A Retrospective Analysis of the Malaria Trend in Yemen Over the Sixteen-Years, from 2006 to 2021

Wadhah Hassan Edrees 1,2✉ Emailedress2020@gmail.com

Wadee Abdullah Al-Shehari 3,4 Emailwadee40@yahoo.com

1 Medical Microbiology Department, Faculty of Applied Sciences Hajjah University Hajjah Yemen

2 Medical Laboratory Department, Faculty of Medical Sciences Al-Razi University Sana’a Yemen

3 Medical Microbiology Department, Faculty of Medical Sciences Ibb University Ibb Ibb, Dr Yemen

4 Medical Laboratory Department, Faculty of Medical Sciences International Malaysia University Ibb Yemen

Wadhah Hassan Edrees ^1,2 *, Wadee Abdullah Al-Shehari ^3,4

¹Medical Microbiology Department, Faculty of Applied Sciences, Hajjah University, Hajjah, Yemen; edress2020@gmail.com

²Medical Laboratory Department, Faculty of Medical Sciences, Al-Razi University, Sana’a, Yemen.

³Medical Microbiology Department, Faculty of Medical Sciences, Ibb University, Ibb, Ibb, Yemen, Dr.wadee40@yahoo.com

⁴Medical Laboratory Department, Faculty of Medical Sciences International Malaysia University, Ibb, Yemen

*Corresponding Author’s Email: edress2020@gmail.com

Abstract

Background

Malaria is one of the important diseases that threatens the global health system, especially in developing countries, including Yemen. Based on surveillance data, this analysis aimed to assess the trend of malaria in Yemen over the last sixteen years from 2006 to 2021.

Methods

A retrospective analysis was conducted on secondary malaria data from the database from the Ministry of Public Health and Population in Yemen.

Results

Of the 15,153,763 suspected cases, approximately 3,651,508 malaria cases were confirmed by both laboratory and clinical diagnoses. Plasmodium falciparum, P. vivax, mixed infections, P. malariae, and P. ovale were recorded at 1,118,117 (98.72%), 123,28 (1.10%), 1838 (0.16%), 155 (0.01%), and 30 (0.01%), respectively. Approximately 77.2% of all malaria cases were recorded in six governorates. Al Hudaydah recorded the highest number of malaria cases (1,231,294), followed by Hajjah (623,937), Taiz (450,051), Dhamar (167,399), Sa'adah (157,881), and Al-Mahweet (154,763). The overall incidence rate of malaria cases and P. falciparum, respectively, was 8.9 and 2.66 per 1,000 people. The highest mean incidence rate of malaria was recorded in Al Hudaydah, Hajjah, Al-Mahweet, Sa'adah, and Abyan, respectively, at 29.71, 19.49, 14.98, 10.62, and 10.14 per 1,000 people. Yemen reported 704 (0.02%) malaria death cases with an overall rate of case fatality of 0.03% and a mortality rate of 0.18 per 100,000 populations. The trend of case fatality decreased from 0.029% in 2006 to 0.015% in 2020, while the mortality rate per 100,000 individuals decreased from 0.3 in 2006 to 0.08 in 2021.

Conclusion

It currently suggests a continuous increase in the malaria burden without specifying trends or fluctuations and is becoming a public health threat and causing widespread concern. Therefore, the treatment and prevention of malaria infection are crucial for reducing mortality and complications by increasing the use of vector control tools and promoting early diagnosis and treatment.

Keywords:

Case Fatality

Incidence Rate

Malaria Cases

Mortality Rate

Plasmodium falciparum

Trend

Yemen

Introduction

Malaria remains a major public health problem and poses a significant risk of morbidity, mortality, and economic loss worldwide, particularly in tropical and subtropical region of the world. It is a preventable and treatable disease caused by protozoan parasites belonging to the genus Plasmodium. These types of parasites are most commonly transmitted to people through the bite of an infected female Anopheles mosquito. On rare exceptions, it can be transmitted through blood transfusions, organ transplants, contaminated needles, or congenitally [1–2]. Moreover, there are five types of Plasmodium species, including Plasmodium falciparum, P. vivax, P. malariae, P. ovale, and P. knowlesi that are responsible for causing malaria disease in people worldwide. P. falciparum contribute more than 90% of the global malaria burden [3].

Globally, an approximately 2.1 billion cases of malaria and 11.7 million deaths due to malaria were reported between 2000 and 2022 [4]. Moreover, the number of malaria cases worldwide has increased from 244 million in 2021 with 610 thousand death cases to 249 million in 2022 with 608 thousand death cases [1]. Of the 249 million cases, 233 (93.6%) were recorded in the WHO African Region [1, 5]. The Eastern Mediterranean Region revealed a 38% decrease in malaria cases from 7 million in 2000, with 13,500 deaths, to 4 million cases in 2015, with 7,500 deaths, followed by a 92% increase to 8.3 million in 2022, resulting in 15,900 death cases [4].

Furthermore, the incidence rate of malaria was decreased from 81 per 1000 people in 2000 to 57 per 1000 people in 2019 and then slightly raised to be 58 per 1000 population in 2022 [4]. Globally, the annual estimation of P. falciparum burden was reported at 193.5 million cases, while P. vivax was at 14.3 million cases [6–7]. According to WHO estimation, P. falciparum is the most globally prevalent malaria parasite in the sub Saharan Africa (SSA) (99.7%), South-East Asia Region (50%), Eastern Mediterranean Region (71%), and Western Pacific Region (65%), while the burden of P. vivax is more prevalent in the South-East Asia Region (53%), and Region of the Americas (75%) [8].

Yemen ranks sixth among nations that are endemic to malaria worldwide and is accountable for 11.6% of the total people who are at high risk of malaria in the Eastern Mediterranean Region [4, 9]. Moreover, 60–70% population of Yemen resides in malarious region, with approximately 25% living in high risk areas [10–11]. Additionally, it is reported that a greater than 21 million of Yemenis people lives at malaria-risk areas, which results in more than 1 million malaria cases each year [12].

