2006-mitochondrial dna diagnosis for taeniasis and cysticercosis
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Mitochondrial DNA diagnosis for taeniasis and cysticercosis
Hiroshi Yamasaki a,*, Minoru Nakao a, Yasuhito Sako a, Kazuhiro Nakaya b,Marcello Otake Sato a,c, Akira Ito a
a Department of Parasitology, Asahikawa Medical College, Asahikawa 078-8510, Japanb Animal Laboratory for Medical Research, Asahikawa Medical College, Asahikawa 078-8510, Japan
c Laboratorio de Parasitologia, Escola de Medicina Veterinaria e Zootechnica, Universidade Federal do Tocantins, Araguana-TO, 77804-970, Brazil
Available online 15 December 2005
Abstract
Molecular diagnosis for taeniasis and cysticercosis in humans on the basis of mitochondrial DNA analysis was reviewed. Development and
application of three different methods, including restriction fragment length polymorphism analysis, base excision sequence scanning thymine-
base analysis and multiplex PCR, were described. Moreover, molecular diagnosis of cysticerci found in specimens submitted for histopathology
and the molecular detection of taeniasis using copro-DNA were discussed.
D 2005 Elsevier Ireland Ltd. All rights reserved.
Keywords: Taeniasis; Cysticercosis; Mitochondrial DNA diagnosis; PCR-RFLP; BESS T-base analysis; Multiplex PCR; Biopsied specimen
1. Introduction
Taenia solium, Taenia saginata, and Taenia asiatica are
cestode parasites causing taeniasis in humans. T. solium also
causes cysticercosis in humans; neurocysticercosis is serious
disease characterized by neurologic symptoms including epi-
leptic seizures. BothT. solium and T. saginata are distributed
worldwide, but distribution ofT. asiatica is restricted to Asian
regions. In Asia where these cestodes are distributed sympatri-
cally, differentiation ofT. saginata and T. asiaticais frequently
confused as a result of morphological similarities. Theoretically,
it is possible to differentiate the proglottids of human Taenia
parasites on the basis of morphology, however, it is difficult in
practice. Until recently the only reliable technique for differen-
tiation of taeniid eggs is by DNA-based methods.
In order to improve methods for identifying taeniid
cestodes, various molecular approaches have been developed,
including the use of DNA probes [16], polymerase chain
reaction (PCR) coupled to restriction fragment length poly-
morphism (RFLP) [712], single-strand conformation poly-
morphism (SSCP) [13], PCR-amplified DNA sequences
[7,8,10,14], and random amplified polymorphic DNA
(RAPD)-PCR[1416]. Each of these techniques has advan-
tages and disadvantages, e.g., the use of DNA probes, PCR-RFLP and SSCP are relatively time-consuming; however, PCR
using species-specific primers provides rapid and sensitive and
reliable diagnostic results [17,18]. Most of these studies have
been focused on the differentiation of T. solium from
T. saginata and intraspecific genetic polymorphism.
Recently, mitochondrial DNA analysis ofT. solium revealed
the presence of two distinct Asian and American/African geno-
types[19,20].Therefore, a comprehensive differential diagnosis
based on mitochondrial DNA forT. saginata, T. asiaticaand two
genotypes ofT. solium parasites has been established[2123].
Differential diagnosis of taeniasis can now be achieved using
copro-DNA [23]. In this review, for the comprehensive
differential diagnosis of human taeniid cestodes, PCR-RFLP,
base excision sequence scanning thymine-base (BESS T-base)
reader analysis and multiplex PCR are discussed. The role of
molecular diagnosis of cysticerci found in histopathological
specimens from patients and the detection method of taeniid
DNA using feces from tapeworm carriers are also discussed.
2. Molecular identification of proglottids, cysticerci and eggs
For molecular identification of taeniid eggs, cysticerci and
proglottids, the parasite materials should be stored in ethanol
1383-5769/$ - see front matterD
2005 Elsevier Ireland Ltd. All rights reserved.doi:10.1016/j.parint.2005.11.013
* Corresponding author. Tel.: +81 166 68 2421; fax: +81 166 68 2429.
