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Phylogenetic identification of Sparganum proliferum as a pseudophyllidean cestode Akatsuki Kokazea, Hiroko Miyaderaa, Kiyoshi Kitaa, Rikuo Machinamib, Oscar Noya”, BelkisyolC Alar&n de Noya’, Munehiro Okamotod, Toshihiro Horii”, Somei Kojimaa,* of Parasitology The I.wtitute of Medical Science, The Uniwrsity of Tokyo, Minato-ku, Tokyo, 108 Japan bDepatirnent of Patholqy, Faculty of Medicine, University of Tokyo, Bunkyo-ku, Tokyo, Japan ‘Section de Biohelmintiasis, Irstituto de Medicina, Fact&ad de Medicina, Universidad Central de Venezuela, Caracas, Venezuela ‘The Institute of Experimental Animal Sciences, Osaka University Medical School, Suita, Osaka, Japan ‘Department of Molecular Protozoohgv, Research institute of Microbial Diseases, Osaka University Medical School, Suita, Osaka, Japan aDepartrnent
Received 26 August 1997; accepted 2 October 1997
Abstract Sparganum proliferum is characterized by continuous branching and budding, the resulting progeny invading all tissues of the human body, causing l’atal sparganosis. Its life cycle, definitive hosts and the route of infection to humans have not yet been disclosed. Because its morphology is similar to Spirometra erinacei, the phylogeny of S. proliferum has been thought to be identical to or closely related to S. erinacei. However, the taxonomy of S. prolifemm has not been established up to present due to the lack of definitive observations. In order to clariljr the phylogenetic relationship between S proliferum and S. erinacei, nucleotide sequences of mitochondrial NADH dehydrogenase subunit 3 gene (ND.3) and four mitochondrial tRNA coding genes of S. proliferum and other pseudophyllidean cestodes were analyzed. The sequences of S. proliferum showed high similarity to those of S. erinacei, although they were clearly different from each other, indicating that the phylogeny of S. proliferum and S. erinacei is distinct. This is the first report showing the phylogenetic relationship among S. proliferum and other pseudophyllidean cestodes at the DN4 sequence level. 0 1997 Elsevier Science Ireland Ltd. Keywords: Sparganumprolijiemm; Mitochondrial DNA
Spirometra erinacei; Pseudophyllidea;
NADH
dehydrogenase
subunit 3 (ND3) gene;
Abbrevations: mtDNA, mitochondrial DN& ND3, NADH dehydrogenase subunit 3 gene; PCR, polymerase chain reaction * Corresponding author, Tel.: + 81 3 5449.7290; fax: + 81 3 54495292; e-mail:
[email protected] 1383-5769/97/$17.00 PZI S1383-5769(97)00037-S
0 1997 Elsevier
Science
Ireland
Ltd. All rights reserved.
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1. Introduction Sparganumproliferum is one of the most mysterious parasites. Since its first report by Ijima in 1905 [ll, 14 cases have been reported in the world. Among them, six cases were reported from Japan, three cases from Taiwan, two cases from the US and one case each from Venezuela, Paraguay and the Philippines [:2-171. It is characterized by continuous branchirrg and budding, the resulting progeny invading all tissues of hosts including bones. In spite of severe symptoms and high mortality of human sparganosis caused by S. prolifenlm, the rare occurrence of cases has hampered epidemiological and pathological studies of this infection. Moreover, little information is available regarding the biology of S. proliferum. For instance, the life cycle, definitive hosts and the route of infection to humans of S. proliferum have not yet been disclosed. Taxonomy of S. prolifencm also remains unclear. Since S. proliferum is morphologically similar to Spirometra erinacei, Ijima classified S. prolifetum as one of the pseudophyllidean cestodes [ 11. Later, Iwata and others suggested that S. proliferum could be morphologically differentiated from S. erinacei [l&20], while others made an assumption that S. prolifemm had acquired the ability of branching and budding by infection of retrovirus [21]. However, all these investigations have been done based on morphological observations and none of them have ever clearly showed whether S. proliferum and S. erinacei are identical species or not. Recently, in-vivo cultivation of S. prolifemm has been established, making it polssible to investigate the biology of S. proliferum [2:!]. The aim of the present study is to clarify the phylogenetic relationship between S. prolifemm and S. erinacei by comparing their nucleotide sequences. The genes investigated are NADH dehydrogenase subunit 3 gene. (ND31 [23,241 and four tRNA genes, encoded on mitochondrial DNA (mtDNA). Because mtDNA is known to show rapid evolution [25], it is widely used for the discrimination of closely related organisms, including cestoda [26-311. We have also compared
