YEXPR 6916

No. of Pages 8, Model 5G

7 August 2014 Experimental Parasitology xxx (2014) xxx–xxx 1

Contents lists available at ScienceDirect

Experimental Parasitology journal homepage: www.elsevier.com/locate/yexpr 4 5

What do we know by now about the genus Naegleria?

3 6

Q1

7 8

Q2

Johan F. De Jonckheere ⇑ de Duve Institute, 1200 Brussels, Belgium Scientific Institute of Public Health, 1050 Brussels, Belgium

10 9 11

h i g h l i g h t s

1 8 3 2 14 15 16

 Naegleria fowleri produces primary

17

 Naegleria australiensis and N. italica

18

produce disease in experimental animals.  Eight different types have been detected within N. fowleri.  The ITS sequences allow to study the distribution of the 47 described Naegleria spp.  The genomes of N. fowleri and N. lovaniensis should be compared to know why the former is pathogenic.

g r a p h i c a l a b s t r a c t

amoebic encephalitis in man.

19 20 21 22 23 24 25 26 27 30

a r t i c l e 3 4 2 1 33 34 35 36 37 38 39 40

Q3

i n f o

Article history: Received 23 November 2013 Received in revised form 7 July 2014 Accepted 22 July 2014 Available online xxxx Keyword: Naegleria review

a b s t r a c t In this short overview of the genus Naegleria a brief historical sketch is given since the discovery of this amoeboflagellate in 1899 and the finding in 1970 that one species, Naegleria fowleri causes primary amoebic meningoencephalitis in man. Eight different types of this pathogen are known which have an uneven distribution over the world. Until now 47 different Naegleria spp. are described, of which two other species cause disease in experimental animals, and their geographical dispersal is indicated. The presence of group I introns in the SSU and in the LSU rDNA in the genus is discussed, as well as the possibility of sex or mating. It is also mentioned that the genome of N. fowleri should not be compared to that of Naegleria gruberi, to know why the former is pathogenic, but to the genome of its closest relative Naegleria lovaniensis. Ó 2014 Published by Elsevier Inc.

42 43 44 45 46 47 48 49 50 51 52 53

54 55

1. Some ancient history

56

One has to go back to the end of the 19th century to see the first mention of an amoeba which transforms into a flagellate. At that time it was called Amoeba gruberi by Franz Schardinger (1899). He published the first drawings of the amoebae, the cysts and the flagellates, but in the text and figures he called it Amoeba lobosa instead of A. gruberi, which was only mentioned in the title and one table. It is interesting to note that already in these first drawings one can observe that some flagellates have more than 2 flagella

57 58 59 60 61 62 63

⇑ Address: de Duve Institute, Avenue Hipocrate 74-75, 1200 Brussels, Belgium. E-mail address: [email protected]

and that there might be even an indication that flagellates could divide. I will come back on this phenomenon in Section 4. One has to wait another 13 years before Alexeieff (1912) coined the genus name Naegleria. Again there are drawings of the amoebae, the cysts, and the biflagellated swimming form. But Alexeieff also included in the genus Naegleria all Vahlkampfia spp., which do not form flagellates, as such abolishing the genus name Vahlkampfia. One year later Calkins (1913), however, emended the genus description by stating that the genus name of Vahlkampfia should be kept, and that only those amoebae that transform into a flagellate stage should be placed in the genus Naegleria. One has to mention the publication of Craig (1913) one year Q4 later, for a special reason, because not only did he conclude that

http://dx.doi.org/10.1016/j.exppara.2014.07.011 0014-4894/Ó 2014 Published by Elsevier Inc.

Please cite this article in press as: De Jonckheere, J.F. What do we know by now about the genus Naegleria? Exp. Parasitol. (2014), http://dx.doi.org/ 10.1016/j.exppara.2014.07.011

64 65 66 67 68 69 70 71 72 73 74 75 76

YEXPR 6916

No. of Pages 8, Model 5G

7 August 2014 2

J.F. De Jonckheere / Experimental Parasitology xxx (2014) xxx–xxx

81

Calkins was right to keep both genus names Vahlkampfia and Naegleria, note the mistake in spelling the genus name (Naegleria), but he also stated that the genus Naegleria is of little interest to physicians as it contains no organism occurring in man. Well, 100 years later we know better.