E-mail address: hyamasak@asahikawa-med.ac.jp (H. Yamasaki).
Parasitology International 55 (2006) S81 S85
www.elsevier.com/locate/parint
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(>80%) after collection. DNA analysis of formalin-fixed
samples for histopathology is also possible, however it may
be difficult to lyse the parasite tissue and to amplify more than
1-kb DNA markers, because of the fragmentation of the DNA
as mentioned in Section 3. For preparation of DNA from
parasite materials, the use of a commercially available kit (e.g.,
DNeasy Tissue Kit, Qiagen) is convenient.
2.1. Polymerase chain reaction coupled to restriction fragment
length polymorphism (PCR-RFLP)
This is a simple method in which a PCR-amplified target
DNA is digested with particular restriction enzymes and used
to compare the subsequent fragment patterns. The method has
been applied for differentiation of T. saginata and T. solium
[611]. In addition, Yamasaki and others [22] reported
comprehensive PCR-RFLP analysis including T. asiatica and
two genotypes of T. solium. On the basis of complete
nucleotide sequences of cytochrome c oxidase subunit1 (cox1) and cytochrome b genes (cob) from human taeniid
cestodes, restriction enzyme sites unique for T. saginata,
T. asiatica, and two genotypes ofT. solium are found. In cases
of cox1, we use TaqI, BamHI, NcoI and DdeI unique for
T. saginata, T. asiatica and Asian and American/African
genotypes of T. solium, respectively. For example, if PCR-
amplifiedcox1is digested withBamHI, the taeniid cestode can
be identified as T. asiatica [22].As in case ofcob , differential
RFLP profiles are provided when Sty I forT. saginata, Vsp I
for T. asiatica, SnaBI and Ssp I for Asian and American/
African genotypes ofT. solium, respectively, are used [22].
2.2. Base excision sequence scanning thymine-base
(BESS T-base) reader analysis
This method was originally developed for the identification
of genetic variations at sites involving thymine bases (T) [24]
and then was applied to the identification of human taeniid
cestodes[21,22]. The principle is as follows: a forward primer
should be designed to include diagnostic nucleotides involving
T (e.g., positions 153, 189, 195, 723, 867, 1065 and 1608 in
cox1) and labeled with fluorescent dye. The BESS T-Base
Reader Kit is commercially available. During PCR amplifica-
tion of a target gene, limiting amounts of dUTP are randomly
incorporated into a PCR product at the T sites. Subsequently,N-glycosylase treatment of the PCR product results in removal
of uracil, creating an abasic site at the location of dUTP
incorporation. Furthermore, endonuclease IV treatment cleaves
the phosphodiester bonds at the abasic sites, generating a DNA
ladder virtually identical to T-sequencing ladder. The sample is
electrophoresed in a 6% polyacrylamide gel containing 8 M
urea, and data obtained are analyzed using GeneScan.
Subsequently, the appearance or disappearance of T-base peaks
serves as diagnostic markers for differentiation of human
taeniid cestodes.
InFig. 1, BESS T-base analysis data with a cox1 fragment
are shown. Most T bases are well-conserved among the taeniid
species, however, several nucleotides are species- andT. solium
genotype-specific (e.g., positions 153, 174, 189 and 195). Anucleotide at position 153 in T. asiatica is T, but nucleotides at
the same position are guanine inT. saginata andT. solium. In
BESS T-base analysis, thus a T-base peak appears at the
position in T. asiatica, but no T-base peaks appear at the
positions in T. saginata and T. solium. In T. saginata,
nucleotides at positions 174 and 189 are T, so that diagnostic
T-base peaks appear at both positions. In the differentiation of
two genotypes ofT. solium, if T-base peaks appear at positions
189 and 195, the taeniid cestode can be identified as the
American/African genotype of T. solium. If a T-base peak
appears at position 195, the T. solium parasite is the Asian
genotype. Comparison of T-base peak profiles allows differ-
entiation of human taeniid cestodes without the need for DNA
sequencing. In BESS T-base analysis, since 100200-bp PCR
products containing diagnostic positions are more convenient
for analysis, the method will be applicable for the accurate
identification of formalin-fixed parasite materials in which
DNA is fragmented.