the sequences of S. proliferum with those of another pseudophyllidean cestode, Diphyllobothrium nihonkaiense, to examine the phylogenetic relationship among them. 2. Materials
and methods
2.1. S. proliferum and otherpseudophyllidean cestodes
Two different isolates of S. prolijkrum were investigated in the present study. One isolate was obtained from multiple cutaneous lesions of a Venezuelan patient [13], which has been maintained in outbred albino mice by serial intraperitoneal passages as described [22]. The other isolate was obtained from the second Japanese case found in 1907 [5,6]. The specimens were derived from the lung tissue preserved in formalin for 87 years in the Medical Museum of the University of Tokyo. Two isolates of adult D. nihonkaiense CD. nihonkaiense-1 and D. nihonkaiense-2) [32] were obtained from clinical cases. Two isolates of plerocercoids of S. erinacei (S. erinacei-1 and S. erinacei-2) were obtained from snakes captured in different locations in Japan. 2.2. Isolation of total DNA
Total DNA containing mtDNA was prepared from frozen, alcohol or formalin preserved isolates of each species of cestodes, using standard extraction techniques [33]. Approx. 20 frozen worms of S. proliferum were digested in a reaction mixture containing 10 mM Tris-HCl (pH 7.4), 25 mM EDTA, 10 mM NaCl, 1.0% sodium dodecyl sulfate (SDS), protease K (200 pg/ml) for 24 h at 37°C. The solution was treated three times with a phenol-chloroform mixture. After precipitation of nucleic acids with ethanol, total DNA was dissolved in 200 ~1 of 10 mM Tris-HCl (pH 7.4) and 1 mM EDTA. For the preparation of total DNA of both isolates of S. erinacei, approx. 20 frozen plerocercoids were digested. The total DNA of D. nihonkaiense was prepared from several proglottids of one adult worm.
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For each isolate, three clones were used for determination of sequence of both strands.
COI
I)
primer A
p mzl
El H 1 OObp
Fig. 1. The arrangement of genes on the Fasciola hepatica mtDNA reported by Garey and Wolstenholme [34]. The six tRNA genes are identified by the one-letter amino acid codes. The three protein genes are subunit 1 and 3 of the respiratory chain NADH dehydrogenase (ND1 and ND3, respectively) and subunit I of cytochorome c oxidase (COI). All genes are transcribed in the same direction, from left to right in this figure. The sequences of each primer are described in Section
2.4. SequenceanaZysis
Amino acid sequences were deduced according to the modified genetic codes used in Dugesia japonica and F. hepatica [34-361, except for AAA specifying lysine which we assigned asparagine as indicated by Ohama et al. [37]. The sequence alignment and phylogenetic tree construction were performed by CLUSTAL W [38-401.
n
L.
3. Results 2.3. Cloning of ND3 and four mt tRNA genesby polymerase chain reaction (PCR)
To clone the genes for ND3 acrid mt tRNAs, homology probing by PCR was carried out. A primer set was designed from the mtDNA sequence of Fasciola hepatica [34]. Primer A was designed for the F. hepatica tRNAAs”, 5’GGTAAAATCGTAAGGCTGTT,.3’, and primer B was designed for the conserved region of cytochrome oxidase subunit I (COI) gene, 5’A(AGT>‘TTNCC(AG>AANCCNCC(AGT)AT-3’, where N indicates A, T, G and C (see Fig. 1). PCR was performed with the use of PROGRAM TEMP CONTROL SYSTEM PC-700 (ASTEC). The primers (0.2 PM each) described above and total DNA were combined with 5 ~1 of 10 X Taq polymerase buffer (Boehringer Mannheim) and 4 ~1 of 25 mM magnesium chloride. The volume was brought to 50 ~1 with distilled water and 2.5 units of Taq DNA polymerase were added. Each amplification cycle consisted of DNA denaturation at 95°C for 0.5 min, primer annealing at 50°C for 0.5 min and extension at 72°C for 1 min. After running this cycle 30 times, appr’ox. 980 bp PCR products containing ND3 and four tRNA genes (tRNAPro, tRN&le, tRNALys, tRN&‘p) were obtained and cloned into the plasmid vector by using a TA cloning kit (Invitrogen). The sequence of cloned plasmid was determi.ned by a DNA sequencer DSQ-1 (Shimadzu), using a reaction kit for BcaBest DNA polymerase system (Takara).
