Major Article Two Decades of Tuberculosis in A City in Northeastern Brazil: Advances and Challenges in Time and Space
Major Article Two Decades of Tuberculosis in A City in Northeastern Brazil: Advances and Challenges in Time and Space
Major Article Two Decades of Tuberculosis in A City in Northeastern Brazil: Advances and Challenges in Time and Space
[1]. Núcleo de Estudos em Saúde Coletiva, Centro de Pesquisas Aggeu Magalhães, Fundação Oswaldo Cruz, Recife, Pernambuco, Brasil.
ABSTRACT
Introduction: This study presents two decades of epidemiological data on tuberculosis (TB), in order to understanding the disease
profile and its spatiotemporal dynamics. Methods: This descriptive study was performed in the City of Olinda/Pernambuco,
Brazil, from 1991-2010, and it analyzed new patients with TB living in the city. We used the χ²-test with a p-value <0.05 to
identify differences in trends. Incidence and cluster distribution were identified using spatial scan statistics. Results: In total,
6202 new cases were recorded during the two decades. The highest incidence occurred in 1995 (110 cases/100,000 inhabitants),
and the lowest occurred in 2009 (65 cases/100,000 inhabitants) (β=-1.44; R²=0.43; p=0.0018). The highest mortality occurred
in 1998 (16 deaths/100,000 inhabitants), and the lowest occurred in 2008 (5 deaths/100,000 inhabitants) (β=-0.19; R²=0.17;
p=0.07). There was a male predominance (65%), and ages ranged from 20-49 years (65%). There was a substantial increase in
the number of patients that were cured after treatment (60% to 67%; p<0.001) as well as those tested for HIV (1.9% to 58.5%;
p<0.001). During the first decade, clusters with p-values <0.05 included 29% of the total notified cases, and in the second decade,
that percentage was 12%. Conclusions: We observed a decreasing trend in incidence, which was significant, and mortality rates,
which was not significant. The increased number of laboratory tests performed reflects advances in surveillance, and a reduction
in the proportion of cases in primary clusters suggests, among other things, that the disease is spreading across the region.
Keywords: Tuberculosis. Epidemiological surveillance. Spatial analysis.
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TABLE 1 - Operational and epidemiological characteristics of patients with tuberculosis in Olinda, Pernambuco State, from 1991 to 2010.
Operational and epidemiological
characteristics 1991-1995 1996-2000 2001-2005 2006-2010 Total
n % n % n % n % n %
Total number of cases 1,747 - 1,981 - 1,649 - 1,547 - 6,924 -
Type of entry
new case 1,647 94.3 1,647 83.1 1,495 90.7 1,413 91.3 6,202 89.6
relapse 57 3.3 153 7.7 83 5 69 4.5 362 5.2
return after abandonment 43 2.4 181 9.2 71 4.3 65 4.2 360 5.2
Raçe/color*
black - - 155 9.4 638 42.7 899 63.6 1,692 27.3
non-black - - 99 6 343 22.9 407 28.8 849 13.7
not informed 1,647 100 1,393 84.6 514 34.4 107 7.6 3,661 59
Form of disease*
pulmonary 1,478 89.7 1,392 84.5 1,225 81.9 1,170 82.8 5,265 84.9
extrapulmonary 167 10.1 202 12.3 213 14.3 185 13.1 767 12.4
pulmonary + extrapulmonary 1 0.1 46 2.8 57 3.8 58 4.1 162 2.6
not informed 1 0.1 7 0.4 - - - - 8 0.1
Case result*
cure 980 59.5 770 46.8 1,036 69.3 948 67.1 3,734 60.2
abandonment 200 12.1 178 10.8 129 8.7 133 9.4 640 10.3
death 107 6.5 196 11.9 171 11.4 154 10.9 628 10.1
others 360 21.9 503 30.5 159 10.6 178 12.6 1,200 19.4
Sputum smear*
performed 1,233 74.9 1,059 64.3 1,008 67.4 1,013 71.7 4,313 69.5
positive 937 828 785 769 3,319
negative 296 231 223 244 994
not performed 412 25 520 31.6 487 32.6 400 28.3 1,819 29.4
not informed 2 0.1 68 4.1 - - - - 70 1.1
Sputum culture*
performed 70 4.3 51 3.1 68 4.5 99 7 288 4.6
positive 43 34 48 54 179
negative 27 17 20 45 109
performed – in progress 23 1.4 75 4.6 107 7.2 93 6.6 298 4.8
not performed 1,552 94.2 1,461 88.7 1,320 88.3 1,221 86.4 5,554 89.6
not informed 2 0.1 60 3.6 - - - - 62 1
HIV Testing*
performed 31 1.9 104 6.3 207 13.8 827 58.5 1,169 18.8
positive 29 54 93 155 331
negative 2 50 114 672 838
performed – in progress 2 0.1 84 5.1 225 15.1 251 17.8 562 9.1
not performed 1,611 97.8 1,384 84 1,063 71.1 335 23.7 4,393 70.8
not informed 3 0.2 75 4.6 - - - - 78 1.3
HIV: human immunodeficiency virus. * Indicators calculated from the total of new cases notified during the five-year period.
