EMHJ • Vol. 22 No. 4 • 2016 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale

Report Control of malaria outbreak due to Plasmodium vivax in Governorate, A. Kandeel,1 A.A. Haggag,1 M. Abo El Fetouh,1 M. Naiel,1 S.A. Refaey, 1 A.H. Hassan 2 and R.M.R. Ramzy 3

مكافحة وباء املالريا الذي سببه "بالزموديم فيفاكس يف" حمافظة أسوان بمرص عمرو قنديل، آيات حجاج، مريم أبو الفتوح، حممد نايل، سمري رفاعي، أمحد حسن، رضا رمزي اخلالصــة: : يف عــام 2014- وبعــد عــدة ســنوات مــن احلفــاظ عــى الصفــر مــن حــاالت املالريــا الواطنــة - شــهدت مــر وبــاء "للبالزموديــم فيفاكــس": 21 حالــة مؤكــدة خــالل شــهري مايو/أيــار ويونيو/حزيــران مــن عــام 2014. فقامــت وزارة الصحــة والســكان – ًتصديــا منهــا هلــذا الوبــاء - بإطــالق اســتجابة طارئــة مــن خــالل اكتشــاف احلــاالت ًباكــرا ومعاجلتهــا ًفــورا، ومكافحــة النواقــل، وتثقيــف اجلمهــور، والتعــاون بــن القطاعــات. لقــد وجــد أن عرشيــن حالــة )%2. ( 95مــن ســكان قريــة الشــيخ مصطفــى بمنطقــة إدفــو يف حمافظــة أســوان جنــوب مــر. وقــد تــم التعــرف عــى مجيــع احلــاالت التــي تعقــب احلالــة الدالــة مــن خــالل زيــارات ترصــد مــن منــزل إىل منــزل. كــا تــم التعــرف يف نفــس القريــة عــى " " حالــة واحــدة مصابــة بعــدوى البالزموديــوم فالســيبارم . ُوبــدئ بمعاجلــة مجيــع احلــاالت املصابــة بالعــدوى عقــب تأكيدهــا ًخمتربيــا. إن تصــدي وزارة الصحــة والســكان الرسيــع واحتــواء الوبــاء يثبــت القــدرة املؤسســية عــى اكتشــاف حــاالت املالريــا وتأكيدهــا ومعاجلتهــا، وعــى مكافحــة األوبئــة التــي يمكــن أن حتــدث بعــد التخلــص مــن املــرض.

ABSTRACT In 2014, after several years of maintaining zero malaria indigenous cases, Egypt had an outbreak of Plasmodium vivax: 21 confirmed cases during May-June 2014. In response to the outbreak, the Ministry of Health and Population (MoHP) launched an emergency response through early detection and prompt treatment of cases, vector control, public education and intersectoral collaboration. Twenty cases (95.2%) were residents of El-Sheikh Mostafa village, district, , southern Egypt. All cases, consequent to the index case were identified through house-to-house surveillance visits. OneP. falciparum-infected case was also identified in the same village. Treatment of all infected cases was initiated following laboratory confirmation. The MoHP’s rapid response to and containment of the outbreak demonstrates the institutional capacity for detection and control of outbreaks which can occur after elimination.

Lutte contre une flambée de paludisme àPlasmodium vivax dans le Gouvernorat d’Assouan (Égypte)

Résumé En 2014, après s’être maintenue plusieurs années sans aucun cas autochtone de paludisme, l’Égypte a connu une flambée de Plasmodium vivax : 21 cas confirmés entre mai et juin 2014. En réponse à la flambée, le ministère égyptien de la Santé publique et de la Population a mis en place un plan d’urgence comprenant le dépistage précoce et le traitement rapide des cas, la lutte antivectorielle, la sensibilisation du public et la collaboration intersectorielle. Vingt de ces cas (95,2 %) se sont déclarés chez des résidents du village d’El-Sheikh Mostafa, dans la circonscription d’Edfou (Gouvernorat d’Assouan, au sud de l’Égypte). Suite au cas indicateur, la totalité des cas a été identifiée grâce aux visites de surveillance effectuées au porte-à-porte. Un cas d’infection à P. falciparum a également été identifié dans le même village. Après confirmation en laboratoire, le traitement de l’ensemble des cas infectés a été entrepris. La réponse rapide du ministère de la Santé publique et de la Population et l’endiguement de la flambée attestent de ses moyens institutionnels pour la détection, la confirmation et le traitement du paludisme, ainsi que la maîtrise des flambées susceptibles de survenir après l’élimination de la maladie.

