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BMC Infectious Diseases

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Factors associated with unreported tuberculosis cases in Spanish hospitals

  • Concepción Morales-García1, 2Email author,
  • Teresa Rodrigo1, 3, 10,
  • Marta M. García-Clemente1, 4,
  • Ana Muñoz1, 5,
  • Pilar Bermúdez1, 5,
  • Francisco Casas1, 6,
  • María Somoza1, 7,
  • Celia Milá1, 8,
  • Antón Penas1, 9,
  • Carmen Hidalgo1, 2,
  • Martí Casals1, 10,
  • Joan A. Caylá1, 10, 11 and
  • Working Group on Under-reporting of Tuberculosis in Spain
Contributed equally
BMC Infectious Diseases201515:295

https://doi.org/10.1186/s12879-015-1047-0

Received: 28 December 2014

Accepted: 21 July 2015

Published: 29 July 2015

Abstract

Background

Under-reporting of tuberculosis (TB) cases complicates disease control, hinders contact tracing and alters the accuracy of epidemiological data, including disease burden. The objective of the present study is to evaluate the proportion of unreported TB cases in Spanish healthcare facilities and to identify the associated factors.

Methods

A multi-center retrospective study design was employed. The study included TB cases diagnosed in 16 facilities during 2011–2012. These cases were compared to those reported to the corresponding public health departments. Demographic, microbiological and clinical data were analyzed to determine the factors associated with unreported cases. Associated factors were analyzed on a bivariate level using the x2 test and on a multivariate level using a logistic regression. Odds ratios (OR) and 95 % confidence intervals (CI) were calculated.

Results

Of the 592 TB cases included in the study, 85 (14.4 %) were not reported. The percentage of unreported cases per healthcare center ranged from 0–45.2 %. The following variables were associated to under-reporting at a multivariate level: smear-negative TB (OR = 1.87; CI:1.07-3.28), extrapulmonary disease (OR = 2.07; CI:1.05-4.09) and retired patients (OR = 3.04; CI:1.29-7.18). A nurse case manager was present in all of the centers with 100 % reporting. The percentage of reported cases among the smear-positive cases was 9.4 % and 19.4 % (p = 0.001) among the rest of the study population. Smear-positive TB was no associated to under-reporting.

Conclusions

It is important that TB Control Programs encourage thorough case reporting to improve disease control, contact tracing and accuracy of epidemiological data. The help from a TB nurse case manager could improve the rate of under-reporting.

Keywords

NotificationsUnder-reportingReportingTuberculosisSpain

Background

Tuberculosis (TB) continues to be an important public health problem worldwide. In 2013, 9 million people developed TB and 1.5 million people died from the disease [1]. An estimated three million people with TB in 2012, one third of the total cases, were not reported to a national surveillance system [1]. Prevention and control requires quick and systematic reporting of new TB cases to surveillance centers to ensure treatment compliance and to facilitate contact tracing.

The incidence of reported TB cases in the European Union countries is 13.5 per 100,000 inhabitants [2] and is predominant among vulnerable populations [3]. Spain is considered a country of low TB incidence, with a rate of 14.7 cases per 100,000 in 2012 [2]. However, the distribution between different regions, or autonomous communities, is not equal, and ranges between 8 and 29 cases per 100,000 inhabitants [4].

The low TB incidence observed in Spain during recent years could be not only a result of disease control, but could also be a reflection of missed diagnoses or under-reporting [5, 6]. The potentially missed diagnoses or unreported cases would affect TB incidence in the country. This has been previously observed and published in other countries [612], but not well-studied in Spain. Data published on rate of unreported cases in Spain is limited to only one region [1315], and was estimated at around 20 % [1316]. In Galicia and Barcelona, two areas with effective TB control programs, the TB incidence is higher than the national average. This may be also due to under-reporting in other parts of Spain.

Identifying factors that are associated with under-reporting will allow us to target areas in need of better TB diagnosing and reporting, to in turn improve disease control. The objective of the present study is to describe the extent of unreported TB cases from healthcare facilities in various regions in Spain, and to identify the factors associated with unreported cases.

