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Published in: Malaria Journal 1/2018

Open Access 01-12-2018 | Review

On the epidemiology of Plasmodium vivax malaria: past and present with special reference to the former USSR

Authors: Anatoly V. Kondrashin, Lola F. Morozova, Ekaterina V. Stepanova, Natalia A. Turbabina, Maria S. Maksimova, Evgeny N. Morozov

Published in: Malaria Journal | Issue 1/2018

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Abstract

Presently, many malaria-endemic countries in the world are transitioning towards malaria elimination. Out of the 105 countries with ongoing malaria transmission, 10 countries are classified as being in the pre-elimination phase of malaria control, and 9 countries are in the malaria elimination stage, whereas 7 countries are classified as being in the prevention of introduction phase. Between 2000 and 2015, 17 countries eliminated malaria (i.e., attained zero indigenous cases for 3 years or more). Seven countries were certified by the WHO as having successfully eliminated malaria. The purpose of this review was to analyse the epidemiological characteristics of vivax malaria during the various stages of malaria eradication (elimination) programmes in different countries in the past and present. Experiences of the republics of the former USSR with malaria are interesting, particularly since the data overwhelmingly were published in Russian and might not be known to western readers. Among the most important characteristics of Plasmodium vivax epidemiology at present are changes in the ratio of the short-incubation P. vivax to long-incubation P. vivax, the incidence of severe P. vivax cases, the increased numbers of asymptomatic P. vivax cases, the reduced response to anti-malarials and a few others. Various factors contributing towards the peculiarities of P. vivax epidemiology are discussed.
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Literature
1.
go back to reference WHO. World malaria report 2016. Geneva: World Health Organization; 2016. WHO. World malaria report 2016. Geneva: World Health Organization; 2016.
2.
go back to reference WHO. World malaria report 2017. Geneva: World Health Organization; 2017. WHO. World malaria report 2017. Geneva: World Health Organization; 2017.
3.
go back to reference Pampana E. A textbook of malaria eradication. London: Oxford University Press; 1963. Pampana E. A textbook of malaria eradication. London: Oxford University Press; 1963.
4.
go back to reference Duchanina NN. Plasmodium vivax malaria with long incubation, its distribution in the USSR and epidemiological consequences. Thesis, Doctor of Medicine, Moscow, 1957: 60 (in Russian). Duchanina NN. Plasmodium vivax malaria with long incubation, its distribution in the USSR and epidemiological consequences. Thesis, Doctor of Medicine, Moscow, 1957: 60 (in Russian).
5.
go back to reference Rybalka VM, Beljaev AE, Lysenko AY. Population studies on Plasmodium vivax. 2. Distribution of manifestations of Plasmodium vivax in malaria foci. Bull World Health Organ. 1978;55:559–65 (in Russian). Rybalka VM, Beljaev AE, Lysenko AY. Population studies on Plasmodium vivax. 2. Distribution of manifestations of Plasmodium vivax in malaria foci. Bull World Health Organ. 1978;55:559–65 (in Russian).
6.
go back to reference Alekseev AN, Baranova AM. On probable relationship in mosquito vectors of malaria and increase of number of late manifestations of Plasmodium vivax. In: Orlov VS, Duchanina NN, editors. Malaria control in the USSR at present. Moscow; 1985, p. 281–5 (in Russian). Alekseev AN, Baranova AM. On probable relationship in mosquito vectors of malaria and increase of number of late manifestations of Plasmodium vivax. In: Orlov VS, Duchanina NN, editors. Malaria control in the USSR at present. Moscow; 1985, p. 281–5 (in Russian).
7.
go back to reference Sergiev VP, Baranova AM, Kouznetsov RL. Changes in the epidemiological pattern of Plasmodium vivax populations on the territory of the CIS. Giorn Ital Med Trop. 1972;1–4:33–5. Sergiev VP, Baranova AM, Kouznetsov RL. Changes in the epidemiological pattern of Plasmodium vivax populations on the territory of the CIS. Giorn Ital Med Trop. 1972;1–4:33–5.
8.
go back to reference Baranova AM, Sergiev VP. Changes in the characteristics of manifestations of Plasmodium vivax in the CIS. Med Parazitol (Mosk). 1995;1:11–3 (in Russian). Baranova AM, Sergiev VP. Changes in the characteristics of manifestations of Plasmodium vivax in the CIS. Med Parazitol (Mosk). 1995;1:11–3 (in Russian).
9.
go back to reference Sergiev VP, Baranova AM, Arsenieva LP. Importation of malaria to the USSR from Afghanistan. Med Parazitol (Mosk). 1992;3:15–7 (in Russian). Sergiev VP, Baranova AM, Arsenieva LP. Importation of malaria to the USSR from Afghanistan. Med Parazitol (Mosk). 1992;3:15–7 (in Russian).