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Cabral Silva APS et al. - Two decades of tuberculosis in a Brazilian city
120 30
Incidence Mortality
deaths/100,000 inhabitants
80 20
cases/100,000 inhabitants
60 15
40 10
20 5
y = -0,1918x + 11,536
R² = 0,1737
0 0
0
10
12
13
14
15
16
17
18
19
20
21
11
20
Obs: Incidence: β1= -1.44 (CI -2.27;-0.61); p=0.0018; t=0-> y0=99.9; t=20->y20=71.1; i= √(71.1/99.9)- 1= -1.7%
20
Mortality: β1= -0.19 (CI -0.399;+0.15); p=0.0675; t=0-> y0=11.5; t=20->y20=7.7; i= √(7.7/11.5)- 1= -2.0%
FIGURE 1- Incidence and mortality trends for tuberculosis in Olinda, Pernambuco State, from 1991 (t=1) to 2010 (t=20).
TABLE 2 - Distribution, incidence (cases/100,000 inhabitants), and relative risk of new TB cases according to patient age and sex in
Olinda, Pernambuco State, from 1991 to 2010.
1991-1995 1996-2000 2001-2005 2006-2010
n % incid RR n % incid RR n % incid RR n % incid RR
Age group (years)
<20 215 13.3 28.5 1.0 172 10.6 25.0 0.9 139 9.4 20.0 0.7 123 8.8 19.3 0.7
20–49 1,047 65.0 137.9 1.0 1,023 63.2 127.5 0.9 996 67.6 114.4 0.8 883 63.5 92.2 0.7
≥50 350 21.7 143.5 1.0 424 26.2 153.6 1.1 339 23.0 107.1 0.7 386 27.7 101.5 0.7
Sex
male 1,078 65.5 130.4 1.0 1,008 61.2 121.5 0.9 976 65.3 110.9 0.9 906 64.1 98.6 0.8
female 569 34.5 61.1 1.0 639 38.8 68.3 1.1 519 34.7 51.9 0.8 507 35.9 48.0 0.8
TB: tuberculosis; n: number; %: percentage; incid: incidence; RR: relative risk.