Methods

Study design

This is a multi-center, retrospective study on a cohort of TB cases diagnosed in 16 hospitals in Spain (Fig. 1) from January 1st, 2011 to December 31st, 2012. The study includes TB cases detected by microbiological, pathological and clinical records of each healthcare facility, which were then compared to cases registered by healthcare facilities at their corresponding public health departments, including the Public Health Department of Andalusia, Asturias, Catalonia, Cantabria, Galicia, The Rioja, The Basque Country, Valencia and Madrid. Each case was classified as reported or not reported.
Fig. 1

Geographical location of the participating healthcare centers in the study

Case definitions and data collection

Clinical, microbiological, and pathological documents were obtained from each healthcare facility, in both electronic and paper form. The following criteria were used for pulmonary and extrapulmonary TB diagnosis: microbiological confirmation of Mycobacterium tuberculosis complex, pathology report compatible with TB (ie caseous granulomas by biopsy), or absence of microbiological confirmation but medically-deemed active TB by clinical and radiological findings. TB cases per healthcare facility records were linked to a list of TB cases provided by the corresponding public health department.

Unreported case was defined as a case that was detected in hospital records but not present in the TB registry of the corresponding public health department.

TB cases were classified as smear-positive, smear-negative or extrapulmonary, according to WHO criteria [17].

Clinical and epidemiological data was collected from patient records and registries, and stored in a database with electronic access using identifying information with a password for each of the study investigators.

The following variables were studied: socio-demographic data (age, sex, country of origin, employment, living situation, site of diagnosis and toxic habits), clinical data (HIV co-infection, history of previous TB treatment, disease involvement and radiographic findings), and microbiological data (smear, culture and anti-TB drug sensitivity results).

Ethics

The study was performed in accordance with the requirements stipulated in the Declaration of Helsinki (Tokyo revision, October 2004) and the Spanish Data Protection Act of 15/1999. The study was approved by the Independent Ethics Committees of the participating healthcare facilities (see Additional file 1).

Statistical analysis

Reported TB cases were classified as “0” and unreported cases as “1.” The proportion of total unreported cases and proportion of unreported cases by healthcare facility were calculated. Absolute and relative frequencies were calculated for each variable and factors associated with unreported cases were analyzed on a bivariate level using the x2 test. A multivariate logistic regression model was constructed with the variables significant at the bivariate level, using manual stepwise selection to consider the factors with a p < 0.05 on a bivariate level. All variables without the presence of colinearity were included in the final model and interaction of covariates was evaluated.

Odds ratio (OR) and corresponding 95 % confidence intervals (CI) were calculated, and goodness of fit was tested using the Hosmer and Lemeshow test. P < 0.05 was considered statistically significant. IBM SPSS Statistics version 19.0 (SPSS Inc, Chicago, IL, USA) was used to perform all statistic analyses.

Results

Of the 592 TB cases diagnosed between 2011–12 at the 16 participating healthcare facilities (Table 1), 85 cases (14.4 %) were not identified in the public health department registries. This proportion ranged from 0 to 45.2 % according to healthcare facility. One hundred percent of the TB cases from 5 healthcare facilities were reported to the corresponding public health department (all of which have a nurse case manager). The average of unreported cases was 20.7 % among the other 11 healthcare facilities. Microbiological confirmation was present for 509 cases (86 %).
Table 1

Distribution of the diagnosis and reported of tuberculosis according to healthcare facilities

Healthcare facility

Number of tuberculosis cases

Total

Reported

Unreported

(N / %)

(N / %)

(N / %)