10.
go back to reference Adak T, Sharma VP, Orlov VS. Studies on the relapse pattern in Delhi, India. Am J Trop Med Hyg. 1998;59:175–9.CrossRef Adak T, Sharma VP, Orlov VS. Studies on the relapse pattern in Delhi, India. Am J Trop Med Hyg. 1998;59:175–9.CrossRef
11.
go back to reference Kim JR, Nandy A, Maji AK, Addy M, Dondorp AM, Day NP, et al. Genotyping of Plasmodium vivax reveals both short and long latency relapse patterns in Kolkata. PLoS ONE. 2012;7:e39645.CrossRef Kim JR, Nandy A, Maji AK, Addy M, Dondorp AM, Day NP, et al. Genotyping of Plasmodium vivax reveals both short and long latency relapse patterns in Kolkata. PLoS ONE. 2012;7:e39645.CrossRef
13.
go back to reference Shu H, Lou S, Lin D, Fu R. Observations on hypnozoite of different isolates of Plasmodium vivax in untreated malaria. Zhongguo Ji Sheng Chong. 1995;13:185–8 (in Chinese). Shu H, Lou S, Lin D, Fu R. Observations on hypnozoite of different isolates of Plasmodium vivax in untreated malaria. Zhongguo Ji Sheng Chong. 1995;13:185–8 (in Chinese).
14.
go back to reference Yang BL, Wang WJ, Wang WR, Hu HX, Li HX, Li XL, et al. Experimental studies on the biological characteristics of Plasmodium vivax in South Yunan. Zhongguo Ji Sheng Chong. 1986;4:101–4 (in Chinese). Yang BL, Wang WJ, Wang WR, Hu HX, Li HX, Li XL, et al. Experimental studies on the biological characteristics of Plasmodium vivax in South Yunan. Zhongguo Ji Sheng Chong. 1986;4:101–4 (in Chinese).
15.
go back to reference Kondrashin AV, Baranova AM, Sergiev VP. Widespread use of primaquine for control of Plasmodium vivax epidemics in a population with varying degrees of G6PD deficiency. Med Parazitol (Mosk). 2010;4:29–34 (in Russian). Kondrashin AV, Baranova AM, Sergiev VP. Widespread use of primaquine for control of Plasmodium vivax epidemics in a population with varying degrees of G6PD deficiency. Med Parazitol (Mosk). 2010;4:29–34 (in Russian).
16.
go back to reference Srivastava HC, Sharma SK, Bhatt RM, Sharma VP. Studies on Plasmodium vivax relapse pattern in Kheda district, Gujarat. Indian J Malariol. 1996;33:173–9.PubMed Srivastava HC, Sharma SK, Bhatt RM, Sharma VP. Studies on Plasmodium vivax relapse pattern in Kheda district, Gujarat. Indian J Malariol. 1996;33:173–9.PubMed
17.
go back to reference Asma UE, Taufiq F, Khan W. Prevalence and clinical manifestations of malaria in Aligarh, India. Korean J Parasitol. 2014;52:621–9.CrossRef Asma UE, Taufiq F, Khan W. Prevalence and clinical manifestations of malaria in Aligarh, India. Korean J Parasitol. 2014;52:621–9.CrossRef
18.
go back to reference Kassirski IA, Plotnikov NN. The diseases in countries with hot climate. Moscow: Medgiz; 1964 (in Russian). Kassirski IA, Plotnikov NN. The diseases in countries with hot climate. Moscow: Medgiz; 1964 (in Russian).
19.
go back to reference Tareev EM. Clinical malaria. Moscow: Medgiz; 1946. Tareev EM. Clinical malaria. Moscow: Medgiz; 1946.
20.
go back to reference Loban K, Polozok E. Le paludisme. Paris: MEDSI; 1983. p. 311. Loban K, Polozok E. Le paludisme. Paris: MEDSI; 1983. p. 311.
21.
go back to reference Baird JK. Evidence and implications of mortality associated with acute Plasmodium vivax malaria. Clin Microbiol Rev. 2013;26:36–57.CrossRef Baird JK. Evidence and implications of mortality associated with acute Plasmodium vivax malaria. Clin Microbiol Rev. 2013;26:36–57.CrossRef
22.
go back to reference Douglas NM, Pontoronig G, Lampah DA, Yeo TW, Kenagalem E, Poespoprodjo JR, et al. Mortality attributable to Plasmodium vivax malaria: a clinical audit from Papua, Indonesia. BMC Med. 2014;12:217–8.CrossRef Douglas NM, Pontoronig G, Lampah DA, Yeo TW, Kenagalem E, Poespoprodjo JR, et al. Mortality attributable to Plasmodium vivax malaria: a clinical audit from Papua, Indonesia. BMC Med. 2014;12:217–8.CrossRef
23.
go back to reference Limaye CS, Londhey VA, Nabar ST. The study of complications of vivax malaria in comparison with Plasmodium falciparum malaria in Mumbai. J Assoc Physic India. 2012;60:15–8. Limaye CS, Londhey VA, Nabar ST. The study of complications of vivax malaria in comparison with Plasmodium falciparum malaria in Mumbai. J Assoc Physic India. 2012;60:15–8.
24.
go back to reference Naing C, Whittaker MA, Wai VN, Mak JW. Is Plasmodium vivax malaria a severe malaria? A systematic review and meta-analysis. PLoS Negl Trop Dis. 2014;8:e3071.CrossRef Naing C, Whittaker MA, Wai VN, Mak JW. Is Plasmodium vivax malaria a severe malaria? A systematic review and meta-analysis. PLoS Negl Trop Dis. 2014;8:e3071.CrossRef
25.
go back to reference Rahimi BA, Thakkinstian A, White NJ, Sirivichyaku C, Dondorp AM, Chokeijindachai W. Severe vivax malaria: a systematic review and meta-analysis of clinical studies since 1900. Malar J. 2014;13:481.CrossRef Rahimi BA, Thakkinstian A, White NJ, Sirivichyaku C, Dondorp AM, Chokeijindachai W. Severe vivax malaria: a systematic review and meta-analysis of clinical studies since 1900. Malar J. 2014;13:481.CrossRef
26.
go back to reference WHO. World malaria report 2014. Geneva: World Health Organization; 2014. WHO. World malaria report 2014. Geneva: World Health Organization; 2014.
