Rev Peru Med Exp Salud Publica. 2022;39(4):463-68.
BRIEF ORIGINAL
                                        MALARIA IN THE ECO-EPIDEMIOLOGICAL
                                        REGION OF THE COLOMBIAN CARIBBEAN,
                                        1960-2019
                                        Luis Acuña-Cantillo                  , Mario J. Olivera
                                                                           1,a                      1,b
                                                                                                       , Julio Cesar Padilla-Rodríguez               2,c
                                        1
                                            Instituto Nacional de Salud de Colombia, Bogotá, Colombia
                                        2
                                            Knowledge Management, Research and Innovation in Malaria Network, Instituto Nacional de Salud de Colombia, Bogotá,
                                            Colombia
                                        a
                                            Biologist; b Physician, master in Clinical Epidemiology and Health Economics; c Physician, specialist in Public Health and
                                            Epidemiology
                                        ABSTRACT
                                        Malaria has a heterogeneous and variable behavior among Colombian regions. In order to establish its
                                        epidemiological behavior in the Colombian Caribbean region between 1960 and 2019, we carried out an
                                        observational, descriptive and retrospective study based on records from the Ministry of Health and other
                                        secondary sources. We defined epidemiological variables and used measures of frequency and central tendency.
                                        A total of 155,096 cases were registered. The decades with the highest number of cases were 1990-1999 (20.5%)
                                        and 1980-1989 (18.9%). The average number of cases per decade was 25,849.3. The highest parasite rates were
                                        recorded in 1970 (3.3 per 1000 population) and 1981 (3.9 per 1000 population). Plasmodium vivax was the
                                        most frequent species and most of the burden by age group was found in people under 29 years of age, between
                                        2010-2019. Malaria showed an endemic-epidemic pattern of low and very low transmission intensity, with a
                                        decreasing trend.
                                        Keywords: Malaria; Epidemiology; Plasmodium vivax; Plasmodium falciparum; Caribbean; Colombia
                                        (Source: MeSH NLM)
                                        INTRODUCTION
                                        In Colombia, malaria accounts for 54.7% of the cumulative burden of cases of vector-borne
                                        diseases (1). In the last five years, there has been a change in the prevalence of the parasitic spe-
Cite as: Acuña-Cantillo L, Olivera      cies in the country, with Plasmodium falciparum being the most frequent one (2,3).
MJ, Padilla-Rodríguez JC. Malaria in
                                              This disease persists as a public health problem, imposing a high economic and social bur-
the eco-epidemiological region of the
Colombian Caribbean, 1960-2019.         den (4,5). Its transmission is endemic-epidemic, heterogeneous and varies from medium to low
Rev Peru Med Exp Salud Publica.
2022;39(4):463-68. doi: https://doi.    intensity in the eco-epidemiological regions throughout the national territory, under different
org/10.17843/rpmesp.2022.394.11359.
_________________________________
                                        conditions of receptivity and vulnerability.
                                              In the Caribbean region, the disease is confined and of very low transmission (6). In 2018, it con-
Correspondence: Luis Acuña-
Cantillo; lacuna@ins.gov.co             tributed 3% of the national malaria burden, and most cases were imported from other regions with
_________________________________
                                        varying degrees of transmission intensity (7). Despite this, few studies have been carried out on the
Received: 19/05/2022
Approved: 26/10/2022
                                        subject in this region, which have been specific and with limited dissemination, making it difficult
Online: 05/12/2022                      to make evidence-based decisions for the definition and implementation of eradication strategies (8).
