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Nicolas Yanez, MD, MS,* Juan Nicolas Useche, MD,† Hernan Bayona, MD,‡
Alexandra Porras, PhD,* and Gabriel Carrasquilla, PhD*
Background: Stroke is the second cause of death and the first cause of disability
worldwide. However, although numerous reports regarding stroke epidemiology
in Latin America have been published, they differ widely in terms of employed
methods and end points. This is the first of a series of articles that describes the epi-
demiology of stroke and other cerebrovascular diseases (CVD) in the nation, as
well as their correlation with recognized risk factors and social variables. Methods:
Descriptive analyses were performed using the Colombian vital registration system
and social security information system as primary data sources. Rates and ratios
were calculated, corrected for under-registration, and standardized. Secondary
analyses were made using data from national surveys and government organiza-
tions on hypertension, diabetes mellitus, sedentarism, obesity, tobacco and alcohol
consumption, and unsatisfied basic needs. Factorial multivariate multiple regres-
sion analyses were performed to evaluate correlations. Concentration curves and
indices were calculated to evaluate for inequities in the distribution of events.
Results: Global CVD had a national mortality rate and a prevalence ratio of 28 and
142 per 100,000 persons, respectively. Nontraumatic intracranial hemorrhage had
the highest mortality rate (ie, 15 per 100,000), while cerebral infarction and transi-
tory cerebral ischemia had the highest prevalence ratios (ie, 28 and 29 per 100,000,
respectively). Hypertension and tobacco use were the most relevant risk factors for
most of the simple and multiple models, and cerebral amyloid angiopathy and non-
pyogenous intracranial venous thrombosis were the disease categories with the
most socially unequal distribution of deaths and cases (ie, concentration indices of
.34 and .29, respectively). Conclusions: CVDs are a cause for concern in Colombia
and a marker of healthcare inequality and social vulnerability. Nationwide control
of risk factors such as hypertension and tobacco use, as well as the design and con-
duct of public policy focused on the vulnerable and medically underserved regions
and on standardizing mandatory CVD registries might ease its burden.
Key Words: Stroke—cerebrovascular disorders—mortality—prevalence—
socioeconomic factors—epidemiology
© 2020 Elsevier Inc. All rights reserved.
From the *Master of Science in Epidemiology Program, Universidad El Bosque, Bogota D.C, Colombia; †Department of Diagnostic Imaging, Hos-
pital Universitario Fundaci on Santa Fe de Bogota, Bogota D.C, Colombia; and ‡Department of Neurology, Hospital Universitario Fundaci on Santa
Fe de Bogota, Carrera 7 No. 117 15, Bogota D.C, Colombia.
Received June 27, 2019; revision received December 17, 2019; accepted January 25, 2020.
Sources of Funding: There are no funding sources to disclose. NY, as the corresponding author, had access to all the data in the study and had
final responsibility for the decision to submit for publication.
Address correspondence to Nicolas Yanez, MD, MS, Master of Science in Epidemiology Program, Universidad El Bosque, Carrera 9 No. 131A-02
Edificio Fundadores, Piso 5, Bogota D.C, Colombia. E-mail: nyanez@unbosque.edu.co.
1052-3057/$ - see front matter
© 2020 Elsevier Inc. All rights reserved.
https://doi.org/10.1016/j.jstrokecerebrovasdis.2020.104699
Journal of Stroke and Cerebrovascular Diseases, Vol. &&, No. && (&&), 2020: 104699 1
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2 N. YANEZ ET AL.
