Iranian J Arthropod-Borne Dis, 2010, 4(1): 31–41 AA Hanafi-Bojd et al.: Malaria Situation Analysis…

Original Article Malaria Situation Analysis and Stratification in Abbas County, Southern , 2004–2008

*AA Hanafi-Bojd1, H Vatandoost1, E Philip2, E Stepanova3, AI Abdi4, R Safari5, GH Mohseni5, MI Bruhi6, A Peter7, SH Abdulrazag8, G Mangal9

1Department of Medical Entomology & Vector Control, School of Public Health, University of Medical Sciences, Iran 2Torit State hospital, Ministry of Health, Eastern Equatoria State, Government of South Sudan 3Martinoskvy Institute, Moscow, Russia 4Ministry of Health, Somalia 5Province Public Health Centre, Hormozgan University of Medical Sciences, , Iran 6Senior Evaluator of Malaria Control Program, SINDH province, Pakistan 7Acting Director General for Malaria Control Program, Upper Nile State- Malakal, State Ministry of Health,Government of South Sudan 8Ministry of Health, Republic of Sudan 9Health Center of Khost province, Afghanistan

(Received 5 Apr 2010; accepted 19 May 2010)

Abstract Background: The aim of this study was that the past five years data were collected to analyze the situation of ma- laria and health facilities in this area for better understanding malaria problem and to find solutions. Methods: In this retrospective study data of the last 5 years were obtained from health center of Bandar Abbas, pub- lished papers and reports, weather forecasting organization of the city and annual reports of Hormozgan official authorities. An excel databank was created and analysis was conducted using this software. Results: According to the national health system, Bandar Abbas also has referral net work system from periphery to the district health center. The maximum and minimum Annual Parasitic Index (API) were observed in 2005 (1.31) and 2008 (0.17), respectively. The prevalence of cases in villages was more than city, except for 2008. More than 97.6% of indigenous malaria cases were caused by Plasmodium vivax, although P. falciparum, P. ovale and mix infection were also reported. Anopheles stephensi, An. dthali and An. fluviatilis are the main malaria vectors in rural area, while only the first species is distributed in the . Conclusion: According to results and many variables including API, Bandar Abbas is divided in two strata. From the situation analysis of Bandar Abbas it is postulated that the main activities of this district could be accuracy of data, and malaria vector control.

Keywords: Malaria stratification, Iran Introduction Malaria disease is a worldwide prob- The disease is transmitted by a variety of lem that can be found in vast area of the female Anopheline mosquitoes (WHO 2009). world, where great portions of population are Iran is one of the countries that face at risk. Unfortunately number of people lost this problem. Before starting any malaria con- their live because of this disease, and still it trol program in Iran about 60% of population is one of the main problems in global health. of the country was living in endemic areas

*Corresponding Author: Mr Ahmad Ali Hanafi-Bojd, 31 E-mail: [email protected]

Iranian J Arthropod-Borne Dis, 2010, 4(1): 31–41 AA Hanafi-Bojd et al.: Malaria Situation Analysis…

