Malaria in Haiti: A Descriptive and Temporal Study from 2009 to 2018.

Haiti is one of the Caribbean countries where malaria still persists. Malaria occurs throughout the country at altitudes below 600 meters. More than 99% of the malaria cases are caused by Plasmodium falciparum and the main vector is Anopheles albimanus. This paper aims to describe the epidemiological prole of malaria in Haiti between 2009 and 2018.

region to another between 400 mm and 3,000 mm. There are two primary rainy seasons that occur from April to June and from September to November. Haiti is prone to hurricanes and seasonal tropical storms [25].
Literature review. To carry out this descriptive research, articles in the national and international literature were indexed in MEDLINE, PUBMED, Scielo, Roll Back Malaria (RBM) and World Health Organization (WHO) reports from 2009 to 2019, adapting the method of "integrative literature review" [26]. The results and conclusions of previous studies with epidemiological data on malaria in Haiti were summarized to assess the state of the art within the proposed subject. This method is mainly used in medical and nursing practice [27].
Data compilation. This work was also carried out based on reported cases of malaria in the ten departments of Haiti. Data were obtained from MSPP statistical reports published on the website https://mspp.gouv.ht which can be accessed freely. The reports provide information on the malaria positive lamina index and positivity rate for malaria by 10000 inhabitants per year and Department. Therefore, the numbers of malaria cases reported in Haiti from 2009 to 2018 were evaluated and analyzed from those data.
Statistical analysis. Descriptive analyzes of the variables used were performed. A database was built in Excel with the data obtained from the Ministry of Health of Haiti. Occurrence measures or morbidity indicators (the annual parasite index, incidence rate, prevalence and prevalence rate) and the proportion of malaria cases con rmed by department and per year were used.
As previously mentioned, in some MSPP statistical reports only the suspected cases and the proportions of the corresponding con rmed cases are shown. As the number of cases is a discrete quantitative variable, for its calculation, the following formula was applied: Results with decimal values are rounded up to the rst decimal place, upwards: ≥ 5 and downwards: ≤ 4.
As the WHO data only shows the global malaria cases, and not by Haitian Departments, the calculation of the annual parasite index (API) was done only with the MSPP data. The API of each department for each year studied was integrated into Geographic Information Systems (GIS), allowing analyzes to have a spatial vision of malaria risk in Haiti by department and by year. For these analyzes, we used ArcGIS 10 software (Environmental Systems research Institute, Redlands, CA) and IBM (Chicago, IL) SPSS Statistics 22 software.

Results
Between 2009 and 2018, a total of 232,479 and 303,295 con rmed malaria cases were respectively reported by the MSPP and the WHOfor Haiti. Between 2010 and 2018, Haiti strongly reduced the number of malaria cases: from 84,153 to 8,828 considering the WHO data, and from 36,106 to 9,128, according to MSPP ( Fig. 2 Table 2 shows from the MSPP data, the exposed population, the number of con rmed cases and the API per year and department in Haiti from 2009 to 2018. The API of each department varies depending on the corresponding population and the case number for each year. Figure 3 shows the API per year (2009)(2010)(2011)(2012)(2013)(2014)(2015)(2016)(2017)(2018) in each department of Haiti. The proportions of malaria cases are displayed in Fig. 4, where we can observe from 2016 to 2018 a concentration of malaria transmission mainly in three (3) of the ten (10) departments: Grand'Anse, Sud, and Ouest. These three departments reported together over 80% of all malaria cases in Haiti. Grand'Anse Department, whose proportion of malaria cases did not exceed 7% per year during the period 2009-2013, experienced an elevated level of malaria transmission in 2014. The number of malaria cases tripled in 2014, as compared to those in 2013. In that department, a signi cant increase was also observed after the hurricane Matthew in 2016 with approximately a half (49%) of malaria cases reported in Haiti that year. Therefore, Grand'Anse registered the highest proportion of malaria cases in 2016 for the period 2009-2018. Grand'Anse was the only department where there was an increase in malaria cases between 2009 and 2018 (158%). And, considering the period 2009-2017, the increase was even more pronounced (450%).
