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. 2021 Apr 22;45(4):986–994. doi: 10.1007/s12639-021-01391-0

Significant decline of malaria incidence in a low socioeconomic area in the southeast of Iran: 10 years field assessment during malaria elimination programme

Mehdi Zare 1, Hossein Farshidi 2, Moussa Soleimani-Ahmadi 3,4,✉, Seyed Aghil Jaberhashemi 5, Alireza Sanei-Dehkordi 3,4
PMCID: PMC8556429  PMID: 34789982

Abstract

Although malaria burden and its active foci have sharply declined after the implementation of elimination programme since 2010, it is still considered as a major public health problem in southeast Iran. This descriptive-analytical study aimed to determine 10-years of malaria epidemiological trends in Bashagard County. Data were collected from 7 selected malarious region of the county based on active and passive surveillance of clinical cases. For diagnosis of malaria, the examination of microscopic slides and rapid diagnostic test, were used. In total, 237 malaria cases were found from 2009 to 2018. Plasmodium vivax was the dominant parasite species and identified in 232 (97.9%) individuals. Males were infected more than females and the majority of malaria cases (67.4%) were recorded from rural areas. Although about 98% of malaria cases were indigenous, they have decreased form 200 cases in 2009 to zero indigenous transmission in 2018. During the study period, malaria cases had decreased significantly by about 99% and the incidence rate had declined from 5.47/1000 cases in 2009 to 0.002/1000 in 2018. The incidence of malaria, especially indigenous cases, in Bashagard County has decreased dramatically in the past 10 years. However, there is still probability of malaria re-introduction and outbreak in the county due to climatical and geographical conditions. Therefore, it is necessary to implement an active surveillance system to detect and treat malaria cases quickly, during the elimination phase in this county.

Keyword: Malaria, Incidence, Elimination, Socioeconomic, Bashagard, Iran

Background

Malaria is one of the most important vector borne diseases in tropical and subtropical areas caused by Plasmodium parasite (Ashley et al. 2018). According to the recent world malaria report, almost half of the world’s population was at risk of malaria infection, approximately 229 million malaria cases occurred worldwide, and the number of malaria deaths reached to 409,000 in 2019 (WHO 2020).

There are seven proven malaria vectors in Iran including Anopheles culicifacies sensu lato (s.l.), An. dthali, An. fluviatilis s.l., An. maculipennis s.l., An. sacharovi, An. stephensi, and An. superpictus (Hanafi-Bojd et al. 2011). In this regard, An. pulcherrimus and An. hyrcanus are reported as the suspected and possible vectors, respectively in the country (Azari-Hamidian et al. 2019).

Malaria is endemic in south and southeast Iran including Kerman, Sistan-Baluchestan, and Hormozgan Provinces, and four-fifths of malaria cases have been reported from these areas (UCSF 2015). The malaria eradication programme was started in 1951 in Iran, and changed to malaria control in 1985 because of the restrictions and challenges (Edrissian 2006). This country has been in the elimination phase since 2010 and is aiming to become entirely malaria-free by 2025 (UCSF 2015).

Hormozgan Province is a malaria endemic area. It constitutes about 10% of the total population of Iran, and 38% of all country malaria cases have occurred in this province (Ghahremani et al. 2019). According to the results of previous studies, P. vivax is responsible for the majority of malaria cases in Hormozgan Province, followed by P. falciparum. Few cases are also caused by the mix of P. vivax and P. falciparum (Schapira et al. 2018; Hanafi-Bojd et al. 2010). Moreover, a case of malaria infection has been reported due to P. ovale detected in an African football player came to Bandar Abbas in 2008 (Nateghpour et al. 2010).

Bashagard is a malarious county in Hormozgan Province and indigenous malaria cases have been frequently reported from different regions of this county (Sanei-Dehkordi et al. 2019). In this area, active malaria circulation occurs in the autumn and spring which are the malaria vector breeding seasons (Hanafi-Bojd et al. 2012). Socio-economic conditions and tropical climate make favorable conditions for malaria occurrence and persistent transmission in this county (Soleimani-Ahmadi et al. 2012). In Bashagard County, the malaria elimination programme has been started since 2010 and, similar to other malarious regions, vector control measures such as application of long-lasting insecticidal nets and larvicides and indoor residual spraying have been considered as the main vector control methods in this area (Madani et al. 2017).

