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Epidemiology of Imported Malaria in Netrokona District of Bangladesh 2013-2018: Analysis of Surveillance Data

Epidemiology of Imported Malaria in Netrokona District of Bangladesh 2013-2018: Analysis of... Hindawi Malaria Research and Treatment Volume 2019, Article ID 6780258, 9 pages https://doi.org/10.1155/2019/6780258 Research Article Epidemiology of Imported Malaria in Netrokona District of Bangladesh 2013-2018: Analysis of Surveillance Data 1 2 1 Md Abdul Karim , M. Moktadir Kabir, Md Ashraf Siddiqui , 1 3 1 Md Shahidul Islam Laskar , Anjan Saha , and Shamsun Naher Communicable Disease (Malaria) Programme, BRAC, Bangladesh Communicable Disease (Malaria) and Water Sanitation & Hygiene Programme, BRAC, Bangladesh National Malaria Elimination Programme, Bangladesh Correspondence should be addressed to Md Abdul Karim; karim.mis@gmail.com Received 29 November 2018; Revised 11 April 2019; Accepted 18 April 2019; Published 13 June 2019 Academic Editor: Sasithon Pukrittayakamee Copyright © 2019 Md Abdul Karim et al. is Th is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Introduction. Netrokona is one of the first phase malaria elimination targeted 8 districts of Bangladesh by 2021. The district constitutes only 7% of the population but contributes half of the malaria cases in that area. Most of the cases of that district are imported from Meghalaya State of India. The study was conducted to understand the epidemiology of these imported malaria cases for further strategy development to prevent both imported and introduced cases. Methodology. eTh study was retrospectively conducted on the malaria cases confirmed by microscopy and/or RDT by the government and/or NGO service providers between 2013 and 2018. The information of the cases was collected from the verbal “investigation” report of individual malaria confirmed cases. The respondents of the “investigation” were either the patients or their family members. Out of the 713 cases during the study period, descriptive analysis of 626 cases (based on the completeness of “investigation form”) of the district was done using MS Excel version 2016. Results. Proportion of imported malaria in Netrokona district increased from 60% in 2013 to 95% in 2018 which persists throughout the year with a little seasonal u fl ctuation. eTh overall contribution of these imported cases is 93% by cross-border workers by population type and 84%, 66%, and 95% by male, labour, and tribal population considering the factors of sex, occupation, and ethnicity, respectively. Population aged between 15 and 49 years contributed 82% of these imported cases. All of these cases occurred in the internationally bordering belt with Meghalaya State of India. Species-wise distribution revealed lower P. falciparum (63%) and higher mixed (28%) infection in imported cases compared to the 71% Pf and 20% mixed infection among the indigenous infections whereas P. vivax is similar in both cases. Conclusion. Imported malaria is an emerging issue that has a potential risk of increased local transmission which might be a challenge to malaria elimination in that area. Appropriate interventions targeting the cross-border workers are essential to prevent the introduced cases and subsequently avoid reestablishment when elimination of the disease is achieved. 1. Introduction of the disease through three phases: 2021, 2025, and 2030 [2] (Figure 1(a)). The north and northeast 8 districts of the Bangladesh is one of the 87 malaria endemic countries country are the rfi st phase malaria elimination targeted areas of the country by 2021 [2]. and territories of the world in 2017 [1]. Currently, a total population of 17.52 million in 13 bordering districts of the Netrokona is one of these rfi st phased malaria elimination country are at risk of the disease [2]. With the financial targeted districts of the country. The district is situated support from the Global Fund, the country intensified the in the northern part of Bangladesh. Out of the total 10 programme activities in partnership between government administrative upazilas (subdistrict), 2 upazilas (consisting and BRAC led NGO consortium and achieved remarkable of 15 unions) with internationally bordering with Meghalaya reduction of malaria burden in the last ten years. This results State of India are historically malaria endemic (Figure 1(b)). in shifting the country strategy from control to elimination The endemic upazilas of the district constitute 7% of the BANGLADESH Malaria Non-endemic Area 2 Malaria Research and Treatment Meghalaya (INDIA) Mymensingh (Bangladesh) Durgapur Kalmakanda Sunamganj (Bangladesh) Purbadhala Barhatta Netrokona Sadar Mohanganj Atpara Khaliajuri Mymensingh Kendua (Bangladesh) Madan Kishoreganj (Bangladesh) 0 2.5 5 10 15 20 Miles Malaria Elimination Targeted Area KM Malaria Endemic Area By 2021 By 2025 By 2030 Need to Start Surveillance to Ensure Malaria Free (a) Phase-wise Malaria elimination target from Bangladesh by 2030 (b) Malaria endemic upazilas in Netrokona district Meghalaya INDIA Lengura Durgapur Kullagora Rongchati Kharnai Chandigarh Kalmakanda Birishiri Kalmakanda Nazirpur Gaokandia Durgapur Bakaljora Kailati Kakairgara Bara Kharpan Pagla BANGLADESH 02 1 4 6 8 Miles Malaria Cases in 2018 Zero Case 3 Cases 1 Case 34 Cases 2 Cases (c) Union-wise malaria case load in Netrokona in 2018 Figure 1 BANGLADESH Malaria Research and Treatment 3 malaria endemic population of the north and northeast 8 2.2. Study Design, Data Collection, and Analysis. The study districts of the country whereas they contribute half of the was retrospectively conducted on the malaria cases con- malariaburden of thatarea[2, 3]. The majority ( >60%) of the firmed by Rapid Diagnostic Test (RDT) and/or microscopy by the government and/or NGO service providers in the population, especially in the international border-belt of the endemic area (Figure 1(c)), is tribal aborigines contributing study site between 2013 and 2018. A total of 713 malaria the highest number of malaria cases of the district [2]. Pree- cases (601 cases by NGO service providers and 112 cases by limination activities were initiated and surveillance system government