Research Endemic malaria: an 'indoor' disease in northern Europe. Historical data analysed Lena Huldén* 1, Larry Huldén 2 and Kari Heliövaara 1 - PDF

Malaria Journal BioMed Central Research Endemic malaria: an 'indoor' disease in northern Europe. Historical data analysed Lena Huldén* 1, Larry Huldén 2 and Kari Heliövaara 1 Open Access Address: 1 Department

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Malaria Journal BioMed Central Research Endemic malaria: an 'indoor' disease in northern Europe. Historical data analysed Lena Huldén* 1, Larry Huldén 2 and Kari Heliövaara 1 Open Access Address: 1 Department of Applied Biology, Faculty of Agriculture and Forestry, University of Helsinki, Finland and 2 Finnish Museum of Natural History, University of Helsinki, Finland Lena Huldén* - Larry Huldén - Kari Heliövaara - * Corresponding author Published: 25 April 2005 Malaria Journal 2005, 4:19 doi: / This article is available from: Received: 20 January 2005 Accepted: 25 April Huldén et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Background: Endemic northern malaria reached 68 N latitude in Europe during the 19 th century, where the summer mean temperature only irregularly exceeded 16 C, the lower limit needed for sporogony of Plasmodium vivax. Because of the available historical material and little use of quinine, Finland was suitable for an analysis of endemic malaria and temperature. Methods: Annual malaria death frequencies during extracted from parish records were analysed against long-term temperature records in Finland, Russia and Sweden. Supporting data from were used in the interpretation of the results. The life cycle and behaviour of the anopheline mosquitoes were interpreted according to the literature. Results: Malaria frequencies correlated strongly with the mean temperature of June and July of the preceding summer, corresponding to larval development of the vector. Hatching of imagoes peaks in the middle of August, when the temperature most years is too low for the sporogony of Plasmodium. After mating some of the females hibernate in human dwellings. If the female gets gametocytes from infective humans, the development of Plasmodium can only continue indoors, in heated buildings. Conclusion: Northern malaria existed in a cold climate by means of summer dormancy of hypnozoites in humans and indoor transmission of sporozoites throughout the winter by semiactive hibernating mosquitoes. Variable climatic conditions did not affect this relationship. The epidemics, however, were regulated by the population size of the mosquitoes which, in turn, ultimately was controlled by the temperatures of the preceding summer. Background Endemic malaria was declining in western Europe from the 18 th century onwards, but in the 19 th century it was still common in the north and north-east of Europe. In the 1930s, endemic malaria finally disappeared from most parts of Europe, with the exception of occasional epidemics during the Second World War [1]. There is very little modern research on the historical conditions of the disease or even its historical distribution. Most published studies of historical distribution do not include the cases in Finland [2]. Imported cases during the Second World War, however, have attracted some attention [3]. Page 1 of 13 Northern malaria has usually been connected with Plasmodium vivax. After infection, the sporozoites enter human hepatocytes and develop into hypnozoites. These remain in dormancy for a variable time, and the patient may occasionally suffer from malaria for up to four years and have symptoms every second month [4]. Sokolova & Snow [5] report that Plasmodium falciparum occurred in Archangelsk and Vologda in the northern part of the Soviet Union in the 1930s. It is usually assumed that P. falciparum lacks a dormant stage. In the Finnish medical reports the symptoms of malaria included tertian, quotidian and quartan malaria. The tertian form was the most common and Sievers [6] connected this form with P. vivax. The possible historical occurrence of other Plasmodium species in Finland remains uncertain. The temperatures needed for the sporogony have been studied in laboratory conditions [4]. Garnham [7,8] limits the range of malaria to summer temperatures. The northern range of the occurrences of endemic malaria has been estimated to coincide with a summer isotherm of 16 C. However, even a superficial examination shows that malaria also occurred in the northern parts of Sweden and Finland, where the summer temperature was considerably below 16 C. The present study aims to establish that malaria can spread in a cold climate, even when the outside temperature is lower than needed for the sporogony of the Plasmodium. Because of the high quality of available historical sources, of demographic, medical and temperature data, Finland is a very suitable area for the study. The study focused on the period , since the only effective drug, quinine, was not then frequently used by the common people. Its wide use