1Ministry of Health and Population, , Egypt. 2Research Institute of Medical Entomology, General Organization for Teaching Hospitals and Institutes, Cairo, Egypt. 3National Nutrition Institute, General Organization for Teaching Hospitals and Institutes, Cairo, Egypt (Correspondence to R.M.R. Ramzy: [email protected]). Received: 09/06/15; accepted: 09/06/16

274 املجلة الصحية لرشق املتوسط املجلد الثاين و العرشون العدد الرابع

Introduction the achievement of malaria elimina- searched for all the contacts, who had tion and enormous efforts should be blood taken for malaria screening. Egypt has achieved a steady decline in directed towards controlling them. Subsequent screening involved ex- malaria transmission over the past dec- This article describes an outbreak amination of those were not present ades. In 1989, Egypt was listed among which resulted in 21 cases of Plas- at the initial visit, and re-examination malaria-endemic countries with nation- modium vivax in Aswan governorate, of persons with fever and their con- wide malaria control programs (1). The Egypt between May and June 2014. tacts, including household members, disease control efforts were shared be- In particular, it describes the intensive neighbours, friends and associates who tween the Malaria Control Programme malaria control activities carried out by were likely to have a similar exposure. and the general health services based on the MoHP central officials and local This exercise involved two successive primary health care. In 1999, the Roll health authorities in the affected village screenings of 2 279 and 2 669 people. Back Malaria initiative was launched and its surroundings, and the outcomes. Furthermore, 2 116 randomly selected in the Eastern Mediterranean Region residents of six surrounding villages (2). Egypt was among the countries were interviewed and screened for ma- that updated its national strategies for Outbreak and response laria. The sample included 25 Sudanese malaria control and elimination accord- who were temporarily visiting or resid- ing to the objectives of the initiative. By On 26 May 2014 the first confirmed ing in the study villages. 2001, malaria was firmly under control, malaria case in Aswan governorate therefore, the Ministry of Health and was reported to the Preventive Sec- Case confirmation Population (MoHP) modified its goal tor, MoHP. The index case was a Malaria cases were confirmed on to elimination of malaria transmission male (37 years of age) from El-Sheikh laboratory diagnosis which was based through a strong, time-limited attack Mostafa village (24º 57' 52.2144" N on a rapid diagnostic test (RDT) and on residual foci according to Roll Back and 32º 54' 55.53" E) in Edfu district, microscopy for confirmation by identi- Malaria established principles of ma- located approximately 120 km north fication of the malaria species. The RDT laria eradication. During 2010–2013, of Aswan city. It had a population of (CareStart™ Malaria HRP2/pLDH Egypt successfully eliminated malaria approximately 4 600 inhabitants. On antigen test, produced by American (maintained zero indigenous cases), 28 May, the MoHP mounted an emer- Access Bio Company; batch number but remained in the stage of preven- gency response which included early MV14D02, period of validity to March tion of re-introduction of malaria (3). case identification, prompt treatment, 2016) was used as a primary screen- In fact, the country has had reports of vector control, public education and ing test. For each RDT-positive case or introduced cases or limited outbreaks of intersectoral collaboration for environ- suspected case based on recent history indigenous cases (4). One of the major mental manipulation. The overall co- of fever, thick and thin blood smears challenges in controlling malaria is the ordination of the response was carried were prepared. Thick films were exam- re-introduction of the infection due to out by a mission from the Preventive ined by two observers and the malaria international travel and cross-border Sector MoHP. species was confirmed by an additional population movement from malaria- experienced technician. endemic countries (5). Mobilization of surveillance Prompt treatment Re-introduction of malaria (or small teams for early case identification outbreaks) has occurred in some East- Malaria-confirmed cases were treated ern Mediterranean Region countries During May–June, 2014, 20 surveil- at the Edfu Fever Hospital. P. vivax that have been free of malaria. For in- lance teams, each formed of 2 public infected cases were treated with Coar- stance, an imported case from Pakistan health workers and 2 laboratory techni- tem (20 mg artemether and 120 mg resulted in a small outbreak (30 cases cians, visited all houses in El-Sheikh lumefantrine), twice a day with a meal of vivax malaria) in Jordan during 1990 Mostafa village and interviewed 3 409 for 3 days (6 doses). On the fourth day (6). In 1998, due to Somali refugees, a households. Data were collected on and onwards for 14 days, after the blood small outbreak (21 cases of falciparum residents with fever or recent history of film became negative for malaria, Pri- malaria) occurred in Oman which had fever (in the previous 3 days) and their maquine (0.25 mg⁄ kg) single dose was been free of falciparum malaria (but blood was screened for malaria. Teams administered. TheP. falciparum infected not vivax) (6). Also, in Lebanon 2 small were also charged to take a meticulous case was treated similarly with Coartem. outbreaks of vivax malaria occurred dur- case history with a detailed travel his- Laboratory reassessments were ing 1997–1998 (6). Malaria outbreaks tory from all confirmed cases and elicit made on days 1, 2 and 3 post Coar- represent a clear threat to maintaining names of their contacts. The teams then tem treatment, before subjects were