Earlier epidemiological investigations conducted in different regions of Yemen found that the overall prevalence of malaria was 32.4% in Hodeidah between 2018 and 2019 [13], 18.1% in the Abs district of Hajjah governorate in 2016 [14], and 18.8% in Hadhramout between July 2011 and May 2012 [15]. In addition, the overall prevalence of malaria was recorded at 15.3% in Yemen in 2010 [16]. P. falciparum is the most prevalent malaria species in Yemen and is responsible for over 99% of all cases, while P. vivax and P. malariae had a low rate [11].

Yemen is considered one of the poorest countries in the world and faces many political and financial challenges. In addition, the continuation of the war since 2015 until now has led to the destruction of infrastructure and has greatly contributed to increasing rates of poverty and famine among the majority of the population. Furthermore, there are other factors that may have contributed significantly to the transmission of epidemic diseases in Yemen, such as climate change and the occurrence of floods, as well as the suspension of programs to control disease vectors and improving the environmental level [17–20].

Previous investigations carried out in Yemen have been neither adequate or comprehensive to shed light on the epidemiology of malaria in all governorates and for long periods. Given the limited comprehensive analysis of malaria trends across all Yemeni governorates, this retrospective study aims to characterize the epidemiological patterns of malaria in Yemen between 2006 and 2021, focusing on incidence, mortality, and the prevalence of different Plasmodium species.

Methods

Study area and period

A retrospective analysis based on reported secondary malaria case data recorded between 2006 and 2021 in the surveillance center at the Ministry of Public Health and Population (MoPHP) in Yemen. Additionally, it consists of 21 administrative governorates and all these were included in this analysis (Fig. 1). Moreover, Yemen can be divided into four regions: The coastal regions, known Tihama region, extend from the Saudi border in the west to the Oman border in the far east and exhibit high temperatures and humidity, with an annual rainfall rate ranging from 50 to 100 mm. Mountainous highlands extend from the far north of Yemen to its far south and have a moderate summer climate, a cold winter, and low humidity, with a rainfall rate ranging from 400 to 1100 mm. Plateau regions, which cover the eastern part of Yemen, are typically hot and dry, with average rainfall of 100 mm. The desert region extending north of Yemen and has high temperatures, rare rainfall, and low humidity.

The differences in temperature, humidity, and rainfall seasons as a result of climate changes in these areas are considered major factors in providing suitable conditions for the multiplication and reproduction of the malaria vector. Furthermore, valleys coming from the mountain highlands flow into the Tihama region, which is considered very fertile and suitable for agriculture. According to previous reports, more than 60% of the malaria burden in Yemen is transmitted in the Tihama region [4, 11].

Fig. 1

Map of the Republic of Yemen

Cases definition

The malaria cases were classified based on the WHO guidelines [21] into the following categories:

Suspected malaria case: Illness suspected by a health worker to be due to malaria generally on the basis of the presence of fever, with or without other symptoms. This should not be confused with presumed cases.

Rapid tested: Number of suspected malaria cases who received a rapid test.

Microscopy tested: Number of suspected malaria cases who received a microscopy test.

Confirmed malaria cases: Malaria cases in which the parasite has been detected in a diagnostic test (microscopy or RDT diagnostic test).

Presumed malaria cases: Cases suspected of being malaria that are not confirmed by a diagnostic test.

Total malaria cases (confirmed + presumed): Total of laboratory confirmed + total of presumed cases.

Data collection and analysis

Sixteen years of secondary malaria data were obtained from an epidemiological surveillance center at the MoPHP, Yemen for the period 2006–2021. Moreover, malaria data were collected from health facilities in all governorates by the epidemiological surveillance team of the Ministry of Health according to the WHO Guideline [21]. Office administrators and healthcare workers received a clear explanation of the concepts and purposes of this analysis. In Yemen, microscopy is commonly used in hospitals, health centers, and laboratories to detect Plasmodium parasites in blood samples using Giemsa staining to stain peripheral blood smears. In addition, some malaria cases were diagnosed based on clinical signs and symptoms, and laboratory diagnosis using a rapid test. Furthermore, data were extracted from the surveillance center database and managed in Microsoft Excel.

Furthermore, missing data were processed systematically using the SPSS software. The extent and patterns of missing values in the database were determined. The mean or median imputation was used for variables with insignificant missingness. While variables with significant missing values, multiple imputation techniques were used to estimate missing data entries based on observed data relationships. In contrast, cases with excessive missing values that could not be reliably accounted for were excluded through listwise deletion. Additionally, consistency checks were performed after handling missing data to ensure the dataset’s accuracy and reliability.

Furthermore, the database included the following variables: the year of infection, the names of the governorates, the total number of suspected cases examined for rapid or microscopic examinations, the number of positive cases for rapid testing, the number of positive cases for P. falciparum, P. vivax, P. ovale, P. malariae, and mixed infections, and the number of clinically diagnosed cases.

Retrospective data analysis was performed using the office system in Microsoft Excel 2016 and the statistical package for the social sciences (SPSS, version 26) program. Descriptive analysis was performed to determine the count and proportion of malaria cases (confirmed by laboratory tests and clinically) and Plasmodium species by governorate and year. In addition, the annual incidence of malaria cases and P. falciparum by governorate and year, case fatality rate (CFR), and mortality rate were estimated. The total population size [22] was used as the denominator to calculate the incidence rates of malaria and P. falciparum, separately, per 1000 people.

The overall incidence rate was calculated by dividing the total incidence rate for all years by the number of years. Additionally, the mean incidence rate for each governorate for every four years was calculated as the total incidence rate divided by the number of years. Furthermore, the case fatality rate (CFR) and malaria mortality rate per 100,000 populations of malaria cases were estimated.

The overall case fatality rate was calculated by dividing the total case fatality rate for all years by the number of years. Moreover, the general mortality rate per 100,000 people was calculated by dividing the total mortality rate for all years by the number of years. Additionally, geographical maps for the trend of malaria and P. falciparum in Yemeni governorates between 2006 and 2021 were generated using ArcGIS Pro 3.3 (Esri) software.