with 30 to 40% malaria morbidity (Edrissian space of time and the health status, system 2006). Iran has been classified into four dif- and resource available for controlling the dis- ferent strata according to the epidemiology of ease. In succession to planning to go to the the disease (Raeisi et al. 2004). At present, district, there is need to use of the information malaria problem in Iran is mostly concen- that is already available and analyzing in such a trated in southern part. More than 90% of way to understand the problems. The main cases are reported from Sistan and Baluchis- objective of the situational analysis is to col- tan, and Hormozgan Provinces in lect the data from respective references such south-east of the Country (Moosa-Kazemi et as: health network office, hospital, health cen- al. 2007). It is unstable with two seasonal ters, communities, metrology department and peaks mainly in spring and autumn. Outbreaks others for conducting anti-malarial measures. due to P. vivax usually occur after rainy Bandar Abbas is the most important season (Manouchehri et al. 1992). In this part seaport of Iran in northern part of the Persian of the country six anopheline mosquitoes Gulf. This city has thousands of passengers including Anopheles culicifacies, An. stephensi, from different parts of Iran, as well as ship- An. dthali, An. fluviatilis, An. superpictus are men and immigrants from malarious areas of known proven vectors. Anopheles pulcherri- different countries. Regarding to favorable con- mus was mentioned as suspected malaria ditions for malaria transmission, the city can vector (Jalali-Moslem 1956, Manouchehri et be an important focus for the disease in al. 1972, Eshghi et al. 1976, Manouchehri et . The aim of this study was that al. 1992, Zahirnia et al. 2001, Edrissian 2006). the past five years data were collected to ana- The national strategy on malaria was revised lyze the situation of malaria and health facili- in 2006, with the goal of eliminating of Plas- ties in this area for better understanding ma- modium falciparum malaria in 3–4 yr and laria problem and to find solutions. only introduced cases of P. falciparum might occur, further reducing the number of auto- Materials and Methods chthonous P. vivax malaria in a period of 7 yr. In the third stage of the new strategy, the Study area objective will be a drastic reduction of local covers an area of transmission of P. vivax in the residual and 71139.62 km2. It is located in south of Iran active malaria foci. At the end of the third and north of the . Bandar Abbas stage only 500–700 autochthonous cases could is the of the province. It is lo- be reported in the country per year. cated in southern part of this province be- Reported studies in 2008 show that out tween 54o 53’–56 o 03’ E and 26 o 53’–27 of 11460 malaria cases of Iran, 8% was due o31’ N on flat ground with an average alti- to P. falciparum, while 90% were infected tude of 9 m above sea level. The nearest ele- by P. vivax (Minsitry of Health 2008). In vated area is Geno Mountain, 17 km north of WHO malaria report 2009, Iran showed evi- Bandar Abbas. The city has a hot and humid dence of a sustained decrease in the number climate. Maximum temperature in summers of cases associated with wide scale implemen- can reach up to 49° C while in winters the tation of malaria control activities. This country minimum temperature drops to about 5° C. is classified as in the pre-elimination stage The average of total annual rainfall was 118.44 (WHO 2009). mm during 2004–2008 and the mean annual The aim of conducting a situational ana- relative humidity was 63.4% (www.weather.ir). lysis is to systematically understand the ma- In 2008 total population was 521657, from laria epidemiology of an area in a very short which 47% female and 53% male. About 77%

32 Iranian J Arthropod-Borne Dis, 2010, 4(1): 31–41 AA Hanafi-Bojd et al.: Malaria Situation Analysis…

of population of this district is living in ur- coming from rural areas and from other coun- ban area and 23% in rural area. Foreign po- tries such as Afghanistan and Pakistan, but pulation in this year was 15087 (Management in rural area most of cases are due to local and Programming Organization 2008). transmission. All these cases are diagnosed by taking blood and then examined microscopi- Data collection cally, and then reported and treated in the This study was a retrospective survey public centers. All these activities are free of conducted using data obtained from health net- charge. Usually the cases from the health house work of Bandar Abbas, as well as published reach the health centers within same day and documents on weather, population, history of about 80% of slide positive cases (slide ex- malaria and previous studies on malaria in amination take less 30 min) get treatment this area. The data bank was created in Excel within 24 h according to national guideline. In software. Situation analysis and stratification those areas which are not covered by primary was conducted based on the obtained data. health care system, the anti-malaria activities carried by mobile team. The private sectors Results can investigate the cases but should refer them to the public sectors for treatment. Bandar Health system and general health profile Abbas is divided into 19 areas for malaria Health care and public health services detection and treatment (Fig. 1). in Iran are provided through a national wide During 2004–2008 a total of 1519 cases net. This network consists of a referral system were reported to be positive out of 140620 starting from primary care center in the pe- taken slides (Table 2). Most of cases were riphery going through secondary hospital in Iranian (79.3%). The disease morbidity in- the capital and tertiary hospital in major cities. creased up to 2005 and after that had a de- The public sector provide primary, secon- creasing trend to 2008. Plasmodium vivax dary and tertiary health services and some of was the main causative agent of malaria in these services such as prenatal care and vac- Bandar Abbas (97.69%), followed by P. fal- cination are free of charge (Table 1). The ciparum (2.17%). There was also one mixed private sector plays a significant role in the infection case and a report of malaria due to health care focused on secondary and tertiary P. ovale detected in an African football player health care in urban areas. There are also came to Bandar Abbas in 2008. Cases re- many non-governmental organizations acting in ported in rural area of Bandar Abbas (64.3%) health issue in Iran. They provide activities were more than urban area (35.7%). Most of in special field like children with cancer, dia- cases (70.7%) had over 14 yr old. Males betes and thalassemia. (64.5%) were infected more than females There is one university for medical (35.5%). The transmission season was mainly sciences education in Bandar Abbas and health between April and November (Fig. 2). network is working under vice chancellor for health. Bandar Abbas health facilities during Vectors our study period are showed in Table 1 (Man- Previous studies in the area show that agement and Programming Organization Hormozgan Province has five Anopheles vec- 2004-2008). tor species, the most important of them are Anopheles stephensi, An. fluviatilis and An. Malaria situation dthali. Cases: Based on our findings the ma- Anopheles stephensi is the main malaria laria cases in Bandar Abbas City are mainly vector in Bandar Abbas region, mainly can be