Besides being one of the three departments of Haiti where malaria was more concentrated during the ten-year period studied, the Sud Department has registered remarkable proportions of malaria cases between 2009 and 2013, and has been explicitly ranked the rst place during this period and the second place in 2012 (Fig. 4). The number of malaria cases declined signi cantly from over 20% to less than 8% in 2014 and 2015. Despite malaria cases decrease between 2014 and 2015, Sud Department returned to occupy the third place with more than 15% of the malaria cases in 2016 and the second place in 2017 and 2018 with 30% of all malaria cases registered in Haiti for the respective years.
Data on malaria morbidity among pregnant women and children under-ve (U5) in Haiti is available only from 2015 to 2018 from MSPP (Table 3) (Fig. 2). Curiously, the number of malaria cases estimated by the WHO in the 2009-2018 period is higher than that reported by the MSPP (Table 2). Nevertheless, both the MSPP and WHO data showed a decrease in malaria incidence from 2011 as compared to 2010, while the MSPP data showed a small increase in 2012 contrasting with the decline recorded by the WHO. Additionally, the number of malaria cases reported by the MSPP decreased in 2013, while they increased according to WHO.
A considerable difference between malaria cases reported in 2009 and 2010 by the MSPP and the WHO was detected (Fig. 2). The data of both institutions overlap between 2011 and 2018 (post-earthquake period), with the exception of 2013, when values deviate slightly. Therefore, the con icting values for the rst two years of the series may be due to the different Haitian sources of primary data. Even before the 2010 earthquake, Haiti faced socioeconomic problems [28], which inevitably affected the country's health system. In 2010, in response to the earthquake, the MSPP in collaboration with the CDC and various NGOs, established a surveillance system for infectious diseases including malaria [29]. The incongruity of MSPP data with those from WHO between 2009 and 2010 may be related to de ciencies in the epidemiological surveillance system prior to the support of CDC and NGOs. This may interfere with data collection and updating of the o cial MSPP database. Boncy and collaborators [16] pointed out some di culties in the delivery of monthly reports of laboratory results to the central level of the MSPP and the lack of communication from the central to the local structures in Haiti.
Improving malaria data collection in Haiti. It should be noted that malaria data after the 2010 earthquake in Haiti is more robust. The reduction in con icting data from 2011 is probably due to the MSPP's actions in collaboration with their partners in the days and months following the earthquake. Although apparently con icting, data from WHO and MSPP showed the same trend of malaria in Haiti during the ten years studied. In other words, malaria declined during the 2009-2018 period with little variation since 2011 (Fig. 2).
Malaria in the different departments/ regions of Haiti. Challenges and suggestions. Our analysis suggests that Grand'Anse Department has always been one of the highest malaria-burden areas of Haiti, and malaria cases were probably underreported in the years prior to 2014. Te underreporting of malaria cases in Grand'Anse may be related to the di culty of access by land route to malaria foci in the municipalities of the department who presents rugged terrain [30]. Consequently, Grand'Anse and its spread and remote municipalities remain isolated. This problem results in particularly di cult and expensive access to health care, particularly in locations of high malaria burden [31], where people must walk hours to access medical care [32]. Lack of access to health facilities can be a discouraging factor, and may lead residents to use self-medication as the rst alternative. It is worth noting that in Haiti, a country where the sale of drugs is not regulated, anyone can buy any drug from informal street drug vendors or in informal pharmacies without a doctor's prescription. In any case, apparently the surveillance and case records of malaria in this department in the analyzed period were more effective and realistic than in the others, for several reasons such as a major scale-up community case management such as diagnostic testing deploying RDTs and reporting thanks to the nancial support provided by a global fund in 2012 to ght against AIDS, tuberculosis and malaria in Haiti [32,33]. No work has been published exploring on why Sud Department is a malaria-prone endemic area. However, some ecological determinants may hypothetically explain the fact that Sud presents high malaria endemicity, as observed in the years prior to the passage of Hurricane Matthew in October 2016, that is, since the beginning of the series in 2009. According to MSPP [34], Sud is considered to be one of the departments where the highest number of malaria cases has always been registered. The southern department is mainly made up of plains located along the coast. The hydrographic network of the Sud is dense because it is made up of 69 rivers, 250 springs, 20 ponds, one lake and 11lagoons [34], what favors the formation of larval habitats of anophelines. This large plain faces the green Massif de la Hotte which favors the precipitation and in ltration of rainwater.
