 −89.0
Kazakhstan a 1857.4 1164.9 967.1 1102.9 1002.3 −46.7 −18.6 13.1 −9.6 −14.3
Kyrgyzstan a 2081.1 3038.5 2602.4 2238.7 1623.4 37.8 −15.5 −15.1 −32.1 −6.0
Latvia 1031.3 748.5 754.2 557.8 −32.1 0.8 −30.2 −18.5
Lithuania 660.0 557.4 513.6 818.3 718.8 −16.9 −8.2 46.6 −13.0 2.2
Luxembourg 152.4 0.0 0.0 0.0 0.0 −100.0 0.0 0.0 −100.0
Malta 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
Monaco 0.0 0.0 0.0 0.0
Montenegro 64.2 74.6 15.0 15.0
Netherlands 37.2 11.6 37.7 68.0 24.0 −116.3 117.5 59.0 −104.0 −10.4
Poland 192.4 218.2 302.3 230.3 230.8 12.6 32.6 −27.2 0.2 4.7
Portugal 378.5 421.9 261.3 237.7 348.9 10.9 −47.9 −9.5 38.4 −2.0
Republic of Moldova a 1765.7 1809.4 2228.8 1275.4 1165.7 2.4 20.8 −55.8 −9.0 −9.9
Romania 699.0 567.8 579.0 466.0 553.3 −20.8 2.0 −21.7 17.2 −5.7
Russian Federation a 1683.6 1543.3 1503.8 1335.9 1259.7 −8.7 −2.6 −11.8 −5.9 −7.0
San Marino 0.0 0.0 0.0 0.0 0.0 0.0
Serbia 145.8 145.8 103.1 75.0 37.0 0.0 −34.7 −31.8 −70.6 −29.0
Slovakia 284.3 209.7 211.9 219.2 204.0 −30.4 1.0 3.4 −7.2 −8.0
Slovenia 0.0 0.0 0.0 0.0 0.0 0.0
Tajikistan a 1300.0 900.0 990.0 748.1 806.7 −36.8 9.5 −28.0 7.5 −11.2
North Macedonia 153.8 148.1 111.1 323.9 100.0 −3.8 −28.8 107.0 −117.5 −10.2
Turkey 89.4 76.9 75.3 53.8 55.3 −15.0 −2.2 −33.5 2.6 −11.3
Ukraine a 1982.8 1875.7 1405.2 1222.2 1424.2 −5.6 −28.9 −14.0 15.3 −7.9
United Kingdom 43.2 35.1 29.0 23.8 28.3 −20.7 −19.1 −19.8 17.4 −10.0
EECA 1703.9 1491.4 1403.6 1254.5 1192.8 −13.3 −6.1 −11.2 −5.0 −8.5
Non-EECA 158.2 128.1 132.5 116.3 107.4 −21.1 3.4 −13.1 −7.9 −9.2
All Countries 1084.6 920.7 861.3 759.9 682.2 −16.4 −6.7 −12.5 −10.8 −10.9

EECA: east European central Asia; WHO: World Health Organization. Note: TB notification rate: number of new and relapse tuberculosis cases registered and reported per 100,000 population. a EECA country; in bold are the countries groups averages

Figure 2.

Figure 2

Notification rate of incident TB cases in the penitentiary sector per 100,000 population, WHO European Region, 2018. TB: tuberculosis; WHO: World Health Organization.

There was observed a decreasing trend in the notification of new TB cases and relapses both in the penitentiary and in the civil sector in 2014–2018 (Table 2 and Figure 3).

Figure 3.

Figure 3

Figure 3

Trends in TB notification rates in the civilian and penitentiary sectors, WHO European Region, 2014–2018. TB: tuberculosis; WHO: World Health Organization. a EECA country. Note: TB notification rate: number of new and relapse tuberculosis cases registered and reported per 100,000 population.

In the 42 countries analysed, the average annual change in incident TB rates during the study period was −7.0% in the civilian sector and −10.9% in the penitentiary sector. The decline in incident TB rates among inmates in the nine EECA countries included in this study should be noted (from −6.0% in Kyrgyzstan to −16.5% in Georgia) (Table 2).

TB cases registered in prison’s inmates accounted for approximately 7% for all notified new and relapse TB patients in EECA countries, with the highest level in the Russian Federation (10%); in comparison, in the other countries in the region the proportion was 1.5%, with the highest level in Slovakia (6.3%) in 2014–2018.