27.
go back to reference Joshi H, Prajapati SK, Verma A, Kanga’a S, Carlton JM. Plasmodium vivax in India. Trends Parasitol. 2008;24:228–35.CrossRef Joshi H, Prajapati SK, Verma A, Kanga’a S, Carlton JM. Plasmodium vivax in India. Trends Parasitol. 2008;24:228–35.CrossRef
28.
go back to reference Lampah DA, Yeo TW, Malloy M, Kenangalem E, Douglas NM, Ronaldo D, et al. Severe malarial trombocytopenia: a risk factor for mortality in Papua, Indonesia. J Infect Dis. 2015;211:623–34.CrossRef Lampah DA, Yeo TW, Malloy M, Kenangalem E, Douglas NM, Ronaldo D, et al. Severe malarial trombocytopenia: a risk factor for mortality in Papua, Indonesia. J Infect Dis. 2015;211:623–34.CrossRef
29.
go back to reference Baird K. Origins and implications of neglect of G6PD deficiency and primaquine toxicity in Plasmodium vivax malaria. Pathog Glob Health. 2015;109:91–104.CrossRef Baird K. Origins and implications of neglect of G6PD deficiency and primaquine toxicity in Plasmodium vivax malaria. Pathog Glob Health. 2015;109:91–104.CrossRef
30.
go back to reference Kochar DK, Das A, Kochar A, Middha S, Acharya J, Tanwar GS, et al. A prospective study on adult patients of severe malaria caused by Plasmodium falciparum, Plasmodium vivax and mixed infections from Bikaner, northwest India. J Vector Borne Dis. 2014;51:200–10.PubMed Kochar DK, Das A, Kochar A, Middha S, Acharya J, Tanwar GS, et al. A prospective study on adult patients of severe malaria caused by Plasmodium falciparum, Plasmodium vivax and mixed infections from Bikaner, northwest India. J Vector Borne Dis. 2014;51:200–10.PubMed
31.
go back to reference Poespoprodjo JR, Fobia W, Kenangalem E, Lampah DA, Hasanuddin A, Warikar N, et al. Vivax malaria: a major cause of morbidity in early infancy. Clin Infect Dis. 2009;48:1704–12.CrossRef Poespoprodjo JR, Fobia W, Kenangalem E, Lampah DA, Hasanuddin A, Warikar N, et al. Vivax malaria: a major cause of morbidity in early infancy. Clin Infect Dis. 2009;48:1704–12.CrossRef
32.
go back to reference Douglas NM, Anstey NM, Buffet PA, Poespoprodio JR, Yeo TW, White NJ, et al. The anaemia of Plasmodium vivax malaria. Malar J. 2012;11:135.CrossRef Douglas NM, Anstey NM, Buffet PA, Poespoprodio JR, Yeo TW, White NJ, et al. The anaemia of Plasmodium vivax malaria. Malar J. 2012;11:135.CrossRef
33.
go back to reference Quispe AM, Pozio E, Guerrero E, Durand S, Baldeviano GC, Edgel KA, et al. Plasmodium vivax hospitalizations in monoendemic malaria region: severe vivax malaria? Am J Trop Med Hyg. 2014;91:11–7.CrossRef Quispe AM, Pozio E, Guerrero E, Durand S, Baldeviano GC, Edgel KA, et al. Plasmodium vivax hospitalizations in monoendemic malaria region: severe vivax malaria? Am J Trop Med Hyg. 2014;91:11–7.CrossRef
34.
go back to reference Kondrashin AV, Baranova AM, Morozova LF, Stepanova EV. Actual tasks of malaria elimination. Med Parazitol (Mosk). 2011;3:3–9 (in Russian). Kondrashin AV, Baranova AM, Morozova LF, Stepanova EV. Actual tasks of malaria elimination. Med Parazitol (Mosk). 2011;3:3–9 (in Russian).
35.
go back to reference Moshkovski SD. Basic principles of malaria epidemiology. Moscow: USSR Academy of Medical Science; 1950. p. 5–11 (in Russian). Moshkovski SD. Basic principles of malaria epidemiology. Moscow: USSR Academy of Medical Science; 1950. p. 5–11 (in Russian).
36.
go back to reference Duchanina NN. Distribution of P. vivax malaria with long incubation period in the USSR. In: Proceedings of Martzinovski Institute of Medical Parasitology and Tropical Medicine, 1959, Moscow, p. 103–106 (in Russian). Duchanina NN. Distribution of P. vivax malaria with long incubation period in the USSR. In: Proceedings of Martzinovski Institute of Medical Parasitology and Tropical Medicine, 1959, Moscow, p. 103–106 (in Russian).