service providers) were diagnosed. Out of which, was strengthened in the district since 2012 and subsequently 626 cases were investigated. The source of infection of 87 cases elimination was started in 2017. (in 2013: 55; in 2014: 26; in 2015: 1; and in 2017: 5) remained The surveillance data show that most of the cases of unknown, so they were excluded from the analysis. the district are imported from Meghalaya State of India [4]. The completed “investigation” reports of individual cases were collected and preserved in the central level. These data of This imported malaria has a potential risk of increased local transmission and might cause the reintroduction of local “investigation” report was entered into MS Excel version 2016 cases, which could be a major challenge for elimination of and the descriptive analysis was done for age, sex, occupation, species, and seasonal and geographical distribution of the the disease from that area [5–7]. This challenge warrants the conducting of the study to understand the epidemiology of cases. The comparison of these factors between imported the imported cases for future strategy development required and indigenous infections has been done tabularly and/or to prevent both imported and introduced malaria with graphically and presented in the report. appropriate interventions. 2.3. Operational Definition. In this study, “imported malaria” has been defined as “the malaria case occurring outside 2. Methodology the national boundary but diagnosed within the national 2.1. Surveillance and Case Investigation. Like other rs fi t boundary” which is measured by the individual’s history of phased malaria elimination targeted districts, active and pas- staying in malaria endemic country within previous one sive surveillance are in place in Netrokona. Service providers month, considering the incubation period of the disease. “Cross- are available from facilities down to the community in the border workers” refer to the inhabitants (Bangladeshi citizens) whole endemic area. The catchment area is fixed for every of the endemic area of Netrokona district who cross the service provider who frequently moves and searches for international border between Bangladesh and India for their malaria cases by conducting household visits, organising occupational purpose, stay in Meghalaya State of India, and fixed and mobile health camps at the community. When work there. The two malaria endemic upazilas represent any malaria case is diagnosed, surveillance by community district and will be referred to as “Netrokona district”. “Static health workers, such as searching for malaria suspects within population” refers to the inhabitants of endemic area of the households within a 500-metre radius of the index case or district who do not stay at night outside the international the nearest 60 households, whichever is less, performing border for occupation purpose like cross-border workers. parasitological tests for malaria within 3 days, and follow-up of this surroundings for next 30 days, is done to identify if any 2.4. Ethical Consideration. The ethical issues such as ano- reactive case is transmitted from the index case. Besides, the nymity of the respondents were maintained, and nothing service providers have the list of cross-border workers (which was done during the study which could hamper the regular varies between 700 and 800; list is updated accordingly) activity of the respondents or programme or be harmful for who work in the Meghalaya State of India and contribute the cases, respondents, or other family members. most of the imported cases of the district. The parasitological tests are done at the time of their returning to home from 3. Results their work. Subsequently, they are followed up to ensure the diagnosis and treatment services if their malaria symptoms Between 2013 and 2018, imported cases contributed 60% to appear later on. u Th s, the strengthened surveillance system the 95% malaria burden in Netrokona district (Figure 2). covered the diagnosis and treatment services of all the malaria The mean age of these imported cases is 32 years and most cases (there were no missing cases) of the district during the of the cases (82%) were between 15 and 49 years old. The period. distribution of these imported cases by population type When one malaria case is confirmed by Rapid Diagnostic showed overall 93% (88% to 95%) contribution by the cross- Test (RDT) and/or microscopy, detailed information of it is border workers (Figure 3). sent to national programme and NGO central level through Distribution of the malaria cases by different factors such mobile SMS immediately. The detailed investigation of the as sex, occupation, and ethnicity revealed the contribution case is done verbally by local management staff (government of the imported cases by male (84%), labour (66%), and and/or NGO) using the prescribed form of the programme. tribal population (95%) which is quite higher in each category The respondents of the investigation are either the cases or compared to the same one for indigenous infection. their family members. After completion of the investigation, Geographical distribution revealed that all the imported the investigators classify the source of infection based on the cases occurred in populations of bordered (with Meghalaya, traveling, outstay, and dwelling history of the case during last India) 5 unions constituting 28% of the endemic popu- one month, considering the incubation period of the disease. lation of the district (Figure 4). Imported cases occurred 4 Malaria Research and Treatment Table 1: Comparison between imported and indigenous cases by dieff rent factors. Imported cases Indigenous cases Factors Category Number % Number % <55 1% 3 2% 5-14 32 6% 36 28% Age group (Year) 15-49 408 82% 67 53% 50+ 54 11% 21 17% Cross-border worker 465 93% 8 6% Population type Static population 17 3% 119 94% Indian citizen 17 3% - - Male 418 84% 86 68% Sex Female 81 16% 41 32% Labour 328 66% 17 13% Farmer 75 15% 31 24% Occupation Housewife 35 7% 27 21% Student 35 7% 31 24% Others 26 5% 21 17% Tribal 472 95% 76 60% Ethnicity Bengali 27 5% 50 40% P. falciparum (Pf) 312 63% 91 71% Species P. vivax (Pv) 46 9% 