Prison’s inmates in the Russian Federation and Slovakia had the highest risks of developing an active TB disease compared with their respective civilian populations (RR = 25, confidence interval CI: 25–26, and RR = 57 (CI: 35–92)), respectively, in the last reported year. (Table 3 and Figure 4).

Table 3.

Notifications of new and relapse TB cases in the civilian and penitentiary sectors and relative risks (RR) of developing TB for inmates in relation to the civilian population, WHO European Region, 2014–2018.

Country N&R Notified, n N&R Notified, Civilian Sector, n a N&R Notified, Penitentiary Sector, n RR (95% CI) Reported Year
Albania 440 437 3 3.74 (1.20–11.64) 2018
Andorra 2 2 0 0 2018
Armenia b 734 720 14 16.15 (9.53–27.38) 2018
Austria 619 619 0 0 2016
Azerbaijan b 5038 4822 216 22.78 (19.89–26.09) 2018
Belarus b 2359 2253 106 12.56 (10.34–15.26) 2018
Belgium 916 896 20 23.96 (15.39–37.30) 2017
Bosnia and Herzegovina 666 666 0 0 2018
Bulgaria 1323 1307 16 12.33 (7.54–20.18) 2018
Croatia 449 449 0 0 2016
Czechia 499 474 25 25.19 (16.85–37.66) 2017
Estonia 145 140 5 18.83 (7.72–45.90) 2018
France 4839 4774 65 12.93 (10.12–16.51) 2017
Georgia b 2315 2272 43 7.86 (5.82–10.62) 2018
Hungary 737 728 9 6.33 (3.28–12.21) 2016
Iceland 8 8 0 0 2014
Ireland 294 294 0 0 2018
Israel 280 278 2 10.19 (2.50–41.45) 2015
Kazakhstan b 1283 12,479 353 14.55 (13.10–16.17) 2018
Kyrgyzstan b 6338 6198 140 13.24 (11.21–15.63) 2018
Latvia 543 522 21 20.68 (13.39–31.95) 2017
Lithuania 1268 1214 54 19.29 (14.70–25.30) 2017
Luxembourg 42 42 0 0 2018
Malta 42 42 0 0 2017
Monaco 0 0 0 0 2015
Montenegro 80 79 1 5.92 (0.82–42.50) 2015
Netherlands 791 784 7 5.22 (2.48–10.97) 2018
North Macedonia 217 214 3 9.71 (3.11–30.33) 2018
Poland 5196 5025 171 17.35 (14.90–20.20) 2018
Portugal 1856 1812 44 21.38 (15.86–28.83) 2018
Republic of Moldova b 3022 2933 89 16.16 (13.1–19.93) 2018
Romania 15,586 11,472 114 9.35 (7.78–11.24) 2018
Russian Federation b 78,258 70,967 7291 25.46 (24.85–26.07) 2018
San Marino 0 0 0 0 2018
Serbia 641 637 4 5.11 (1.91–13.65) 2018
Slovakia 228 210 18 56.66 (35.03–91.64) 2017
Slovenia 118 118 0 0 2016
Switzerland 531 527 4 9.16 (3.43–24.49) 2015
Tajikistan b 5726 5605 121 12.98 (10.85–15.53) 2018
Turkey 11,576 11,421 155 3.97 (3.39–4.65) 2018
Ukraine b 26,512 25,745 767 24.12 (22.46–25.90) 2018
United Kingdom 5248 5226 22 3.0 (1.98–4.57) 2017

CI: confidence interval; EECA: east European central Asia; N&R: new and relapse TB cases; RR: relative risks; TB: tuberculosis; WHO: World Health Organization. a Reference data for risk comparison. b EECA country.

Figure 4.

Figure 4

Relative risks of developing TB among prisons’ inmates compared to civilian population, WHO European Region, 2014–2018. TB: tuberculosis; WHO: World Health Organization.

3.2. Treatment Outcomes in TB Patients on First-Line Drug (FLD) Treatment Schemes

A total of 39 (74%) countries in the WHO European Region reported treatment outcomes for at least one cohort of TB patients, both civilians and inmates, who started on one of the FLD treatment schemes between 2012 and 2016 (Table 1 and Figure 1). Table 4 shows both the favourable and unfavourable treatment outcomes for civilians and inmates in these 39 countries.

Table 4.