37.
go back to reference Baranova AM. Characteristics of epidemiological process of malaria in Tajik SSR under malaria control. In: Orlov VS, editor. Actual malaria problems, Ministry of Health, Kurgan Tube [Tajik SSR] 1988:63–72 (in Russian). Baranova AM. Characteristics of epidemiological process of malaria in Tajik SSR under malaria control. In: Orlov VS, editor. Actual malaria problems, Ministry of Health, Kurgan Tube [Tajik SSR] 1988:63–72 (in Russian).
38.
go back to reference Baranova AM, Losev OL, Sabgaida TP. Peculiarities of epidemiological process in malaria foci of various types in Geokchai district of Azerbaijan SSR. In: Orlov VS, Duchanina NN, editors. Malaria control in the USSR at present. Moscow: Ministry of Health; 1985. p. 57–67 (in Russian). Baranova AM, Losev OL, Sabgaida TP. Peculiarities of epidemiological process in malaria foci of various types in Geokchai district of Azerbaijan SSR. In: Orlov VS, Duchanina NN, editors. Malaria control in the USSR at present. Moscow: Ministry of Health; 1985. p. 57–67 (in Russian).
39.
go back to reference Baranova AM. Malaria in Russia and in the CIS. Med Parazitol (Mosk). 1988;3:58–60 (in Russian). Baranova AM. Malaria in Russia and in the CIS. Med Parazitol (Mosk). 1988;3:58–60 (in Russian).
40.
go back to reference Sergiev VP, Baranova AM, Sabgaida TP. Decreasing P. vivax parasitaemia in the blood films of patients in malaria residual foci. Abstracts, II European Congress of Parasitology, Paris, France, 1995:28. Sergiev VP, Baranova AM, Sabgaida TP. Decreasing P. vivax parasitaemia in the blood films of patients in malaria residual foci. Abstracts, II European Congress of Parasitology, Paris, France, 1995:28.
41.
go back to reference Abdullaev HI, Davidova MA, Ahmedova AA, Djafarov AA. On activities of Central Control Laboratory of Parasitology Department of the Republican Sanitary Epidemiological Station of Azerbaijan. In: Orlov VS, editor. Actual problems of malaria. Moscow: Ministry of Health; 1988. p. 100–3 (in Russian). Abdullaev HI, Davidova MA, Ahmedova AA, Djafarov AA. On activities of Central Control Laboratory of Parasitology Department of the Republican Sanitary Epidemiological Station of Azerbaijan. In: Orlov VS, editor. Actual problems of malaria. Moscow: Ministry of Health; 1988. p. 100–3 (in Russian).
42.
go back to reference WHO. Guidelines for the treatment of malaria. 3rd ed. Geneva: World Health Organization; 2015. WHO. Guidelines for the treatment of malaria. 3rd ed. Geneva: World Health Organization; 2015.
43.
go back to reference Sergiev PG, Yakusheva AI. Control of malaria in the USSR. Moscow: Medgiz; 1956. p. 308 (in Russian). Sergiev PG, Yakusheva AI. Control of malaria in the USSR. Moscow: Medgiz; 1956. p. 308 (in Russian).
44.
go back to reference Bakradze GL, Macharadze TG. On clinical manifestations of P. vivax malaria and some parasitological changes during consolidation phase of malaria eradication in Georgia. Transactions of Virsaladze Institute of Medical Parasitology and Tropical Medicine, Tbilisi, 1965; p. 49–50 (in Russian). Bakradze GL, Macharadze TG. On clinical manifestations of P. vivax malaria and some parasitological changes during consolidation phase of malaria eradication in Georgia. Transactions of Virsaladze Institute of Medical Parasitology and Tropical Medicine, Tbilisi, 1965; p. 49–50 (in Russian).
45.
go back to reference Rabinovich SA, Kondrashin AV, Tokmalaev AK, Maksakovskaya EV, Sadikova VD, Burchik MA, et al. Peculiarities of imported P. vivax malaria caused by Chesson-like strains. Med Parazitol (Mosk). 2012;4:7–11 (in Russian). Rabinovich SA, Kondrashin AV, Tokmalaev AK, Maksakovskaya EV, Sadikova VD, Burchik MA, et al. Peculiarities of imported P. vivax malaria caused by Chesson-like strains. Med Parazitol (Mosk). 2012;4:7–11 (in Russian).
46.
go back to reference Kondrashin AV. Materials and approaches to malaria stratification in relation to the rational use of antimalarial drugs in South Asia. WHO/MAL/987;1035:3–51 (in Russian). Kondrashin AV. Materials and approaches to malaria stratification in relation to the rational use of antimalarial drugs in South Asia. WHO/MAL/987;1035:3–51 (in Russian).
47.
go back to reference Basavaraj HR. Observations on the treatment of 678 malaria cases with primaquine in an area free from malaria transmission in Mysore State, India. Indian J Malariol. 1960;14:269–81.PubMed Basavaraj HR. Observations on the treatment of 678 malaria cases with primaquine in an area free from malaria transmission in Mysore State, India. Indian J Malariol. 1960;14:269–81.PubMed
48.
go back to reference Sharma RC, Gautam AS, Orlov V, Sharma VP. Relapse pattern of Plasmodium vivax in Kheda district, Gujarat. Indian J Malariol. 1990;27:95–9.PubMed Sharma RC, Gautam AS, Orlov V, Sharma VP. Relapse pattern of Plasmodium vivax in Kheda district, Gujarat. Indian J Malariol. 1990;27:95–9.PubMed
49.