Furthermore, the data were summarized and presented as frequencies, percentages, and incidence rates according to the text, tables, and figures. Moreover, the Statistical Package for Social Sciences SPSS (Version 26, IMB^®, SPSS Inc., US) was used to evaluate the differences between subgroups of variables. Additionally, a probability (P) value was considered to be statistically significant at ≤ 0.05.

Results

Characteristics of enrolled malaria cases

Between 2006 and 2021, 15, 153, 763 cases of suspected malaria infection were enrolled in this retrospective analysis. Yemen reported 3,651,508 (24.1%) laboratory- and clinically-diagnosed malaria cases positive (P = 0.000). Of the 2,901,604 patients subjected to rapid testing for malaria diagnosis, only 626,573 (22.3%) tested positive with a statistical difference (P = 0.000). Furthermore, out of 12,252,159 cases diagnosed by microscopy, 1,118,117 (10.3%) were positive for malaria infection. Additionally, approximately 1,906,818 presumed cases were clinically diagnosed based on the signs and symptoms without laboratory confirmation (Fig. 2).

Fig. 2

Frequency of malaria cases in Yemen between 2006 and 2021

Frequency of Plasmodium species

The microscopic examination revealed that P. falciparum had the highest frequency in the current findings, accounting for 1,103,766 cases with a percentage of 98.72%, while the lowest was P. ovale with 30 cases (0.01%), as summarized in Table (1).

Table 1

Frequency of Plasmodium species in Yemen between 2006–2021
Plasmodium species	Frequency	Percent (%)
P. falciparum	1103766	98.72
P. vivax	12328	1.10
P. ovale	30	0.01
P. malariae	155	0.01
Mixed infection	1838	0.16
Total	1,118,117	100.0

Trends of malaria cases

Figure 3 shows that the largest number of malaria cases was reported in 2014 at 788,856 (21.6%), followed by 2019 at 369,431 (10.12%), 2020 at 325,054 (8.9%), and 2015 at 318,281 (8.38%), while the lowest was reported in 2009 at 135,620 (3.71%) with statistically significant differences (P = 0.041). Furthermore, the overall incidence rate of malaria cases was 8.9 per 1,000 people listed during the 16-year period. Additionally, the highest malaria incidence rate was recorded in 2014 with 30.39/1,000 people, followed by 2019 with 12.45 per 1,000 people, 2015 with 11.93 per 1,000 people, 2007 with 10.24 per 1,000 people, and 2006 with 10.24/1,000 people. While the lowest rate was observed in 2021 with 4.94 per 1,000 people, with significant differences (P = 0.024).

Fig. 3

Total, percent, and incidence rate of malaria cases by year of infection in Yemen between 2006–2021

Figure 4 reveals that the governorate of Al Hudaydah recorded a higher total number of malaria at 1,231,294 cases, followed by Hajjah at 623,937, Taiz at 450,051, Dhamar at 167,399, and Sa'adah at 157,881. Conversely, Soqatra governorate had the fewest instances of malaria, with only 12 cases with statistically significant differences (P = 0.000). Furthermore, the highest mean incidence of malaria was recorded in Al Hudaydah at 29.71/1,000, followed by Hajjah at 19.49/1,000, Al-Mahweet at 14.98/1,000, Sa'adah at 10.62/1,000, and Abyan at 10.14/1,000, while Soqatra recorded the lowest rate at 0.02 per 1,000, with statistically significant differences (P = 0.000).

Fig. 4

Overall incidence rate of malaria cases in Yemen from 2006 to 2021

The Spatial analysis showed that the overall number of malaria cases in the Lahj, Raimah, Sana'a, and Al Jawf governorates has remained consistent over the years. In contrast, a decrease was recently observed in Abyan, Marib, and Hadhramout governorates (Fig. 5-A). This analysis showed that the mean incidence rate per 1,000 people of malaria cases recently increased significantly in Al Hudaydah, Taiz, and Hajjah governorates. Furthermore, the mean incidence rate has remained stable at low levels over the years in Ibb, Al Dhale'e, Hadhramout, and Sana'a governorates. The mean incidence rate has been observed to decrease slightly in recent years in Al Maharah, Marib, and Al-Mahweet governorates (Fig. 5-B).



A Figure 5-A. Geographic distribution of overall malaria cases in each four years by governorates, from 2006 to 2021


Figure 5-B. Geographic distribution of mean incidence rate per 1,000 population of malaria cases in each four years by governorates, from 2006 to 2021.

Trends of Plasmodium falciparum cases

In this study, the highest number of P. falciparum was in 2019 with 202,474 cases (18.34%), followed by 2020 with 95,236 cases (8.63%), 2018 with 83,373 cases (7.55%), and the lowest number recorded in 2014 with 38,015 cases (3.44%). In addition, the overall incidence rate of P. falciparum cases was 2.66 per 1,000 people. Moreover, 2019 recorded the highest incidence of P. falciparum at 6.83 per 1,000 people, followed by 2010 at 3.34 per 1,000 people and 2020 at 3.13 per 1,000 people. A lower rate was recorded in 2014 at 1.46 per 1,000 individuals (Fig. 6). Additionally, the statistical analysis revealed that there are no significant differences between the total number of P. falciparum by the year of infection (P > 0.05).

Fig. 6

Total, percent, and incidence rate of P. falciparum by year of infection in Yemen between 2006–2021

Figure 7 shows that Al Hudaydah recorded a higher number of P. falciparum at 373,107 cases, followed by Hajjah at 222,496 cases, Taiz at 183425 cases, and Aden at 565,55 cases, while Soqatra governorate had the fewest cases of P. falciparum, with only 8 cases (P = 0.000). Incidence rates with P. falciparum were highest in Al-Hudaydah (7.97 per 1,000 people), then in Hajjah (6.71 per 1,000 people), then in Aden (4.5 per 1,000 people), then in Taiz (3.74 per 1,000 people), and finally in Abyan (3.64 per 1,000 people). Socotra had the lowest rate (0.002 per 1,000 people), and there were no statistically significant differences in the rates of Incidence between governorates (P = 0.063).