11 9% Mixed 141 28% 25 20% 200 149 150 149 139 139 (82%) 88 121 86 (93%) (87%) (60%) 88 111 (91%) 82 (93%) (71%) 50 38 (95%) 50 38 (95%) (92%) 18 17 9 7 0 2 (89%) (88%) 2013 2014 2015 2016 2017 2018 Imported cases 2013 2014 2015 2016 2017 2018 Indigenous cases Total imported cases Total no. of cases Imported cases in cross-border workers Figure 2: Trend of malaria cases in Netrokona district: 2013-2018. Figure 3: Trend of imported cases and contribution by cross-border workers. throughout the year with seasonal uc fl tuation (Figure 5). Species-wise distribution shows lower P. falciparum (63%) and higher mixed (28%) infection among imported cases mostly contributed by adult male and labour by occupation compared to the indigenous (71% Pf and 20% mixed) infec- [11]. tion whereas P. vivax is similar in cases of both types (Table 1). Due to geographic location of the area nearby the international border (between Bangladesh and India), the population have a very little scope of work within the national 4. Discussion boundary. Based on the accessibility and scope of work in Imported malaria is an emerging issue in the elimination the bordering area of Meghalaya, the number of cross-border settings in many countries [8, 9]. This study reviewed workers and their contribution to the imported cases differ in the situation of imported malaria in Netrokona district the bordering unions of the district (Table 2, Figures 7 and 8). of Bangladesh where malaria burden has reduced by 91% Therefore, breadwinners including other family members between 2008 and 2018 and elimination of the disease by cross the border and work in high malaria endemic Megha- 2021 is the goal [2, 10]. The higher reduction of indigenous laya State of India throughout the year [12]. Males mostly (97%) infection, compared to imported (56%) cases between work as coalmine-labour in the winter and wood-cutter in the 2013 and 2018 (Figure 6), results in the increased portion of rainy season on a contract basis. They took their adolescent imported malaria burden of the district over the years. Like boys there to support their contracted work. They need to stay other elimination settings, imported malaria in this district is there continuously almost for one month for their work. They Malaria cases Number of cases Malaria Research and Treatment 5 2013 2014 2015 2016 2017 2018 (N=86) (N=149) (N=121) (N=88) (N=17) (N=38) Rongchati Langura Durgapur Kullagara Kharnoi Figure 4: Union-wise distribution of imported cases: 2013-2018. J F M A M J J A S O ND J F M A M J J A S O ND J F M A M J J A S O ND J F M A M J J A S O ND J F M A M J J A S O ND J F MA M J J A S O ND 2013 2014 2015 2016 2017 2018 Total malaria cases Imported malaria cases Figure 5: Seasonal trend of total versus imported malaria cases in Netrokona district: 2013-2018. 125% 100% 97% 88% 100% 84% 69% 100% 75% 80% 43% 50% 56% 25% -2% 0% 2013 2014 2015 2016 2017 2018 −25% −50% -41% −75% -73% −100% Imported cases Indigenous cases Figure 6: Reduction of imported and indigenous malaria infection in Netrokona compared to the year 2013. become higher susceptible to mosquito bites due to outdoor contribute to the increased imported malaria cases compared to indigenous cases. Larger number of imported P. vivax and work, living in poor conditioned houses, lack of personal mixed (Pf and Pv) species infection in imported cases can protection, immunity, and awareness and bear the most of be one of the major challenges to malaria elimination due to the imported malaria cases [9, 13]. Adult female members dormant hypnozoites in liver cells and parasite transmission are involved in other activities such as household work or from gametocytes before appearance of symptoms [12, 14]. In running a shop and supply of food to the labours. Children also need to cross the border when their parents went addition, people with different occupations such as farmers, there for long period. They (cross-border workers and their students, housewives, service holders, teachers, and business- family members) stay there without personal protection from men, living in the bordering villages need to work in hilly mosquito bites as many of them do not hang Long Lasting Meghalaya border and frequently cross the border (but do Insecticidal Mosquito Nets (LLINs) regularly before sleeping not stay there at night) due to the location of their lands and at night due to their fatigue aer ft laborious work from dawn houses, and they contribute to the imported cases. Besides, to dusk.Thus,these population groups become infected and some Indian citizens living in bordering area receive malaria Number of cases Percentage Number of malaria cases 6 Malaria Research and Treatment API ( < 1% ) W E API ( 1% - 10% ) API ( 11% - 20% ) 0 1.5 3 6 km API ( 21% - 30% ) API ( 30% + ) Figure 7: Union-wise Annual Parasite Incidence (API) in cross-border workers in Durgapur upazila: 2013-2018. Malaria Research and Treatment 7 API ( < 1% ) W E API ( 1% - 10% ) S API ( 11% - 20% ) 0 1.5 3 6 km API ( 21% - 30% ) API ( 30% + ) Figure 8: Union-wise Annual Parasite Incidence (API) in cross-border workers in Kalmakanda upazila: 2013-2018. 8 Malaria Research and Treatment Table 2: Union-wise present number of cross-border workers. transmission which might be a challenge to malaria elimi- nation in that area. Appropriate interventions targeting the Name of high-risk population group (cross-border workers and their Name of Upazila No. of cross-border workers Union family members) are essential to prevent the introduced cases Durgapur 100 and subsequently avoid reestablishment when elimination of Durgapur Kullagara 238 the disease is achieved. Rongchati 317 Kalmakanda Lengura 34 Data Availability Kharnoi 67 The data used to support the findings of this study are Total 756 available from the corresponding author upon request. diagnosis and treatment services in Bangladesh through their Conflicts of Interest relatives and sometimes they stay in Bangladesh (in their The authors declare that they have no conflicts of interest. relatives’ houses) during treatment. us Th movement of popu- lation between endemic/high endemic and nonendemic/low endemic countries due to globalization/occupational pur- Authors’ Contributions poses has increased the emergence of imported malaria [9, 11]. Consequently, cross-border workers can contribute a Md Abdul Karim was responsible for data analysis and significant number of imported cases, which has the potential interpretation (type of data analysis, tools to be used for risk of local transmission of the disease to the area where the analysis, type of graphs, tables and maps to be used and their transmission has already been interrupted and, thus, can be interpretation in the paper). Md Abdul Karim, M Moktadir a major challenge to malaria elimination [6, 7, 11]. It is an Kabir, and Shamsun Naher equally contributed to the design increasing problem in many countries for the last decades of the work (study objective, literature review, study type, and caused thousands of cases worldwide and large number study site, study population, methodology). Md Abdul Karim of deaths every year [9–11, 13]. History of malaria outbreaks wrote the whole paper, while M Moktadir Kabir and Shamsun due to introduced cases in the elimination settings evidences Naher played supporting roles in the writing process. Md the imported cases as challenge to malaria elimination [15– Abdul Karim critically revised the logical sequence and the 18]. technical and scientific soundness of the paper; M Moktadir In-depth orientation of cross-border workers on malaria; Kabir assisted in identifying and addressing the logical standby treatment during staying in high endemic zone; sequence and technical and scientific soundness of the paper; continuation of parasitological tests of all individuals during Md Ashraf Siddiqui assisted in addressing the issues arising entrance to the country from Meghalaya; continuation of during the review process (especially in the methodology and follow-up of the returnee (from coalmine and/or forest); results sections); Md Shahidul Islam Laskar and Anjan Saha universal access of cross-border worker by distributing sup- assisted in addressing the issues arising during the review plementary LLINs; and ensuring their utilization during process (especially in the methodology section); Shamsun staying in endemic zone can be pivotal to prevent introduced Naher assisted in identifying and addressing the logical malaria and reestablishment of the disease when elimination sequence, the technical and scientific justification of the will be achieved. paper, and addressing the issues arising during the review process. Md Ashraf Siddiqui, Md Shahidul Islam Laskar, and Anjan Saha equally contributed to acquisition, analysis, and 5. Limitations of the Study interpretation of data and preparation of graphs, maps, and Some cases diagnosed by the government service providers tables. All the authors approved the final version of the paper were left out of the investigation especially during the rfi st for publication and agreed to be accountable for all aspects of two years of the initiation of the preelimination activity. the work, taking the responsibility if any issue arises during These cases were excluded from the analysis. Due to verbal and/or after the publication of the paper. investigation of the cases, potential of recall bias of the respondentscannotbeavoided.Theresultscould notbecom- Acknowledgments pared with the n fi dings of other studies due to nonavailability of studies in similar settings, and the results might be unique The authors are grateful to both government and NGO in the district where the study was conducted. malaria service providers of Netrokona district. The authors are especially thankful to Upazila Health and Family Planning Ocffi ers (UH&FPO), NGO Project Manager and 6. Conclusion Upazilla Managers of Durgapur and Kalmakanda for their Drastic reduction of indigenous malaria between 2013 support during the study. The authors also acknowledge the and 2018 leads to increased portion of imported cases contribution of field and central level malaria team of national in Netrokona district. These imported cases constitute an programme and BRAC for their continuous support in this emerging issue and have the potential risk of increasing local regard. Malaria Research and Treatment 9 References [18] T. Zoller, T. J. Naucke, J. May et al., “Malaria transmission in non-endemic areas: case report, review of the literature and [1] World Health Organization, World Malaria Report 2018,WHO, implications for public health management,” Malaria Journal, Geneva, Switzerland, 2018. vol. 8, no. 71, 2009. [2] National Malaria Elimination Programme, Directorate General of Health Services, and Ministry of Health and Family Welfare, National Strategic Plan for Malaria Elimination: 2017-2021, Dhaka, Bangladesh, 2017. [3] National Malaria Elimination Programme, Malaria Monthly MIS Report 2018, Directorate General of Health Services, Ministry of Health and Family Welfare., 2018. [4] BRAC, Malaria Case investigation report 2012-2018. [5] Z. Li, Q. Zhang, C. Zheng et al., “Epidemiologic features of overseas imported malaria in the People’s Republic of China,” Malaria Journal,vol.15,no. 1, 2016. [6] S.Odolini,P.Gautret,and P. Parola,“Epidemiology of imported malaria in the mediterranean region,” Mediterranean Journal of Hematology and Infectious Diseases,vol. 4, no. 1, article e2012031, 2012. [7] UNWTO, Tourism Highlights, UNWTO Publications Depart- ment, Madrid, Spain, 2011, http://www.e-unwto.org/doi/pdf/ 10.18111/9789284413935. [8] A.J.Tatem and D.L.Smitha,“International population move- ments and regional Plasmodium falciparum malaria elimina- tion strategies,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 107, no. 27, pp. 12222–12227, [9] Y. Liu, M. S. Hsiang, H. Zhou et al., “Malaria in overseas labourers returning to China: an analysis of imported malaria in Jiangsu Province, 2001–2011,” Malaria Journal,vol.13, no. 29, [10] National Malaria Control Programme, Malaria Monthly Disease Specific Report 2008 , Directorate General of Health Services, Ministry of Health and Family Welfare, 2017. [11] S. Zhou, Z. Li, C. Cotter et al., “Trends of imported malaria in China 2010–2014: analysis of surveillance data,” Malaria Journal,vol.15,no.1,article 39,2016. [12] V. Dev, B. M. Sangma, and A. P. Dash, “Persistent transmission of malaria in Garo hills of Meghalaya bordering Bangladesh, north-east India,” Malaria Journal,vol.9, no. 263,2010. [13] M. Zhang, Z. Liu, H. He et al., “Knowledge, attitudes, and practices on malaria prevention among Chinese international travelers,” Journalof TravelMedicine,vol. 18, no.3, pp. 173–177, [14] World Health Organization, Control and Elimination of Plas- modium Vivax Malaria a Technical Brief,WHO,Geneva, Switzerland, 2016. [15] G. N. L.Galappaththy,S. D.Fernando, and R. R.Abeyasinghe, “Imported malaria: a possible threat to the elimination of malaria from Sri Lanka?” Tropical Medicine & International Health,vol.18,no.6,pp.761–768,2013. [16] A. Kru¨ger, A.Rech, X.