33 Iranian J Arthropod-Borne Dis, 2010, 4(1): 31–41 AA Hanafi-Bojd et al.: Malaria Situation Analysis…

found in south urban part, flat and the coastal Anopheles fluviatilis is also secondary areas. It considers being endophilic, but biting vector with An. dthali, distributed in moun- outdoor during summer months. Its seasonal tainous area from the east to west of Hor- activity started at beginning of May reach the mozgan Province. This species is exophilic, peak in August and gradually decrease up to exophagic and zoophilic (Naddaf et al. 2003) December in the mountainous area, but in with larval habitat in slow moving water on the coastal areas it is active all the year with margin of river, stream with or without ve- two peaks one in the April–May and second getation with high dissolved oxygen and pits in the August up to September (Manouchehri around springs. The biting of this species on et al. 1976a). Another study reported the human bait started from 18.00 h and contin- peak of activity in September in mountain- ued until 04.00 h, but most of bites on human ous and October in coastal regions. This spe- and cow bait took place in the first half of cies is absent during the cold winter months, the night, and there was no bite after 04.00 h but has high density during spring and au- (Manouchehri et al. 1975a). Seasonal activ- tumn in mountainous and coastal region, re- ity of An. fluviatilis showed two peaks in spectively (Vatandoost et al. 2006). The larva November and May. This species was active can be found in different bodies of water. In throughout the night with one peak of blood rural areas, it is found in pool streambeds at meal, 22:00–23:00 h on animal and 24:00– the margin of the streams, in the seepage and 01:00 h on human (Edalat and Moosa-Kazemi marshy area with gentle flow water, animal 2005). Sporozoite rate of this species is re- hoof print, and around the seepage marsh ported between 1.7–11% in south of Iran area (Vatandoost et al. 2004, Vatandoost et (Eshghi et al. 1976). al. 2006). Sporozoite rates for An. stephensi were reported 0.2–1.8% from southern part Vector control of Iran (Jalali-Moslem 1956). The past program for malaria eradica- Anopheles dthali plays a secondary tion in Iran was based on vector control us- role as malaria vector in Bandar Abbas after ing very large quantities of DDT started in An. stephensi. It is found mainly in Siahoo 1949 which resulted in dramatic reduction in mountainous area, north of Bandar Abbas malaria incidence. Vector population recovery city. This Anopheles has two peaks of activ- happens mainly due to resistant to DDT in ity during autumn (December-February) and Anopheles stephensi as well as DDT lack of absent during cold winter and hot weather selectivity affecting target population of mos- (June-August). The mosquito is resting outdoor quito (Edrissian 2006). Therefore, other in- in animal house as well as human dwelling secticide belongs to organophosphate, orga- (Vatandoost et al. 2007). In rural area of Bandar nochlorine, carbamate and pyrethroid were Abbas, the anthropophilic index and sporo- used in following years. However, extensive zoite rate in salivary glands for this species is use of chemical insecticides against mosquito reported 25% and 1.4%, respectively (Manou- vectors for about four decades has resulted chehri et al. 1972). in resistance to DDT, dieldrin and malathion The larvae of An. dthali are found in (Maouchehri et al. 1992, Edrissian 2006). mineral water in high salinity with tempera- Susceptibility tests of insecticides against adult ture of 13–28o C and pH of 6.9–8. The larva mosquitoes using standard impregnated pa- is most abundant in September and October pers provided by WHO showed An. ste- which is the end of hot season in Bandar phensi was resistance to DDT, dieldrin and Abbas (Vatandoost et al. 2007). malathion, while An. dthali and An. fluviatilis