Introduction America. In keeping with this spirit, this paper is the first
of a series that describes and characterizes the epidemiol-
In 2015, neurological disorders were the largest cause
ogy and burden of stroke and other cerebrovascular dis-
group of disability-adjusted life years (DALYs) and the sec-
eases (CVDs), as well as the cost-effectiveness of the
ond largest behind cardiovascular diseases in terms of
treatment options offered in the health benefits plan of the
global deaths, accounting for 10.2% of DALYs and 16.8%
nation’s social security system. The research portrayed in
of deaths, respectively.1 Stroke, in particular, accounted for
this article had 2 objectives: (1) to estimate the mortality
almost half of the total DALYs and more than two-thirds
and prevalence of CVDs, including stroke, in Colombia,
of the deaths among all neurological disorders analyzed in
with stratification according to age, sex, and geographic
the Global Burden of Diseases, Injuries, and Risk Factor
location; and (2) to describe the correlation between the
2015 Study (GBD 2015 Study).1 However, despite substan-
estimated measures of frequency with hypertension, diabe-
tial decreases in mortality rates from stroke and communi-
tes mellitus, dyslipidemia, physical inactivity, obesity, and
cable neurological disorders in the last 3 decades, there
tobacco and alcohol use, as well as with unsatisfied basic
have been significant increases in the absolute number of
needs (UBN). This report adheres to the STROBE guide-
cases, deaths, and DALYs associated to stroke and other
lines for transparent reporting of observational studies.17,18
neurological conditions.2,3 This situation is even more con-
cerning when some studies predict that the number of
stroke events, at least for the United States, will more than Methods
double in 2050 as compared to those that occurred in 2010.4
This cross-sectional study is divided in 2 phases: (1)
The GBD 2015 study also showed a statistically signifi-
descriptive analyses of mortality and prevalence and (2)
cant increase in the proportional contribution of stroke-
secondary analyses of their correlations with risk factors
related DALYs and deaths in developing countries, a trend
and sociodemographic variables for the Colombian popu-
on the one hand explained by the widening gap in stroke
lation for which data were available during the 2014-2016
prevention and management between developed and
time period. An exploratory review of the literature was
developing countries and on the other hand conditioned
performed in order to identify the International Classifica-
by the effects of the epidemiologic and demographic transi-
tion of Diseases (ICD-10) codes to be used for the study
tions.5,6 During the past decades, the countries of Latin
and to define the categories of disease analysis (Table 1).
America have been the focus of social changes that have
led to a slowing in population growth, an increase in urban
Primary Descriptive Analyses of Mortality and
dwelling, and the steadily aging of their populations.7 This
Prevalence
has led to a gradual increase in the frequency of noncom-
municable disease risk factors to the point of almost herald- Primary data for mortality were obtained from the
ing an imminent cardiovascular disease epidemic.8 As is Colombian national vital registration system operated by
the case in most countries, hypertension, smoking, diabetes the National Administrative Department of Statistics
mellitus, physical inactivity, obesity, and atrial fibrillation (DANE, in Spanish) and publicly available at their official
have been identified as the leading risk factors for stroke in website.19 An individual identification number was
Latin America by several studies, including the CARMELA assigned for each registry in the crude anonymized data-
(Cardiovascular Risk Factor Multiple Evaluation in Latin base and the age variables were recodified to a new 5-year
America) and INTERSTROKE (Risk Factors for Ischemic age interval variable. Causes of death (CoD) were codified
and Intracerebral Hemorrhagic Stroke in 22 Countries) to each category of disease analysis according to the ICD-
studies.9-12 Additionally, conditions such as Chagas dis- 10 rules for selection of underlying CoD.20 If an underlying
ease, which is associated with cardiomyopathy, arrhyth- cause was senility or an ill-defined condition, the sequence
mias, and cardioembolic events in almost a third of the of the other multiple causes was analyzed in order to deter-
cases, have also been recently recognized as important mine if an ICD-10 code of interest was the actual CoD. Reg-
region and country-specific risk factors.13 However, the istries where then recodified to reflect the change in CoD.