CHAI and collaborators [1] have described the high risk of malaria transmission along the coast of Haiti. Malaria is mostly distributed along the coasts of the southern region of the country where are located both the Sud and Grand'Anse departments [35]. This coastal distribution of malaria is mainly related to the main anopheline vector bioecology, besides low local socioeconomic conditions. An. Albimanus has been described as essentially a coastal mosquito and often found in brackish water [36]. This species of anopheline is also considered a lowland mosquito [37] that breeds in a wide variety of sunny breeding sites at altitudes below 400 m [38]. Therefore, in the, there are very favorable ecological conditions for malaria transmission. Port-au-Prince, the capital of Haiti is located in Ouest. The department has also recorded high malaria incidence in Haiti, with its municipalities accounting for 53% of malaria cases reported between 2012 and 2014 [41]. This data though, seems to be misleading. Patients travel long distances to receive better health care and malaria cases' reports are based on the health unit location where the diagnosis occurred not where the patient lives [42].
To estimates malaria risk at the department level in this study we have used API. The results showed that malaria occurs in all departments of Haiti with a degree of risk ranging from low (0.02 to 7.71) to medium (10.68 to 23.38) ( Table 2). It is known that API is in uenced by the size of the population, which grows each year, regardless whether the number of cases increases [43]. Therefore, a given area may have a very low API even with high number of cases, and Hence, the increase and decrease of the API value depends on the denominator that is the population size at a given time; that is; the larger the population, the lower the API will be, and vice versa.
Malaria control efforts in Haiti. Despite the objective set by Haiti and DR to eliminate malaria on the island of Hispaniola until 2020 was not achieved, an overall trending decline in the number of malaria cases in Haiti in the last years was recorded. Due to Haiti's efforts to reduce the malaria burden over the past decade prior 2019, the number of malaria cases considerably dropped in the country from 2010 to 2018. Access to early diagnosis and treatment is one of the most important strategies for malaria control and elimination. This includes two components: 1) the patient must seek care, as soon as possible when sick; 2) health facilities with diagnosis and adequate treatment within easy access to the patient must be available [44]. Consequently, progress has been seen in improving access to malaria diagnosis and treatment in Haiti over the last years.
The use of bednets for malaria control in Haiti. The use of insecticide-treated nets (ITNs) is currently the most effective means of individual protection against malaria. ITNs have been implemented since 2010 in almost all the endemic areas of Haiti [45]. In the same context, approximately 800 thousand ITNs were distributed by The Menthor Initiative in collaboration with UNICEF from October to December 2010 [46,35]. More than 350 thousand families in four departments of the country have bene ted. In the same period, thousands of other mosquito nets were distributed by the Haitian Red Cross [47]. Subsequently, 2 million long-lasting insecticidal nets (LLINs) were distributed in Haiti by PSI in 2012. This resulted in that for the rst time in the Americas it was reported that a higher number of people were protected by ITNs than by indoor residual spraying (IRS), the most common method used for malaria vector control [31].
Additionally, the Global Fund to ght AIDS, Tuberculosis and Malaria subsidized more than 400,000 mosquito nets in Haiti in December 2016 [48]. ITNs ensure individual protection by helping to limit contact between the individual and vector, as it is one of the best strategies against malaria. According to the WHO, a coverage rate with impregnated mosquito nets above 80% reduces infant and juvenile mortality by about 25% and guarantees effective protection of more than 60% against parasitemia [49]. Therefore, considering the reduction in the number of cases between 2011 and 2018, it can be said that, probably, there was an effect of the mosquito nets distribution campaigns in the reduction of malaria cases that we analyzed in the country.
The outstanding departments for malaria reduction in Haiti. While only three departments reported over 80% of all malaria cases in Haiti from 2016 to 2018, ve departments (Nord, Nord-Est, Nord-Ouest, Sud-Est and Centre) showed together less than 7% of malaria cases, the smallest proportion of cases, during the period 2009-2018. In terms of reducing malaria cases over the period 2009-2018, the most outstanding departments for malaria reduction of Haiti were: Nord, Nord-Est, and Sud-Est.