Bashagard County, is susceptible to malaria epidemics due to several factors including tropical climate, low socio-economic conditions, and the existence of five potential malaria vectors including An. stephensi, An. fluviatilis s.l., An. dthali, An. culicifacies s.l., and An. superpictus s.l (Madani et al. 2017; Azari-Hamidian et al. 2019). In addition, vicinity of this county to other malaria endemic areas increases the possibility of imported malaria cases and the risk of local transmission that may result in the reintroduction of local cases and a considerable challenge for malaria elimination in this area. Therefore, continuous monitoring of epidemiological aspects of malaria is essential for effective and sustainable malaria elimination programme in this area. This study was conducted to determine the trends of malaria incidence during 2009–2018 years in Bashagard County.

Methods

Study area

The study was conducted in Bashagard County which is located in Hormozgan Province, southeast Iran. This county has an area of 16,000 km2 and is placed between longitudes 57°23′–59°02′ E and latitudes 26°04′–26°58′ N, with 43,000 population according to 2016 census from which 51% were males and 49% females. The area is mountainous with low precipitation.

Bashagard has a tropical climate with a mean annual temperature of 28.1 °C ranging from 18.4 to 37.2 °C. Maximum temperature can reach up to 47.4 °C in summers, while the minimum temperature drops to about 1 °C in winters. The rainfall happens through the November–May with a 10-year annual average of 254 mm during 2009–2018 (Fig. 1). The average maximum and minimum relative humidity during the study period reported to be 38.6% in February and 16% in May (Hormozgan meteorological administration). Bashagard is a low socioeconomic area and the majority of people in this area live in small houses made of cement blocks and shelters (Fig. 2). Livestock herding and agriculture are the main occupations in this area.

Fig. 1.

Fig. 1

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Ten-year average of meteorological parameters during 2009–2018 in Bashagard County, southeast Iran

Fig. 2.

Fig. 2

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Typical human and animal habitats in Bashagard County, southeastern Iran. Cemented brick houses (a), sheds made with palm leaves (b) and domestic animal shed (c) (Original photos)

Study design and data collection

This descriptive-analytical study, evaluated 10-years of malaria epidemiological trends in Bashagard County, southeast Iran. To conduct this study, Bashagard County was divided into 7 regions of malaria detection and treatment. These regions included Jagdan (26°43′ N, 57°74′ E, 909 m), Sardasht (26°45′ N, 57°89′ E, 729 m), Goharan (26°59′ N, 57°89′E, 925 m), Tidar (26°75′ N, 57°83′ E, 1277 m), Tisur (26°30′ N, 58°15′ E, 480 m), Khomeynishahr (26°61′ N, 58°03′ E, 1080 m), and Site-e-macity (26°26′ N, 58°24′ E, 395 m) (Fig. 3). Data were collected from these malaria regions from 2009 to 2018. In these regions, active and passive case detection was performed amongst suspected cases with relevant symptoms such as fever. For diagnosis of malaria, the examination of microscopic slides was used. In this regard from all suspected malaria subjects, thin and thick blood smears were prepared by finger-prick blood samples (Fig. 4). The smears were stained using 10% Giemsa and then air dried. Peripheral blood smears were observed by an optical microscope in order to detect the parasite. If no parasites were found in a sample, after examining 100 fields, the case was reported as negative. At first, thick films were examined for the detection of malaria parasites and if malaria parasites were identified in thick films, their thin films were examined for species identification according to the WHO standard (WHO 2010). For quality assurance of malaria diagnostic tests, standard operating procedures were performed for 10% of negative and all positive slides (UNDP 2017). The rapid diagnostic test (RDT) was used, during outbreaks, when microscopic detection is not possible (Schapira et al. 2018).

Fig. 3.

Fig. 3

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Map showing the provinces of Iran, highlighting the location of Hormozgan province and malarious regions in Bashagard County

Fig. 4.

Fig. 4

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Diagnosis of malaria parasites using microscopy and RDT kit in Bashagard County, southeastern Iran. Active case detection (a), passive case detection (b) (Original photos)

All of the positive malaria cases were treated according to the national malaria treatment protocol. Another data relevant to malaria patients including gender, age group (0–4, 5–14, 15 years, and older), place of residence (rural, urban), type of malaria parasite (Plasmodium vivax, P. falciparum, and P. malariae), and transmission type (imported, introduced, relapse, and indigenous) were recorded in checklists. In this regard, malaria cases in which the infection had been acquired outside the study area (non-indigenous), were considered as imported cases (WHO 2016). Moreover, malarial cases in low transmission seasons, according to epidemiological evidence, were considered as relapse cases (WHO 2016). The collected data and laboratory tests results were analyzed using SPSS V. 21 software. The frequency distribution of dependent and independent variables were worked out with crosstab. The data were finally described and presented using figures.