Fig. 7

Overall number and mean incidence rate of P. falciparum cases in Yemen from 2006 to 2021

The results indicated a significant increase in the overall cases of P. falciparum in the governorates of Al Hudaydah, Hajjah, and Taiz in recent years, compared to a slight increase in the governorates of Dhamar, Al-Mahweet, and Aden. On the other hand, the governorates of Al Maharah, Marib, and Al Dhale'e consistently maintained low levels of P. falciparum infection (Fig. 8-A). Furthermore, it was noted that the average incidence rate per 1000 people of P. falciparum increased during the current years in the governorates of Al Hudaydah, Taiz, and Hajjah. The incidence rate of P. falciparum decreased in the Al Maharah governorate and remained at a low level in most governorates (Fig. 8-B).



A Figure 8-A. Geographic distribution of overall P. falciparum cases in each four years by governorates, from 2006 to 2021


Figure 8-B. Geographic distribution of mean incidence rate per 1,000 population of P. falciparum cases in each four years by governorates, from 2006 to 2021

Trend of malaria death in Yemen

The total death cases by malaria were recorded at 704 (0.02%) in Yemen throughout the study period. Moreover, this analysis revealed an overall case fatality rate of 0.03% and an overall mortality rate of 0.18 per 100,000 populations. The trend of total malaria cases showed a decline from 63 in 2006 to 38 cases in 2009, an increase to 92 cases in 2009, a decrease to 14 cases in 2014, an increase to 65 cases in 2016, a decrease to 6 cases in 2020, and a slight increase to 25 cases in 2021. Furthermore, the trend of case fatality rate was relatively stable between 2006 and 2009 and slightly increased to 0.052% in 2011 and decreased to 0.002% in 2020. In addition, the trend of mortality rate per 100,000 individuals decreased from 0.3 in 2006 to 0.19 in 2009 and increased to 0.4 in 2010 and decline to 0.08 in 2021 (Fig. 9).

Fig. 9

Trend of malaria death by year in Yemen between 2006 and 2021

Discussion

Malaria remains a major public health concern worldwide, particularly in low-income nations such as Yemen. Since the establishment of the National Malaria Control Program (NMCP) in Yemen in 2000, remarkable success has been achieved in combating malaria in various regions of the country. Many strategies have been implemented to significantly reduce the prevalence of malaria in malaria-endemic areas. However, due to the ongoing conflict since 2015, his efforts have been severely hampered [11].

This finding revealed that overall 3,651,508 (24.1%) malaria cases out of 15,153,763 suspected individuals were reported in Yemen over 16 years. According to a similar retrospective analysis, there were 2,957,672 malaria cases in Uganda [23], 8925 cases in Saudi Arabia [24], 2.6 million cases in Pakistan [5], 8629 cases in Ghana [25], 1,285,271 cases in Nigeria [26], 29,554 cases in southern Ethiopia [27], and 22,225,699 cases in Burundi [28]. It is possible to attribute the high malaria burden reported in this study to a combination of factors: the persistence of political conflict since 2011 and armed conflict since March 2015, which has deteriorated the health and economic systems and suppressed epidemiological surveillance programs. Therefore, health institutions in Yemen must establish international cooperation with neighboring countries to implement an effective strategy to eliminate malaria in Yemen.

In the present study, approximately 14.5% of malaria cases were confirmed using rapid and microscopic diagnostics. This finding is higher than that reported in studies conducted in Ethiopia, which reported overall malaria cases between 7.7% and 13.4% [29–31]. However, this result is lower than that reported at 18.8% in Hadhramout governorate [15], 59.4% in Nigeria [26], 21.8% in southern Ethiopia [27], and 16.4% in northwest Ethiopia [32]. The reason behind using the rapid test more instead of microscopic examination is that rural areas in Yemen lack microscopic diagnostic techniques as a result of the lack of electricity, unqualified staff, or the high cost of microscopic examination. Therefore, rapid diagnostic tests should not be relied upon to diagnose cases alone, and all cases should be subjected to microscopic examination as it is more accurate and reliable.

Furthermore, approximately 52.22% of reported malaria cases were diagnosed based on clinical symptoms, and this indicates that laboratory confirmation of malaria cases remains weak in Yemen. This is due to the lack of laboratory diagnostic techniques in the various governorates of Yemen and limited resources. Therefore, all suspected cases of malaria must be subject to laboratory confirmation to avoid misdiagnosis as febrile diseases other than malaria, such as dengue fever and typhoid fever, with high efficiency and effectiveness.

In the current finding, P. falciparum was the predominant species, followed by P. vivax, mixed species of Plasmodium, P. malariae, and P. ovale (0.01%). This outcome is consistent with reports conducted in Yemen [4, 15, 33–35], in Saudi Arabia [24, 36], and in Ethiopia [27, 30]. In contrast, P. vivax had a significantly higher prevalence compared to P. falciparum [29, 37–39]. The increase in P. falciparum parasites in this finding could potentially be attributed to Yemen's geographic proximity to African countries, including Sudan, Somalia, and Ethiopia, where P. falciparum parasite is most prevalent and transmitted to Yemen since ancient times throughout history. Yemen is considered a major transit country for the migration and displacement of many migrants from African countries, which also explains the high prevalence of malaria in Yemen. Therefore, vector-control measures seem insufficient; surveillance and management of Africa migrants to Yemen should also be strengthened to reduce the possibility of a malaria outbreak in Yemen.

Furthermore, the overall incidence rate of malaria cases was 8.9 per 1,000 people, and this finding is higher than the reported with previous research [31]. In contrast, this outcome is lower than the reported rate with the results of several studies [27, 30, 40]. According to this finding, the incidence rate of malaria cases was decreased from 10.53/1,000 people in 2006 to 5.92/1.000 people in 2013 and then rapidly increased to 30.39/1,000 people in 2014 and decreased again to 4.94/1,000 people in 2021. According to previous reports, the incidence rate of malaria per 1,000 people increased in Sudan from 32.7 cases in 2010 to 73.4 cases in 2020 [40], Somalia from 43.7 cases in 2010 to 52.2 cases in 2020 [41], African region from 225 cases in 2019 to 234 cases in 2020 [1, 42], and Djibouti from 2.5 cases in 2013 to 97.6 cases in 2020 [43].