to a total of 58.5% of cases reported during the last five years p<0.001) and, over the same period, treatment abandonment
(RR=73.6; χ²=1502 9; p<0.001) (Table 1). However, given the was reduced from 12.1% to 9.4% (RR=0.75; χ²=9.4; p=0.002)
evolution of laboratory testing, there is an outstanding number of (Table 1). The model estimates an initial incidence of
results classified as in progress, both for the sputum culture and 99.9 cases / 100,000 inhabitants and a final incidence of
HIV testing, which in the last five years reached 17.8% (Table 1). 71.1 cases/100,000 inhabitants (Figure 1). With an average
Cure rates started at 59.5% in the first five-year period and incidence of 86 cases/100,000 inhabitants, these three values
reached 67.1% between 2006 and 2010 (RR=1.39; χ²=63.0; guided the construction of spatial distribution categories. Rates
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Rev Soc Bras Med Trop 49(2):211-221, Mar-Apr, 2016
Incidence Clusters
1991- 1995
1996 - 2000
2001- 2005
Incidence (% of census
tracts per class) P-value
< 71.1 (62.2%)
71.1 – 86.0 (12.7%) < 0.05
86.1 – 99.9 (4.7%) 0.05 – 0.20
> 99.9 (20.4%) >0.20
2006- 2010
Incidence (% of census
tracts per class) P-value
< 71.1 (66.6%)
71.1 – 86.0 (7.7%) < 0.05
86.1 – 99.9 (6.0%) 0.05 – 0.20
> 99.9 (19.7%) >0.20
0 3000 6000 9000
meters
FIGURE 2 - Incidence (cases/100,000 inhabitants) and TB clusters according to residential census tracts in Olinda, Pernambuco State, from 1991 to
2010. TB: tuberculosis.
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Cabral Silva APS et al. - Two decades of tuberculosis in a Brazilian city
above 99.9 cases/100,000 inhabitants suggest that, over the territory (Figure 2). Cluster analysis confirmed this hypothesis
study period, the sectors presented (or remained) in a situation by demonstrating that in both five-year periods of the first decade
similar to conditions observed in the early 1990s. almost 30% of cases were concentrated within the clusters
By comparing the four five-year periods, there was a with p<0.05, which had numbers of TB cases greater than
significant reduction in the proportion of census tracts in which would be expected if the spatial distribution was homogeneous.
the incidence was higher than 99.9 cases/100,000 inhabitants, These values were significantly lower in the third and
although with 6% of the confidence interval (CI) 86-99.9, fourth five-year periods, suggesting a greater disease spread
suggesting the possibility of a homogeneous TB trend within the (Figure 2 and Table 3).
continue....
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TABLE 3 - Continuation.
Number of cases
Clusters Number of sectors observed expected RR P value Population (%)* Cases (%)**
2001 to 2005
1 5 58 23 2.6 7.8x10-7 2.1 5.2
2 1 14 2 6.1 1.6x10 0.2
-4
1.2
3 4 35 15 2.4 0.007 1.3 3.1
4 4 35 17 2.1 0.059 1.5 3.1
5 1 15 5 2.8 0.319 0.5 1.3
6 7 44 27 1.7 0.590 2.4 3.9
7 1 15 6 2.5 0.638 0.5 1.3
8 5 29 17 1.8 0.876 1.5 2.6
9 3 19 10 1.9 0.990 0.9 1.7
10 1 7 2 3.0 0.993 0.2 0.6
11 1 7 2 3.0 0.993 0.2 0.6
12 2 17 9 1.9 0.999 0.8 1.5
13 2 13 6 2.0 0.999 0.6 1.2
14 3 21 12 1.7 0.999 1.1 1.9
2006 a 2010
1 11 74 31 2.5 1.2x10-7 2.9 6.8
2 8 63 29 2.3 3.4x10-5 2.6 5.8
3 4 36 17 2.2 0.026 1.5 3.3
4 4 34 16 2.2 0.054 1.5 3.1
5 7 49 27 1.8 0.107 2.5 4.5
6 2 17 6 2.7 0.194 0.6 1.6
7 2 15 7 2.3 0.887 0.6 1.4
8 3 21 11 1.9 0.966 1.0 1.9
9 2 15 8 2.0 0.996 0.7 1.4
10 4 24 15 1.7 0.998 1.3 2.2
11 3 23 14 1.6 0.999 1.3 2.1
12 1 7 3 2.4 0.999 0.3 0.6
TB: tuberculosis; RR: relative risk. *Percentage of the total population in the city living in the cluster. **Percentage of the total number of cases in the city that
occurred within the cluster.