go back to reference Gogtay N, Carg M, Kadam V, Kamtekar K, Kshirsagar NA. A 5-day primaquine regimen an antirelapse therapy for Plasmodium vivax. Trans R Soc Trop Med. 1998;92:341.CrossRef Gogtay N, Carg M, Kadam V, Kamtekar K, Kshirsagar NA. A 5-day primaquine regimen an antirelapse therapy for Plasmodium vivax. Trans R Soc Trop Med. 1998;92:341.CrossRef
50.
go back to reference Adak T, Valecha N, Sharma VP. Plasmodium vivax polymorphism in a clinical trial. Clin Diagn Lab Immunol. 2001;8:891–4.PubMedPubMedCentral Adak T, Valecha N, Sharma VP. Plasmodium vivax polymorphism in a clinical trial. Clin Diagn Lab Immunol. 2001;8:891–4.PubMedPubMedCentral
51.
go back to reference Yadav RS, Ghosh SK. Radical curative efficacy of five-day regimen of primaquine for treatment of Plasmodium vivax in India. J Parasitol. 2002;88:1042–4.CrossRef Yadav RS, Ghosh SK. Radical curative efficacy of five-day regimen of primaquine for treatment of Plasmodium vivax in India. J Parasitol. 2002;88:1042–4.CrossRef
52.
go back to reference Anvikar AR, Arora U, Sonal GS, Mishra N, Shatri B, Savargaonkar D, et al. Antimalarial drug policy in India: past, present and future. Indian J Med Res. 2014;139:205–15.PubMedPubMedCentral Anvikar AR, Arora U, Sonal GS, Mishra N, Shatri B, Savargaonkar D, et al. Antimalarial drug policy in India: past, present and future. Indian J Med Res. 2014;139:205–15.PubMedPubMedCentral
53.
go back to reference Rashina MG. Role of asymptomatic malaria in epidemiology of malaria. News Medicine. 1952;27:22–8 (in Russian). Rashina MG. Role of asymptomatic malaria in epidemiology of malaria. News Medicine. 1952;27:22–8 (in Russian).
54.
go back to reference Jukova TA, Gozodova GE, Prisyagin LA. On asymptomatic malaria carriers of P. vivax in Massali district of Azerbaijan SSR. Med Parazitol (Mosk). 1961;5:572–9 (in Russian). Jukova TA, Gozodova GE, Prisyagin LA. On asymptomatic malaria carriers of P. vivax in Massali district of Azerbaijan SSR. Med Parazitol (Mosk). 1961;5:572–9 (in Russian).
55.
go back to reference Harris I, Sharrock WW, Main LM, Gray KA, Bobogare A, Boaz L, et al. A large proportion of asymptomatic Plasmodium infections with low and sub-microscopic parasite densities in the low transmission setting of Temotu Province, Solomon Islands: challenges for malaria diagnostics in an elimination setting. Malar J. 2010;9:254.CrossRef Harris I, Sharrock WW, Main LM, Gray KA, Bobogare A, Boaz L, et al. A large proportion of asymptomatic Plasmodium infections with low and sub-microscopic parasite densities in the low transmission setting of Temotu Province, Solomon Islands: challenges for malaria diagnostics in an elimination setting. Malar J. 2010;9:254.CrossRef
56.
go back to reference Starzengruber P, Fuehrer HP, Ley B, Thrimer K, Swoboda P, Habler VE, et al. High prevalence of asymptomatic malaria in south-eastern Bangladesh. Malar J. 2014;13:6.CrossRef Starzengruber P, Fuehrer HP, Ley B, Thrimer K, Swoboda P, Habler VE, et al. High prevalence of asymptomatic malaria in south-eastern Bangladesh. Malar J. 2014;13:6.CrossRef
57.
go back to reference Lysenko AY, Kondrashin AV, Ejov MN. Malariology. 2nd ed. Copenhagen: World Health Organization, Regional Office for Europe; 2003. Lysenko AY, Kondrashin AV, Ejov MN. Malariology. 2nd ed. Copenhagen: World Health Organization, Regional Office for Europe; 2003.
58.
go back to reference Yakusheva AI. Malaria curve types and relationship spring new cases of malaria with autumn incidence. Med Parazitol (Mosk). 1939;3:262–80 (in Russian). Yakusheva AI. Malaria curve types and relationship spring new cases of malaria with autumn incidence. Med Parazitol (Mosk). 1939;3:262–80 (in Russian).
59.
go back to reference Remennikova MA. Importance of asymptomatic malaria carriers in P. vivax and P. falciparum in malaria epidemiology and magnitude of it in intensive malaria focus. Med Parazitol (Mosk). 1943;4:47–57 (in Russian). Remennikova MA. Importance of asymptomatic malaria carriers in P. vivax and P. falciparum in malaria epidemiology and magnitude of it in intensive malaria focus. Med Parazitol (Mosk). 1943;4:47–57 (in Russian).