-Z.Su,and E. Tannich,“Twocases of autochthonous Plasmodium falciparum malaria in Germany with evidence for local transmission by indigenous Anopheles plumbeus,” Tropical Medicine and International Health,vol. 6, no.12,pp.983–985, 2001. [17] J. E. Limongi, K. M. Chaves, M. B. Paula et al., “Malaria outbreaks in a non-endemic area of Brazil, 2005,” Revista da SociedadeBrasileiradeMedicina Tropical, vol.41,no. 3,pp.232– 237, 2008. 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Epidemiology of Imported Malaria in Netrokona District of Bangladesh 2013-2018: Analysis of Surveillance Data

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Copyright © 2019 Md Abdul Karim et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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Abstract

Hindawi Malaria Research and Treatment Volume 2019, Article ID 6780258, 9 pages https://doi.org/10.1155/2019/6780258 Research Article Epidemiology of Imported Malaria in Netrokona District of Bangladesh 2013-2018: Analysis of Surveillance Data 1 2 1 Md Abdul Karim , M. Moktadir Kabir, Md Ashraf Siddiqui , 1 3 1 Md Shahidul Islam Laskar , Anjan Saha , and Shamsun Naher Communicable Disease (Malaria) Programme, BRAC, Bangladesh Communicable Disease (Malaria) and Water Sanitation & Hygiene Programme, BRAC, Bangladesh National Malaria Elimination Programme, Bangladesh Correspondence should be addressed to Md Abdul Karim; karim.mis@gmail.com Received 29 November 2018; Revised 11 April 2019; Accepted 18 April 2019; Published 13 June 2019 Academic Editor: Sasithon Pukrittayakamee Copyright © 2019 Md Abdul Karim et al. is Th is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Introduction. Netrokona is one of the first phase malaria elimination targeted 8 districts of Bangladesh by 2021. The district constitutes only 7% of the population but contributes half of the malaria cases in that area. Most of the cases of that district are imported from Meghalaya State of India. The study was conducted to understand the epidemiology of these imported malaria cases for further strategy development to prevent both imported and introduced cases. Methodology. eTh study was retrospectively conducted on the malaria cases confirmed by microscopy and/or RDT by the government and/or NGO service providers between 2013 and 2018. The information of the cases was collected from the verbal “investigation” report of individual malaria confirmed cases. The respondents of the “investigation” were either the patients or their family members. Out of the 713 cases during the study period, descriptive analysis of 626 cases (based on the completeness of “investigation form”) of the district was done using MS Excel version 2016. Results. Proportion of imported malaria in Netrokona district increased from 60% in 2013 to 95% in 2018 which persists throughout the year with a little seasonal u fl ctuation. eTh overall contribution of these imported cases is 93% by cross-border workers by population type and 84%, 66%, and 95% by male, labour, and tribal population considering the factors of sex, occupation, and ethnicity, respectively. Population aged between 15 and 49 years contributed 82% of these imported cases. All of these cases occurred in the internationally bordering belt with Meghalaya State of India. Species-wise distribution revealed lower P. falciparum (63%) and higher mixed (28%) infection in imported cases compared to the 71% Pf and 20% mixed infection among the indigenous infections whereas P. vivax is similar in both cases. Conclusion. Imported malaria is an emerging issue that has a potential risk of increased local transmission which might be a challenge to malaria elimination in that area. Appropriate interventions targeting the cross-border workers are essential to prevent the introduced cases and subsequently avoid reestablishment when elimination of the disease is achieved. 1. Introduction of the disease through three phases: 2021, 2025, and 2030 [2] (Figure 1(a)). The north and northeast 8 districts of the Bangladesh is one of the 87 malaria endemic countries country are the rfi st phase malaria elimination targeted areas of the country by 2021 [2]. and territories of the world in 2017 [1]. Currently, a total population of 17.52 million in 13 bordering districts of the Netrokona is one of these rfi st phased malaria elimination country are at risk of the disease [2]. With the financial targeted districts of the country. The district is situated support from the Global Fund, the country intensified the in the northern part of Bangladesh. Out of the total 10 programme activities in partnership between government administrative upazilas (subdistrict), 2 upazilas (consisting and BRAC led NGO consortium and achieved remarkable of 15 unions) with internationally bordering with Meghalaya reduction of malaria burden in the last ten years. This results State of India are historically malaria endemic (Figure 1(b)). in shifting the country strategy from control to elimination The endemic upazilas of the district constitute 7% of the BANGLADESH Malaria Non-endemic Area 2 Malaria Research and Treatment Meghalaya (INDIA) Mymensingh (Bangladesh) Durgapur Kalmakanda Sunamganj (Bangladesh) Purbadhala Barhatta Netrokona Sadar Mohanganj Atpara Khaliajuri Mymensingh Kendua (Bangladesh) Madan Kishoreganj (Bangladesh) 0 2.5 5 10 15 20 Miles Malaria Elimination Targeted Area KM Malaria Endemic Area By 2021 By 2025 By 2030 Need to Start Surveillance to Ensure Malaria Free (a) Phase-wise Malaria elimination target