would have biased the statistics of the causes of death. High resolution temperature data are also available for that period. Methods The known distribution of three Anopheles species in Finland was published by Utrio [9]. The distribution unit of km 2 gives a reasonably good resolution of the distribution of these species in Finland. Additional information from Sweden and Estonia was also used for comparison [10,11]. Life cycles, behaviour and the phenology of the mosquito has been interpreted according to the literature [12-18] and field samplings in the southwest archipelago by the first author. The data of historical malaria cases were collected and tested by historical methods. Although the historical data can be questioned, it should be emphasized that the Finnish sources give a good picture of the actual situation, and that the statistics are of a better quality than in most other countries. Causes of death were especially recorded by ministers in hundreds of parishes and, although there probably are some mistakes, most of the entries were correct. There are two different kinds of source for collecting the records of malaria cases in Finland during the years : 1) reports by the district physicians and 2) the causes of death that were recorded by the local ministers. The physicians wrote an annual report to the medical board in Helsinki about the health conditions in their district. At the end of the century a separate report on epidemics was added. Malaria is mentioned in both kinds of reports. The reports had a free format and the number of sick patients was only rarely mentioned. Usually the physician formulated an opinion of the severity of the actual epidemics. Many districts were so large that the physician could hardly know the actual situation in the more remote parts, especially in the north. The archival series of physicians' reports include reports from the beginning of the 19 th century. The oldest reports contained very general information. They improved in 1857 when the number of districts increased to 50 [19]. Malaria was mentioned in 542 reports between 1826 and Sievers [6], who studied malaria in Finland, based his opinion solely on these reports. Sievers' interpretation was compared with the original documents, that can be examined in the National Archives in Helsinki, Finland. The reports cannot be used for quantitative analyses, but they mention the years in which they were epidemics and these coincide with the epidemic years in the death statistics. From 1749, the minister had to record the cause of death for every diseased parish member in the burial records. The parish burial registers can therefore be used for detailed statistics on malaria. For this study these local records were used. The minister often attended the deathbed and, in contrast to the district physician, actually saw the patient. Ministers were probably very familiar with the typical symptoms of malaria, as it was a common disease. They often had some medical knowledge because the training in medicine for students of theology had developed rapidly duringthe second half of the 18 th century. The minister was not only responsible for the spiritual guidance of his parish members, but also for their bodily welfare [20]. In the present study, only those cases which the ministers recorded as malaria (5,431 death cases) have been taken into account. In the parish records, several words were used for malaria. Frossa, fråssa, frossfeber were the most common and other frequently used words were kallfeber, kallsot, kylfeber, skälvan, skälvasot, tertian, tredjedagsfrossa, vardagsfrossa, skärgårdsfeber, växelfeber, omväxlingsfeber, intermittent feber and malaria. The district physicians used frossa, tredjedagsfrossa, vardagsfrossa, tertian, quartana or quotidiana. These words were used in both Swedish and Finnish medical research from the 18th to the 20th century along with skärgårdsfeber [6,20-27]. Page 2 of 13 The use of the above-mentioned words was strictly separated from the use of other words for diseases, which included fever or resembled malaria like hetsig feber, flussfeber, feber, scharlakansfeber, älta and förkylning. The consistent use of these malaria words is also confirmed by comparative correlation analyses. The statistics for cause of death is most representative for the period of The data are collected from digitalized parish records, which were made available on the Internet by the Finnish Genealogical Society through Dec. 31 st, 2003 [28]. The project is not yet finished, but most of the material before 1850 has been digitalized. The period of is not very representative and only material from a few parishes is included. In the present study all cases recorded in southern Finland until 1870 are included but the last decade is under-represented in the material. It must be stressed that the records only show the number of deaths due to malaria but that the relation between the number of infected and the death rate is uncertain. The longest Finnish temperature record from Helsinki, starting from 1829, is used as the basis for climatic correlations for the years Temperatures from St. Petersburg (Russia) ( ), Tornedalen (Sweden)( ) and Stockholm (Sweden)( ) are used as supporting data for the extended period of (Figure 1). These are the best high resolution temperature data available at the present time [29-32]. 