Nord-Est is one of the departments of Haiti where malaria was a major concern in the years prior to 2014. Due to the binational project between Haiti and Dominican Republic, covering the border communities of Ouanaminthe (a municipality of Nord-Est Department) and Dajabon (a municipality in the Dominican Republic) [17], malaria cases in Nord-Est dropped from 3,888 in 2010 to 87 cases in 2016, a reduction of 97.76% (Table 2). The department is also characterized by its rainfall de cits which are recorded for decades (600 mm at most) and by high risks of drought [52]. Probably the highest proportion of the population of the department lives in the mountains. As the transmission of malaria in the southern region of Haiti occurs mainly at the coastal areas [4,35], the low incidence of malaria, historically recorded in the Sud-Est Department, is probably due to the fact that the proportion of the population of the department exposed to the risk of contracting malaria is low.
Malaria in Pregnant and Children under 5 years old. According to WHO [53], malaria is considered one of the greatest health threats to children under ve and pregnant women in malaria-burden areas. In high transmission areas, the majority of malarial disease occurs in young children without acquired immunity.
The most commons of the severe clinical pictures of malaria seen in children are: severe anaemia, hypoglycemia and cerebral malaria. One of the WHO recommendations for the prevention of malaria in children is the use of long-lasting insecticidal nets (LLINs). As shown in Table 3 Malaria infection during pregnancy represents substantial risks for the pregnant woman, her fetus, and the newborn child having as consequences maternal illness and low birth weight [54]. According to WHO [55], the levels of acquired immunity may increase in areas of high burden of P. falciparum malaria. In those areas, malaria is usually asymptomatic in pregnant women with the presence of parasites in the placenta. This might contribute to maternal anaemia without peripheral parasitemia. Therefore, low con rmed malaria case among pregnant women in Haiti does not mean absence of Plasmodium spp. infection among them. In other words, the low number of cases registered among pregnant women during the study period may not show the malaria trend in pregnant women in Haiti. Because of the lack of health facility and education, pregnant women, especially in rural zones, do not have the habit of doing prenatal care before the third trimester of pregnancy, unless they feel really seek (personal communication).
On the other hand, in areas of low density of malaria transmission, women of reproductive age have relatively little acquired immunity to malaria. To avoid the risk of severe malaria that can lead to miscarriage, stillbirth, and prematurity and low birth weight, all pregnant women, regardless of their gestational age, are very vulnerable to malaria [54]. As solution, the WHO recommends an intermittent preventive treatment in pregnancy (IPTp), in all areas with moderate to high malaria transmission, especially in Africa. This therapy consists of administering to pregnant women at least two doses of an antimalarial drug, currently sulphadoxine-pyrimethamine (SP), at each scheduled antenatal visit after the rst trimester of pregnancy, whether or not they have symptoms malaria [54]. At the date of writing of this paper, the Ministry of Health of Haiti has no IPTp in its malaria treatment protocol and, no scienti c and o cial data on malaria case management among pregnant women were published by the MSPP.  (Table 3). At community level, and for each municipality in Haiti, MUF risk factors linked to socio-economic and environmental factors such as type of dwelling, access to health care, parental education level, household size and bed nets use should be investigated. These factors signi cantly in uence the odds for MUF [56].

Conclusions
The results from this study indicate that in Haiti, the o cial malaria data from 2009 to 2018 were reported by department instead of by municipality. According to data from 2015 to 2018, malaria also affects both U5 children and pregnant women. In view of those facts, malaria risk should be assessed at municipal level in order to target appropriate speci c local interventions. As well, prevention efforts should be focused on U5 and IPTp should be included in the malaria treatment for pregnant women in Haiti. This set of actions may help Haiti achieve the goal of eliminating malaria and prevent the reintroduction of the disease in areas where it will be eliminated.

Declarations
Authors' contributions JRJ, TFNS and JA conceived and designed the study; JRJ and EJB collected the data; TFSN, HA, MGRF and MCSM contributed to the analyses of the data; JRJ drafted the manuscript, MGRF, MCSM, CR, JA and TFNS helped with manuscript editing. All authors read and approved the nal manuscript.
Map of Haiti with the ten Departments. Note: The designations employed and the presentation of the material on this map do not imply the expression of any opinion whatsoever on the part of Research Square concerning the legal status of any country, territory, city or area or of its authorities, or concerning the delimitation of its frontiers or boundaries. This map has been provided by the authors. territory, city or area or of its authorities, or concerning the delimitation of its frontiers or boundaries. This map has been provided by the authors. Square concerning the legal status of any country, territory, city or area or of its authorities, or concerning the delimitation of its frontiers or boundaries. This map has been provided by the authors.