Results

In total, 237 malaria cases were recorded in Bashagard County during the study period of 2009–2018. Plasmodium vivax was the dominant parasite species and the main causative agent of malaria in 232 (97.9%) individuals. Plasmodium falciparum was also responsible for 2.1% of malaria cases. Men were infected more than women, with only 39.7% of cases occurred in women over the study period. People with 15 or more years of age had the highest infection rate and the lowest infection rate was in under 5 years old group (Table 1). The majority of malaria cases were from rural areas (93.7%), while only 6.3% of patients lived in urban areas. (Table 1).

Table 1.

Frequency of all malaria cases in terms of sex, age group, and residence place in Bashagard County, southeast Iran, 2009–2018

Year Sex Age groups Residence place Total
Male Female < 5 5–14 > 14 City Village
No. % No. % No. % No. % No. % No. % No. % No.
2009 120 59.7 81 40.3 35 17.4 59 29.4 107 53.2 14 7 187 93 201
2010 7 63.4 4 36.3 1 9.1 5 45.5 5 45.5 0 0 11 100 11
2011 8 80 2 20 0 0.0 1 10 9 90 1 10 9 90 10
2012 3 50 3 50 0 0.0 2 20 4 80 0 0 6 100 6
2013 0 0.0 0 0.0 0 0.0 0 0.0 0 0.0 0 0 0 0 0
2014 0 0.0 0 0.0 0 0.0 0 0.0 0 0.0 0 0 0 0 0
2015 2 50 2 50 1 25 1 25 2 50 0 0 4 100 4
2016 0 0.0 0 0.0 0 0.0 0 0.0 0 0.0 0 0 0 0 0
2017 2 50 2 50 0 0.0 1 25 3 75 0 0 4 100 4
2018 1 100 0 0.0 0 0.0 0 0.0 1 100 0 0 1 100 1
Total 143 60.3 94 39.7 37 15.6 69 29.1 131 55.3 15 6.3 222 93.7 237
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In this study, most of the malaria penitents had no formal education (54.4%), and 23.9% had completed primary school education (Fig. 5). Epidemiological classification of malaria in Bashagard County showed that the majority of cases were indigenous (97.9%). Moreover, 1.7% and 0.4% of the cases were respectively imported and relapse (Table 2). Although about 98% of malaria cases were indigenous, they have decreased form 200 cases in 2009 to zero in 2018. Results of this study indicated a downward trend of malaria cases in Bashagard County. In this regard, malaria cases have decreased form 201 cases in 2009 to 1 case in 2018 (Fig. 6). Moreover, malaria incidence rate has significantly declined from 5.47/1000 cases in 2009 to 0.002/1000 in 2018. Of note, during the study period, no deaths were recorded from malaria in Bashagard County.

Fig. 5.

Fig. 5

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Frequency of malaria cases in terms of educational level in Bashagard County, southeast Iran, 2009–2018

Table 2.

Frequency of malaria cases in terms of transmission type, plasmodium species, and some of the malaria indicators in Bashagard County, southeast Iran, 2009–2018

Years Transmission type Plasmodium species Total cases Total slides Malaria indicators
Indigenous Imported Relapse P. vivax P. falciparum API SPR ABER
No. % No. % No % No. % No. %
2009 200 99.5 1 0.5 0 0 196 97.5 5 2.5 201 26,739 5.45 0.07 85.4
2010 11 100 0 0.0 0 0 11 100 0 0.0 11 23,893 0.28 0.05 74.1
2011 10 100 0 0.0 0 0 10 100 0 0.0 10 27,095 0.24 0.04 67.7
2012 6 100 0 0.0 0 0 6 100 0 0.0 6 23,683 0.14 0.02 62.4
2013 0 0.0 0 0.0 0 0 0 0.0 0 0.0 0 18,812 0.00 0.00 57.8
2014 0 0.0 0 0.0 0 0 0 0.0 0 0.0 0 17,733 0.00 0.00 53.7
2015 2 50 2 50 0 0 4 100 0 0.0 4 18,102 0.09 0.02 51.2
2016 0 0.0 0 0.0 0 0 0 0.0 0 0.0 0 12,173 0.00 0.00 34.7
2017 3 75 1 25 0 0 4 100 0 0.0 4 10,723 0.11 0.04 30.2
2018 0 0.0 0 0.0 1 100 1 100 0 0.0 1 8556 0.002 0.01 20.1
Total 232 97.9 4 1.7 1 0.4 232 97.9 5 2.1 237 187,409 – – –
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Fig. 6.