                                              The intensification of environmental, economic, social, political, and cultural interactions
                                        in the last decade could change the transmission dynamics in the Caribbean region in the
This work is licensed under a
                                        coming years, favoring the reemergence, continuity, and intensification of endemic-epidemic
Creative Commons Attribution 4.0        levels in the region           . Therefore, the aim of this study was to identify the epidemiological
                                                                     (9)
International4.0 Internacional
                                        behavior of malaria in the Colombian Caribbean region between 1960 and 2019.
https://doi.org/10.17843/rpmesp.2022.394.11359                                                                                                                 463
Rev Peru Med Exp Salud Publica. 2022;39(4):463-68.                                               Malaria in the Colombian Caribbean, 1960-2019
THE STUDY
                                                                         KEY MESSAGES
Design, population and study area
A descriptive study was conducted in the Colombian Cari-                 Motivation for the study: the information available on the
bbean region. This region is located in northern Colombia                epidemiology of malaria in the Colombian Caribbean region
and is made up of the departments of Atlántico, Bolívar,                 is incomplete, poorly systematized and its dissemination is
Cesar, La Guajira, Magdalena, Sucre and the Archipelago of               limited. This has led to a lack of knowledge of its magnitude and
San Andrés, Providencia and Santa Catalina. It has an area               a low perception of its importance as a public health problem.
of 107,027 km2 and represents 9.4% of the Colombian terri-               Main findings: the behavior of malaria is endemic-epidemic,
tory. The region includes 167 municipalities and has an esti-            with low to very low transmission, focused and with irregular
mated population of 8,900,000 inhabitants, 22% (1,963,548                outbreaks. Plasmodium vivax infections predominate.
inhabitants) of whom are at potential risk of malaria, and
of these, 13% (260,544 inhabitants) are in areas with active             Implications: the results of this study contribute to improve
transmission and presence of vectors.                                    evidence-based decision making for the implementation of
                                                                         malaria eradication plans.
Study variables and inclusion criteria
We selected and included the universe of confirmed cases
of uncomplicated malaria reported by the Departmental
Health Secretariats to the Public Health Surveillance System         te index) and specific ones such as AFI (annual P. falciparum
(SIVIGILA) during the study period, as registered in the             index) and AVI (annual P. vivax index): [No. cases (total or
Integrated Social Protection Information System (SISPRO)             by parasite species x 1000) / (Population at risk)]. We deter-
(https://www.sispro.gov.co/Pages/Home.aspx). In addition,            mined percentage distributions of cases per decade and per
secondary information from the National Malaria Program              department. Finally, dispersion measures such as standard
for the period 1960-1999, available at the Ministry of Health        deviation (SD), maximum and minimum values were used.
and Social Protection was included.                                  The distribution by age group was estimated from the cu-
     We used the official case definition of uncomplicated ma-       mulative percentage distribution in the country during the
laria. The number of malaria cases and variables of place (de-       2010-2019 period. The coefficient of determination (R2) was
partments) and time (year, decades and period) were used. In         estimated in order to establish the time trend.
Colombia, it is mandatory that all malaria cases reported to
the surveillance system be confirmed using parasitological-          Ethical Aspects
diagnosis by microscopy, rapid diagnostic tests or polymerase        We followed the ethical requirements established in Reso-
chain reaction. Microscopy examination is the gold standard          lution 8430 of 1993 (Article 11) of the Colombian Ministry
for diagnosis of the disease in the country (8). Information on      of Health and Social Protection, which defines this research
the population at risk was obtained from national census pro-        as risk-free and therefore it does not require approval by an
jections of the National Administrative Department of Sta-           ethics committee (10).
tistics (DANE) (http://www.dane.gov.co/) for the years 1964,
1973, 1985, 1993, 2005 and 2018, corresponding to the rural          FINDINGS
population of the region. Malaria transmission intensity crite-
ria by eco-epidemiological regions were assumed according to         Between 1960 and 2019, 155,096 malaria cases were registered
the classification established in a previous study (6). The Carib-   in the Caribbean Region. The mean number of cases per deca-
bean region, like the other regions, is made up of departments       de was 25,849.3 SD: 4,192.3). The decades 1990-1999 (31,815
and municipalities that share similar social and environmen-         cases) and 1980-1989 (29,286 cases) had the highest number of
tal characteristics.                                                 cases. Among the departments, Bolivar with 43.4% (67,330 ca-
                                                                     ses), La Guajira with 14.4% (22,330 cases) and Sucre with 12.1%
Data analysis                                                        (18,827 cases) contributed to the highest
The data of the variables were stored and analyzed with the          burden in the region (Table 1).