Saint Millan-Saint Pedro Hospital

21

10

31

67.7 %

32.3 %

100.0 %

Tarrasa Health Consortium

38

0

38

100.0 %

0.0 %

100.0 %

Carlos III Hospital

18

7

25

72.0 %

28.0 %

100.0 %

Xeral-Calde Hospital

29

5

34

85.3 %

14.7 %

100.0 %

Castellon General Hospital

24

3

27

88.9 %

11.1 %

100.0 %

Saint Agustin Hospital

17

14

31

54.8 %

45.2 %

100.0 %

Sierrallana Hospital

27

1

28

96.4 %

3.6 %

100.0 %

Carlos Haya Hospital

69

0

69

100.0 %

0.0 %

100.0 %

Asturias Central Hospital

46

24

70

65.7 %

34.3 %

100.0 %

Jaen Hospital

11

1

12

91.7 %

8.3 %

100.0 %

Saint Boi Hospital

21

0

21

100.0 %

0.0 %

100.0 %

Saint Ana Hospital

16

8

24

66.7 %

33.3 %

100.0 %

Saint Marina Hospital

19

0

19

100.0 %

0.0 %

100.0 %

Saint Cecilio Hospital

39

6

45

86.7 %

13.3 %

100.0 %

Virgen de las Nieves Hospital

77

6

83

92.7 %

7.3 %

100.0 %

Prevention and Control Tuberculosis Unit

35

0

35

100.0 %

0.0 %

100.0 %

TOTAL

507

85

592

85.6 %

14.4 %

100.0 %

The characteristics of the study population can be found in the Tables 2, 3 and 4. The majority of the cases presented with pulmonary or mixed TB, almost half were smear-positive, and more than one third presented with cavitation on chest x-ray. One third of the patients were over 50 years of age and almost two thirds were between 18 and 50 years old (64.7 %). More than 20 % of the cases lived alone, in a group, or were homeless, and 32.3 % were immigrants. More than half of the study population was diagnosed in the emergency department. Almost half (46.3 %) were smokers or ex-smokers, and around 20 % were alcoholics. HIV co-infection was present in 4.2 % of the population, although HIV status was unknown in 18.6 % of the cases. Almost 6 % of the TB cases were relapse. Four hundred and eleven (69.5 %) were diagnosed in either the emergency department or specialty clinics (Table 2).
Table 2

Clinical and epidemiological characteristics of tuberculosis cases

 

Total

 

Reported

 
 

N = 592

 

N = 507

 

Variables

n

%

n

%

Age (years)

    

18-30

146

24.7

128

25,25

31-50

237

40

212

41,81

51-64

62

10.5

52

10,26

>65

121

20.4

92

18,15

Unknown

26

4.4

23

4,54

Sex

    

 Male

368

62.2

321

63,31

 Female

214

36.1

179

35,31

 Unknown

10

1.7

7

1,38

Employment

    

 Employed

205

34.6

174

34,32

 Unemployed

184

31.1

169

33,33

 Retired

125

21.1

94

18,54

 Unknown/On disability

78

13.2

70

13,81

Living situation

    

 With family

423

71.5

371

73,18

 Alone

42

7.1

33

6,51

 In a group

64

10.8

53

10,45

 Homeless

14

2.4

11

2,17

 Incarcerated

10

1.7

8

1,58

 Unknown

39

6.6

31

6,11

Center of diagnosis

    

 Emergency department

320

54.1

283

55,82

 Primary care

113

19.1

94

18,54

 Specialized center

91

15.4

76

14,99

 Unknown or other

68

11.5

54

10,65

Smoking

    

 Non-smoker

318

53.7

272

53,65

 Smoker

194

32.8

176

34,71

 Ex-smoker

80

13.5

59

11,64

Alcohol Use

    

 Yes

116

19.6

104

20,51

 No

467

78.9

395

77,91

 Unknown

9

1.5

8

1,58

HIV status

    

 Positive

25

4.2

23

4,54

 Negative

446

75.3

384

75,74

 Not known by patient

110

18.6

91

17,95

 Unknown

11

1.9

9

1,78

Previous tuberculosis treatment

    

 No

543

91.7

464

91,52

 Yes

34

5.7

29

5,72

 Unknown

15

2.5

14

2,76

Country of origin

    

 Spain

401

67.7

334

65,88

 Other

191

32.3

173

34,12

Drug resistance

    

 No

579

97.8

496

97,83

 Yes

13

2.2

11

2,17

Chest radiograph

    

 Abnormal with cavitation

208

35.1

191

37,67

 Abnormal without cavitation

284

48

235

46,35

 Normal

71

12

57

11,24

 Unknown

29

4.9

24

4,73

Microbiology

    

 Smear-positive

287

48.5

260

51,28

 Smear-negative and  culture-positive

222

37.5

179

35,31

 Smear-negative and  culture-negative

67

11.3

55

10,85

 Other

16

2.7

13

2,56

Tuberculosis involvement

    

