Browse > Article
http://dx.doi.org/10.3347/kjp.2019.57.3.233

Malaria Prevalence in a Low Transmission Area, Jazan District of Southwestern Saudi Arabia  

Hawash, Yousry (Clinical Laboratories Sciences Department, College of Applied Medical Science, Taif University)
Ismail, Khadiga (Clinical Laboratories Sciences Department, College of Applied Medical Science, Taif University)
Alsharif, Khalaf (Clinical Laboratories Sciences Department, College of Applied Medical Science, Taif University)
Alsanie, Walaa (Clinical Laboratories Sciences Department, College of Applied Medical Science, Taif University)
Publication Information
Parasites, Hosts and Diseases / v.57, no.3, 2019 , pp. 233-242 More about this Journal
Abstract
Detailed description of malaria in low transmission areas is crucial for elimination. The current study aimed to provide a comprehensive description for malaria transmission in Jazan, a low transmission district, southwestern Saudi Arabia. Patients at a tertiary care hospital were recruited in our study between August 2016 and September 2018. Malaria diagnosis was performed through a species-specific nested polymerase chain reaction (nested PCR), microscopy and Paramax-$3^{TM}$ rapid detection test (RDT). Malaria was detected in 30 patients by the PCR, with point prevalence of 10.9%. Of these malaria infections, 80% was imported, 26.6% was asymptomatic and 23.3% was sub-microscopic. Malaria was reported throughout the year, with February/March and September/October peaks. Infection was significantly more in males than in females (P=0.01). Likewise, infections were detected more in febrile than in non-febrile patients (P=0.01). Adult aged 15-24 years, fever and travel were identified as high-risk factors. Malaria was primarily attributed to Plasmodium falciparum mono-infections, followed by P. vivax mono-infections and lastly to falciparum/vivax mixed infections accounting 76.6%, 16.6%, and 6.6% of PCR-confirmed malaria cases, respectively. The nested PCR was superior to the smear microscopy (sensitivity 76.6%; specificity 100%) and the RDT (sensitivity 83.3%, specificity 94.2%). The overall percent agreement between microscopy and the RDT was 92.7% (kappa=0.63). High proportion of imported malaria including sub-microscopic and sub-patent cases were described. We suggest that incorporation of molecular tool into the conventional malaria diagnosis is beneficial in Jazan district.
Keywords
Malaria diagnosis; nested PCR; Paramax-$3^{TM}$; sub-microscopic/asymptomatic infections; Saudi Arabia;
Citations & Related Records
연도 인용수 순위
  • Reference
1 World Health Organization. World Malaria Report 2017. Geneva, Switzerland. World Health Organization. 2017.
2 Zhou R, Li S, Zhao Y, Yang C, Liu Y, Qian D, Wang H, Lu D, Zhang H. Characterization of Plasmodium ovale spp. imported from Africa to Henan Province, China. Sci Rep 2019; 9: 2191.   DOI
3 Bousema T, Drakeley C. Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clin Microbiol Rev 2011; 24: 377-410.   DOI
4 Bronzan RN, McMorrow ML, Kachur SP. Diagnosis of malaria: challenges for clinicians in endemic and non-endemic regions. Mol Diagn Ther 2008; 12: 299-306.   DOI
5 Mathison BA, Pritt BS. Update on malaria diagnostics and test utilization. J Clin Microbiol 2017; 55: 2009-2017.   DOI
6 Roth JM, Korevaar DA, Leeflang MM, Mens PF. Molecular malaria diagnostics: a systematic review and meta-analysis. Crit Rev Clin Lab Sci 2016; 53: 87-105.   DOI
7 Coleman M, Al-Zahrani MH, Coleman M, Hemingway J, Omar A, Stanton MC, Thomsen EK, Alsheikh AA, Alhakeem RF, McCall PJ, Al Rabeeah AA. A country on the verge of malaria elimination-the Kingdom of Saudi Arabia. PLoS One 2014; 9: e105980.   DOI
8 Al-Zanbagi NA. Review of malaria in Saudi Arabia, current status and future prospects. J Int Acad Res Multidiscip 2014; 2: 1-15.