2.3. Multiplex PCR
Compared to PCR-RFLP and BESS T-base analysis,
multiplex PCR is a simpler and more rapid method. It amplifies
particular genes using multiple primer pairs in a single tube.
Yamasaki and others [23] established multiplex PCR for acomprehensive identification of human taeniid cestodes. For
this purpose, forward primers were designed to be amplified as
PCR products of different sizes unique for T. saginata,
T. asiatica, and two genotypes ofT. solium. Fig. 2 shows a
typical multiplex PCR data with cox1. The diagnostic products
with molecular sizes of 827, 269, 720, and 984 bp are
successfully amplified in T. saginata, T. asiatica, and the
American/African and Asian genotypes of T. solium, respec-
tively. When a mixture ofT. saginata andT. asiatica eggs was
tested by multiplex PCR, two products with molecular sizes of
827 and 269 bp were amplified. The successful amplification
by multiplex PCR depends on the ratio of the forward and
reverse primers and sequences of primers. The primer used for
T. saginata
T. asiatica
T. soliumAmerican
T. soliumAfrican
T. soliumAsian
153 174 189 195
T G T G A T T T T T T T T T G A T T A C T A A T C A T G G A A T
T G T T A T T T T T TT T T G A T T A C TAAC C A T G G A A T
T G T G A T T T A T T T T T G A T T A C T A A T C A T G G T A T
T G T G A T T T A T T T T T G A T T A C T A A T C AT G G T A T
T G T G A T T T A T T T T T G A T T A C T A A C CA T G G T AT
153 174 189 195
T G T G A T T T T T T T T T G A T T A C T A A T C A T G G A A T
T G T T A T T T T T TT T T G A T T A C TAAC C A T G G A A T
T G T G A T T T A T T T T T G A T T A C T A A T C A T G G T A T
T G T G A T T T A T T T T T G A T T A C T A A T C AT G G T A T
T G T G A T T T A T T T T T G A T T A C T A A C CA T G G T AT
Fig. 1. BESS T-base reader analysis with cox1 for human taeniid parasites. T-
base peak profiles from T. saginata, T. asiatica, and American/African and
Asian genotypes ofT. solium are illustrated. Arrows indicate diagnostic T-base
peaks (modified from [21]).
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T. asiatica has been recently modified to reduce the amplifi-
cation of additional products [25].
3. Molecular diagnosis of cysticerci found in
histopathological specimens
The clinical diagnosis of cysticercosis in humans is
performed by imaging diagnosis and serology. Histopatholog-
ical examination of biopsy specimens is also a useful method
for confirmation of the causative cysticercus. However, it is not
always easy to make a definitive diagnosis of the cysticercus as
a result of the preparation of tissue sections and the degree of
degeneration and/or calcification of the tissue. Prior to 2004
there was only a report on the DNA diagnosis of a cysticercus
found in a black bear [26]. More recently, two cases of
neurocysticercosis in humans were confirmed by mitochondrial
DNA analysis of biopsied lesions[27,28].DNA was extracted
from 45 paraffin sections with a 5-Am thickness using 0.02N
NaOH containing proteinase K solution or a commercially
available kit. In the former case [27], a cysticercus character-
ized by suckers and spiral canals was observed. Although the
specimen was fixed with formalin, 1.8-kb and 984-bp cox1
fragments were successfully amplified by conventional PCR
using a primer set[20,21]and DNA sequencing confirmed as
T. solium Asian genotype. In the latter case [28], histopatho-
logical findings were not confirmatory because of the
degeneration of the tissue. However, smaller sizes of cox1andcob fragments (100400 bp) were successfully amplified,
demonstrating the causative agent was the Asian genotype of
T. solium by DNA sequencing. The authors have also reported
a case of systemic intramuscular cysticercosis confirmed by
mitochondrial DNA analysis of extremely calcified cysts [29].