82

2. Naegleria as a pathogen

77 78 79 80

83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117

It was not until the late 1960 that it was discovered that a Naegleria could provoke a dreadful disease I mention only one (Culbertson et al., 1968) of the several publications over the years 1966–1968 implicating Naegleria in primary amoebic meningoencephalitis (PAM). This pathogenic Naegleria was later described by Carter (1970) as a separate species, Naegleria fowleri, in honor of Fowler who described the first cases in Australia. And that is the time that the new era of research on the genus Naegleria started. The pathogenic N. fowleri has been reported to be present on all continents, except Antarctica (Fig. 1 in De Jonckheere, 2011). There are only about 250 reported PAM cases worldwide, so the disease is rare, but every year a few more cases are discovered. Very few cases are reported from Africa and South America, but why would they be interested in such a rare disease while millions of people are dying of other infections on these continents. But it remains a serious problem for public health as PAM is almost always fatal, with only about 5% of patients surviving (Table 1), and it affects mostly children in good health. It has been shown that N. fowleri is present in many cooling waters of industry, mainly of electricity power plants (De Jonckheere, 2012). As growth of this amoeba is very difficult to control in cooling waters, the public health ministry of France established an upper limit of 100 N. fowleri per liter, not to be exceeded in water courses where human exposure is possible Q5 (Cabanes and Wallet, 2001). Unfortunately, this upper limit has also been used for swimming areas, such as the geothermal baths in Guadeloupe, a tropical overseas territory of France. There has been a N. fowleri infection in a geothermal bath in Guadeloupe (Nicolas et al., 2010), after which a lot of information was gained from studying the presence of N. fowleri in geothermal waters in Q6 Guadeloupe (Moussa et al., 2013). At the case site the authorities have posted a sign (Fig. 1) indicating that the concentration of N. fowleri has never exceeded 5/L, so that bathing should not be denied at the place because it remains below the level of 100/L

Fig. 1. Poster at geothermal bathing area in Guadeloupe indicating it is safe to swim as the norm of 100 N. fowleri/L has not been surpassed.

Table 1 Cases surviving PAM infection.

Q9

Age (years)

Sex

Place

References

6 4 14 9 ? 18 61 30 38 26 10 0.8 0.5 73 0.1

F F M F M F M M M F M M M M M

UK UK Australia California (USA) Pennsylvania (USA) Thailand Thailand Italy Hong Kong India Mexico India Iran India India

Apley et al. (1970)* Apley et al. (1970)* Anderson and Jamieson (1972) Seidel et al. (1982) Brown (1991) Sirinavin et al. (1989) Poungvarin and Jariya (1991) Loshiavo et al. (1993) Wang et al. (1993) Jain et al. (2002) Vargas-Zepeda et al. (2005) Rai et al. (2008) Movahedi et al. (2012) Gautam et al. (2012) Yadav et al. (2013)

* Although there is some doubt whether these were PAM cases, as N. fowleri was not isolated.

admitted by law. I think this is criminal, and the authorities seem to recognize this as they recommend the use of a nose clip. The upper acceptable level of 100/L was never demonstrated to have been attained in the water at that site, while a PAM case occurred. Therefore, absence of N. fowleri in 1 L should be the norm to indicate that it is safe to swim at a place. For example, for Salmonella the total absence in 1 L is the international standard for bathing areas, while this bacterium does not even kill young people in excellent health. Australia is the only other country which has adopted a legal standard for Naegleria in surface water. By as early as 1980, the government of Western Australia established an amoeba alert for when the water temperature is 28 °C (Lugg and Psaila-Savona, 2001). But in 2000, a guideline level of five thermophilic Naegleria per liter, and an action level of two thermophilic Naegleria per liter was implemented in this state. The guideline does not even specify that it is the pathogenic N. fowleri that is identified. Every Naegleria sp. growing at 42 °C is considered in this standard. So the Australians seem to be more cautious than the French appear to be.