60.
go back to reference Lin JT, Saunders DL, Meshnick SR. The role of submicroscopic parasitemia in malaria transmission: what is the evidence? Trends Parasitol. 2014;30:183–90.CrossRef Lin JT, Saunders DL, Meshnick SR. The role of submicroscopic parasitemia in malaria transmission: what is the evidence? Trends Parasitol. 2014;30:183–90.CrossRef
61.
go back to reference Laishram DD, Sutton PL, Nanda N, Sharma WL, Sobti RC, Carlton JM, et al. The complexities of malaria disease manifestations with a focus on asymptomatic malaria. Malar J. 2012;11:29.CrossRef Laishram DD, Sutton PL, Nanda N, Sharma WL, Sobti RC, Carlton JM, et al. The complexities of malaria disease manifestations with a focus on asymptomatic malaria. Malar J. 2012;11:29.CrossRef
62.
go back to reference Howes RE, Piel FB, Patil AP, Nyangiri OA, Gething PW, Dewi M, et al. G6PD deficiency prevalence and estimates of affected populations in malaria endemic countries: a geostatistical model-based map. PLoS Med. 2012;9:1001339.CrossRef Howes RE, Piel FB, Patil AP, Nyangiri OA, Gething PW, Dewi M, et al. G6PD deficiency prevalence and estimates of affected populations in malaria endemic countries: a geostatistical model-based map. PLoS Med. 2012;9:1001339.CrossRef
63.
go back to reference Allison AC, Clyde DF. Malaria in African children with deficient erythrocyte glucose-6-phosphate dehydrogenase. Br Med J. 1961;1:1346–9.CrossRef Allison AC, Clyde DF. Malaria in African children with deficient erythrocyte glucose-6-phosphate dehydrogenase. Br Med J. 1961;1:1346–9.CrossRef
64.
go back to reference Livingstone FB. Aspects of the population dynamics of the abnormal hemoglobin and glucose-6-phosphate dehydrogenase deficiency genes. Am J Human Genet. 1965;16(4):435–50. Livingstone FB. Aspects of the population dynamics of the abnormal hemoglobin and glucose-6-phosphate dehydrogenase deficiency genes. Am J Human Genet. 1965;16(4):435–50.
65.
go back to reference Siniscalco M, Bernini G, Filippi B, Latte P, Khan M, Piomelli S, et al. Population genetics of haemoglobin variants, thalassaemia and glucose-6-phosphate dehydrogenase deficiency, with particular reference to the malaria hypothesis. Bull World Health Organ. 1966;34:379–93.PubMedPubMedCentral Siniscalco M, Bernini G, Filippi B, Latte P, Khan M, Piomelli S, et al. Population genetics of haemoglobin variants, thalassaemia and glucose-6-phosphate dehydrogenase deficiency, with particular reference to the malaria hypothesis. Bull World Health Organ. 1966;34:379–93.PubMedPubMedCentral
66.
go back to reference Cappadoro M, Giribaldi G, O’Brien E, Turrini F, Mannu F, Ulliers D, et al. Early phagocytosis of glucose-6-dehydrogenease (G6PD)-deficient erythrocytes parasitized by Plasmodium falciparum may explain malaria protection in G6PD deficiency. Blood. 1998;92:2527–34.PubMed Cappadoro M, Giribaldi G, O’Brien E, Turrini F, Mannu F, Ulliers D, et al. Early phagocytosis of glucose-6-dehydrogenease (G6PD)-deficient erythrocytes parasitized by Plasmodium falciparum may explain malaria protection in G6PD deficiency. Blood. 1998;92:2527–34.PubMed
67.
go back to reference Alexeeva MI, Abrashkin-Jouckov RG, Lysenko AY, Glazunova ZI, Gorbunova YP, Mirsiyabov AU, et al. Distribution of the G6PD deficiency in Azerbaijan and its malariological significance. In: Lysenko AY, editor. Actual problems of malaria prevention in the USSR. Baku: Ministry of Health; 1973. p. 91–4 (in Russian). Alexeeva MI, Abrashkin-Jouckov RG, Lysenko AY, Glazunova ZI, Gorbunova YP, Mirsiyabov AU, et al. Distribution of the G6PD deficiency in Azerbaijan and its malariological significance. In: Lysenko AY, editor. Actual problems of malaria prevention in the USSR. Baku: Ministry of Health; 1973. p. 91–4 (in Russian).
68.
go back to reference Santana MS, de Lacerda MVG, Barbosa MD, Alecrim WD, Alecrim M. Glucose-6-phosphate dehydrogenase deficiency in an endemic area of malaria in Manaus: a cross-sectional survey in the Brazilian Amazon. PLoS ONE. 2009;4:e5259.CrossRef Santana MS, de Lacerda MVG, Barbosa MD, Alecrim WD, Alecrim M. Glucose-6-phosphate dehydrogenase deficiency in an endemic area of malaria in Manaus: a cross-sectional survey in the Brazilian Amazon. PLoS ONE. 2009;4:e5259.CrossRef
69.
go back to reference Santana MS, Monteiro WM, Siqueira AM, Costa MF, Sampaio L, Lacerda MV, et al. Glucose-6-phosphate degydrogenase deficient variants are associated with reduced susceptibility to malaria in the Brazilian Amazon. Trans R Soc Trop Med Hyg. 2013;107:301–6.CrossRef Santana MS, Monteiro WM, Siqueira AM, Costa MF, Sampaio L, Lacerda MV, et al. Glucose-6-phosphate degydrogenase deficient variants are associated with reduced susceptibility to malaria in the Brazilian Amazon. Trans R Soc Trop Med Hyg. 2013;107:301–6.CrossRef
70.