Microsoft 365® Excel software. The distribution of quantita-             The secular behavior of transmission in the Caribbean
tive variables was evaluated using the Kolmogorov-Smirnov            Region showed a significant downward trend, with a variable
test. We constructed absolute frequency indicators such as           endemic-epidemic, low-intensity pattern. P. vivax infections
total and specific cases. We calculated measures of central          predominated. The most important outbreaks occurred in 1970
tendency such as mean number of cases and median accor-              (API: 3.3 per 1,000 population), followed by 1981 (API: 3.9 per
ding to the distribution and measures of relative frequency          1,000 population). The coefficient of determination (R2) was
as general malariometric indices such as API (annual parasi-         0.24 (Figure 1).
464                                                                                           https://doi.org/10.17843/rpmesp.2022.394.11359
Rev Peru Med Exp Salud Publica. 2022;39(4):463-68.                                                                          Acuña-Cantillo L et al.
     Sixty-two percent (96,072/155,096) of the registered ma-              is endemic-epidemic, focalized and with low-intensity, with P.
laria cases in the region were P. vivax, except in the depart-             vivax being the most frequent species. Indigenous people are the
ments of Cesar and Magdalena where P. falciparum infections                most affected group, mainly those between 10 and 49 years of
predominated with 55.3% (9,574/17,328 cases) and 52.6%                     age. In addition, there is a permanent flow of immigrants from
(8,086/15,362 cases), respectively (Table 2). Cases were found             different countries and continents that increase vulnerability (14).
in all age groups, and the most vulnerable people were those               In Venezuela, a re-emergence ofmalaria transmission has been
under 29 years of age. These contributed 76% (17,802/23,517                reported in recent years, nonetheless, in the coastal states of
cases) of the cumulative burden of cases registered in the 2010-           Sucre and Zulia the intensity of transmission is low, with a pre-
2019 decade. Of the latter, the 15-29 age group was the most               valence of P. vivax in more than 90% of the cases, affecting the
affected with 39% (9,148/23,517) of the cases (Figure 2).                  economically active population (15).
                                                                                In Colombia, the eco-epidemiological regions of the Pa-
DISCUSSION                                                                 cific, Urabá-Bajo Cauca Sinú San Jorge and Amazonia are the
                                                                           ones that contributed most to the malaria burden in the coun-
This study showed that malaria in the Caribbean region is of               try between 2010-2019 (6). In the Caribbean region, active and
low transmission intensity, with a variable endemic-epidemic               focal transmission has only been described in municipalities
pattern, with a significant downward trend and a predominan-               in southern Bolivar and La Guajira, where occasional epide-
ce of P. vivax cases.                                                      mic outbreaks are reported. In Bolívar, transmission is explai-
    The territory presents suitable conditions of receptivity and          ned by the migration of susceptible populations and parasite
vulnerability for transmission, such as changes caused by de-              carriers from other endemic areas in Colombia, due to social
forestation, increased number illicit crops and illegal mining,            and political conflicts as well as economic interests, such as
which favor the reproduction of Anopheles vectors (11). The                illegal gold mining (11). The latter has been a fundamental
described situation is similar to that observed in transmission            factor in the transmission of malaria in that area, where the
scenarios in neighboring endemic countries in the Caribbean                vectors An. darlingi, An. nuneztovari, and An. neomaculi-
basin.                                                                     palpus (16) have been reported.