 Pulmonary

405

68.4

362

71,40

 Extrapulmonary

71

12

54

10,65

 Mixed

44

7.4

36

7,10

 Unknown

72

12.2

55

10,85

Table 3

Demographic characteristics of tuberculosis cases and factors associated with unreported cases

 

Total

Reported

 

Unreported

 

Bivariate analysis

 

Multivariate analysis

 
 

N = 592

N = 507

 

N = 85

 

OR (95 % CI)

p-value

OR (95 % CI)

p-value

Variables

 

n

%

n

%

    

Age (years)

         

 18-30

146

128

87.7

18

12.3

1.19 [0.62-2.27]

0.592

  

 31-50

237

212

89.5

25

10.5

Ref.

Ref.

  

 51-64

62

52

83.9

10

16.1

1.64 [0.71-3.56]

0.238

  

 >65

121

92

76

29

24

2.66 [1.48-4.84]

0.001

  

 Unknown

26

23

88.5

3

11.5

1.15 [0.25-3.66]

0.835

  

Sex

         

 Male

368

321

87.2

47

12.8

Ref.

Ref.

  

 Female

214

179

83.6

35

16.4

1.34 [0.83-2.14]

0.235

  

 Unknown

10

7

70

3

30

3.00 [0.59-11.5]

0.165

  

Employment

         

 Employed

205

174

84.9

31

15.1

1.54 [0.70-3.7]

0.296

1.75 (0.74-4.09)

0.197

 Unemployed

184

169

91.8

15

8.2

0.77 [0.32-2.02]

0.581

0.88 (0.35-2.23)

0.801

 Retired

125

94

75.2

31

24.8

2.84 [1.27-7.04]

0.01

3.04 (1.29-7.18)

0.011

 Unknown/On  disability

78

70

89.7

8

10.3

Ref.

Ref.

 

Ref.

Living situation

         

 With family

423

371

87.7

52

12.3

Ref.

Ref.

  

 Alone

42

33

78.6

9

21.4

1.96 [0.84-4.21]

0.116

  

In a group

64

53

82.8

11

17.2

1.49 [0.70-2.96]

0.287

  

 Homeless

14

11

78.6

3

21.4

2.01 [0.42-6.81]

0.338

  

 Incarcerated

10

8

80

2

20

1.88 [0.25-7.95]

0.477

  

 Unknown

39

31

79.5

8

20.5

1.86 [0.76-4.12]

0.166

  

Center of diagnosis

         

 Emergency  Department.

320

283

88.4

37

11.6

Ref.

Ref.

  

 Primary care

113

94

83.2

19

16.8

1.55 [0.83-2.80]

0.163

  

 Specialty clinic

91

76

83.5

15

16.5

1.52 [0.77-2.87]

0.223

  

 Unknown or other

68

54

79.4

14

20.6

1.99 [0.98-3.88]

0.058

  

Country of origin

         

 Spain

401

334

83.3

67

16.7

Ref.

Ref.

  

 Other

191

173

90.6

18

9.4

0.52 [0.29-0.89]

0.016

  
Table 4

Clinical characteristics of tuberculosis cases and factors associated with unreported cases

 

Total

Reported

 

Unreported

 

Bivariate analysis

 

Multivariate analysis

 
 

N = 592

N = 507

 

N = 85

 

OR (95 % CI)

p-value

OR (95 % CI)

p-value

Variables

 

n

%

n

%

    

Smoking

         

 Non-smoker

318

272

85.5

46

14.5

1.64 [0.94-3.00]

0.084

  

 Smoker

194

176

90.7

18

9.3

Ref.

Ref.

  

 Ex-smoker

80

59

73.8

21

26.3

3.46 [1.72-7.03]

0.001

  

Alcohol use

         

 Yes

116

104

89.7

12

10.3

Ref.

Ref.

  

 No

467

395

84.6

72

15.4

1.56 [0.84-3.14]

0.162

  

 Unknown

9

8

88.9

1

11.1

1.20 [0.04-7.67]

0.877

  

HIV status

         

 Positive

25

23

92

2

8

Ref.

Ref.