The decrease in the incidence rate of malaria between 2006 and 2009 may be due to the efforts of the NMCP in various regions of Yemen. The return to the highest rate in 2014 may have resulted from the political crisis of the 2011 revolution, which led to a change in the political system in Yemen and resulted in the suspension of malaria control efforts in some areas. Moreover, Yemen witnessed a war that lasted from 2015 until now, which led to the spread of epidemics as a result of the deterioration of the economic and health situation, explaining the increase in the spread of malaria in Yemen.

In terms of malaria distribution by governorate, the highest number of malaria was reported in Al Hudaydah, followed by Hajjah, Taiz, Dhamar, Sa'adah, and Al-Mahweet, accounting for 77.2% of all cases. Moreover, Al Hudaydah is one of the Yemen governorates that is most affected by malaria incidence followed by Hajjah, Al-Mahweet, Sa'adah, and Abyan. According to the Yemen map, the Tihama region, which extends along the western coast, is considered the most malaria-endemic area in Yemen [11]. Al Hudaydah and Hajjah governorates occupy the largest part of the Tihama region, and these two governorates are considered to have the greatest areas at high risk of malaria transmission according to the Malaria Indicator Survey (MIS) in 2013. While areas at relatively high risk of malaria transmission are the low-altitude areas of Sa'adah and Taiz governorates and the western edges of Al-Mahweet, Raimah, and Lahj governorates [4, 11]. This explains why malaria is more widespread in these governorates compared with others.

Furthermore, Al Hudaydah, Hajjah, and Sa'adah governorates together reported 69% of the total confirmed malaria cases in 2016 [4, 11]. In addition, malaria incidence was increased from 1.1 to 13.1 cases per 1000 people in Aden city between 2016 and 2020 [43]. Accordingly, the overall prevalence of malaria was reported in the Al Hudaydah governorate at 16.2% in 2003 [44] and 32.4% in 2019 [13], and 8.0% in 2020 [45]. Moreover, 17.3% was recorded in Sana’a city between 1998 and 2000 [46] and 18.6% in Taiz in 2006 [33]. Several factors contribute to the prevalence of malaria in Yemen, including climate variability, climate change, demographics, and socioeconomic factors such as population growth, social instability, and poverty. During the past decade, Yemen and its neighboring countries have experienced severe floods due to unusually high temperatures and rainfall. As a result, mosquitoes are more likely to breed in these conditions, potentially explaining Yemen's recent epidemics and high malaria incidences [44].

This study showed that the overall incidence rate of P. falciparum cases was 2.66 per 1,000 people, with an increase from 2.54 cases in 2006 to 6.83 cases in 2019. Similarly, some reports documented the decrease in P. falciparum cases from 117 cases to 43 cases between 2011 and 2016 in Myanmar [38], from 232.3 million in 2005 to 193.9 million in 2017 in sub-Saharan Africa [7], and from 20,628 cases to 3158 cases between 2014 and 2018 in Ethiopia [30]. In India, P. falciparum cases declined from 1.14 million in 1995 to 101068 cases in 2022, and the rate has gradually increased from 39% in 1995 to 63.84% in 2020 [37]. The main reason for the increase in the incidence of P. falciparum can be due to the continuation of the armed conflict, which led to the disruption of the majority of health institutions, in addition to the restrictions imposed on Yemen by the coalition countries from 2015 until now [47–48]. Therefore, the Ministry of Health and Environment in Yemen must work in international cooperation to implement effective strategies in combating and eliminating mosquitoes that transmit the malaria parasite.

This analysis revealed that the governorate of Al Hudaydah recorded the highest total number of P. falciparum cases, followed by Hajjah, Taiz, Aden, and Dhamar. Moreover, this finding observed that Al Hudaydah recorded the highest cumulative incidence of P. falciparum, followed by Hajjah, Aden, Taiz, and Abyan governorates. These results are in consonance with previous studies that were conducted in different regions of Yemen [13, 33, 44–46]. The variance in findings might be due to differences in quality of the techniques used in malaria diagnosis, as well as the geographic location, socio-demographic characteristics, and implementation programs for malaria prevention and control. Therefore, it is necessary for the NMCP to implement a robust surveillance system for early identification and rapid response, as well as to combine various control measures aimed at eliminating malaria mosquito breeding and preventing malaria transmission.

Worldwide malaria mortality rates decreased by 60% between 2000 and 2019, reducing from 143 to 57 deaths per 100,000 population at risk, before increasing in 2020 to 61 deaths, and subsequently decreasing again in 2022 to 56 [4]. This report is in line with our findings that revealed a decline in the CFR of malaria from 0.029% with 36 deaths to 0.015%, with 25 deaths between 2006 and 2021. This result is comparable with a contemporary result that presented the CFR as 0.04% and decreased from 0.06% in 2015 to 0.01% in 2017 [28]. Furthermore, the overall mortality rate of 0.18 per 100,000 people fell from 0.3 in 2006 to 0.08 in 2021. According to the previous reports in Yemen documented that the malaria mortality rates ranged from 2.1 to 4.7% in children [16, 33, 44, 49–53]. Moreover, studies in Ethiopia [28, 54], Europe [55], and sub-Saharan Africa [7] have reported a decline in malaria death cases.

The noticeable decrease in malaria-related deaths in this study is due to a change in treatment policy in various malaria-endemic countries, including Yemen, and this was documented by World Health Organization reports [4]. In addition, NMCP, Yemen has been implements several interventions to combat malaria, including mosquito nets with insecticides, indoor residual spraying, diagnosis, treatment, and proactive and reactive case monitoring [15].