from Bangladesh by 2030 (b) Malaria endemic upazilas in Netrokona district Meghalaya INDIA Lengura Durgapur Kullagora Rongchati Kharnai Chandigarh Kalmakanda Birishiri Kalmakanda Nazirpur Gaokandia Durgapur Bakaljora Kailati Kakairgara Bara Kharpan Pagla BANGLADESH 02 1 4 6 8 Miles Malaria Cases in 2018 Zero Case 3 Cases 1 Case 34 Cases 2 Cases (c) Union-wise malaria case load in Netrokona in 2018 Figure 1 BANGLADESH Malaria Research and Treatment 3 malaria endemic population of the north and northeast 8 2.2. Study Design, Data Collection, and Analysis. The study districts of the country whereas they contribute half of the was retrospectively conducted on the malaria cases con- malariaburden of thatarea[2, 3]. The majority ( >60%) of the firmed by Rapid Diagnostic Test (RDT) and/or microscopy by the government and/or NGO service providers in the population, especially in the international border-belt of the endemic area (Figure 1(c)), is tribal aborigines contributing study site between 2013 and 2018. A total of 713 malaria the highest number of malaria cases of the district [2]. Pree- cases (601 cases by NGO service providers and 112 cases by limination activities were initiated and surveillance system government service providers) were diagnosed. Out of which, was strengthened in the district since 2012 and subsequently 626 cases were investigated. The source of infection of 87 cases elimination was started in 2017. (in 2013: 55; in 2014: 26; in 2015: 1; and in 2017: 5) remained The surveillance data show that most of the cases of unknown, so they were excluded from the analysis. the district are imported from Meghalaya State of India [4]. The completed “investigation” reports of individual cases were collected and preserved in the central level. These data of This imported malaria has a potential risk of increased local transmission and might cause the reintroduction of local “investigation” report was entered into MS Excel version 2016 cases, which could be a major challenge for elimination of and the descriptive analysis was done for age, sex, occupation, species, and seasonal and geographical distribution of the the disease from that area [5–7]. This challenge warrants the conducting of the study to understand the epidemiology of cases. The comparison of these factors between imported the imported cases for future strategy development required and indigenous infections has been done tabularly and/or to prevent both imported and introduced malaria with graphically and presented in the report. appropriate interventions. 2.3. Operational Definition. In this study, “imported malaria” has been defined as “the malaria case occurring outside 2. Methodology the national boundary but diagnosed within the national 2.1. Surveillance and Case Investigation. Like other rs fi t boundary” which is measured by the individual’s history of phased malaria elimination targeted districts, active and pas- staying in malaria endemic country within previous one sive surveillance are in place in Netrokona. Service providers month, considering the incubation period of the disease. “Cross- are available from facilities down to the community in the border workers” refer to the inhabitants (Bangladeshi citizens) whole endemic area. The catchment area is fixed for every of the endemic area of Netrokona district who cross the service provider who frequently moves and searches for international border between Bangladesh and India for their malaria cases by conducting household visits, organising occupational purpose, stay in Meghalaya State of India, and fixed and mobile health camps at the community. When work there. The two malaria endemic upazilas represent any malaria case is diagnosed, surveillance by community district and will be referred to as “Netrokona district”. “Static health workers, such as searching for malaria suspects within population” refers to the inhabitants of endemic area of the households within a 500-metre radius of the index case or district who do not stay at night outside the international the nearest 60 households, whichever is less, performing border for occupation purpose like cross-border workers. parasitological tests for malaria within 3 days, and follow-up of this surroundings for next 30 days, is done to identify if any 2.4. Ethical Consideration. The ethical issues such as ano- reactive case is transmitted from the index case. Besides, the nymity of the respondents were maintained, and nothing service providers have the list of cross-border workers (which was done during the study which could hamper the regular varies between 700 and 800; list is updated accordingly) activity of the respondents or programme or be harmful for who work in the Meghalaya State of India and contribute the cases, respondents, or other family members. most of the imported cases of the district. The parasitological tests are done at the time of their returning to home from 3. Results their work. Subsequently, they are followed up to ensure the diagnosis and treatment services if their malaria symptoms Between 2013 and 2018, imported cases contributed 60% to appear later on. u Th s, the strengthened surveillance system the 95% malaria burden in Netrokona district (Figure 2). covered the diagnosis and treatment services of all the malaria The mean age of these imported cases is 32 years and most cases (there were no missing cases) of the district during the of the cases (82%) were between 15 and 49 years old. The period. distribution of these imported cases by population type When one malaria case is confirmed by Rapid Diagnostic showed overall 93% (88% to 95%) contribution by the cross- Test (RDT) and/or microscopy, detailed information of it is border workers (Figure 3). sent to national programme and NGO central level through Distribution of the malaria cases by different factors such mobile SMS immediately. The detailed investigation of the as sex, occupation, and ethnicity revealed the contribution case is done verbally by local management staff (government of the imported cases by male (84%), labour (66%), and and/or NGO) using the prescribed form of the programme. tribal population (95%) which is quite higher in each category The respondents