70 N latitude Kittilä Arctic Circle Tornedalen Tornedalen FINLAND Archangelsk Helsinki Stockholm Helsinki Stockholm St. St. Petersburg malaria study area temperature series northernmost malaria epidemics Map Figure of malaria 1 study area and locations of temperature series Map of malaria study area and locations of temperature series. Page 3 of 13 Results The distribution and life cycle of anophelines in Finland Three Anopheles species have been reported from Finland [9]. Anopheles beklemishevi has a northern distribution in Finland, while the other common species, Anopheles messeae, is dominant in the southern part of the country [17]. Anopheles claviger is recorded from the Aland Islands and was also found by the authors in the south-western archipelago. In December 2004 and January 2005 flying specimens of an unidentified Anopheles (cf. messeae) were observed in summer cottages in two different localities in southern Finland. Because of many taxonomical problems in the Anopheles genus, there is conflicting information on the details of the life cycles of the separate species. A general feature of the northern species is that the adult female hibernates. There are possibilities of a summer generation, at least in warm summers as in 1901 in Finland (possibly A. messeae)[9,12]. A. claviger hibernates as larvae [33] and, at least in England, seems to be bivoltine [34]. In Finland, the majority of the hibernating females reach the adult stage in the middle of August. The male is short lived and dies soon after mating. The female may suck blood or honey-dew before seeking shelter in sheds and houses for hibernation. Because of the cold climate the female cannot leave the hibernation site before spring. In the traditional agricultural society of Finland many of the mosquito females spent the main part of their adult life together with man and domestic animals. In warm conditions the female may take several blood meals during the hibernation, but it will not lay eggs before the spring [13]. A. messeae has been considered an important vector of historical endemic malaria in several parts of Europe and was also an important vector in the Soviet Union [4,15]. In the northern parts of Russia and along the Baltic coast, A. beklemishevi was an important vector [35]. A. claviger has also locally been reported as a vector [15]. Some recent research, however, has questioned A. messeae as a vector of malaria [36]. Jaenson & Ameneshewa [37] reported that blood-feeding was not a prerequisite for hibernation of A. messeae. This does not exclude the possibility of repeated indoor blood-feeding in warm indoor conditions. There is still unresolved and conflicting information on the feeding, resting and hibernation habits of the female (exophagy or endophagy, zoophily or anthropophily, exophily or endophily, complete diapause or semiactive winter habit). The anophelines in the northern region, however, must be flexible in their habits to survive the strong annual and seasonal fluctuations in temperature (- 51 C to +33 C in Finland and rain/snow). In any case, one or more species, distributed over the whole of Finland, have been vectors of malaria in Finland. Yet it is likely that one or more additional species, still not reported from Finland, will be found as four additional species have been reported from Estonia and Sweden [10,11]. For the time being it is not possible to define which mosquito species was important for the malaria transmission in Finland. Endemic malaria in Finland The Anopheles species, which have been vectors of malaria in Finland, presumably have existed here since prehistoric times. It is, however, probable that malaria reached Finland only during the 17 th century. There are several cases of malaria in the Mälaren region to the west of Stockholm in Sweden during that time. Both 1692 and 1693 are reported as years of severe fever [38], which spread rapidly also to the east. A total of 1,803 persons died of malaria in the western parts of Finland and in the south-western archipelago during the years [23]. Haartman [21] reports severe epidemics in the region of Turku in the years and the physician F.W. Radloff mentioned that malaria was very common in the Aland Islands in 1795 [39]. From 1800 to 1870, there were at least 5,431 death from malaria in Finland. During this period the Finnish population grew from 832,700 to 2,032,700 people [40]. In a few epidemics, the mortality can be estimated to % [6]. The number of deaths from malaria increased when the number of malaria cases increased and thus a change in virulence of the Plasmodium is not to be assumed. The total number of malaria cases in