Although the cystic lesions were calcified, had been fixed in
formalin and decalcified for histopathology, a 984-bp cox1
fragment was successfully amplified by conventional PCR,
confirming that the calcified cyst was derived from T. solium
Asian genotype by DNA sequencing of the product.
The amplification of DNA markers from histopathological
specimens seems to be dependent on the preservation and/or
fixation condition of the parasite materials used, probably as a
result of the fragmentation of DNA. Thus, the amplification by
multiplex PCR seems to be difficult and subsequently, DNAsequencing of the PCR product is indispensable for further
confirmation[27 29].
4. Importance of molecular identification of biopsy
specimens
The majority of Taenia species causing cysticercosis in
humans is known to be T. solium. However, there are many
other potentially zoonotic taeniid species including T. taeniae-
formis, T. pisiformis, T. hydatigena, T. serialis, T. multiceps
and Echinococcus spp. [30] and several of these are highly
zoonotic. Taeniid cestodes might infect humans by accidental
ingestion of eggs and be diagnosed or misdiagnosed as
Cysticercus spp., Cysticercus racemosus, Coenurus spp.
Cysticercosis/coenurosis in humans caused by the infection
of such zoonotic species has been reviewed[31]. Cysticercosis
due to Taenia crassiceps has been reported in patients with
HIV-AIDS[3235]. Most recently, a racemose-type cysticer-
cus has been diagnosed as T. solium based on mitochondrial
cox1 and NADH dehydrogenase subunit 1 gene analysis [36].
There were case reports suggesting cysticercosis due to
T. saginata in humans [3739]. Ito [40] speculated on the
possibility of human cysticercosis due to T. asiatica, since both
T. asiatica and T. solium require pigs as the intermediate host.
However, based on the molecular studies, Ito and others [41]now conclude that cysticercosis ofT. asiatica in humans does
not occur similar to its sister species T. saginata.
More recent work by Nakaya and others[42]has shown that
the number of hooks of T. solium developed in non-obese
diabetic/Shi-severe combined immunodeficiency (NOD/Shi-
scid) mice was highly variable from null to 28. Margono and
others[43]also reported variable formation of hookets in 135-
day-oldT. soliummetacestodes, suggesting that the presence of
hooklets is not always an adequate marker for identification of
the species.
Morphological identification of taeniid species is problem-
atic. Data for molecular phylogeny of taeniid cestodes
[20,4446] are expected to be highly informative and useful
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T. soliumAsian genotype
Fig. 2. Differential diagnosis of human taeniid cestodes by multiplex PCR. Cox1-fragments with molecular sizes of 827, 269, 720 and 984 bp are amplified in
T. saginata, T. asiatica, American/African and Asian genotypes of T. solium. An asterisk indicates a mixture sample of T. saginata and T. asiatica eggs
(modified from[23]).
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for molecular identification of taeniid species[26]. In order to
confirm or dispel the notion that human cysticercosis may
sometimes be caused by T. asiatica or T. saginata, or to
provide evidence-based confirmed diagnosis, it is essential to
obtain specimens for molecular identification [47,48]. It is
important to stress the importance of fixing biopsy specimens
in ethanol (or even in formalin for a short time) for adequatepreparation of paraffin sections of such specimens in order to
obtain crucial DNA confirmation[2729],since approximate-
ly 50% of solitary cysticercosis cases [4952] and inactive
cysticercosis with calcified lesions are expected to be sero-
negative[29].