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are susceptible (Mofidi et al. 1958, Mofidi et al. 1960; Manouchehri et al. 1975b, Manouche- Treated mosquito nets were used in May hri et al. 1976b, Vatandoost 2004; Vatan- 2005 as ITNs when epidemic started in the doost and Vaziri 2004; Vatandoost and area, but now LLITNs are using (personal Borhani 2004; Vatandoost et al. 2005). In re- communications). They are distributed accord- cent studies, it was found that the field sam- ing to the following priorities: Villages with- ples of An. stephensi from Bandar Abbas out electricity, active foci and high popula- were resistant to DDT, dieldrin and fipronil, tion movement; villages with electricity, ac- and susceptible to other insecticides includ- tive foci and high population movement; vil- ing malathion in Bandar Abbas (Davari et al. lages with only one of the above mentioned 2006, Vatandoost et al. 2006,). There is also factors; villages without electricity. a newly report of tolerance to DDT and diel- Larviciding using B. thuringiensis is drin from (Abai et al. 2008). another vector control measure in the area. It Study on susceptibility status on An. fluviatilis is also limited to the infected villages of moun- to diagnostic dose of 10 insecticides includ- tainous area, north of Bandar Abbas. In addi- ing DDT 4%, dieldrin 4%, malathion 5%, feni- tion some other measures are conducted for trothion 1%, propoxour 0.1%, bendiocarb larval control. 0.1%, permethrin 0.75%, deltamethrin 0.05%, lambda-cyhalothrin 0.05% and cyfluthrin 0.15% Treatment and drug resistance showed 100% mortality in all tests (Shahi et In Iran there is no recommended policy al. 2006). Evaluation of standard solutions of for chemoprophylaxis to the pregnant women 5 larvicides against these 3 species from Ban- and travelers. Quinine, chloroquine, fansidar, dar Abbas showed they were susceptible (Va- primaquine, artesunate, clindamycin, doxycy- tandoost et al. 2004, Vatandoost and Hanafi- chline and coartem are recommended for ma- Bojd 2005, Hanafi-Bojd et al. 2006). laria treatment in Iran. They are used in dif- Now the main measures in Iran for ferent combinations based on severity of the malaria vector control are: Indoor residual disease, age of patient and Plasmodium type. spraying using Lambda-cyhalothrin WP 10% There is also special recommendation for preg- and deltamethrin WP 10% in malarious areas, nant women (Saebi et al. 2006). larviciding by Chlorpyrifos-methyl, Bacillus Several studies were carried out on drug thuringiensis and some larvivorous fish like resistant in the southern part of Iran. The Aphanius dispar and Gambusia affinis and results of studies during 1968–1976 (Manou- distributing LLINTs. At present, B. thuringien- chehri et al. 1973, Sutoso et al. 1978) by In sis and larvivorous fish are using for lar- vivo test showed that P. falciparum was viciding in the area as well as impregnated sensitive to chloroquine, but in 1983 (Edris- mosquito nets. This measure have been wel- sian et al. 1985) In vivo and In vitro tests comed by people at various level, it was been show chloroquine resistant with rate of 5.1% introduced in 2003 as ITNs and nowadays which increased to 51.1% by 1996 (Edris- LLITNs are used in malarious areas of Iran sian et al. 1999). This rate in Bandar Abbas (Moosa-Kazemi et al. 2007). was 32.5% in 1986, 64.8% in 1994–1996 In Bandar Abbas district, the main and 68% to 84% by 1997 (Edrissian 2006). measures for vector control are Indoor Residual Spraying (IRS), larviciding and LLITNs. Dur- ing the period of our study, the vector control activity was restricted to some villages of mountainous area.