275 EMHJ • Vol. 22 No. 4 • 2016 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale

discharged from the hospital, and then as their breeding sites in Edfu district. creating mosquito breeding sites, were weekly for the remainder of the follow- Two additional geographically adjacent found in Edfu district. These are breed- up period (i.e. on days 7, 14, 21 and districts (, governorate and ing sites where larvicide application is 28). Patients were advised to return on , Aswan governorate) were not effective. Therefore, in collaboration any day during the follow-up period if surveyed to determine the distribution with the Ministry of Environment, the symptoms returned and not to wait for of anopheles malaria vector mosquitoes. borrow-pits were filled with soil and the scheduled visit. Anopheles sergentii has been recorded as covered with earth. a malaria vector in the southern part Public education and of the Valley, Egypt (7). Detec- community mobilization tion of anopheles vector was followed Outcomes Several training sessions for local health by systematic application of different Identification and treatment workers were conducted to ensure interventions in combination and in that they carried out their tasks cor- synergy with each other. Application of A total of 1 436 houses were visited rectly. In addition, health workers were chemical methods for vector control, from 26 May to 14 June during the equipped with necessary information which included larviciding and adul- community surveillance, 12 938 peo- on malaria to deliver to communities ticiding, indoor residual spraying and ple were interviewed and 164 fever during the field surveys. This included space spraying, conformed to WHO cases were identified and referred correct knowledge of causes (mosquito guidelines (8). to Edfu Fever Hospital. Of these, 21 transmission) and symptoms of malaria A total of seven sanitary teams were (12.8%) cases of vivax malaria were (high fever most frequently with peaks formed. Of these, four were assigned confirmed on laboratory diagnosis every 2–3 days, generally with chills to work in Edfu district, two in Kom (Figure 1). While 20 P. vivax infected and strong headache), use of indoor Ombo and one in Esna. A team was cases were from El-Sheikh Mostafa residual spraying for vector control, composed of a supervisor, six sanitary village, 1 (male, 23 years of age) was and availability of free diagnosis and inspectors, five health workers and a from a surrounding village (Om treatment services. Training sessions malaria prevention worker. Entomo- Salama village). Figure 2 shows the included health workers in the rural logical surveillance and vector control distribution of malaria cases as plotted health centre of El-Sheikh Mostafa vil- activities were implemented in affected on an aerial imagery of El-Sheikh Mo- lage as well as male and female health areas as appropriate. To support vector stafa village created by Google Earth care providers recruited from 28 other control activities, an entomology labo- program A P. falciparum infected case rural health centres in Edfu district. ratory was set up at the premises of the (a female of about 90 years of age) Malaria posters in Arabic were posted Edfu Central Hospital. The laboratory was coincidentally identified upon at points of maximum visibility in the was equipped to support assessment of screening a randomly selected sample rural health centres and hospitals. Simi- mosquito density, mosquito examina- from villages surrounding El-Sheikh larly, pamphlets, brochures, fliers and tion and identification of wild caught Mostafa village. She had no malaria fact sheets in Arabic were distributed mosquitoes. signs or symptoms and was not able by health workers. To further raise the to confirm previous infection or treat- awareness in Edfu district communi- Intersectoral collaboration for ment of malaria. All infected subjects ties, physicians and trained health care environmental management were treated and discharged from the providers conducted several meetings Environmental management as a Edfu Fever Hospital. None of the cases with community leaders and other "in- means for eliminating or destroying had any complications and the last fluential" residents at all levels including mosquito breeding sites was carried case had onset of symptoms on 14 local authorities, school teachers and out in collaboration with the Ministry June 2014 and was discharged on 1 religious leaders. Television interviews of Agriculture and Ministry of Environ- July 2014. The ages ranged from 6 to and short advertising programmes were ment. Environmental management or 90 years and 11 were males (Table broadcast to cover Aswan and other manipulation to destroy breeding sites 1). All cases were discharged from the southern governorates through a local included increasing water flow in irriga- fever hospital after successive negative television station. tion drainage canals by mechanical re- blood films in 4 consecutive days. moval of weeds and other vegetation as Vector control well as making their shorelines steeper Vector control The vector control plan included identi- to reduce shallow spaces suitable for Investigations of malaria vector in fication of the anopheles vector species, mosquito breeding. Several borrow-pits Edfu district included an area of 38 their distribution and densities as well filled with ground water and bushes, km2 and 16 villages. Adult and aquatic