  

 Negative

446

384

86.1

62

13.9

1.74 [0.49-11.9]

0.435

  

 Not known by patient

110

91

82.7

19

17.3

2.25 [0.59-16.2]

0.264

  

 Unknown

11

9

81.8

2

18.2

2.48 [0.23-27.0]

0.431

  

Previous tuberculosis treatment

         

 No

543

464

85.5

79

14.5

Ref.

Ref.

  

 Yes

34

29

85.3

5

14.7

1.04 [0.34-2.56]

0.942

  

 Unknown

15

14

93.3

1

6.7

0.48 [0.02-2.42]

0.436

  

Drug resistance

         

 No

579

496

85.7

83

14.3

Ref.

Ref.

  

 Yes

13

11

84.6

2

15.4

1.15 [0.16-4.47]

0.861

  

Chest radiograph

         

 Abnormal with cavitation

208

191

91.8

17

8.2

Ref.

Ref.

  

 Abnormal without cavitation

284

235

82.7

49

17.3

2.33 [1.32-4.29]

0.003

  

 Normal

71

57

80.3

14

19.7

2.75 [1.25-5.96]

0.012

  

 Unknown

29

24

82.8

5

17.2

2.37 [0.71-6.72]

0.149

  

Microbiology

         

 Smear-positive

287

260

90.6

27

9.4

Ref.

Ref.

 

Ref.

 Smear-negative and  culture-positive

222

179

80.6

43

19.4

2.30 [1.38-3.91]

0.001

1.87 (1.07-3.28)

0.028

 Smear-negative and  culture-negative

67

55

82.1

12

17.9

2.11 [0.97-4.36]

0.059

1.59 (0.68-3.72)

0.280

 Other

16

13

81.3

3

18.8

2.29 [0.48-7.80]

0.264

1.24 (0.30-5.06)

0.759

Tuberculosis involvement

         

 Pulmonary

405

362

89.4

43

10.6

Ref.

Ref.

 

Ref.

 Extrapulmonary

71

54

76.1

17

23.9

2.65 [1.38-4.94]

0.004

2.07 (1.05-4.09)

0.035

 Mixed

44

36

81.8

8

18.2

1.89 [0.77-4.18]

0.156

1.50 (0.63-3.53)

0.353

 Unknown

72

55

76.4

17

23.6

2.61 [1.36-4.84]

0.005

2.01 (0.97-4.15)

0.059

HIV: Human immunodeficiency virus

On a bivariate level, the following variables were associated with unreported cases: age over 65 years, retirement, smoking history, immigrant status, normal or non-cavitary chest x-ray, smear-negative TB, and the presence of extrapulmonary TB. On a multivariate level, the following variables were associated with unreported TB: retirement (OR: 3.04, CI 1.29-7.18), smear- negative TB (OR: 1.87, CI 1.07-3.28) and the presence of extrapulmonary TB (OR: 2.07, CI 1.05-4.09) (Tables 3 and 4). The percentage of reported cases among the smear-positive cases was 9.4 % and 19.4 % (p = 0.001) among the rest of the study population. Smear-positive TB was no associated to under-reporting.

Discussion

We found that 14.4 % of TB cases were not reported to a public health department and the proportion of unreported cases ranged between 0 and 45.2 % according to healthcare facility. It is notable that the five healthcare facilities that reported 100 % of their TB cases to the public health department employed a nurse case manager who acted as a liaison between the medical team and the infection control team, assisted with data collection, contact tracing, and case reporting to the public health department.

Previous studies in Europe have estimated the rate of unreported TB cases is over 20 % [7, 10, 11, 18, 19]. A rate of 27 % was described in central Italy [10], 38-49 % in the United Kingdom [7], and 80 % in Greece [11]. Studies from Spain estimate rates of unreported TB range from 20 % to 46 % [1315, 19], but these percentages represent a limited geographical area (the Baleares Islands, Area 15 of Alicante, León and Asturias). This range is wide and may be due to the local TB organization.