35 Iranian J Arthropod-Borne Dis, 2010, 4(1): 31–41 AA Hanafi-Bojd et al.: Malaria Situation Analysis…

Table 1. Health facilities in Bandar Abbas, 2004–2008, Bandar Abbas County

Health facilities 2004 2005 2006 2007 2008 Teaching hospitals 2 4 4 4 4 Total district hospitals 11 10 10 10 11 Private hospitals 7 6 6 6 7 Governmental hospitals 4 4 4 4 4 Urban health centers, polyclinics 54 58 66 73 66 Rural health centers 21 21 17 23 19 Health houses 128 131 106 106 107 Laboratories 33 33 36 37 39 Pharmacies 36 32 42 45 46

Table 2. Malaria information in Bandar Abbas County, Hormozgan Province, 2004–2008, Bandar Abbas County At risk population population risk At Nationality Sex Age groups Species Re-checked slides Residence place Positive fromPositive Total slides slides Total Total cases cases Total re-checked P. falciparum Non-Iranian Non-Iranian ABER ABER Years SPR SPR P. ovale ovale P. P. vivax vivax P. Iranian API Female Female Male Male 5-14 5-14 Mix 14< 14< <5 <5 City Village

2004 453658 160 147 243 64 7 60 240 309 1 0 0 41174 307 0.68 0.75 9.07 21414 28 147 160 2005 471816 556 64 362 258 28 166 426 609 11 0 0 34462 620 1.31 1.79 7.30 15465 26 164 456 2006 479040 355 30 213 172 35 118 232 378 7 0 0 27819 385 0.8 1.38 5.80 9203 17 110 275 2007 514450 95 24 81 38 4 20 95 116 3 0 0 17247 119 0.23 0.68 3.35 15078 32 53 66 2008 521657 38 50 81 7 3 4 81 75 11 1 1 19918 88 0.17 0.44 3.81 13260 11 68 20 Total -- 1204 315 980 539 77 368 1074 1484 33 1 1 140620 1519 -- 1.08 -- 74420 114 542 977

API = Annual parasite incidence, SPR = Slide positive rate, ABER = Annual blood examination rate

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Table 3. Stratification of malaria in Bandar Abbas, Hormozgan Province, Iran 2004–2008, Bandar Abbas County

Variables Stratum I Stratum II Geography Mountainous Coastal Vector An. stephensi An. dthali, An. fluviatilis Mostly An. stephensi Water source Pools, rivers, and containers Water pipe, rivers, swage Population movement No Present People behavior during transmission season Sleeping out side Sleeping in side API 1%< <0.5%

Fig. 1. Malaria registration centers of Bandar Abbas, Hormozgan Province, Iran, Bandar Abbas County

Fig. 2. Malaria cases in different months of year during 2004–2008, Bandar Abbas, Hormozgan Province, Iran

37 Iranian J Arthropod-Borne Dis, 2010, 4(1): 31–41 AA Hanafi-Bojd et al.: Malaria Situation Analysis…

Fig. 3. Malaria stratification in Bandar Abbas, Hormozgan Province , Iran 2004–2008, Bandar Abbas County

Discussion careless may be due to case reduction in pre- There was no considerable change in vious years as well as poor entomological the number of health facilities during the study data. After this epidemic, different control ac- period (Table 1). The reduction of health tivities such as LLINTs, IRS and larviciding houses that are the first step of the referral were strengthened parallel to case detection system is due to newly geographical changes and treatment resulted to drop positive cases that pass them to neighbor cities. There was in the area, so that in 2008 the local trans- a dramatic increase in malaria cases of 2005 mission that usually occurs in rural area was compared to 2004. As showed in Table 2, about one third of reported cases in urban during 2005–2006 the cases in rural area area. Reports of health services showed most were more than two times higher than urban of cases in Bandar Abbas City in this year areas. There is a limited population movement were imported. in the rural area, so this epidemic occurred Major determinates of malaria stratifica- due to local transmission and this is attrib- tion in Bandar Abbas were: geography, vec- uted to the weakness of surveillance system tor, water sources, population movement, peo- in that years. As it can be seen in Table 2, ple behavior and API. Stratification is done the total slides taken decrease year by year. based on the above determinates which are Also the amount of insecticides used during illustrated in table 3 and fig 3. So Bandar epidemic was very limited, e.g. only 400 kg Abbas were divided into two strata. of pyrethroid insecticides and 510 kg Bacil- From the situation analysis of Bandar lus thuringiensis as larvicide were applied Abbas we found the main problems of this during the epidemic of 2005 (Management and township are: inaccuracy of data and malaria Programming Organization 2005), and the vector control activities. For elimination of ma- control program started after the first peak of laria in Bandar Abbas it is suggested to do the disease. We found that the entomological the following activities: Proper case manage- data in the area are poor and not enough and ment by early detection and prompt treatment, reliable for designing a control program. This routine evaluation of drug resistance, biweekly 38 Iranian J Arthropod-Borne Dis, 2010, 4(1): 31–41 AA Hanafi-Bojd et al.: Malaria Situation Analysis…