of the investigation are either the cases or compared to the same one for indigenous infection. their family members. After completion of the investigation, Geographical distribution revealed that all the imported the investigators classify the source of infection based on the cases occurred in populations of bordered (with Meghalaya, traveling, outstay, and dwelling history of the case during last India) 5 unions constituting 28% of the endemic popu- one month, considering the incubation period of the disease. lation of the district (Figure 4). Imported cases occurred 4 Malaria Research and Treatment Table 1: Comparison between imported and indigenous cases by dieff rent factors. Imported cases Indigenous cases Factors Category Number % Number % <55 1% 3 2% 5-14 32 6% 36 28% Age group (Year) 15-49 408 82% 67 53% 50+ 54 11% 21 17% Cross-border worker 465 93% 8 6% Population type Static population 17 3% 119 94% Indian citizen 17 3% - - Male 418 84% 86 68% Sex Female 81 16% 41 32% Labour 328 66% 17 13% Farmer 75 15% 31 24% Occupation Housewife 35 7% 27 21% Student 35 7% 31 24% Others 26 5% 21 17% Tribal 472 95% 76 60% Ethnicity Bengali 27 5% 50 40% P. falciparum (Pf) 312 63% 91 71% Species P. vivax (Pv) 46 9% 11 9% Mixed 141 28% 25 20% 200 149 150 149 139 139 (82%) 88 121 86 (93%) (87%) (60%) 88 111 (91%) 82 (93%) (71%) 50 38 (95%) 50 38 (95%) (92%) 18 17 9 7 0 2 (89%) (88%) 2013 2014 2015 2016 2017 2018 Imported cases 2013 2014 2015 2016 2017 2018 Indigenous cases Total imported cases Total no. of cases Imported cases in cross-border workers Figure 2: Trend of malaria cases in Netrokona district: 2013-2018. Figure 3: Trend of imported cases and contribution by cross-border workers. throughout the year with seasonal uc fl tuation (Figure 5). Species-wise distribution shows lower P. falciparum (63%) and higher mixed (28%) infection among imported cases mostly contributed by adult male and labour by occupation compared to the indigenous (71% Pf and 20% mixed) infec- [11]. tion whereas P. vivax is similar in cases of both types (Table 1). Due to geographic location of the area nearby the international border (between Bangladesh and India), the population have a very little scope of work within the national 4. Discussion boundary. Based on the accessibility and scope of work in Imported malaria is an emerging issue in the elimination the bordering area of Meghalaya, the number of cross-border settings in many countries [8, 9]. This study reviewed workers and their contribution to the imported cases differ in the situation of imported malaria in Netrokona district the bordering unions of the district (Table 2, Figures 7 and 8). of Bangladesh where malaria burden has reduced by 91% Therefore, breadwinners including other family members between 2008 and 2018 and elimination of the disease by cross the border and work in high malaria endemic Megha- 2021 is the goal [2, 10]. The higher reduction of indigenous laya State of India throughout the year [12]. Males mostly (97%) infection, compared to imported (56%) cases between work as coalmine-labour in the winter and wood-cutter in the 2013 and 2018 (Figure 6), results in the increased portion of rainy season on a contract basis. They took their adolescent imported malaria burden of the district over the years. Like boys there to support their contracted work. They need to stay other elimination settings, imported malaria in this district is there continuously almost for one month for their work. They Malaria cases Number of cases Malaria Research and Treatment 5 2013 2014 2015 2016 2017 2018 (N=86) (N=149) (N=121) (N=88) (N=17) (N=38) Rongchati Langura Durgapur Kullagara Kharnoi Figure 4: Union-wise distribution of imported cases: 2013-2018. J F M A M J J A S O ND J F M A M J J A S O ND J F M A M J J A S O ND J F M A M J J A S O ND J F M A M J J A S O ND J F MA M J J A S O ND 2013 2014 2015 2016 2017 2018 Total malaria cases Imported malaria cases Figure 5: Seasonal trend of total versus imported malaria cases in Netrokona district: 2013-2018. 125% 100% 97% 88% 100% 84% 69% 100% 75% 80% 43% 50% 56% 25% -2% 0% 2013 2014 2015 2016 2017 2018 −25% −50% -41% −75% -73% −100% Imported cases Indigenous cases Figure 6: Reduction of imported and indigenous malaria infection in Netrokona compared to the year 2013. become higher susceptible to mosquito bites due to outdoor contribute to the increased imported malaria cases compared to indigenous cases. Larger number of imported P. vivax and work, living in poor conditioned houses, lack of personal mixed (Pf and Pv) species infection in imported cases can protection, immunity, and awareness and bear the most of be one of the major challenges to malaria elimination due to the imported malaria cases [9, 13]. Adult female members dormant hypnozoites in liver cells and parasite transmission are involved in other activities such as household work or from gametocytes before appearance of symptoms [12, 14]. In running a shop and supply of food to the labours. Children also need to cross the border when their parents went addition, people with different occupations such as farmers, there for long period. They (cross-border workers and their students, housewives, service holders, teachers, and business- family members) stay there without personal protection from men, living in the bordering villages need to work in hilly mosquito bites as many of them do not hang Long Lasting Meghalaya border and frequently cross the border (but do Insecticidal Mosquito Nets (LLINs) regularly before sleeping not stay there at night) due to the location of their lands and at night due to their fatigue aer ft laborious work from dawn houses, and they contribute to the imported cases. Besides, to dusk.Thus,these population groups become infected and some Indian citizens living in bordering area receive malaria Number of cases Percentage Number of malaria cases 6 Malaria Research and Treatment API ( < 1% ) W E API ( 1% - 10% ) API ( 11% - 20% ) 0 1.5 3 6 km API ( 21% - 30% ) API ( 30% + ) Figure 7: Union-wise Annual Parasite Incidence (API) in cross-border workers in Durgapur upazila: 2013-2018. Malaria Research and Treatment 7 API ( < 1% ) W E API ( 1% - 10% ) S API ( 11% - 20% ) 0 1.5 3 6 km API ( 21% - 30% ) API ( 30% + ) Figure 8: Union-wise Annual Parasite Incidence (API) in cross-border workers in Kalmakanda upazila: 2013-2018. 