Regarding the factors associated with unreported TB cases, studies have described high rates of unreported cases among older patients [10, 13], among those without microbiological confirmation [10], among patients with absence of cavitary lesions on chest x-ray [10, 13], and among non-immigrant patients [13]. Our study showed the same results on a bivariate level, but without statistical significance on a multivariate level for age, x-ray findings or country of origin. Retirement was associated with a higher risk of under-reporting, even independent of age. This has also been demonstrated in studies performed in other countries [20], which describe 25 % of unreported cases among patients over 60 years of age. This may be due to the higher rate of comorbidity conditions and multiple reasons for hospital admission, which could distract the provider that would diagnose and report the TB case.

We also found an association between unreported cases and extrapulmonary TB and smear-negative TB, for which the diagnosis may be delayed or without microbiological histology or culture. This was also described in many other studies [7, 10, 13, 20, 21], and maybe due to the fact that the provider think that transmission is lower among these cases. Nonetheless, reporting TB cases to the public health department is important to identify affected patients promptly thereby lowering transmission, to calculate an accurate incidence, and also to identify the TB index cases.

Smear-positive TB patients are more contagious and thus case reporting and contact tracing is crucial. Our study found that 9.4 % of smear-positive cases were not reported, which is actually lower than rates described in other studies [19].

The majority of the cases were diagnosed and reported from emergency departments and specialty clinics in our study as well as from other published studies [13, 15], and half of which were diagnosed in the emergency department. Case detection in the primary care setting is essential for early diagnosis and eventual disease control. We found that the diagnosis of TB in primary care centers is not associated with under-reporting (Table 3), which differs from one Spanish study [13]. However the percentage of TB cases diagnosed in primary centers is small and could represent an initial opportunity for diagnosis that was missed. This suggests disease control in the primary care setting may be weak and could be a target for strategies to improve TB diagnosis. Training programs for the diagnosis of TB targeting the general public and primary care providers should be implemented.

When TB is not diagnosed or unreported, an opportunity to prevent disease transmission is lost and the disease can spread. All patients with a concern for TB should be immediately evaluated and the diagnosis should be reported to the public health department without delay [5, 6]. This requires coordination between the hospital, the department of epidemiology, and the microbiology and pathology departments. For example, electronic reporting systems, in which case reports are sent electronically from local to centralized databases, have been implemented in other countries [22, 23].

Our study also has limitations that are inherent to retrospective studies because of missing information. However, a prospective study design could have led to a bias of high compliance and reporting. The large number of participating healthcare facilities in our study offers a good estimation of unreported TB cases, even with a retrospective design. Additionally, the number of patients who were not evaluated at a specialty clinic is low. The patients who were diagnosed and followed by primary care centers have microbiological data recorded in a microbiology registry compiled with data from specialty clinics, but no electronic medical record.

Conclusions

It is important that TB Control Programs encourage thorough case reporting to improve disease control, contact tracing and accuracy of epidemiological data. This is particularly relevant for TB cases that are smear-negative, given the association with under-reporting. As seen from our study results, the help from a TB nurse case manager could improve the rate of under-reporting.

Notes

Declarations

Acknowledgements

We would like to acknowledge the Public Health Departments of Andalusia, Asturias, Cantabria, Catalonia, Galicia, The Rioja, Madrid, The Basque Country, and Valencia, and the Preventive Medicine Departments of participating hospitals who made significant contributions in the acquisition of data. We would also like to thank to Jeanne Gambucci for her role as the scientific medical writer.

The present study was carried out at the Integrated TB Program (PII TB) of the Spanish Society of Lung Pathology (SEPAR) and was financed by a SEPAR research grant.

Authors’ Affiliations

(1)
Programa Integrado de Investigación en Tuberculosis (PII-TB) de la Sociedad Española de Neumología y Cirugía Torácica (SEPAR)
(2)
Hospital Universitario Virgen de las Nieves de Granada
(3)
Fundación Respira de la SEPAR
(4)
Hospital Central de Asturias de Oviedo
(5)
Hospital Universitario Carlos Haya de Málaga
(6)
Hospital Universitario San Cecilio de Granada
(7)
Consorcio Sanitario de Tarrasa
(8)
Unitat de Prevenció i Control de Tuberculosis de Barcelona
(9)
Hospital Xeral-Calde de Lugo
(10)
Agencia de Salud Publica
(11)
CIBER de Epidemiologia y Salud Pública (CIBERESP)

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Copyright

© Morales-García et al. 2015

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

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