118

3. N. fowleri

137

The rDNA in the genus Naegleria, and all other vahlkampfiidae, is on a circular plasmid of which around 4000 copies are present in each cell (Clark and Cross, 1987). This is in contrast to the situation in most other eukaryotes where the rDNA is in tandem repeats on the chromosomes (Coleman, 2003). The internal transcribed spacers (ITS) and 5.8S rDNA are between the SSU and LSU rDNA, and it is the ITS and 5.8S rDNA sequences that are of most interest in the study of Naegleria. Based on difference in the ITS1 length and a one bp difference in the 5.8S rDNA, eight types of N. fowleri have been detected (Table 2 in De Jonckheere, 2011). Of these eight types, only four have been identified until now in patients (Table 3 in De Jonckheere, 2011). The eight types have an uneven distribution over the world (Fig. 2 in De Jonckheere, 2011), but more data are necessary to substantiate this observation. Of the eight types, seven are detected in Europe. The only type (type 5) found in the west Pacific (Australia, New Zealand and Japan) is also present in Europe (although only twice observed), while two of the three American types are also present in Europe. Only type 1 has not been detected yet in Europe, only in the USA. It is important to note that the ITS2 sequence of all N. fowleri strains is identical (De Jonckheere, 2002). It is also important to note that other Naegleria spp., which presently number 47 described species, can be identified by their ITS2 sequence.

138

Please cite this article in press as: De Jonckheere, J.F. What do we know by now about the genus Naegleria? Exp. Parasitol. (2014), http://dx.doi.org/ 10.1016/j.exppara.2014.07.011

119 120 121 122 123 124 125 126 127 128 129 130 131 132 133 134 135 136

139 140 141 142 143 144 145 146 147 148 149 150 151 152 153 154 155 156 157 158 159 160

YEXPR 6916

No. of Pages 8, Model 5G

7 August 2014 3

J.F. De Jonckheere / Experimental Parasitology xxx (2014) xxx–xxx

Q10

Table 2 Described species in the genus Naegleria. Species

Author(s), year

Max. Temp. (°C)

Flagellates

N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N. N.

Schardinger (1899), Em. De Jonckheere (2002) Carter (1970) Willaert and Le Ray (1973) Stevens, De Jonckheere and Willaert (1980) De Jonckheere (1981) De Jonckheere, Pernin, Scaglia and Michel (1984) De Jonckheere (1988) De Jonckheere (1988) De Jonckheere (1994) De Jonckheere (1994) De Jonckheere and Brown (1995) Pernin and De Jonckheere (1996) Dobson, Robinson and Rowan-Kelly (1997) Dobson, Robinson and Rowan-Kelly (1997) Dobson, Robinson and Rowan-Kelly (1997) Dobson, Robinson and Rowan-Kelly (1997) De Jonckheere and Brown (1999) De Jonckheere et al. (2001) De Jonckheere et al. (2001) De Jonckheere et al. (2001) De Jonckheere (2002) De Jonckheere (2002) De Jonckheere (2002) De Jonckheere (2002) De Jonckheere (2004) De Jonckheere (2004) De Jonckheere (2004) De Jonckheere (2004) De Jonckheere (2004) De Jonckheere (2004) De Jonckheere (2004) De Jonckheere (2004) De Jonckheere (2004) De Jonckheere (2004) De Jonckheere (2004) Visvesvara et al. (2005) De Jonckheere and Brown (2005) De Jonckheere, (2006) De Jonckheere, (2006) De Jonckheere, (2006) De Jonckheere, (2006) De Jonckheere, (2006) De Jonckheere, (2006) De Jonckheere, (2006) De Jonckheere, (2006) De Jonckheere, (2006) De Jonckheere, (2006)

39 45 35 45 42 42 40 42 37 35 38 41 45 44 45 44 38 35 30 38 42 37 37 40 33 35 ? 37

What do we know by now about the genus Naegleria?

In this short overview of the genus Naegleria a brief historical sketch is given since the discovery of this amoeboflagellate in 1899 and the finding ...
1MB Sizes 0 Downloads 6 Views