entomological survey during the transmission ing. The authors declare that they have no con- season in the high risk area, annual survey flicts of interest. on susceptibility status of vectors to insecti- cides/larvicides, free distribution of the LLITNs References to at risk groups including travelers and refu- gees, improving of housing condition at the Abai MR, Mehravaran A, Vatandoost H, rural areas, conducting training for entomo- Oshaghi MA, Javadian E, Mashayekhi logical survey as larvicidal personnel, spray- M, Mosleminia A, Piyazak N, Edallat ing workers and response team for epidem- H, Mohtarami F, Jabbari H, Rafi F ics, treatment of breeding site by effective (2008) Comparative performance of ima- larvicides and biological measures, participa- gicides on Anopheles stephensi, main ma- tion of school children and community in en- laria vector in a malarious area, southern vironmental management by drainage and fi- Iran. J Vector Borne Dis. 45(4): 307–312. lling the major mosquito sources and small Davarai B, Vatandoost H, Ladonni H, water resources, site selection (establishment Shaeghi M, Oshaghi MA, Basseri HR, of population away from reach of mosquitoes) Enayati AA, Rassi Y, Abai MR, Hanafi- and introduce of animal shelter between breed- Bojd AA, Akbarzadeh K (2006) Com- ing site and human houses for exophilic mos- parative efficacy of different imagicides quitoes, personal protection using insect re- against different strains of Anopheles ste- pellents, early detection of epidemics and im- phensi in the malarious areas of Iran, provement of data collection, training of staff 2004-2005. Pakistan J Biolog Sci. 9(5): on computerization, data collection and excel 885–892. management for updating malaria database, Edalat H, Moosa-Kazemi SH (2005) Ecol- study the health aspect of any project by ogy of Anopheles fluviatilis, the main health authorities and anti malaria services and malaria vector in southern part of Iran, seek assistant to investigate advantages and and its role in the epidemiology of ma- benefits, evaluation of knowledge, attitude and laria. Proceedings of the Fifth Interna- practice of people in high risk area by KAP tional Conference on Urban Pests, 2005 study, and training though mass media (TV, July 10-13, Singapore, pp. 503–504. radio) and leadership (community leaders, Edrissian GH (2006) Malaria past and pre- schools, religious leaders). sent situation in Iran. Iranian J Parasi- tol. 1(1): 1–14. Eshghi N, Motabar M, Javadian E, Ma- Acknowledgements nouchehri AV (1976) Biological fea- This study is result of teamwork and tures of Anopheles fluviatilis and its field exercise study on malaria situation analy- role in the transmission of malaria in sis and stratification, in the 12th International Iran. Trop Geog Med. 28: 41–44. Diploma Course on Malaria Planning and Man- Jalali-Moslem G (1956) History of malaria agement, conducted during November 2009- and its control in Iran until 1955. Insti- January 2010 in WHO Regional Malaria Train- tute of Parasitology and Malariology, Te- ing Centre in Bandar Abbas, Southern Iran. hran University, Tehran, Iran. Publ No. We are thankful from the staff of this centre. 225: 82–92. We would like to thank Dr Masoodi, the di- Hanafi-Bojd AA, Vatandoost H, Jafari R rector and Ms M Mehranzadeh the focal ma- (2006) Susceptibility status of Anophe- laria person in Bandar Abbas health center les dthali and An. fluviatilis to commonly for their kind collaboration and data provid- used larvicides in an endemic focus of

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