Favourable and unfavourable TB treatment outcomes for civilians and inmates on first-line drug treatment schemes, 2012–2016 cohorts, WHO European Region.

a. Civilian Sector
Country Overall, n Favourable Outcome, n (%) Unfavourable Outcome Not Evaluated, n (%) Last Reported Cohort
Failure, n (%) Died, n (%) LTFU, n (%)
Albania 406 355 (87.4) 3 (0.7) 10 (2.5) 20 (4.9) 18 (4.4) 2016
Andorra 4 3 (75.0) 0 (0.0) 1 (25.0) 0 (0.0) 0 (0.0) 2016
Armenia a 861 695 (80.7) 18 (2.1) 48 (5.6) 99 (11.5) 1 (0.1) 2016
Azerbaijan a 1270 1048 (82.5) 71 (5.6) 16 (1.3) 113 (8.9) 22 (1.7) 2016
Belarus a 2076 1849 (89.1) 44 (2.1) 111 (5.3) 68 (3.3) 4 (0.2) 2016
Belgium 955 782 (81.9) 0 (0.0) 58 (6.1) 63 (6.6) 52 (5.4) 2016
Bosnia and Herzegovina 907 505 (55.7) 13 (1.4) 64 (7.1) 3 (0.3) 322 (35.5) 2016
Bulgaria 1488 1270 (85.3) 15 (1.0) 122 (8.2) 81 (5.4) 0 (0.0) 2016
Cyprus 55 37 (67.3) 0 (0.0) 0 (0.0) 0 (0.0) 18 (32.7) 2016
Czechia 492 335 (68.1) 1 (0.2) 82 (16.7) 54 (11.0) 20 (4.1) 2016
Estonia 158 125 (79.1) 3 (1.9) 26 (16.5) 2 (1.3) 2 (1.3) 2016
Georgia a 2666 2226 (83.5) 52 (2.0) 112 (4.2) 232 (8.7) 44 (1.7) 2016
Hungary 847 598 (70.6) 18 (2.1) 101 (11.9) 78 (9.2) 52 (6.1) 2015
Ireland 286 103 (36.0) 0 (0.0) 16 (5.6) 2 (0.7) 165 (57.7) 2016
Israel 261 216 (82.8) 1 (0.4) 19 (7.3) 8 (3.1) 17 (6.5) 2015
Kazakhstan a 13,372 12,188 (91.1) 396 (3.0) 666 (5.0) 122 (0.9) 0 (0.0) 2015
Kyrgyzstan a 5910 4838 (81.9) 108 (1.8) 351 (5.9) 591 (10.0) 22 (0.4) 2016
Latvia 560 477 (85.2) 0 (0.0) 52 (9.3) 28 (5.0) 3(0.5) 2016
Lithuania 1126 949 (84.3) 12 (1.1) 109 (9.7) 51 (4.5) 5 (0.4) 2016
Luxembourg 37 0 (0.0) 0 (0.0) 1 (2.7) 0 (0.0) 36 (97.3) 2014
Malta 49 37 (75.5) 0 (0.0) 1 (2.0) 3 (6.1) 8 (16.3) 2013
Monaco 0 0 0 0 0 0 2014
Montenegro 79 73 (92.4) 0 (0.0) 3 (3.8) 3 (3.8) 0 (0.0) 2015
Netherlands 850 741 (87.2) 0 (0.0) 30 (3.5) 33 (3.9) 46 (5.4) 2016
North Macedonia 260 230 (88.5) 1 (0.4) 18 (6.9) 10 (3.8) 1 (0.4) 2016
Poland 5904 3187 (54.0) 3 (0.1) 578 (9.8) 361(6.1) 1775 (30.1) 2016
Portugal 1833 1298 (70.8) 0 (0.0) 131 (7.1) 60 (3.3) 344 (18.8) 2016
Republic of Moldova a 2909 2398 (82.4) 70 (2.4) 292 (10.0) 114 (3.9) 35 (1.2) 2016
Romania 12,304 10,578 (86.0) 193 (1.6) 996 (8.1) 518 (4.2) 19 (0.2) 2016
Russian Federation a 64,591 47,524 (73.6) 3761 (5.8) 7098 (11.0) 3213 (5.0) 2995 (4.6) 2016
San Marino 0 0 0 0 0 0 2015
Serbia 722 583 (80.7) 6 (0.8) 64 (8.9) 26 (3.6) 43 (6.0) 2016
Slovakia 262 224 (85.5) 0 (0.0) 27 (10.3) 2 (0.8) 9 (3.4) 2016
Slovenia 129 105 (81.4) 0 (0.0) 21 (16.3) 0 (0.0) 3 (2.3) 2015
Tajikistan a 5254 4690 (89.3) 103 (2.0) 223 (4.2) 195 (3.7) 43 (0.8) 2016
Turkey 11,851 10,323 (87.1) 31 (0.3) 698 (5.9) 311 (2.6) 488 (4.1) 2016