study of risk factors is not sufficient to adequately compre- Garbage code redistribution was performed according to
hend the causal network that determines health outcomes. the published literature.21-23 As reported by Truelsen et al,
Socioeconomic status, employment, housing, environmen- there is a significant proportion of stroke-related deaths
tal exposures, and the fulfillment of basic needs are exam- assigned to ill-defined codes.24 In an attempt to adequately
ples of social determinants of health that have been portray the burden of stroke-related deaths in order to
historically compromised in Latin American countries and inform decision-makers and the general population, regis-
which have been related to worse outcomes and quality of tries with I64 as CoD were redistributed to the ischemic or
life in patients with stroke.14-16 nonischemic categories according to the 5-year age interval
In light of the above, there has been an increased interest proportions in the well-codified registries. Specifically,
in the study of stroke, its risk factors and social determi- there were 10,728 registries that had I64 as CoD for the
nants for the guidance of public health policies in Latin 3 years under analysis. About 78% (8277) was redistributed
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CEREBROVASCULAR DISEASE EPIDEMIOLOGY IN COLOMBIA 3
Table 1. Categories of disease analysis and associated ICD-10 codes for mortality and prevalence estimations
Mortality
Disease category ICD-10 codes
1 Global CVD Comprised of disease categories 2-9
2 Cerebral arteritis in infectious and parasitic A18.8, A32.8, A52.0, I68.1
diseases
3 Cerebral amyloid angiopathy E85.0-9, I68.0
4 Vascular dementia F01.0-9
5 Nontraumatic intracranial hemorrhage I60-9, I69.0, I67.0-1, I61.0-9, I69.1, I62.0-9, I69.2
6 Cerebral infarction I63.0-9, I69.3, G45.0-9, R41.3, G46.0-8, I65.0-9, I66.0-9, I67.2-6
7 Cerebral arteritis in other diseases M32.1, I67.7, I68.2
8 Congenital malformations of the cerebral cir- Q28.0-9
culatory system
9 Other cerebrovascular diseases I67.8-9, I68.8, I69.8
Prevalence
Disease category ICD-10 codes
1 Global CVD Comprised of disease categories 2-17
2 Cerebral arteritis in infectious and parasitic A18.8, A32.8, A52.0, I68.1
diseases
3 Cerebral amyloid angiopathy E85.0-9, I68.0
4 Vascular dementia F01.0-9
5 Nontraumatic intracranial hemorrhage I60-9, I61.0-9, I62.0-9
6 Cerebral infarction I63.0-9, G46.0-8
7 Cerebral arteritis in other diseases M32.1, I67.7, I68.2
8 Congenital malformations of the cerebral cir- Q28.0-9
culatory system
9 Transient cerebral ischemic attack G45.0-9, R41.3
10 Occlusion and stenosis in the cerebral circula- I65.0-9, I66.0-9
tory system without infarction
11 Dissection of cerebral arteries without rupture I67.0
12 Cerebral aneurysm without rupture I67.1
13 Cerebral atherosclerosis and progressive vas- I67.2-3
cular leukoencephalopathy
14 Hypertensive encephalopathy I67.4
15 Moyamoya disease I67.5
16 Nonpyogenic thrombosis of the intracranial I67.6
venous system
17 Other cerebrovascular diseases I67.8-9, I68.8, I69.8
Abbreviations: ICD, International Classification of Diseases; CVD, cerebrovascular diseases.
to the nontraumatic intracranial hemorrhage disease cate- year and region to assess for statistical significance and var-
gory, while 22% (2350) was redistributed to the cerebral iance of time trends. Direct standardization and confidence
infarction disease category. The total counts of registries interval calculation were done in Epidat (Version 4.2,
that were redistributed accounted for a 35% and a 32% of Xunta de Galicia, Spain, 2016) while choropleths were
the total registries within each disease category, respec- made using Epi Info (Version 7.2.2.2, Centers for Disease
tively. Mortality counts were adjusted for completeness of Control and Prevention, Atlanta, Georgia, 2016). No choro-
death registration using the Bennett-Horuichi method. As pleths were made for disease categories for which meas-
the last published Colombian population census was per- ures of position could not be computed.
formed in 2005, the population projections for the years In Colombia, social security information system is the
2014, 2015, and 2016 were used to calculate the mortality technological platform that records every contact an indi-
rates per 5-year age interval, sex, geographic region, and vidual may have with the social security system. Health
year of death.25 Crude mortality rates were age adjusted professionals and institutions are required to upload the
using the Colombian census of 2005 as the standard popu- details of the event with information regarding the
lation and mid-p gamma confidence intervals were calcu- patient’s main diagnosis and demographics, as well as the
lated.26 After assessing for goodness of fit, Poisson type and characteristics of the event. As such, it is the pri-
regression was performed for each disease category per mary means to quantify various health variables in
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4 N. YANEZ ET AL.
Figure 1. Global CVD mortality rate and prevalence ratio (x 1,000) geographic distribution in Colombia (2016). Abbreviation: CVD, cerebrovascular diseases.