8 Malaria Research and Treatment Table 2: Union-wise present number of cross-border workers. transmission which might be a challenge to malaria elimi- nation in that area. Appropriate interventions targeting the Name of high-risk population group (cross-border workers and their Name of Upazila No. of cross-border workers Union family members) are essential to prevent the introduced cases Durgapur 100 and subsequently avoid reestablishment when elimination of Durgapur Kullagara 238 the disease is achieved. Rongchati 317 Kalmakanda Lengura 34 Data Availability Kharnoi 67 The data used to support the findings of this study are Total 756 available from the corresponding author upon request. diagnosis and treatment services in Bangladesh through their Conflicts of Interest relatives and sometimes they stay in Bangladesh (in their The authors declare that they have no conflicts of interest. relatives’ houses) during treatment. us Th movement of popu- lation between endemic/high endemic and nonendemic/low endemic countries due to globalization/occupational pur- Authors’ Contributions poses has increased the emergence of imported malaria [9, 11]. Consequently, cross-border workers can contribute a Md Abdul Karim was responsible for data analysis and significant number of imported cases, which has the potential interpretation (type of data analysis, tools to be used for risk of local transmission of the disease to the area where the analysis, type of graphs, tables and maps to be used and their transmission has already been interrupted and, thus, can be interpretation in the paper). Md Abdul Karim, M Moktadir a major challenge to malaria elimination [6, 7, 11]. It is an Kabir, and Shamsun Naher equally contributed to the design increasing problem in many countries for the last decades of the work (study objective, literature review, study type, and caused thousands of cases worldwide and large number study site, study population, methodology). Md Abdul Karim of deaths every year [9–11, 13]. History of malaria outbreaks wrote the whole paper, while M Moktadir Kabir and Shamsun due to introduced cases in the elimination settings evidences Naher played supporting roles in the writing process. Md the imported cases as challenge to malaria elimination [15– Abdul Karim critically revised the logical sequence and the 18]. technical and scientific soundness of the paper; M Moktadir In-depth orientation of cross-border workers on malaria; Kabir assisted in identifying and addressing the logical standby treatment during staying in high endemic zone; sequence and technical and scientific soundness of the paper; continuation of parasitological tests of all individuals during Md Ashraf Siddiqui assisted in addressing the issues arising entrance to the country from Meghalaya; continuation of during the review process (especially in the methodology and follow-up of the returnee (from coalmine and/or forest); results sections); Md Shahidul Islam Laskar and Anjan Saha universal access of cross-border worker by distributing sup- assisted in addressing the issues arising during the review plementary LLINs; and ensuring their utilization during process (especially in the methodology section); Shamsun staying in endemic zone can be pivotal to prevent introduced Naher assisted in identifying and addressing the logical malaria and reestablishment of the disease when elimination sequence, the technical and scientific justification of the will be achieved. paper, and addressing the issues arising during the review process. Md Ashraf Siddiqui, Md Shahidul Islam Laskar, and Anjan Saha equally contributed to acquisition, analysis, and 5. Limitations of the Study interpretation of data and preparation of graphs, maps, and Some cases diagnosed by the government service providers tables. All the authors approved the final version of the paper were left out of the investigation especially during the rfi st for publication and agreed to be accountable for all aspects of two years of the initiation of the preelimination activity. the work, taking the responsibility if any issue arises during These cases were excluded from the analysis. Due to verbal and/or after the publication of the paper. investigation of the cases, potential of recall bias of the respondentscannotbeavoided.Theresultscould notbecom- Acknowledgments pared with the n fi dings of other studies due to nonavailability of studies in similar settings, and the results might be unique The authors are grateful to both government and NGO in the district where the study was conducted. malaria service providers of Netrokona district. The authors are especially thankful to Upazila Health and Family Planning Ocffi ers (UH&FPO), NGO Project Manager and 6. Conclusion Upazilla Managers of Durgapur and Kalmakanda for their Drastic reduction of indigenous malaria between 2013 support during the study. The authors also acknowledge the and 2018 leads to increased portion of imported cases contribution of field and central level malaria team of national in Netrokona district. These imported cases constitute an programme and BRAC for their continuous support in this emerging issue and have the potential risk of increasing local regard. Malaria Research and Treatment 9 References [18] T. Zoller, T. J. Naucke, J. May et al., “Malaria transmission in non-endemic areas: case report, review of the literature and [1] World Health Organization, World Malaria Report 2018,WHO, implications for public health management,” Malaria Journal, Geneva, Switzerland, 2018. vol. 8, no. 71, 2009. [2] National Malaria Elimination Programme, Directorate General of Health Services, and Ministry of Health and Family Welfare, National Strategic Plan for Malaria Elimination: 2017-2021, Dhaka, Bangladesh, 2017. [3] National Malaria Elimination Programme, Malaria Monthly MIS Report 2018, Directorate General of Health Services, Ministry of Health and Family Welfare., 2018. [4] BRAC, Malaria Case investigation report 2012-2018. [5] Z. Li, Q. Zhang, C. 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