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Cabral Silva APS et al. - Two decades of tuberculosis in a Brazilian city
With so many advances, the disconcerting question, Information quality is directly related to the completeness
Why have strategies that have proved efficient for the country as of notification and monitoring tools. The present study revealed
a whole been unsuccessful in attaining the required magnitude that the notification forms supplied to Sinan have become more
of effects on TB indicators in the city of Olinda? remains. thorough, now including variables such as race/color. This
The differences observed between Olinda and the rest of the advancement, however, requires caution when interpreting data,
country suggest that this improvement occurs with different since it is not possible to affirm, for example, that in Olinda there
intensities, possibly due to inequalities between municipalities was an increase in notifications from the black community. It is
and intramunicipal scales. probable that this increase was caused by improved registration,
The TB situation within the municipality not only emphasizes and not necessarily by a change in disease.
the need to optimize the strategies already in place but also to Tuberculosis can affect a number of organs and systems,
adopt others that are able to harness data that go beyond those with the pulmonary form, which in Brazil is detected in 85%
inherent to the health sector and may explain the occurrence of of patients aged 15 years and over, being the most common. In
the disease, such as territory-based surveillance. This approach Olinda, the mean ratio of this form is similar to that recorded for
could provide support for planning and executing actions at the entire country. More often than not, pulmonary bacillary TB
different levels, thus positively influencing TB indicators. are relevant to public health since they maintain the transmission
There was an insignificant trend in mortality reduction. In chain of the disease(16).
2010, mortality exceeded double the state and was more than High proportions of pulmonary TB in a community justify
three times the national average. However, these findings may the need for the sputum smear – a simple and safe method
not only be describing the poor prognosis in the city, as they that should be performed by all public health laboratories and
may have been influenced by SIM quality improvement during authorized private laboratories. When performed properly, the
the two decades analyzed(17) (24) (25). This justification does not test is able to detect between 60-80% of pulmonary TB cases(16).
reduce the importance of implementing a mortality surveillance Over the 20-year period, a mean 70% of patients notified during
system that examines routine relationships between databases, the five-year periods performed the test. Throughout all of
home, and hospital; forms of a multidisciplinary technical group Brazil, this ratio varied from 76.4% to 85.3%(16) (33) (34) (35).
to discuss death and partnerships, such as civil society, and Due to its importance, the sputum smear should be
controls programs for sexually transmitted disease- acquired encouraged, along with other features, such as those offered by
immunodeficiency syndrome (STD/AIDS) and viral hepatitis. the GeneXpert system, which allows the simultaneous detection
The higher proportion of male patients is consistent with of Mycobacterium tuberculosis and rifampicin resistance testing
findings in the current literature, with a possible cultural and using sputum(36). A systematic review involving 18 studies
social determination related to exposure(1) (26) (27) (28). Biological and 10,224 biological specimens demonstrated that a single
factors should also be considered, since there are generally Xpert Mycobacterium tuberculosis (MTB) DNA and resistance
significant sexual differences between respiratory tract infection to rifampicin (RIF) test detected 90.4% of pulmonary TB cases
(RTI) development and outcomes(29). Males appear to suffer from (98.7% smear-positive and 75% smear-negative)(37).
most commonly forms of RTI, and also they usually experience In pulmonary cases with negative sputum smears, sputum
a more severe disease course with higher mortality rates(29) (30). culture can increase bacteriological diagnosis of the disease by
Being aware that only 5% to 10% of individuals who are exposed up to 30%(16). Given this importance, there has been a modest
to Mycobacterium tuberculosis develop TB and that up to 70% increase in performing sputum culture performance from 4.3%
of people who develop the disease are male(29), researchers to 7%.
should be encouraged to investigate in greater depth the manner During the two decades, HIV testing increased significantly.
in which genetic variations and steroid hormones, for example, However, in 41.5% of the cases, tests were either not performed,
differentially influence disease susceptibility between the sexes. or they were performed but results were still in progress. In
In terms of age, over 60% of cases involved patients who were Brazil, testing is still insubstantial, and in a number of localities
between 20 and 49 years old, although there was a high incidence in the frequency of patients who do not undergo the test is over
those aged 50 years or older. Awareness that this population group 80%(38). The low proportion of HIV testing and culture may
is more sensitive to TB reactivation owing to lower immunity while reflect difficulties in laboratory access, delays in receiving
they have higher occurrences of chronic diseases, the Tuberculosis results, lost tests, or even a lack of updated information systems.