30-59 age group (ie, around .4 per 1000), and in the third at north-Andean regions (ie, higher than 1.88 per 1000). The
the 70-74 age group (ie, .44 per 1000) (eFigures 13-29). regions with highest nontraumatic intracranial hemorrhage
Disease distribution according to age-adjusted preva- and cerebral infarction ratios were scattered along the
lence ratios varied significantly from mortality distribution. southern Pacific region bordering Ecuador with a few foci
Global CVD was more frequent in the Caribbean and the in the Andean region. Compared to mortality geographic
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6 N. YANEZ ET AL.
Table 2. Simple and multivariate OLS regression results for global CVD measures and the risk factors under study in Colombia (2014-2016)
Figure 2. Global CVD and UBN concentration curve for mortality rates and prevalence ratios (x 1,000) in Colombia (2016). Abbreviations: CVD, cerebrovascu-
lar diseases; UBN, unsatisfied basic needs.
Table 3. Concentration indices for concentration curves relating noninfectious cerebral arteritis had a statistically significant
disease categories rates and ratios with UBN in Colombia (2016) correlation with hypertension and overweight and obesity,
but in multiple analysis the correlation with overweight and
Mortality Disease category Concentration obesity disappeared and was replaced by alcohol use. These
rates index
and other multivariate simple and multiple regression results
Global CVD .007 for mortality rates are described in eTables 6 and 7.
Infectious cerebral arteritis .176 Arterial hypertension and overweight and obesity were
Cerebral amyloid angiopathy .343 the only statistically significant risk factor for prevalence
Vascular dementia .33 ratios of global CVD with R2 values of .48 and .7, respec-
Nontraumatic intracranial .011 tively. In the case of infectious cerebral arteritis ratios, for
hemorrhage
the 3 statistically significant risk factors found in simple and
Cerebral infarction .034
multiple analyses (ie, hypertension, diabetes mellitus, and
Noninfectious cerebral arteritis .068
Congenital malformations .052 overweight and obesity), only hypertension was found to
Other CVD .043 have a positive correlation. These risk factors were also asso-
Prevalence ciated with cerebral amyloid angiopathy in simple analysis;
ratios however, in multiple analysis hypertension was no longer
Global CVD .092 significant. For vascular dementia ratios, diabetes mellitus
Infectious cerebral arteritis .04 was statistically significant only in simple regression models,
Cerebral amyloid angiopathy .176 while hypertension and tobacco use were significant in both.
Vascular dementia .23 Hypertension was the only risk factor which showed a posi-
Non-traumatic intracranial .03 tive statistically significant correlation with both, nontrau-
hemorrhage
matic intracranial hemorrhage and cerebral infarction. These
Cerebral infarction .065
and other multivariate simple and multiple regression
Noninfectious cerebral arteritis .181
Congenital malformations .18 results for prevalence ratios are described in eTables 8 and 9.
Transitory cerebral ischemia .077 Regarding the social variable UBN, on the one hand, fol-
Occlusion and stenosis of (pre) .144 lowing visual inspection of the concentration curves con-
cerebral arteries structed for mortality rates, cerebral amyloid angiopathy
Unruptured cerebral artery .218 and vascular dementia show the most socially unequal dis-
dissection tribution of deaths, with corresponding concentration indi-
Unruptured cerebral aneurysm .182 ces of .343 and .33. The other disease categories had either
Cerebral vascular atherosclerosis .161 low divergence from or transected the identity line. On the
and leukoencephalopathy other hand, the majority of concentration curves con-
Hypertensive encephalopathy .086
structed for prevalence diverged from the identity line,
Moyamoya disease .068
with nonpyogenous intracranial venous thrombosis,
Nonpyogenous intracranial .294
venous thrombosis unruptured cerebral artery dissection, and unruptured
Other CVD .059 cerebral aneurysm having the highest concentration indices
(ie, .294, .218, and .182, respectively) Concentration curves
Abreviations: CVD, cerebrovascular diseases; UBN, unsatisfied
basic needs. and their corresponding indices are available in Figure 2
and eFigures 41-64, and Table 3, respectively.
update, based on the best available data, of measures of dis- situation which most likely would have cause an underes-
ease mortality and frequency as well as their correlation to timation of the real estimated measures.