Fig. 6

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Annual trend of malaria cases during 2009–2018 in Bashagard County, southeast Iran

In line with the malaria elimination programme in Iran, control measures against malaria are in place in the in Bashagard County. In this regard, from 2009 to 2018, 187,409 blood smears were prepared and examined and 0.13% of them were found to be positive for malaria infection. Blood Examination Rate (ABER) has been reduced from 85.4 in 2009 to 20.1 in year 2018. This reduction has relatively the same pattern as the number of malaria cases and API. Details of malaria indicators are shown in Table 2. In addition, indoor residual spraying takes place bi-annually by Deltamethrin insecticide in the study area and, according to the findings of this study, the mean spray coverage of houses in the target population was about 83%. Moreover, a total of 35,430 long-lasting insecticidal nets had been distributed among the population by government and about 98% of target population had at least one LLIN.

Discussion

A malaria pre-elimination programme was initiated in Iran in 2009 (Kafil 2017). This program was established, with technical support of WHO, to interrupt P. falciparum transmission and eliminate malaria from Iran by the end of 2015 and 2025, respectively (UCSF 2015). Enhanced access to prompt diagnosis and timely treatment, improved surveillance, and expanded implementation of integrated malaria vector management were the main strategic aspects of this programme (UCSF 2015).

According to the results of this study, the prevalence of malaria in Bashagard County has been declining, so that the total number of positive malaria cases has reduced from 201 cases in 2009 to 1 case in 2018. The results of this study shows the relative success of malaria control programs in order to achieve the goal of eliminating malaria in Bashagard County. This is consistent with National Malaria Control Program report which showed a reduction in the number of malaria infections in Iran, from 11,460 cases in 2009 to 960 cases in 2018 (WHO 2020; Vatandoost et al. 2019). Also, according to WHO report, for the first time, there has been no indigenous malaria cases in Iran since 2018 (WHO 2020). This reduction can be attributed mainly to the development of a malaria quick warning system, community volunteers, rural malaria mobile teams, increasing the surveillance, and conducting operational research (Schapira et al. 2018). In addition, improving socio-economic status including increased access to piped water supply and electricity, residual spraying of residential areas, implementation of larvicidal programs, the use of rapid parasite detection methods, and free distribution of long-lasting insecticide nets have been proposed as explanatory reasons for the reduction of malaria cases (Hemami et al. 2013; Nejati et al. 2017).

In this study P. vivax was the dominant malaria parasite species in Bashagard County. This finding is similar to general pattern of malaria disease in Iran (UCSF 2015; Vatandoost et al. 2019; Hemami et al. 2013). In other studies, conducted in Turkey, Armenia, Azerbaijan, Tajikistan, Iraq, Syria, Oman, Yemen, Saudi Arabia, Afghanistan, Pakistan, Vietnam, and Thailand, P. vivax has been reported as the predominant parasite species (Vatandoost et al. 2019; Howes et al. 2016; Gething et al. 2012). Plasmodium vivax has a global distribution and has been reported from tropical and temperate regions including Central Asia, Southeast Asia, and the American continent (Gething et al. 2012; van Dorp et al. 2020). Wider geographical distribution of P. vivax can be due to early appearance of its gametocytes in blood circulation, faster development of sporozoites within Anopheles, efficient transmission by vector mosquitoes at lower parasite density, and wider survival temperature ranges compared to P. falciparum. Another reason for higher prevalence of P. vivax may be that the effective treatments and vector control measures such as ITNs are more effective in reducing P. falciparum transmission than P. vivax (Battle et al. 2012).

Results of this study revealed that most of the malaria cases were in males and people above 15 years old. This finding is in accordance with other epidemiologic studies on malaria in Iran which revealed higher incidence rate of the malaria in men and the age group of over 15 years (Vatandoost et al. 2019; Norouzinejad et al. 2016). Sex does not naturally or directly influence the sensitivity or resistance to malaria, but it may affect people indirectly through their occupation and type of clothing (Norouzinejad et al. 2016). In addition, social activities and the presence of men outside the home, increase their contact with infective vectors. Moreover, as a result of the prevalence of asymptomatic cases with low parasite densities amongst men, they can have a significant role in causing outbreaks (Cotter et al. 2013).