9 Bousema T, Okell L, Felger I, Drakeley C. Asymptomatic malaria infections: detectability, transmissibility and public health relevance. Nature Rev Microbiol 2014; 12: 833-840.   DOI
10 Lin JT, Saunders DL, Meshnick SR. The role of submicroscopic parasitemia in malaria transmission: what is the evidence? Trends Parasitol 2014; 30: 183-190.   DOI
11 El Hassan IM, Sahly A, Alzahrani MH, Alhakeem RF, Alhelal M, Alhogail A, Alsheikh AA, Assiri AM, ElGamri TB, Faragalla IA, Al-Atas M, Akeel MA, Bani I, Ageely HM, BinSaeed AA, Kyalo D, Noor AM, Snow RW. Progress toward malaria elimination in Jazan Province, Kingdom of Saudi Arabia: 2000-2014. Malaria J 2015; 14: 444.   DOI
12 Isozumi R, Fukui M, Kaneko A, Chan CW, Kawamoto F, Kimura M. Improved detection of malaria cases in island settings of Vanuatu and Kenya by PCR that targets the Plasmodium mitochondrial cytochrome c oxidase III (cox3) gene. Parasitol Int 2015; 64: 304-308.   DOI
13 Dafalla OM, Alsheikh AA, Abakar AD, Mohammed WS, Nour BY, Shrwani KJ, Noureldin EM. Identification of Plasmodium species from outdated blood samples by nested-PCR compared with microscopy diagnosis in Jazan region, Saudi Arabia. Biosci Biotech Res Comm 2017; 10: 68-75.   DOI
14 Sen Z, Al Alsheikh A, Al-Turbak AS, Al-Bassam AM, Al-Dakheel AM. Climate change impact and runoff harvesting in arid regions. Arab J Geosci 2013; 6: 287-295.   DOI
15 Makler MT, Palmer CJ, Ager AL. A review of practical techniques for the diagnosis of malaria. Ann Trop Med Parasitol 1998; 92: 419-433.   DOI
16 Hasona N, Amer O, Raef A. Hematological alterations and parasitological studies among infected patients with Plasmodium vivax and Plasmodium falciparum in Hail, Kingdom of Saudi Arabia. Asian Pac J Trop Dis 2016; 6: 695-658.   DOI
17 Wangdi K, Gatton ML, Kelly GC, Clements AC. Cross-border malaria: a major obstacle for malaria elimination. Adv Parasitol 2015; 89: 79-107.   DOI
18 Soliman RH, Garcia-Aranda P, Elzagawy SM, Hussein BE, Mayah WW, Martin Ramirez A, Ta-Tang TH, Rubio JM. Imported and autochthonous malaria in West Saudi Arabia: results from a reference hospital. Malaria J 2018; 17: 286.   DOI
19 Al Zahrani MH, Omar AI, Abdoon AMO, Ibrahim AA, Alhogail A, Elmubarak M, Elamin YE, AlHelal MA, Alshahrani AM, Abdelgader TM, Saeed I, El Gamri TB, Alattas MS, Dahlan AA, Assiri AM, Maina J, Li XH, Snow RW. Cross-border movement, economic development and malaria elimination in the Kingdom of Saudi Arabia. BMC Med 2018; 16: 98.   DOI
20 Al-Farsi HM, Al-Hashami ZS, Dajem SMB, Al-Sheikh AAH, Al-Qahtani A, Beja-Pereira A, Idris MA, Babiker HA. Source of drug resistant Plasmodium falciparum in a potential malaria elimination site in Saudi Arabia. Infect Genet Evol 2012; 12: 1253-1259.   DOI
21 Alshahrani AM, Abdelgader TM, Mohya M, Jubran S, Abdoon AMO, Daffalla AA, Babiker A, Kyalo D, Noor AM, Al-Zahrani MH, Snow RW. Risk associated with malaria infection in Tihama Qahtan, Aseer region, Kingdom of Saudi Arabia: 2006-2007. Malaria Contr Elimination 2016; 5.
22 Farag E, Bansal D, Chehab MA, Al-Dahshan A, Bala M, Ganesan N, Al Abdulla YA, Al Thani M, Sultan AA, Al-Romaihi H. Epidemiology of Malaria in the State of Qatar, 2008-2015. Mediterr J Hematol Infect Dis 2018; 10: e2018050.   DOI
23 Jenkins R, Omollo R, Ongecha M, Sifuna P, Othieno C, Ongeri L, Kingora J, Ogutu B. Prevalence of malaria parasites in adults and its determinants in malaria endemic area of Kisumu County, Kenya. Malaria J 2015; 14: 263.   DOI
24 Al-Zaydani IA, Al-Hakami A, Kumar A, Abdalla SA, Otaif M, Thiqa R, Ahmed H, Alnahili K. Severe unresolving Plasmodium falciparum malaria following artemisinin combination therapy: Emergence of drug resistance in Saudi Arabia. Indian J Med Microbiol 2016; 34: 553.   DOI
25 Baum E, Sattabongkot J, Sirichaisinthop J, Kiattibutr K, Jain A, Taghavian O, Lee MC, Davies DH, Cui L, Felgner PL, Yan G. Common asymptomatic and sub-microscopic malaria infections in Western Thailand revealed in longitudinal molecular and serological studies: a challenge to malaria elimination. Malaria J 2016; 15: 333.   DOI
26 Bin Dajem SM. Molecular investigation of mixed malaria infections in Southwest Saudi Arabia. Saudi Med J 2015; 36: 248-251.   DOI
27 Gupta B, Gupta P, Sharma A, Singh V, Dash AP, Das A. High proportion of mixed-species Plasmodium infections in India revealed by PCR diagnostic assay. Trop Med Int Health 2010; 15: 819-824.   DOI
28 Dawoud HA, Ageely HM, Heiba AA. Evaluation of a real-time polymerase chain reaction assay for the diagnosis of malaria in patients from Jazan area, Saudi Arabia. J Egypt Soc Parasitol 2008; 38: 339-350.