276 املجلة الصحية لرشق املتوسط املجلد الثاين و العرشون العدد الرابع

5

4

3 No. of cases 2

1

0

Date

Figure 1 Confirmed cases ofPlasmodium vivax malaria in Edfu, Aswan by date of onset, May–June 2014

stages of Anopheles spp. were collected borrow-pits of about 5 feddans in area Discussion in several localities. Of the fifteen grids (approximately 2 hectares) and 2 of 2.5 in Edfu district, An. sergentii breed- feddans] filled with ground water and Reported data clearly demonstrate that ing sites were identified in 6, mostly bushes sheltering An. sergentii aquatic the health system in Egypt was quick in irrigation canals and drainage ca- stages were identified around El-Sheikh and effective in responding to the ma- nals around affected communities. Mostafa village. To eliminate the breed- laria outbreak during May–June 2014 Out of 41 and 13 areas investigated ing sites, about 90% of the borrow-pits in Aswan governorate. By the end of in Kom Embo and Esna districts, were filled with soil and covered with June, 2014, the last case was cured and respectively, one area (2.4%) and earth. discharged from the Edfu Fever Hospi- three areas (23.0%) were identified An average of 70–75 adult Anoph- tal. Since then (almost a two years now) with An. sergentii breeding sites. On eles spp. was collected per day using the no malaria case has been diagnosed, 1 June, before any corrective action different collection methods, before the indicating success in controlling the was taken, about 100 mosquito larvae application of adulticiding measures. outbreak. The early case identification were collected per collection station Of these, 20% were identified asAn. strategy employed by the MoHP of in the breeding sites. Of these, about sergentii. Indoor residual insecticide screening contacts and other commu- 20% were identified asAn. sergentii. spraying was used to control adult An. nity members resulted in the identifica- Larvicidal treatment was applied to sergentii. Two types of indoor residual tion of 28.6% of the malaria cases. all water bodies where Anopheles spp. insecticide spraying were applied in were identified and by 8 June 8 and a total of 1 436 houses in El-Sheikh Several factors contributed signifi- onwards, no mosquito larvae could Mostafa village. The walls of 4 704 cantly to the success in controlling the be detected. rooms were painted with indoor re- malaria outbreak. These included dis- A total of 27 irrigation drainage ca- sidual insecticide. In addition, space semination of information to medical nals (each of about 6 km) were cleaned spraying was applied daily before sunset and paramedical staff on malaria status to remove vegetation and improve wa- in all affected communities. Following in affected areas and enhancement of ter movement as a means to destroy such activities, very few adult anopheles malaria awareness among the at-risk breeding sites. This was followed by mosquitoes were collected by 7 June population. Access to free laboratory larvicidal treatment. Six borrow-pits [4 and onwards. diagnosis and treatment was a key issue,

277 EMHJ • Vol. 22 No. 4 • 2016 Eastern Mediterranean Health Journal La Revue de Santé de la Méditerranée orientale

Plasmodium vivax P. falciparum

Health care facility Borrow-pits filled with ground water

Figure 2 Aerial image of El-Sheikh Mostafa village showing the distribution of the malaria cases: created by Google Earth program

particularly for the affected communi- lead to the build-up of insecticide resist- detected by RDT and confirmed by ties who are already socioeconomically ance. It is worth noting that extensive blood smear microscopy. Neither the compromised. These were coupled with efforts by and tremendous resources duration of the infection nor the time of implementation of vector control meas- from MoHP, Ministry of Agriculture previous malaria treatment, if any, could ures aimed at effectively reducing aquat- and Ministry of Environment were re- be verified. Detection of asymptomatic ic stages and adult vector populations quired to control this malaria outbreak. carriers of P. falciparum parasites has and hence malaria transmission. The The coincidental detection of the P. been previously reported (9). Malaria implemented vector control measures falciparum case is of interest. An asymp- infections have been detected in sub- avoided the repeated use of the same tomatic old lady residing in El Fawzah jects after 8–9 years of leaving endemic class of insecticides or insecticides with village (approximately 5 km south- areas (10,11). The time interval from similar modes of action which could west of El-Sheikh Mostafa village) was last possible exposure to malaria and the

Table 1 Age and gender distribution of malaria cases in Edfu district, Aswan governorate, 2014 Age group (years) Males Females Total No. No. No. ≤ 10 1 3 4 11–20 7 3 10 21–30 2 1 3 31–40 1 2 3 41–50 – 1 1 > 50 – 1a 1 Total 11 11 22

aPlasmodium falciparum case.