Control Program needs to be linked to disease surveillance Given the estimations in Olinda of patients coinfected with TB
programs, health care programs for the elderly in order to minimize and HIV, both the efforts of professionals who serve patients
adverse outcomes. On the other hand, a reduction in cases involving and the validity of information are jeopardized due to these
patients who are less than 20 years old may indicate a reduction in structural flaws.
active transmission and recent infection. In Brazil, TB is approximately 30 times more common in
In the present study, 45% of patients reported that they received people living with HIV, compared to the incidence in the general
up to eight years of schooling, including the illiterate(25) (31) (32). Low population(39). Hence, the Ministry of Health recommends that
levels of education reflect a set of poor socioeconomic conditions HIV testing be mandatory for patients with detected cases of
that increase vulnerability to TB and consequently the increase TB, and vice versa(16), which is aimed at initiating immediate
disease incidence, while lowering adherence to treatment(32). intervention. Clinical trials have shown that concomitant
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Rev Soc Bras Med Trop 49(2):211-221, Mar-Apr, 2016
treatment is able to reduce mortality by over 50%(40). Thus, Finally, it is important to consider that there may be
the high numbers of unperformed blood tests or of those still characteristics directly resulting from the disease control
in progress jeopardizes the timely initiation of treatment and program associated with a higher TB incidence, such as cases
hinders the structuring of public health plans in order to prevent of additional treatment and families with two or more affected
and reduce deaths from TB-HIV. persons in the same household(8). This report reveals that the
With regard to case outcomes, during the two decades, a cure incorporation of mapping within routine health surveillance,
rate of 60.2% was identified, reaching a maximum of 67.1% in along with periodic updates of the associated factors, may
the last five-year period, although the rate was still below the contribute to the organization of health services. On the other
85% recommended by PNCT(41). Throughout the entire period, hand, it reinforces the greater responsibility that health services
treatment abandonment and deaths remained at 10%. The have to face with controlled actions that are able to impact
abandonment of treatment not only affects the rising treatment disease incidence.
costs, but it also affects mortality rates and disease recurrence, After a 20-year period, despite a reduction in incidence and
while facilitating the selection of resistant strains(42) (43). a downward trend in mortality, TB rates in Olinda are higher
However, similar to occurrences in other Brazilian than the mean rates of the state and the country as a whole. The
cities(28) (34) (35), case outcome analysis is hampered by the high low number of smear tests and sputum cultures indicate that the
(19.3%) percentage of cases where circumstances at the end of available technologies are underutilized. The high percentage
treatment were classified as ignored, transferred, or changed of HIV tests in progress exemplifies the fragile feedback of the
treatment, thus suggesting failings in appropriate patient monitoring information system, and it hinders the estimates of TB-HIV
by the health team or insufficient flow of existing information. co-infection in the city as well as planning based on the main
instrument for decision making.
In relation to the spatial analysis method used, it should be
highlighted that the differential of this method lies in the manner Analysis of the spatial distribution of cases demonstrated
with which it characterizes the relevant cluster according to the that relevant clusters remained in the same regions during the
exposed population and the concentration of cases in relation two decades, which not only indicates that these areas presented
to the total within the municipality. Contrary to misgivings similar socioeconomic characteristics during the period, but
concerning the use of grouping sectors with low incidence levels it also indicates that the actions to control the disease need to
to generate clusters(44), this was not an issue in the present analysis. be optimized and made more appropriate for this extremely
vulnerable population group.
The adopted cluster sizes grouped up to a maximum of 5% of
the exposed population with the territory analysis characteristics,
such as the distribution of cases and the exposed population. CONFLICT OF INTEREST
Demarcation of the problem based on census tracts has enabled us
to view the heterogeneous distribution of the disease in urban areas, The authors declare that there is no conflict of interest.
thus enabling intervention planning aimed at specific groups(9).
Although there has been a reduction in incidence in Olinda,
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