go back to reference Monteiro WM, Franca GP, Melo GC, Queiroz ALM, Brito M, Peixoto HM, et al. Clinical complications of G6PD deficiency in Latin American and Caribbean populations: systematic review and implications for malaria elimination programmes. Malar J. 2014;13:70.CrossRef Monteiro WM, Franca GP, Melo GC, Queiroz ALM, Brito M, Peixoto HM, et al. Clinical complications of G6PD deficiency in Latin American and Caribbean populations: systematic review and implications for malaria elimination programmes. Malar J. 2014;13:70.CrossRef
71.
go back to reference Bancone G, Chu CS, Somsakchaicharoen R, Chowwiwat N, Parker DM, Charunwattana P, et al. Characterization of G6PD genotypes and phenotypes on the Northwestern Thailand-Myanmar border. PLoS ONE. 2014;9:e0116063.CrossRef Bancone G, Chu CS, Somsakchaicharoen R, Chowwiwat N, Parker DM, Charunwattana P, et al. Characterization of G6PD genotypes and phenotypes on the Northwestern Thailand-Myanmar border. PLoS ONE. 2014;9:e0116063.CrossRef
72.
go back to reference Baird JK, Battle KE, Howes RE. Primaquine ineligibility in anti-relapse therapy of Plasmodium vivax malaria: the problem of G6PD deficiency and cytochrome P-450 2D6 polymorphisms. Malar J. 2018;17:42.CrossRef Baird JK, Battle KE, Howes RE. Primaquine ineligibility in anti-relapse therapy of Plasmodium vivax malaria: the problem of G6PD deficiency and cytochrome P-450 2D6 polymorphisms. Malar J. 2018;17:42.CrossRef
73.
go back to reference Kondrashin AV, Baranova AM, Ashley EA, Recht J, White NJ, Sergiev VP. Mass primaquine treatment to eliminate vivax malaria: lessons from the past. Malar J. 2014;13:51.CrossRef Kondrashin AV, Baranova AM, Ashley EA, Recht J, White NJ, Sergiev VP. Mass primaquine treatment to eliminate vivax malaria: lessons from the past. Malar J. 2014;13:51.CrossRef
74.
go back to reference Warrell DA, Gilles HM. Essential malariology. 4th ed. London: Arnold; 2002. Warrell DA, Gilles HM. Essential malariology. 4th ed. London: Arnold; 2002.
75.
go back to reference Mestiashvili IG. Study on the genogeography of beta-thalassemia with regards to the “malaria hypothesis”. Vestn Akad Med Nauk SSSR. 1984;51:156–265 (in Russian). Mestiashvili IG. Study on the genogeography of beta-thalassemia with regards to the “malaria hypothesis”. Vestn Akad Med Nauk SSSR. 1984;51:156–265 (in Russian).
76.
go back to reference Voronov AA, Gordeuk VR. Genogeography of hemoglobinopathies in the USSR. In: Winter WP, editor. Hemoglobin variants in human populations. Boca Raton: CRC Press, Inc; 1987. Voronov AA, Gordeuk VR. Genogeography of hemoglobinopathies in the USSR. In: Winter WP, editor. Hemoglobin variants in human populations. Boca Raton: CRC Press, Inc; 1987.
77.
go back to reference Nacher M. Interactions between worms and malaria: good worms or bad worms? Malar J. 2011;10:259.CrossRef Nacher M. Interactions between worms and malaria: good worms or bad worms? Malar J. 2011;10:259.CrossRef
78.
go back to reference Nacher M, Singhasicanon P, Traore B, Dejvorakul S, Phumratanaprapin W, Looareesuwan S, et al. Hookworm infection is associated with decreased body temperature during mild Plasmodium falciparum malaria. Am J Trop Med Hyg. 2001;65:136–7.CrossRef Nacher M, Singhasicanon P, Traore B, Dejvorakul S, Phumratanaprapin W, Looareesuwan S, et al. Hookworm infection is associated with decreased body temperature during mild Plasmodium falciparum malaria. Am J Trop Med Hyg. 2001;65:136–7.CrossRef
79.
go back to reference Nacher M, Singhasicanon P, Treeptassetsu S, Krudsood S, Gay F, Mazier D, et al. Association of helminth infections with increased gametocyte carriage during mild falciparum malaria in Thailand. Am J Trop Med Hyg. 2001;65:644–7.CrossRef Nacher M, Singhasicanon P, Treeptassetsu S, Krudsood S, Gay F, Mazier D, et al. Association of helminth infections with increased gametocyte carriage during mild falciparum malaria in Thailand. Am J Trop Med Hyg. 2001;65:644–7.CrossRef
80.
go back to reference Nacher M. Helminth-infected patients with malaria: a low profile transmission hub? Malar J. 2012;1:376.CrossRef Nacher M. Helminth-infected patients with malaria: a low profile transmission hub? Malar J. 2012;1:376.CrossRef
81.
go back to reference Doumbo S, Tran TM, Sangala J, Li S, Doumtabe D, Kone Y, et al. Co-infection of long-term carriers of Plasmodium falciparum with Schistosoma haematobium enhances protection from febrile malaria; a prospective cohort study in Mali. PLoS Negl Trop Dis. 2014;9:e3154.CrossRef Doumbo S, Tran TM, Sangala J, Li S, Doumtabe D, Kone Y, et al. Co-infection of long-term carriers of Plasmodium falciparum with Schistosoma haematobium enhances protection from febrile malaria; a prospective cohort study in Mali. PLoS Negl Trop Dis. 2014;9:e3154.CrossRef
82.