    In Nicaragua, a variable endemic-epidemic pattern was des-                  The department of La Guajira, the northernmost depart-
cribed during the 2000-2019 period, with an initial downward               ment of Colombia, is characterized by its environmental, social
trend between 2000-2007, maintaining low transmission levels               and cultural complexity, which have influenced the dynamics of
until 2014, and then again showing an upward trend until 2019              vector-borne diseases. The behavior of the malaria is of low in-
with predominance of P. vivax infections (12). In Costa Rica, there        tensity, with sporadic epidemic outbreaks, such as the one that
was a significant downward trend in morbidity, low transmis-               occurred between December 1999 and February 2000. During
sion and predominance of P. vivax. In recent years, there has              those months, there was an unusual increase in the number of
been a moderate increase in the number of cases, with nearly               cases, most of which were caused by P. falciparum and affected
50% of cases being imported (13). In Panama, malaria cases are             the rural indigenous population. The main recognized breeding
mostly reported in the Darien region, where the transmission               sites were bodies of water, ponds, “jaguayes” and swamps for-
Table 1. Total malaria cases by decade in the Colombian Caribbean eco-epidemiological region, 1960-2019.
                                                                      Decades                                                   Distribution %
 Departments                                                                                                        Total
                                                                                                                                by department
                                 1960-1969       1970-1979   1980-1989    1990-1999     2000-2009    2010-2019
 Atlantico                           457           1644        1012         10 200         419             169      13,901             9,0
 Bolívar                            6977           8571       12 215        15 352        4016         20 199       67,330            43,4
 Cesar                              2045           3049        1958             784       9251             241      17,328            11,2
 La Guajira                          819           3334        4544             3263      8539             1 831    22,330            14,4
 Magdalena                          7726           2747        1908             819       1936             226      15,362             9,9
 Archipiélago de San Andrés,          0             0            0               1          0               17        18              0,01
 Providencia y Santa Catalina
 Sucre                              2030           5302        7649             1396      1616             834      18,827            12,1
 Total                             20 054         24 647      29 286        31 815        25 777       23 517      155,096             100
 Distribución % por década           12,9          15,9        18,9             20,5       16,6            15,2      100                -
https://doi.org/10.17843/rpmesp.2022.394.11359                                                                                                465
    Rev Peru Med Exp Salud Publica. 2022;39(4):463-68.                                                                   Malaria in the Colombian Caribbean, 1960-2019
                            5
                                                                                                                            Annual Parasitic Index (API)
                           4.5
                                                                                                                            Annual P. vivax index (AVI)
                            4                                          Year 1981 API: 3.9
                                                                                                                            Annual P. falciparum index (AFI)
                           3.5
                                         Year 1970 API: 3.3
API per 1,000 population
                           2.5
                           1.5                                                                                                               y= -0.028x +1.6223
                                                                                                                                                  R2= 0.24
                            1
                           0.5
                               98
                               84
                               86
                               88
                               90
                               92
                               94
                               00
                               16
                               04
                               12
                               14
                              60
                              62
                              64
                              66
                              68
                              70
                              72
                              74
                              76
                              78
                              80
                              82
                              02
                              06
                              96
                              10
                              08
                              18
                            19
                            19
                            19
                            19
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                            20
                            20
                            20
                            20
                            20
                           19
                           19
                           19
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                           19
                           19
                           19
                           19
                           19
                           20
                           20
                           19
                           20
                           20
                           20
                                                                                       Years
    Figure 1. Malaria behavior in the eco-epidemiological region of the Colombian Caribbean, 1960-2019.
    med after the rainy season, where the immature forms of the                                ments in the region have adequate receptivity conditions
    An.albimanus and An. triannulatus vectors breed (17).                                      and competent Anopheles vector species are reported, there
        On the other hand, the predominance of P. falciparum                                   is no active transmission of the disease (20).
    in the departments of Cesar and Magdalena may have been                                         The main limitation of this study is the low perception of
    related to the migration of people attracted by the cotton                                 the magnitude and importance of this problem in the region
    and banana agro-industrial growth between the 1940s and                                    by those responsible of the situation, which could affect the
    1960s (18), these people came from neighboring regions such                                availability and reliability of the information. In addition, it is
    as Urabá - Bajo Cauca Sinú San Jorge and the Pacific, contri-                              likely that the low knowledge of health professionals in the re-
    buting to the predominance of malaria due to P. falciparum.                                gion has an impact on the diagnosis and notification of cases,
    Recently, the proliferation and exploitation of illicit crops                              which could lead to underreporting. On the other hand, it was
    adjacent to the Sierra Nevada de Santa Marta sector and the                                difficult to analyze the age variable because it was not uniformly
    worsening of the armed conflict have caused population dis-                                registered in the different information systems we used. It was
    placements that explain the intensification of transmission (19).                          only possible to obtain this variable from the national reports of
    Another relevant fact is that although the rest of the depart-                             the event in the last decade.