Ukraine a 21,618 16,756 (77.5) 1326 (6.1) 2112 (9.8) 1339 (6.2) 85 (0.4) 2016
United Kingdom 5649 4554 (80.6) 0 (0.0) 315 (5.6) 262 (4.6) 518 (9.2) 2016
Uzbekistan a 13,783 11,667 (84.6) 272 (2.0) 615 (4.5) 677 (4.9) 552 (4.0) 2012
b. Penitentiary sector
Country Overall, n Favourable Outcome, n (%) Unfavourable Outcome Not Evaluated, n (%) Last Reported Cohort
Failure, n (%) Died, n (%) LTFU, n (%)
Albania 3 2 (66.7) 0 (0.0) 0 (0.0) 0 (0.0) 1 (33.3) 2016
Andorra 0 0 0 0 0 0 2016
Armenia a 8 8 (100.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 2016
Azerbaijan a 194 177 (91.2) 2 (1.0) 10 (5.2) 5 (2.6) 0 (0.0) 2016
Belarus a 47 45 (95.7) 1 (2.1) 1 (2.1) 0 (0.0) 0 (0.0) 2016
Belgium 18 11 (61.1) 0 (0.0) 0 (0.0) 4 (22.2) 3 (16.7) 2016
Bosnia and Herzegovina 0 0 0 0 0 0 2016
Bulgaria 22 21 (95.5) 0 (0.0) 0 (0.0) 1 (4.5) 0 (0.0) 2016
Cyprus 1 0 (0.0) 0 (0.0) 0 (0.0) 1 (100.0) 0 (0.0) 2016
Czechia 13 11 (84.6) 0 (0.0) 1 (7.7) 0 (0.0) 1 (7.7) 2016
Estonia 8 8 (100.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 2016
Georgia a 49 37 (75.5) 1 (2.0) 1 (2.0) 3 (6.1) 7 (14.3) 2016
Hungary 4 2 (50.0) 0 (0.0) 0 (0.0) 2 (50.0) 0 (0.0) 2015
Ireland 0 0 0 0 0 0 2016
Israel 2 2 (100.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 2015
Kazakhstan a 634 503 (79.3) 44 (6.9) 8 (1.3) 79 (12.5) 0 (0.0) 2015
Kyrgyzstan a 162 130 (80.2) 4 (2.5) 9 (5.6) 18 (11.1) 1 (0.6) 2016
Latvia 32 28 (87.5) 1 (3.1) 1 (3.1) 1 (3.1) 1 (3.1) 2016
Lithuania 26 18 (69.2) 0 (0.0) 2 (7.7) 6 (23.1) 0 (0.0) 2016
Luxembourg 1 1 (100.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 2014
Malta 0 0 0 0 0 0 2013
Monaco 0 0 0 0 0 0 2014
Montenegro 1 1 (100.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 2015
Netherlands 14 6 (42.9) 0 (0.0) 0 (0.0) 4 (28.6) 4 (28.6) 2016
North Macedonia 3 2 (66.7) 0 (0.0) 0 (0.0) 1 (33.3) 0 (0.0) 2016
Poland 195 113 (57.9) 0 (0.0) 4 (2.1) 3 (1.5) 75 (38.5) 2016
Portugal 39 18 (46.2) 0 (0.0) 1 (2.6) 0 (0.0) 20 (51.3) 2016
Republic of Moldova a 139 117 (84.2) 7 (5.0) 2 (1.4) 9 (6.5) 4 (2.9) 2016
Romania 155 145 (93.5) 0 (0.0) 6 (3.9) 4 (2.6) 0 (0.0) 2016
Russian Federation a 8546 4811 (56.3) 841 (9.8) 325 (3.8) 328 (3.8) 2241 (26.2) 2016
San Marino 0 0 0 0 0 0 2015
Serbia 11 7 (63.6) 0 (0.0) 1 (9.1) 3 (27.3) 0 (0.0) 2016
Slovakia 17 17 (100.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 2016
Slovenia 0 0 0 0 0 0 2015
Tajikistan a 70 61 (87.1) 1 (1.4) 5 (7.1) 3 (4.3) 0 (0.0) 2016
Turkey 166 139 (83.7) 1 (0.6) 7 (4.2) 14 (8.4) 5 (3.0) 2016
Ukraine a 997 478 (47.9) 434 (43.5) 28 (2.8) 48 (4.8) 9 (0.9) 2016
United Kingdom 26 16 (61.5) 0 (0.0) 1 (3.8) 2 (7.7) 7 (26.9) 2016
Uzbekistan a 349 238 (68.2) 38 (10.9) 38 (10.9) 10 (2.9) 25 (7.2) 2012