widely recognized risk factors. This study has several limitations. First, the data sources
Although CVD mortality rates keep in line with published for the estimations of mortality rates and prevalence ratios
available literature and have shown a tendency to decrease were based on the national vital registration and sanitary
over time, the same cannot be said for prevalence ratios.36 For event reporting systems. Miss-classification of disease out-
most disease categories prevalent cases appear to concentrate comes and inappropriate selection of ICD-10 codes are just 2
on the central wealthy urban regions while mortality is high- examples of inadequate coding behavior that is widespread
est on the medically underserved and impoverished regions, across the nation. As most analyzed disease categories
situation especially apparent to nontraumatic intracranial required either special equipment or training to be diagnosed
hemorrhage. Access to medical services and prompt and it is highly likely that rural and medically underserved
appropriate healthcare are essential factors that influence regions either failed to identify them or mistook them for
mortality of any cause. Moreover, in addition to treatment other entities. This is especially true for some uncommon
options such as intravenous thrombolytics, endovascular entities used in the prevalence analyses. Second, although
management, or surgical techniques (ie, craniotomy and ven- vital registration certificates may state CVD as CoD, there is
triculostomy) not being widely available, nonexisting or mal- no way to ascertain the time between event onset and actual
functional prehospital evaluation and notification systems are death. In a similar fashion, there is no way to distinguish
responsible for the transportation of cases to the nearest first-time ever from recurrent events, which results in the
healthcare institutions instead of the most appropriate ones. measurement of aggregate measures of disease mortality
These situations compound to existing social vulnerabilities and prevalence. This is especially true for stroke, as it has
making CVD and stroke prevention and management issues been established that disease mortality is highest during the
that should be addressed from an intersectorial point of view. first month after the event and that the epidemiology of
Even though it is logical that hypertension and tobacco recurrent events varies significantly from first-time ever
use were the risk factors with strongest measures of corre- strokes. Third, given the emphasis on ascertaining differen-
lation, it is not likely that any risk factor under study could ces between geographic regions, true mixed effects modeling
exert a protective effect on stroke and other CVDs. This would have been a more appropriate method for evaluating
was the case for overweight and obesity and for alcohol correlations. However, data on independent variables were
use and could have been the result of unmeasured and only available at an aggregated regional level, without any
uncontrolled ambient confounding. As such, models con- measures of dispersion or uncertainty that could be used to
taining any such variables must be regarded with caution. assess for inter- and intraclass variability. Fourth, ecological
Social inequity analyses can be performed in a number of cross-sectional studies have serious difficulties in quantifying
ways with several possible variables. The UBN index correlation measures and could be fraught with bias if con-
focuses on poor housing conditions and may not be as sensi- founding is not adequately addressed. Moreover, informa-
tive as the multidimensional poverty index in assessing true tion on risk factors were extracted from multiple sources
poverty and social disparity. However, updated and region- which, in turn, varied greatly in methods of data acquisition.
ally disaggregated multidimensional poverty index meas- Nevertheless, the results of this study are the most up-to-
urements were not available for Colombia for the period date epidemiological measures for stroke and other CVDs in
under study, and thus the UBN was used as a proxy. Given Colombia and underscore the importance of creating and
that prevalence is most likely determined by intrinsic and maintaining a national stroke and CVD registry, of regular
extrinsic (un)modifiable risk factors while actual mortality is and reliable national individual-level noncommunicable dis-
most likely influenced by access to prompt and appropriate ease risk factor assessment, and of focusing transectorial
healthcare, it is not surprising that high-cost and difficult-to- public health policies for CVD control on the medically
manage diseases, such as cerebral amyloid angiopathy and underserved regions and socially vulnerable populations.
vascular dementia, have the most socially unequal distribu-
tion of deaths. Access to appropriate healthcare services is
restricted in medically underserved regions, which in turn Acknowledgments
harbor low-income populations that cannot afford transpor-
N.Y. prepared the first draft. A.P. and G.C. reviewed and
tation or out-of-pocket expenses. High-income population,
edited the first draft and final versions of the manuscript. All
in contrast, might be appropriately managed and would
authors reviewed all subsequent drafts, reviewed results, and
eventually die due to other causes.
approved the final version of the manuscript.
It is important to note that the population projections
used in this study were those constructed based on the
2005 Colombian census. However, according to prelimi-
Disclosures
nary analyses of the 2018 census, the total Colombian
population was overestimated in such projections, a The authors have nothing to disclose.
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CEREBROVASCULAR DISEASE EPIDEMIOLOGY IN COLOMBIA 9