Strength and limitations

This study's comprehensive approach, large dataset covering all Yemen governorates, and long duration make a significant contribution to the field of research. In addition, the findings of this analysis provide valuable information to health institutions in developing and implementing an effective malaria control system in Yemen based on monitoring and controlling malaria prevalence in the country. The outcomes of this analysis are considered a basic database that can be used by investigators to conduct further studies that focus on exploring and studying factors related to the spread of malaria, such as sociodemographic structure, population behaviors, climate change, environmental factors, population displacement, and the migration of foreigners from the Horn of Africa to Yemen. Additionally, plans and programs dedicated to monitoring and combating malaria in endemic areas should be evaluated. Nevertheless, this analysis has some limitations. One of the major limitations in exploring the distribution of malaria prevalence by sex or age is the lack of available data for individual variables that will greatly enhance the significance of this investigation. Moreover, this analysis relies on secondary data from a government institution that may lack validity or reliability owing to variations in data quality and consistency from one governorate to another. Not all malaria patients seek healthcare, and some patients self-medicate or seek primary clinics that lack an accurate system, leading to the underreporting of all cases. Further, this analysis is unable to display the trend of malaria cases by month and season due to a lack of available data. The lack of data on the number of malaria deaths by governorate is also considered a shortcoming in this analysis.

Conclusions

This analysis indicates that malaria cases have continued to increase in Yemen, particularly in the last few years. An increasing trend in malaria burden was recorded in the Al Hudaydah, Hajjah, and Taiz governorates, which were the most affected. Plasmodium falciparum has emerged as the most prevalent human malarial parasite in Yemen. The incidence of P. falciparum significantly increased between 2006 and 2021. In contrast, the trends of case fatality and mortality rates decreased between 2006 and 2020. In light of these results, an effective program must be implemented to control and prevent the proliferation of mosquitoes that transmit malarial parasites in Yemen. To reduce the mortality and complications due to severe malaria, it is imperative to scale up vector control tools and encourage early diagnosis and treatment. Furthermore, Yemen's Ministry of Public Health and its governorate offices should prioritize ensuring that malaria data documents are handled effectively across all districts within the governorates for rigorous analysis to promptly identify and respond to outbreaks. We conducted a study to evaluate the resistance of malarial parasites to antimalarial drugs. The introduction of malaria vaccines is a successful and effective step in combating malaria and vaccinating the general population in governorates, most affected by the spread of malaria. Further investigation is required to determine the epidemiological vector-borne mesquite across all governorates and the risk factors associated with malaria transmission. Moreover, it is necessary to conduct a molecular epidemiological investigation of Plasmodium species to determine their genotyping, chains of spread, and distribution in the Yemeni governorates.

Ethical consideration

This analysis was conducted in accordance with Yemeni public health laws and regulations as well as adhering to the Declaration of Helsinki. Furthermore, the Research and Ethics Committee of the College of Applied Sciences, Hajjah University (Reference No. 087/2023, on 9 December 2023) approved the ethical statement for conducting this analysis. Moreover, the Hajjah University also wrote an official letter to the MoPHP, outlining the purpose of this analysis. Accordingly, due to the retrospective nature of the study, the MoPHP granted permission for the use of database data for research purposes in line with Article 51 of the Yemeni Public Health Law No. (4) 2009, without the need for informed consent. To ensure the protection of the personal information of the cases, confidential codes were used, and the data collected were analyzed as anonymous.

Funding

There was no specific funding received for this work.

Conflicts of Interest

The author declares no conflicts of interest.

Data Availability

This published article includes the datasets generated during this study, and the corresponding author (Edrees W) will provide any relevant data upon reasonable request.

Consent for publication

Not applicable.

Author Contribution

Edrees W designed the study; Edrees W and Al-Shehari W collected, analyzed, and interpreted the data; Edrees W wrote the draft manuscript; Al-Shehari W reviewed the manuscript and provided technical support in terms of data analysis and reporting. All the authors have read and approved the manuscript for submission.

Acknowledgment

Authors thankfully acknowledge the Ministry of Public Health and Population for their kind assistance to give the data for this analysis.

Abbreviations

CDC

United States Centers for Disease Control

CFR

Case Fatality Rate

Incidence Rate

MoPHP

Ministry of Public Health and Population

NMCP

National Malaria Control Program

RDT

Rapid Diagnostic Test

SPSS

Statistical Package for Social Sciences

WHO

World Health Organization

References

World Health Organization. World Malaria Report 2022; World Health Organization: Geneva, Switzerland, 2022. Available online: https://www.who.int/teams/global-malaria-programme/reports/world-malaria-report-2022. Accessed on 1 August 2024.

Centers for Disease Control and Prevention. How malaria spreads. March 12. 2024. https://www.cdc.gov/malaria/causes/index.html. Accessed August 4, 2024.

World Health Organization. Malaria. 4 December 2023. Available online: https://www.who.int/news-room/fact-sheets/detail/malaria. Accessed on 1 August 2024.

World Health Organization. World malaria report 2023. Geneva: World Health Organization; 2023. Available online. https://iris.who.int/bitstream/handle/10665/374472/9789240086173-eng.pdf?sequence=1.

Venkatesan P. The 2023 WHO world malaria report. The Lancet Microbe. Published online January 1, 2024. https://doi.org/10.1016/s2666-5247(24)00016-8

Battle KE, Lucas TCD, Nguyen M, Howes RE, Nandi AK, Twohig KA, et al. Mapping the global endemicity and clinical burden of Plasmodium vivax, 2000–17: A spatial and temporal modelling study. Lancet. 2019;394:332–43. https://doi.org/10.1016/s0140-6736(19)31096-7.

Weiss DJ, Lucas TCD, Nguyen M, et al. Mapping the global prevalence, incidence, and mortality of Plasmodium falciparum, 2000–17: A spatial and temporal modelling study. Lancet. 2019;394(10195):322–31. https://doi.org/10.1016/s0140-6736(19)31097-9.

World Health Organization. (WHO, 2019). World Malaria Report 2019. Geneva: World Health Organization; 2019. https://www.who.int/teams/global-malaria-programme/reports/world-malaria-report-2019. Accessed August 4, 2024.

World Health Organization. Yemen. 2011. Available at https://www.emro.who.int/images/stories/rbm/documents/ye.pdf?ua=1. Accessed August 4, 2024.

10.

World Health Organization. World malaria report 2015. https://iris.who.int/bitstream/handle/10665/200018/9789241565158_eng.pdf?sequence=1

11.

International Organisation for Migration (IOM). Malaria in Yemen: Needs assessment 2017. Regional MER Project Management Unit, IOM Publications Platform. https://publications.iom.int/books/malaria-yemen-needs-assessment-2017

12.