the middle of the 19 th century may tentatively be estimated to be 100, ,000 or about 7 20% of the whole population. Although the source value of both the death statistics and the medical reports can be discussed separately, they are strengthened when compared with each other. As sources they are completely independent, and they partly overlap the period , showing similar trends. The district physicians reported 174 local epidemics during and during the same period the deaths from malaria rose to 1,687 cases. In the years and 1877, the number of epidemics also rose and the same trend can be seen in the parish death records. The malaria epidemics and temperature The worst malaria year in Finland was The eastern parts of Finland were particularly affected, including Karelia. Several physician's reports reveal how severe the situation was. In the district of Mikkeli over 4,000 persons became ill. Moreover, in the district of Joensuu 4,000 persons suffered, in Rautalampi several thousands and in the worst parishes in the districts of Viipuri and Muola every third person became ill. In eastern Finland the summer was cold and damp. Malaria epidemics even broke out in Page 4 of 13 Table 1: Annual mean temperature correlated with malaria cases in Year correlated with malaria cases in Source of temperature series Helsinki years Tornedalen years Stockholm years St. Petersburg years malaria year malaria year Table 2: Seasonal mean temperature correlated with malaria cases in Season correlated with malaria cases in Source of temperature series Helsinki years Tornedalen years Stockholm years St. Petersburg years malaria year-1; winter malaria year-1; spring malaria year-1; summer *** *** *** *** malaria year-1; autumn malaria year; winter malaria year; spring malaria year; summer malaria year; autumn Table 3: Monthly mean temperature correlated with malaria cases in Month of preceding year correlated with malaria cases in Source of temperature series Helsinki years Tornedalen years Stockholm years St. Petersburg years malaria year-1; May malaria year-1; June ** *** ** ** malaria year-1; July ** ** *** * malaria year-1; August * malaria year-1; September malaria year-1; October * malaria year-1; November malaria year-1; December Page 5 of 13 Table 4: Monthly mean temperature correlated with square root transformed malaria cases in Month of preceding year correlated with square root transformed malaria cases in Source of temperature series Helsinki years Tornedalen years Stockholm years St. Petersburg years malaria year-1; May malaria year-1; June ** *** *** ** malaria year-1; July ** *** *** ** malaria year-1; August * malaria year-1; September malaria year-1; October ,2145 malaria year-1; November malaria year-1; December deaths from malaria temperature in centigrade years 11 malaria deaths Tornedalen summer temperature Helsinki summer temperature Figure Malaria deaths 2 in southern Finland and mean temperatures of the preceding summer in Helsinki and Tornedalen Malaria deaths in southern Finland and mean temperatures of the preceding summer in Helsinki and Tornedalen Page 6 of 13 August mean temperature in centigrade years HELSINKI TORNEDALEN Mean Figure temperature 3 of August in Helsinki and Tornedalen Mean temperature of August in Helsinki and Tornedalen the north and in Sotkamo in the Kajana district more than a hundred people became ill. The correlation between temperature and the number of malaria deaths was tested on annual, seasonal and monthly levels. The seasons were interpreted as follows: winter (DJF), spring (MAM), summer (JJA) and autumn (SON). The malaria cases were tested against the temperatures of both the current malaria year and the preceding year. In Table 4 the calculations of monthly correlations were repeated with a square root transformation of the number of malaria cases to avoid biases caused by strong peaks during epidemics. Malaria deaths peak late in the spring but for completeness the calculations are extended further to the autumn of the malaria year. The results are presented in Tables 1,2,3,4 and Figure 2. Annual mean temperatures were obviously not significant in the correlations. On the seasonal level the summer of the preceding year is highly significant (0.1% risk level). In all other seasons the risk level was more than 10%. Renkonen [26] tried to show a correlation between malaria epidemics and the temperature of April or spring. The correlation coefficient for both April and the entire spring were close to zero and thus Renkonen's hypothesis can be rejected. June and July of the preceding summer were very significant with a faint tail in August. The weak correlation of October temperatures in the St. Petersburg series (5% and 10% risk level respectively in Tables 3,4) can safely be considered stochastic noise with no support from the other series. Death caused by what were called 'intense fever', hetsig feber (48853 cases), cold, influenza, flussfeber (7670 cases), fever,
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