29 Manjurano A, Okell L, Lukindo T, Reyburn H, Olomi R, Roper C, Clark TG, Joseph S, Riley EM, Drakeley C. Association of sub-microscopic malaria parasite carriage with transmission intensity in north-eastern Tanzania. Malar J 2011; 10: 370.   DOI
30 Al-Harthi SA. Comparison of a genus-specific conventional PCR and a species-specific nested-PCR for malaria diagnosis using FTA collected samples from Kingdom of Saudi Arabia. J Egy Soc Parasitol 2015; 45: 457-466.   DOI
31 Whittaker C, Slater HC, Bousema T, Drakeley C, Ghani A, Okell LC. Variation in the prevalence of sub-microscopic malaria infections: historical transmission intensity and age as key determinants. bioRxiv 2019; 1: 554311.
32 Steenkeste N, Rogers WO, Okell L, Jeanne I, Incardona S, Duval L, Chy S, Hewitt S, Chou M, Socheat D, Babin FX. Sub-microscopic malaria cases and mixed malaria infection in a remote area of high malaria endemicity in Rattanakiri province, Cambodia: implication for malaria elimination. Malaria J 2010; 9: 108.   DOI
33 Ranadive N, Kunene S, Darteh S, Ntshalintshali N, Nhlabathi N, Dlamini N, Chitundu S, Saini M, Murphy M, Soble A, Schwartz A, Greenhouse B, Hsiang MS. Limitations of rapid diagnostic testing in patients with suspected malaria: a diagnostic accuracy evaluation from Swaziland, a low-endemicity country aiming for malaria elimination. Clin Infect Dis 2017; 64: 1221-1227.   DOI
34 Mahende C, Ngasala B, Lusingu J, Yong TS, Lushino P, Lemnge M, Mmbando B, Premji Z. Performance of rapid diagnostic test, blood-film microscopy and PCR for the diagnosis of malaria infection among febrile children from Korogwe district, Tanzania. Malaria J 2016; 15: 391.   DOI
35 Iqbal J, Siddique A, Jameel M, Hira PR. Persistent histidine-rich protein 2, parasite lactate dehydrogenase, and panmalarial antigen reactivity after clearance of Plasmodium falciparum monoinfection. J Clin Microbiol 2004; 42: 4237-4241.   DOI
36 Gatton ML, Ciketic S, Barnwell JW, Cheng Q, Chiodini PL, Incardona S, Bell D, Cunningham J, Gonzalez IJ. An assessment of false positive rates for malaria rapid diagnostic tests caused by non-Plasmodium infectious agents and immunological factors. PLoS One 2018; 13: e0197395.   DOI
37 Koita OA, Doumbo OK, Ouattara A, Tall LK, Konare A, Diakite M, Diallo M, Sagara I, Masinde GL, Doumbo SN, Dolo A. False-negative rapid diagnostic tests for malaria and deletion of the histidine-rich repeat region of the hrp2 gene. Am J Trop Med Hyg 2012; 86: 194-198.   DOI
38 Shakely D, Elfving K, Aydin-Schmidt B, Msellem MI, Morris U, Omar R, Weiping X, Petzold M, Greenhouse B, Baltzell KA, Ali AS, Bjorkman A, Martensson A. The usefulness of rapid diagnostic tests in the new context of low malaria transmission in Zanzibar. PLoS One 2013; 8: e72912.   DOI
39 Kurup R, Marks R. A comparison of microscopic examination and rapid diagnostic tests used in Guyana to diagnose malaria. Malaria Report 2012; 2: e2.   DOI
40 Sepulveda N, Paulino CD, Drakeley C. Sample size and power calculations for detecting changes in malaria transmission using antibody seroconversion rate. Malaria J 2015; 14: 529.   DOI