go back to reference Whitworth J, Morgan D, Qudley M, Smith A, Mayania B, Eotu H, et al. Effect of HIV-1 and increasing immunosuppression on malaria parasitaemia and clinical episodes in adults in rural Uganda: a cohort study. Lancet. 2000;356:105–60.CrossRef Whitworth J, Morgan D, Qudley M, Smith A, Mayania B, Eotu H, et al. Effect of HIV-1 and increasing immunosuppression on malaria parasitaemia and clinical episodes in adults in rural Uganda: a cohort study. Lancet. 2000;356:105–60.CrossRef
83.
go back to reference Berg A, Patel S, Aukrust P, David C, Gonca M, Berg ES, et al. Increased severity and mortality in adults co-infected with malaria and HIV in Maputo, Mozambique: a prospective cross-sectional study. PLoS ONE. 2014;9:e88257.CrossRef Berg A, Patel S, Aukrust P, David C, Gonca M, Berg ES, et al. Increased severity and mortality in adults co-infected with malaria and HIV in Maputo, Mozambique: a prospective cross-sectional study. PLoS ONE. 2014;9:e88257.CrossRef
84.
go back to reference Okonkwo IR, Ibadin MO, Omoigberale AI, Sadon WE. Effect of HIV-1 serostatus on the prevalence of asymptomatic malaria Plasmodium falciparum parasitaemia among children less than 5-year of age in Benin city, Nigeria. J Pediatric Infect Dis Soc. 2016;5:21–8.CrossRef Okonkwo IR, Ibadin MO, Omoigberale AI, Sadon WE. Effect of HIV-1 serostatus on the prevalence of asymptomatic malaria Plasmodium falciparum parasitaemia among children less than 5-year of age in Benin city, Nigeria. J Pediatric Infect Dis Soc. 2016;5:21–8.CrossRef
85.
go back to reference Bharti AR, Saravanan S, Madhavan V, Smith DM, Sharma J, Balakrishnan R, et al. Correlates of HIV and malaria co-infection in southern India. Malar J. 2012;11:306.CrossRef Bharti AR, Saravanan S, Madhavan V, Smith DM, Sharma J, Balakrishnan R, et al. Correlates of HIV and malaria co-infection in southern India. Malar J. 2012;11:306.CrossRef
86.
go back to reference Alemayehu G, Melaki Z, Abreha T, Alemayehu B, Girma S, Tadesse Y, et al. Burden of malaria among adult patients attending general medical department and HIV care and treatment clinics in Oromia, Ethiopia: a comparative cross-sectional study. Malar J. 2015;14:501.CrossRef Alemayehu G, Melaki Z, Abreha T, Alemayehu B, Girma S, Tadesse Y, et al. Burden of malaria among adult patients attending general medical department and HIV care and treatment clinics in Oromia, Ethiopia: a comparative cross-sectional study. Malar J. 2015;14:501.CrossRef
87.
go back to reference Golassa L, Enweji N, Erko B, Aseffa A, Swedberg G. Detection of a substantial number of sub-microscopic Plasmodium falciparum infections by polymerase chain reaction: a potential threat to malaria control and diagnosis in Ethiopia. Malar J. 2013;12:352.CrossRef Golassa L, Enweji N, Erko B, Aseffa A, Swedberg G. Detection of a substantial number of sub-microscopic Plasmodium falciparum infections by polymerase chain reaction: a potential threat to malaria control and diagnosis in Ethiopia. Malar J. 2013;12:352.CrossRef
88.
go back to reference Tadesse FG, Pett H, Baidjoe A, Lanke K, Grignard L, Sutherland C, et al. Submicroscopic carriage of Plasmodium and Plasmodium vivax in low endemic area in Ethiopia where no parasitaemia was detected by microscopy or rapid diagnostic test. Malar J. 2015;14:303.CrossRef Tadesse FG, Pett H, Baidjoe A, Lanke K, Grignard L, Sutherland C, et al. Submicroscopic carriage of Plasmodium and Plasmodium vivax in low endemic area in Ethiopia where no parasitaemia was detected by microscopy or rapid diagnostic test. Malar J. 2015;14:303.CrossRef
89.
go back to reference Mirahmad H, Shahrakipur A, Mehravarana A, Khorashad AS, Rahmati-Balaghaleh M, Zarean M. Evaluation of malaria multiplex/nested PCR performance at low parasite densities and mixed infection in Iran: a country close to malaria elimination. Insect Genet Evol. 2018;65:283–7.CrossRef Mirahmad H, Shahrakipur A, Mehravarana A, Khorashad AS, Rahmati-Balaghaleh M, Zarean M. Evaluation of malaria multiplex/nested PCR performance at low parasite densities and mixed infection in Iran: a country close to malaria elimination. Insect Genet Evol. 2018;65:283–7.CrossRef
Metadata
Title
On the epidemiology of Plasmodium vivax malaria: past and present with special reference to the former USSR
Authors
Anatoly V. Kondrashin
Lola F. Morozova
Ekaterina V. Stepanova
Natalia A. Turbabina
Maria S. Maksimova
Evgeny N. Morozov
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2018
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-018-2495-y

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