LTFU: lost to follow-up; TB: tuberculosis; WHO: World Health Organization. a EECA country.

Our study highlights a few countries where there were higher levels of unfavourable outcomes for inmates when compared with civilians, for example, Cyprus (100% vs. 0%), the Netherlands (29% vs. 9%) and Kazakhstan (21% vs. 9%). On the other hand, a higher proportion of unfavourable treatment outcomes among civilians than among inmates had been registered in the Czech Republic (28% vs. 8%), Andorra (25% vs. 0%), Estonia (20% vs. 0%), Armenia (19% vs. 0%), and Slovenia (16% vs. 0%).

A total of 12 of the 39 countries achieved TB treatment success rates of over 85% among inmates. In two EECA countries, Belarus and Tajikistan and in five other countries, Bulgaria, Latvia, Montenegro, Romania, Slovakia, the favourable outcomes were more than 85% in both sectors civilian and penitentiary.

4. Discussion

Recent systematic review by Cords et al. revealed a concerning scale of TB burden among people experiencing incarceration in different parts of the world and highlighted the high risk of contracting M tuberculosis infection and developing active disease, compared to the general population [12].

This is the first standardized study on TB morbidity and its treatment outcomes monitoring in the penitentiary sectors of such a scale in the WHO European Region. The main finding of our study is that from 2014 to 2018 the annual incident TB notification rates in prisons across the European Region decreased much faster than in the civilian population, which most likely reflects the decline of true burden in the prison populations. This finding highlights the positive impacts of the TB control interventions carried out by national governments, with the support of international agencies [20,21]. Another finding of our study is that, even though the annual decline of the TB burden in WHO European Region prisons was faster than in the civilian sector, the risk of developing TB disease in prisons is up to 57 times higher compared to the civilian sector. The increased risk of TB for inmates in EECA countries is a known feature of the region and has been previously described in several studies [11,22,23,24]. High prevalence of active TB disease in correctional facilities is fuelled by intra-institutional transmission due to prolonged stays in overcrowded facilities with poor ventilation, along with risk factors, which amplify the risk of TB disease, such as HIV, malnutrition, diabetes, smoking, a history of alcohol and illicit drug consumption, and former TB disease [9,10,25,26]. Theoretically, prison settings offer great opportunities for TB control, and there are practical examples from the region’s prisons in which significant improvements in their TB and rifampicin-resistant-TB burdens have been reported, and WHO-recommended screening, diagnostics, treatment, and linkage to civilian health care is ensured [27,28,29,30]. The high TB morbidity rates in the region’s prisons, of up to 1623 per 100,000 population in 2018, underline the need for substantial improvements in TB control among inmates through wider application of the best practices in the field.

In the majority of EECA countries, treatment success rates for TB in inmates were lower compared with rates in civilian populations, which was not evident for the other countries in the region. This emphasizes the critical need for improvements in the TB services available to inmates. Although the specific reasons for unfavourable treatment outcomes in inmates were not analysed in this study, there is evidence that high drug-resistance rates, insufficient laboratory diagnosis capacities and weak integrations between civilian and prison healthcare services, including ensuring the continuity of TB treatment after release from prison, are major factors leading to poor treatment outcomes in prisons [6,31].

Decarceration and other countries’ justice reforms that lead to it would reduce overcrowding, which is a major environmental factor for tuberculosis transmission, and would significantly reduce TB burden and its rising rates in prisons. Meanwhile, improving the TB situation and treatment outcomes for inmates can only be achieved with governmental commitment, inter-department cooperation for ensuring interventions equivalent to those in the civilian system and in close collaboration with it, and partnerships with civil society organizations. National tuberculosis programmes (NTPs) should develop operational plans and policies that optimize TB control in prisons and for inmates after their release and strengthen the capacities of prison health units for TB case management. Improving treatment outcomes for inmates will also prevent transmission of disease to other inmates, prison staff and community members. The End TB Strategy goals [32] will not be met without the implementation of effective measures in prisons where there are a large number of people who are vulnerable to TB and who engage in behaviours, which also put them at high risk for HIV infection.