278 املجلة الصحية لرشق املتوسط املجلد الثاين و العرشون العدد الرابع

accidental diagnosis of the infection has Some residents of Edfu villages have re- Acknowledgements been as long as 13 years (9). Such a find- ported illegal Sudanese border crossing ing highlights the need for improved to teach locals gold mining. Such activity We thank the field teams of the Vector high throughput and low-cost methods would result in the formation of more Control Department, Malaria Control to detect these individuals, probably mosquito breeding places. Department, Surveillance Unit, Com- harbouring low parasite densities. Egypt has achieved malaria elimi- municable Diseases Department, One piece of information lacking on nation (maintained zero indigenous MoHP, the Edfu Fever Hospital, the outbreak is that we have no solid cases) for several years and succeeded Aswan, and the staff of the Research explanation of how the outbreak started. in the containment of the last outbreak. Institute of Medical Entomology for It probably started through illegal cross- However, this does not exclude the pos- their technical assistance. Our thanks border movement of individuals between sibility of re-introduction of malaria to are extended to the Aswan Health Aswan governorate and . However, the country again. Therefore, there is a Directorate, the Edfu Health District none of the malaria infected individuals great need for strengthening collabora- and the Gambia Control Department admitted recent travel to Sudan and all tion with the national services in Sudan in Aswan for their logistical support the Sudanese examined for malaria (n = in order to deal with immigration and when needed. All costs for contain- 25) were free of infection. Nonetheless, cross-border movement and suppress ment of the malaria outbreak were it is known that, locals cross the border the illegal movement of people across met by the MoHP. illegally all the time for different reasons. the border. Competing interests: None declared.

References

1. Consultation on epidemiological malaria information at na- 6. Guidelines on prevention of the reintroduction of malaria. tional and regional levels. Amman, Jordan, 25-30 November Cairo: WHO Regional Office for the Eastern Mediterranean; 1989 (http://applications.emro.who.int/docs/who_em_ 2007 (EMRO Technical Publications Series, 34). mal_217_e_en.pdf, accessed 1 April 2016) 7. Cope SE, Gad AM, Presley SM. New record of the malaria vec- 2. Report on the National Malaria Programme Managers' meet- tor Anopheles sergentii in the southern Nile Valley of Egypt. J ing on Roll Back Malaria (RBM). Damascus, Syrian Arab Am Mosq Control Assoc. 1995 Mar;11(1):145–6. PMID:7616183 Republic, 1–3 April 2001 (http://applications.emro.who.int/ 8. Pesticides and their application for the control of vectors and docs/who_em_mal_267_e_l_en_14389.pdf, accessed 1 April pests of public health importance. Sixth edition. Geneva: 2016). World Health Organization; 2006. 3. Report on the tenth intercountry meeting of national malaria 9. Ashley EA, White NJ. The duration of Plasmodium falciparum programme managers. Sharm El-Sheikh, Egypt 18–20 Febru- infections. Malar J. 2014 Dec 16;13:500. PMID: 25515943 ary 2013 (http://applications.emro.who.int/docs/IC_Meet_ 10. Szmitko PE, Kohn ML, Simor AE. Plasmodium falciparum ma- Rep_2013_EN_14905.pdf?ua=1, accessed 1 April 2016). laria occurring 8 years after leaving an endemic area. Diagn 4. Kenawy MA. Review of anopheles mosquitoes and malaria in Microbiol Infect Dis. 2009 Jan;63(1):105–7. PMID:18945569 ancient and modern Egypt. J Mosq Res. 2015;5(4):1–8. 11. Theunissen C, Janssens P, Demulder A, Nouboussié D, Van- 5. Zucker JR. Changing patterns of autochthonous malaria trans- Esbroeck M, Van-Gompel A, et al. Falciparum malaria in pa- mission in the United States: a review of recent outbreaks. tient 9 years after leaving malaria-endemic area. Emerg Infect Emerg Infect Dis. 1996 Jan-Mar;2(1):37–43. PMID:8964058 Dis. 2009 Jan;15(1):115–6. PMID:19116068

279