5. Detection of taeniasis using copro-DNA
Taeniasis has been diagnosed based on the coproscopic
examination and morphologic characteristics of tapeworm
proglottids. To date, only few molecular methods for diagnosis
of taeniasis have been reported [12,23,53]. Nunes and others[12] performed PCR to detect taeniid DNA in stool samples,
which had been artificially spiked with T. saginata eggs and
reported a detection limit of 137 eggs (corresponding to 1096
pg DNA). Nunes and others[53]have reported PCR-RFLP to
differentiateT. solium and T. saginata egg in fecal samples of
taeniasis patients. The different DraI-RFLP profiles permit
differentiation of the two taeniid species. The authors reported
that the lower detection limit of the PCR-RFLP was 34 eggs in
2 g stool sediment. Furthermore, a 521-bp cox1 fragment was
detected in 8 out of 12 tapeworm carriers providing diagnostic
sensitivity of 66.6% (5 for T. saginata and 3 forT. solium),
which was higher than previous method with HDP2-PCR
repetitive DNA amplification [12]. Yamasaki and others [23]
have established multiplex PCR for differential diagnosis of
T. saginata and two genotypes ofT. solium carriers using fecal
samples. A detection limit of taeniid DNA was 5 eggs/g feces,
but more reliable results were provided at more than 50 eggs/g.
Multiplex PCR using copro-DNA prepared from fecal samples
of tapeworm carriers yielded 720- and 984-bp cox1 fragments
in T. solium carriers from Guatemala (12 out of 14 samples)
and Indonesia (4 out of 9 samples), respectively [23]. In
T. saginata carriers, 827-bp cox1 fragments were successfully
amplified at a sensitivity of 100% (5 out of 5 cases) [23].
Multiplex PCR has advantages of being faster and easier to
perform when compared to other methods. The characteristics ofhigher sensitivity, species-specific or T. solium genotype-
specific diagnosis, and detection of a tapeworm carrier prior to
patency of the infection are also definite advantages. The
diagnostic marker was detected from a T. solium carrier who
expelled only immature proglottids and was egg-free in stool,
implying that it is possible to detect tapeworm carrier prior to
patency. In areas where taeniasis is endemic, therefore, multiplex
PCR diagnosis will be useful for control programs that aim to
detect and treat tapeworm carriers [23]. Multiplex PCR can
cause non-amplification of target DNA marker because of
competition between template DNA and inhibitory substances
present in feces (personal observation), sample heterogeneity on
stool collection and preservation status of stool samples [23]. A
recent evaluation of detection of T. saginata taeniasis by
multiplex PCR reported that the taeniid DNA was detected in
all 10 tapeworm carriers examined when stool samples were
stored in ethanol properly after collection[25].
6. Conclusions
DNA-based differential diagnosis for human taeniid ces-
todes has become a very powerful tool not only for routine
identification but also for taeniasis/cysticercosis control pro-
grams that aim to detect tapeworm carriers and treat them. It is
also indispensable for definitive diagnosis of cysticercosis
cases in which histopathological findings are not confirmatory.
Acknowledgments
We thank the following researchers: T. Ikejima, P. Deku-
myoy, S.P. Sinha Babu, A. Oommen, G. Singh, DC. Qiu, M.
Wulamu, P.C. Fan, K.S. Eom, V.C.W. Tsang, A. Kassuku, S.S.Afonso, A. Zoli, S. Miura, A. Plancarte, W. Benitez-Ortiz,
C.M. Nunes, M. Vilhena, S. Geerts, J.C. Allan, J. Garcia-
Noval, M. Velasquez-Tohom, P.S. Craig, S.S. Margono and T.
Wandra for providing taeniid parasites and fecal samples; S.
Matsunaga, K. Nagakura, K. Suzuki, T. Nagase and Y.
Kiyoshige for providing biopsy materials. This study was
supported in part by a Grant-in-Aid for Scientific Research
from the Japan Society for Promotion of Science to A.I.
(14256001, 17256002) and a Research Grant from the Ohyama
Health Foundation to H.Y.
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