The results of this study also showed that, compared to urban areas, malaria was more prevalent in rural regions. This finding is in agreement with some studies in Iran which revealed high incidence rate of malaria in rural areas (Norouzinejad et al. 2016; WHO 2013).

Many other studies around the world have also indicated malaria as a disease of rural regions, where there are suitable places for anopheles mosquitoes breeding (Keiser et al. 2004; Robert et al. 2003). In this study, an explanation for the greater numbers of malaria cases in rural areas can be due to the existence of many perennial and seasonal rivers in these regions which provide favorite breeding places for mosquitoes and valleys along river beds which can be the resting places for adult mosquitoes. In addition, villages are often located close to the rivers and villagers provide blood sources for anopheline mosquitoes and resulting in higher prevalence of malaria cases. Another reason for higher prevalence of malaria in rural areas in this study, is that more than 90% of the Bashagard County population live in the rural areas.

This investigation indicated high incidence of malaria in illiterate people. Lower educational level is associated with higher malaria risk. This finding is consistent with the results of a previous study in this county which revealed low level of practices concerning malaria prevention in the illiterate households (Madani et al. 2017). The results of another study in Baluchistan area, southeastern Iran, also showed that over two-third (68.7%) of the respondents were illiterate and only one-third considered malaria as an important disease (Rakhshani et al. 2003). Parallel to these findings, other studies in India, Colombia, Uganda, and Nepal indicated that increasing the educational level is a protective factor for malaria morbidity (Shivalli et al. 2016; Forero et al. 2014; Musoke et al. 2018; Joshi and Banjara 2008). In this regard, it has been found that rural dwellers are less educated, and they may not be well aware of the causes, treatment, and control of malaria. Therefore, increasing the level of education can be considered as a preventive measure against malaria (Singh et al. 2017).

According to the results of this study, during the first year (2009), the malaria indigenous cases were 200, while in year 2018, with a drastic reduction of 100%, it reduced to zero. In agreement with this finding, no indigenous cases were reported in Iran in 2018 (WHO 2020; Vatandoost et al. 2019). Indigenous transmission, is considered as a big challenge for implementation of effective malaria elimination programs in malarious areas and malaria elimination involves interrupting indigenous transmission by active control measures (Wickremasinghe et al. 2014; Cohen et al. 2010; Smith et al. 2009).

According to the results of this study, malaria incidence has declined significantly and for the first time, in 2018, zero indigenous cases were reported from Bashagard County, which can be attributed to implementation of intense malaria control activities and close parasitological and entomological monitoring and surveillance. However, there is still possibility of malaria re-introduction in the county due to climatical and geographical conditions which facilitate the transmission of malaria. Moreover, the existence of nearby malaria-endemic countries such as Pakistan and Afghanistan and the possibility of imported cases from these countries remains a serious challenge for the malaria elimination in Bashagard County.

Conclusion

The incidence of malaria, especially indigenous cases, in Bashagard County has declined significantly in the past 10 years (2009–2018), especially after 2009 when Iranian government launched a national malaria elimination programme. Existing strategies and interventions must be continued to achieve the malaria elimination goal which is the absence of indigenous cases for at least 3 consecutive years in the country. In this regard it is necessary to implement an active surveillance system, multi-sectoral cooperation, and community mobilization, to detect and treat malaria cases quickly, during the elimination and post-elimination phases in the study area.

Acknowledgements

The authors of this article are grateful for the support of the director and the staff of Bashagard Health Center who cooperated and participated in this study.

Authors’ contributions

MZ drafted the manuscript. HF designed the study. SAJ coordinated in the field research activities and data collection. MSA and ASD designed the study, coordinated in field activity, collected data, trained field researcher and drafted the manuscript. All authors read and approved the final manuscript.

Funding

This research has been funded by the Research Deputy of Hormozgan University of Medical Sciences (Project No. 24/145).

Declaration

Conflict of interest

The authors declare that they have no competing interests.

Ethics approval and consent to participate

This study has been registered and approved by Hormozgan University of Medical Sciences Ethical Committee (Code No: IR.HUMS.REC.1397.398). Study registration date: Jan 20, 2020.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contributor Information

Mehdi Zare, Email: mzare56@gmail.com.

Hossein Farshidi, Email: hfarshidi6@gmail.com.

Moussa Soleimani-Ahmadi, Email: mussa.sahmadi@gmail.com.

Seyed Aghil Jaberhashemi, Email: jaberhashemi@gmail.com.

Alireza Sanei-Dehkordi, Email: alireza.sanee@gmail.com.

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