One of the limitations of our current study is immediately apparent from the observation of the poor reporting of TB in prisons: in the 5-year study period, there was no available data for 11 WHO European Region countries. In addition, huge fluctuations in the reported annual incident TB rates in prisons reflect uncontrolled epidemics. It is important to note that poor TB reporting affects TB morbidity statistics and, consequently, TB estimates at national and international levels.

This study revealed that some high TB burden countries, such as Turkmenistan and Uzbekistan, have not reported any TB cases among inmates. Cooperation between the institutions responsible for health care in penitentiary systems and the ministries of health should further improve to allow proper TB recording and reporting in both the civilian and penitentiary systems of all countries in the WHO European Region.

5. Conclusions

This review provides an overview of active TB in prisons in the WHO European Region. The completeness of TB reporting for prisons by NTPs was 79% (42 out of 53 countries from the WHO European Region). Our analysis highlights the vulnerability of inmates to TB and emphasises the necessity of improving TB prevention and care policies and their practical application in prisons with respect to active TB detection, infection control, TB treatment and continuity of care. Most countries achieved a substantial decline of TB burden in prisons, which indicates the effectiveness of recent interventions in correctional institutions. These results provide the basis for an understanding that TB prevention and care in prisons should be elevated to be a health care priority and should facilitate intersectional collaboration between civilian health authorities and prison administrations to enable ending TB in the WHO European Region.

5.1. Supporting Information Captions

5.1.1. Evidence Available Prior to This Study

TB surveillance data from the WHO European Region were collected annually from countries via The WHO global TB data collection system [14]. The WHO Regional Office for Europe and the European Centre for Disease Prevention and Control (ECDC) have jointly coordinated the collection and analysis of TB surveillance data in the WHO European Region, aiming to ensure data timeline consistency and comparability, pan-European coverage and avoidance of data duplication [1].

5.1.2. Added Value of the Study

This article provides a full cascade analysis of the TB burden and treatment outcomes at the regional level, designated by countries and subregional groupings.

5.1.3. Implications of All Available Evidence

Further efforts should be made to reduce TB infection transmission, the development of active TB and acquisition of data on treatment outcomes either via WHO data collection or reports from individual countries. In particular, more attention needs to be placed on addressing the known risk factors associated with TB.

Acknowledgments

The authors thank the national TB counterparts in the WHO European Region, including the nominated operational contact points for TB surveillance in the Member States of the WHO European Region for providing data for this analysis based on the WHO mandate for surveillance and response monitoring of the End TB Strategy implementation.

Author Contributions

A.D., S.A. and M.D. prepared the study aims. All authors participated in the design, discussion of the results interpretation, read, edited and agreed with the decision to submit the final version of the paper. A.D., A.C., A.H., N.A. and O.K. designed and executed the analysis. A.D. and A.C. led the data collection and reference reviews. A.C. and A.D. wrote the first draft of the manuscript, and A.H., N.A., E.G., S.D., R.M., O.G., S.A. and M.D. provided substantial revisions to the initial version of the manuscript. M.D. provided substantial revisions to the advanced version of the manuscript. A.D. All authors have read and agreed to the published version of the manuscript.

Funding

This analysis was funded by the United States Agency for International Development via WHO consolidated grant GHA-G-00-09-00003.

Institutional Review Board Statement

We used secondary, aggregated (not case based) data, available on the public domain of WHO. Collection of these data collected is granted by the WHO member states and induced by the resolution EB134.R4 of the 134th session of the World Health Assembly.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data available in a publicly accessible repository hosted by WHO https://www.who.int/teams/global-tuberculosis-programme/data. (accessed on 12 June 2021).

Conflicts of Interest

None of the authors have conflict of interest to declare. The views and opinions expressed in this paper are those of the authors and not necessarily the views and decisions or policies of the World Health Organization, and/or the United States Agency for International Development. The designations used and the presentation of the material in this publication do not imply the expression of any opinion whatsoever on the part of WHO and USAID concerning the legal status of any country, territory, city or area or of its authorities, nor concerning the delimitation of its frontiers or boundaries.

Footnotes

Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

Data available in a publicly accessible repository hosted by WHO https://www.who.int/teams/global-tuberculosis-programme/data. (accessed on 12 June 2021).


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