World Health Organization. Stopping malaria at the source. 23 April 2023. Geneva: World Health Organization. https://www.emro.who.int/yemen/news/stopping-malaria-at-the-source.html

13.

Abdul-Ghani R, Mahdy MAK, Alkubati S, et al. Malaria and dengue in Hodeidah city, Yemen: High proportion of febrile outpatients with dengue or malaria, but low proportion co-infected. PLoS ONE. 2021;16(6):e0253556. https://doi.org/10.1371/journal.pone.0253556.

14.

Shnawa HB, Al-Ezzi AA, Abed GH, Al-Salahy MB, Mandour AM, Mohamed M. Prevalence of Plasmodium falciparum in Abs, Hajjah governorate northwest Yemen. Int J Biosci. 2016;9(1):59–71. http://dx.doi.org/10.12692/ijb/9.1.59-71.

15.

Bamaga OA, Mahdy MA, Mahmud R, et al. Malaria in Hadhramout, a southeast province of Yemen: Prevalence, risk factors, knowledge, attitude and practices (KAPs). Parasites Vectors. 2014;7(351). https://doi.org/10.1186/1756-3305-7-351.

16.

Abdulsalam AM, Mohammed AKM, Ahmed AA, Fong MY. Clinical situation of endemic malaria in Yemen. Trop Biomed. 2010;27(3):551–58.

17.

Al-Shehari WA, Yin Y-A, Wang X, Wang Y, Sun H, Fu Y, Zhang F. Prevalence and surveillance of tuberculosis in Yemen from 2006 to 2018. Epidemiol Infect. 2022;150(e146):1–10. https://doi.org/10.1017/S0950268822001261.

18.

Torbosh A, Al Amad MA, Al Serouri A, Khader Y. The impact of war in Yemen on immunization coverage of children under one year of age: descriptive study. JMIR Public Health Surveill. 2019;5(4):e14461. https://doi.org/10.2196/14461.

19.

Edrees WH, Abdullah QY, Al-Shehari WA, Alrahabi LM, Khardesh AAF. COVID-19 pandemic in Taiz governorate, Yemen, between 2020 and 2023. BMC Infect Dis. 2024;24(1). https://doi.org/10.1186/s12879-024-09650-0.

20.

UNICEF. Yemen crisis. 19 August 2024. Available at https://www.unicef.org/emergencies/yemen-crisis

21.

World Health Organization. Malaria surveillance assessment toolkit, Implementation Reference Guide 2 August 2022. https://iris.who.int/bitstream/handle/10665/361178/9789240055278-eng.pdf?sequence=1

22.

OCHA. Humanitarian data exchange, Yemen: Humanitarian Needs Overview. https://data.humdata.org/dataset/yemen-humanitarian-needs-overview? Accessed September 05, 2024.

23.

Zalwango MG, Bulage L, Zalwango JF, Migisha R, Agaba BB, Kadobera D et al. Trends and distribution of severe malaria cases, Uganda, 2017–2021: analysis of health management information system data. Uganda Natl Inst Public Health Kampala, 2023. https://uniph.go.ug/trends-and-distribution-of-severe-malaria-cases-uganda-2017-2021-analysis-of-health-management-information-system-data/

24.

Amer OS, Waly MI, Burhan IW, Al-Malki ES, Smida A, Al-Benasy KS. Epidemiological trends of malaria in the Western regions of Saudi Arabia: A cross sectional study. J Infect Developing Ctries. 2020;14(11):1332–37. https://doi.org/10.3855/jidc.13246.

25.

Deku JG, Lokpo SY, Kye-Amoah KK, et al. Malaria burden and trend among clients seeking healthcare in the western region: A 4-year retrospective study at the Sefwi-Wiawso Municipal Hospital, Ghana. Open Microbiol J. 2018;12(1):404–11. https://doi.org/10.2174/1874285801812010404.

26.

Visa TI, Ajumobi O, Bamgboye E, Ajayi I, Nguku P. Evaluation of malaria surveillance system in Kano State, Nigeria, 2013–2016. Infect Dis Poverty. 2020;9(1). https://doi.org/10.1186/s40249-020-0629-2.

27.

Dabaro D, Birhanu Z, Yewhalaw D. Analysis of trends of malaria from 2010 to 2017 in Boricha district, Southern Ethiopia. Malar J. 2020;19(88). https://doi.org/10.1186/s12936-020-03169-w.

28.

Ndoreraho A, Shakir M, Ameh C, et al. Trends in malaria cases and deaths: assessing national prevention and control progress in Burundi. East Afr Health Res J. 2020;4(2):182–88. https://doi.org/10.24248/eahrj.v4i2.642.

29.

Mulugeta A, Assefa A, Eshetie A, et al. Six-year trend analysis of malaria prevalence at University of Gondar Specialized Referral Hospital, Northwest Ethiopia, from 2014 to 2019. Sci Rep. 2022;12(1411). https://doi.org/10.1038/s41598-022-05530-2.

30.

Tesfaye S, Yesuf A. Trend analysis of malaria surveillance data in West Wallaga, West Oromia, Ethiopia: a framework for planning and elimination. Malar J. 2024;23(52). https://doi.org/10.1186/s12936-024-04874-6.

31.

Moltot T, Bekele G, Gebreegziabher ZA, et al. A five years malaria surveillance data analysis of North Shewa zone, Amhara region, Ethiopia: July 2018 to June 2023. Malar J. 2024;23(1). https://doi.org/10.1186/s12936-024-05006-w.

32.

Eshetu T, Muhamed B, Awol M et al. A retrospective analysis of malaria trends in Maksegnit health center over the last seven years, northwest Ethiopia: 2014–2020. Journal of Parasitology Research. 2022; 2022:1–8. https://doi.org/10.1155/2022/5170550

33.

Alkadi HO, Al-Maktari MT, Nooman MA. Chloroquine-resistant Plasmodium falciparum local strain in Taiz governorate, Republic of Yemen. Chemotherapy. 2006;52(4):166–70. https://doi.org/10.1159/000093592.

34.