    Table 2. Distribution of cumulative malaria cases by parasite species in the departments of the Colombian Caribbean eco-epidemiological region,
    1960-2019.
                                                                                    P. falciparum                            P. vivax                     Total
             Department
                                                                           No. of cases               %           No. of cases           %             No. of cases
             Atlantico                                                        1366                   9.8             12,535             90.2              13,901
             Bolívar                                                          23,520                 34.9            43,810             65.1              67,330
             Cesar                                                            9574                   55.3             7754              44.7              17,328
             La Guajira                                                       9503                   42.6            12,827             57.4              22,330
             Magdalena                                                        8086                   52.6             7276              47.4              15,362
             Archipelago of San Andrés, Providencia y Santa Catalina            7                    38.9              11               61.1                18
             Sucre                                                            6968                   37.0            11,859             63.0              18,827
             Total                                                            59,024                 38.0            96,072             62.0             155,096
466                                                                                                                   https://doi.org/10.17843/rpmesp.2022.394.11359
Rev Peru Med Exp Salud Publica. 2022;39(4):463-68.                                                                                             Acuña-Cantillo L et al.
         4000                                     76%*
                                  37%**                            39%***
         3500
         3000
         2500
         2000
Cases
         1500
         1000
          500
            0
                   <1      1a4       5a9      10 a 14 15 a 19 20 a 24 25 - 29 30 - 34 25 - 29                40 - 44 45 - 49 50 - 54 55 - 59          60 - 64       > 65
                                                                            Age groups
* Cumulative burden of malaria <29 years (17,802 cases). ** Cumulative burden of malaria <14 years (8,654 cases). *** Cumulative burden of malaria 14 to 29 years
(9,148 cases). Cumulative cases in the 2010-2019 period: 23,517.
Figure 2. Distribution and percentage of malaria cases by age group, 2010-2019.
     This study provided a baseline on the epidemiology of mala-                       dation of epidemiological intelligence and decision making;
ria in the Caribbean region.                                                           and to lead social and sectoral empowerment. Finally, basic
     In conclusion, malaria in the Caribbean region has had                            and applied research lines should be established on clinical,
an endemic-epidemic behavior, with very low transmission                               epidemiological, entomological, environmental, social, pre-
intensity and with the presence of delimited foci of active                            vention and control measures, among others.
transmission that contribute the greatest cumulative burden
of cases in the region.                                                                Acknowledgments: the authors would like to thank the Secretaries of
     We recommend developing micro-stratification studies                              Health of the departments of the Caribbean region and the
in municipalities with active transmission, considering the                            Ministry of Health and Social Protection for facilitating access to the
feasibility and viability of malaria elimination in order to                           information.
implement plans, programs and projects in the region. This
                                                                                       Author contributions: LAC and JCPR participated in the conception
will strengthen local capacity regarding the technical-opera-                          and design of the study, data collection and organization. LAC, MJO
tional response for the implementation of regular preventive                           and JCPR participated in the statistical analyses, drafting, revision and
and timely control programs. It will also strengthen conti-                            approval of the final version of the manuscript.
nuing medical education programs to improve knowledge
                                                                                       Conflicts of interest: the authors declare that they have no conflicts
and practice in order to ensure timely care of cases requiring
                                                                                       of interest.
diagnostic and treatment services. The development of com-
prehensive information systems is required for the consoli-                            Funding: the research was self-funded.
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