Al-Mekhlafi AM, Al-Mekhlafi HM, Mahdy MA, Azazy AA, Fong MY. Human malaria in the highlands of Yemen. Ann Trop Med Parasitol. 2011;105(3):187–95. https://doi.org/10.1179/136485911x12987676649421.

35.

Al-Mekhlafi AM, Mahdy MA, Azazy A, et al. Molecular epidemiology of Plasmodium species prevalent in Yemen based on 18s rRNA. Parasites Vectors. 2020;3(110). https://doi.org/10.1186/1756-3305-3-110.

36.

Elagali A, Shubayr M, Noureldin E, Alene KA, Elagali A. Spatiotemporal distribution of malaria in the Kingdom of Saudi Arabia. Trop Med Infect Disease. 2024;9(1):16. https://doi.org/10.3390/tropicalmed9010016.

37.

Rijal KR, Adhikari B, Ghimire P, et al. Epidemiology of Plasmodium vivax malaria infection in Nepal. Am J Trop Med Hyg. 2018;99(3):680–87. https://doi.org/10.4269/ajtmh.18-0373.

38.

Geng J, Malla P, Zhang J, et al. Increasing trends of malaria in a border area of the Greater Mekong Subregion. Malar J. 2019;18(1). https://doi.org/10.1186/s12936-019-2924-6.

39.

Panzi EK, Kandala NI, Kafinga EL, Tampwo BM, Kandala NB. Forecasting malaria morbidity to 2036 based on Geo-Climatic factors in the Democratic Republic of Congo. Int J Environ Res Public Health. 2022;19(19):12271. https://doi.org/10.3390/ijerph191912271.

40.

Ahmed A, Pignatelli P, Elaagip A, Hamid MM, Alrahman OF, Weetman D. Invasive malaria vector Anopheles stephensi mosquitoes in Sudan, 2016–2018. Emerg Infect Dis. 2021;27:2952. https://doi.org/10.3201/eid2711.210040.

41.

World Health Organization (WHO). Malaria threats map. Geneva. https://apps.who.int/malaria/maps/threats/

42.

Badmos AO, Alaran AJ, Adebisi YA, Bouaddi O, Onibon Z, Dada A, et al. What sub-Saharan African countries can learn from malaria elimination in China. Trop Med Health. 2021;49:86. https://doi.org/10.1186/s41182-021-00379-z.

43.

Al-Eryani SMA, Kelly-Hope L, Harbach RE, et al. Entomological aspects and the role of human behaviour in malaria transmission in a highland region of the Republic of Yemen. Malar J. 2016;15(1). https://doi.org/10.1186/s12936-016-1179-8.

44.

Al-Maktari MT, Bassiouny HK, Al-Hamd ZS, Assabri AM, El-Massry AG, Shatat HZ. Malaria status in Al-Hodeidah Governorate, Yemen: malariometric parasitic survey and chloroquine resistance P. falciparum local strain. J Egypt Soc Parasitol. 2003;33:361–72. [PubMed] [Google Scholar].

45.

Azazy AA, Raja'a YA. Malaria and intestinal parasitosis among children presenting to the paediatric centre in Sana'a. Yemen East Mediterr Health J. 2003;9:1048–53. [PubMed] [Google Scholar].

46.

Al-Quhaiti MA, Abdul-Ghani R, Mahdy AK, Assada MA. Malaria among under-five children in rural communities of Al-Mahweet governorate, Yemen. Malar J. 2022;21(1). https://doi.org/10.1186/s12936-022-04371-8.

47.

Ali M, Edrees WH, Al-Shehari WA, Xue G, Al-Hammadi S, Qasem EA. Chaulagain RPand Lal N. Antifungal susceptibility pattern of Candida species isolated from pregnant Women. Front Cell Infect Microbiol 14. 2024;1434677. https://doi.org/10.3389/fcimb.2024.1434677.

48.

Al-Aomary NM, Edrees WH, Al-Ofairi BA, Thabit JM. Nasal carriage of Staphylococcus aureus and its antibacterial susceptibility profiles among food handlers in Sana’a restaurants, Yemen. Israa Univ J Appl Sci. 2024;7(2):1–16. https://doi.org/10.52865/DDHP5456.

49.

Mohanna BS, Sanchez LJ, Ferrufino Ll JC, Bravo PF, Gotuzzo HE. Lymph node involvement in classic Kaposi sarcoma: report of three cases. Rev Med Chil. 2007;135(9):1166–70. http://dx.doi.org/10.4067/S0034-98872007000900011.

50.

Al-Mansoob MAK, Al-Mazzah MM. The role of climate on malaria incidence rate in four governorates of Yemen. Med J Malaysia. 2005;60(3):349–57. [PubMed] [Google Scholar].

51.

National Center for Vector Borne Diseases Control (NCVBDC). Magnitude of the problem. September 06. 2024. https://ncvbdc.mohfw.gov.in/index4.php?lang=1&level=0&linkid=420&lid=3699

52.

Alwajeeh TS, Abdul-Ghani R, Allam AF, et al. Uncomplicated falciparum malaria among schoolchildren in Bajil district of Hodeidah governorate, west of Yemen: Association with anaemia and underweight. Malar J. 2020;19(358). https://doi.org/10.1186/s12936-020-03431-1.

53.

Al-Taiar A, Jaffar S, Assabri A, Al-Habori M, Azazy A, Al-Mahdi N, Ameen K, Greenwood BM, Whitty CJ. Severe malaria in children in Yemen: Two site observational study. BMJ. 2006;333(7573):827. https://doi.org/10.1136/bmj.38959.368819.BE.

54.

Deribew A, Dejene T, Kebede B, Tessema GA, Melaku YA, Misganaw A, et al. Incidence, prevalence and mortality rates of malaria in Ethiopia from 1990 to 2015: analysis of the global burden of diseases 2015. Malar J. 2017;16:271. https://doi.org/10.1186/s12936-017-1919-4.

55.

Tunesi S, Tambuzzi S, Decarli A, Cattaneo C, Russo AG. Trends in mortality from non-natural causes in children and adolescents (0–19 years) in Europe from 2000 to 2018. BMC Public Health. 2023;23(1):2223. https://doi.org/10.1186/s12889-023-17040-5.

Yes