In order to investigate the sequence of ND3 and tRNA genes of S. proliferum and pseudophyllidean cestodes, we designed primers based on partial mtDNA sequence of platyhelminth F. hepUtica, on which three genes for the subunits of respiratory enzyme complexes, NDl, ND3 and COI, and six tRNA genes are arranged as shown in Fig. 1 [34]. Products of the expected size of approx. 980 bp were observed after PCR with primer A and B (see Section 21, when total DNAs from S. prolifemm, S. erinacei and D. nihonkaiense were used as templates. These DNA fragments contained full-length sequences of ND3 gene which encodes one of the hydrophobic subunit of NADH-ubiquinone oxidoreductase complex (complex I) in the mitochondrial respiratory chain and several mt tRNA genes. The nucleotide sequences of ND3 from pseudophyllidean cestodes determined in the present study are shown in Fig. 2A. Sequences of both Venezuelan and Japanese isolates of S. proliferum were identical with no difference among all clones. However, some heterogeneity was found between S. erinacei-1 and S. erinacei-2. D. nihonkxiense also showed sequence difference between two isolates. The sequence of S. prolz$erum showed higher similarity with the sequence of S. erinacei (86.3%) than with that of D. nihonkaiense (73.1%). ND3 sequences of S. proliferum and S. erinacei were same in length (369 bp), while that of D. nihonkaiense was shorter (354 bp). Comparison of the entire amino acid sequence of the S. proliferum ND3 deduced from the nu-
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cleotide sequence with those of ND3s from other pseudophyllidean cestodes is presented in Fig. 2B. The homology of S. proli,ferum ND3 with S. erinacei ND3 was 87.0%, which was much higher than the value between S. prol@um ND3 and D. nihonkaiense ND3 (75.4%).
In addition to ND3, four tRNA genes, tRNAfi”, tRNA”‘, tRNALyS, tRNprr were encoded in this 980-bp PCR product (Fig. 3). These genes consisted of approx. 65 nucleotides and secondary
46 (1997)
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structures predicted from their sequences were typical clover-leaf as shown in Fig. 4. The arrangement of the four tRNA genes were the same as in F. hepatica (Fig. 1) except for tRNA”“‘AGN which is encoded between ND3 and tRNAT’r in F. hepatica [34]. Instead, 5-bp hairpin-loop structures were commonly found in the corresponding region in all three cestodes in this study (Fig. 3B). In each tRNA coding region, similarity between S. prolife’erumand S. erinacei
232 232
S.erinacei-1 S.erinacei-2 S.proliferm
***tt+C*~IT**t*tttt**Cf\tT**A*tClff"***.tf****fT*G**Affft*t* t*tt*tCITT**t**tt.**C**Tt*Af*f*fft*****f.G**A*******
S.eriaacei-1 S.erinacei-2 S.proliferum D.niho~~~s+l D.,iho&ai-e2
****G**l*****Att~tt****.**t*Gt*t*t*f.****,***~*****T** t*ttG***Ctt**A***t*ttt**t**ttt**G*ftffC*****.~*.*******T*,
290 290
n;CCCGAGCAM;GmA~A~TPCTAAATTTA~A~AT~A~~~TA~ ***\tT**ZA*Tlt*t*G*.G***Tftflt**fCf*C**fTIAtf*CIIGA**AI tt*CT***AtTlttt*GtCGCCfGG***TtftCtt**CttC***TIAlt*CICIPI**AC
290 290 290
s.eriaacei-1 s.erinacei-2 S.prOliferum D.aihonkaieIMe-1 D.aihonkaiease-2
+r++*+TA*n;'*'C'**'A*****A"'****TG"*'*****.*"**T.*~ *+**r*T**n;**'**"A***'***'*'***TCff"".*C*,.**..****T..~
348 348
GT'lWXCGTMGTmTT TITTGTGAC;G'ITATGTTCC'ITGGGGG l t*ttAt,*t***tttttt*C*.A**T**T**~ T**M*'IYT**G*Cf'*G*TTCT'*A T**AA*TT *t Gl C l t*GIITCT**Att***AtCC*t**tftC**fCttAttT*tT111
s.eriaacei-1 S.eriaacei-2
l r+*++*T'**A*+'*""*+*+
S.proliferm
AGGAATIYGGTTGGGTTACTGCTAA
D.aihoaka.ieaSe-1 D.aihonkaiezM&2
‘A***A!PAG
TlTTCTl!TACTGG~TTTTGTAATCTTTGA-
r+**,**T"'A""'****+c+
l A***A.TAG
TTPCTCmmm232
372 372 372 357 357
TACTGA
340 346 346
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*FS~F***F*fC**F********+**SSV*G****S********T***** *FS”F***F**C**F****‘********SG”*G****S**************
215 52
52
.S.erinacei-2 S.proliferum D.nihonkaiense-1
MLGLLFGLGIFSLLVLVISFFTSGLFNKFIGGAFCWGGPYECGFCSSSLSFN **A"F**GF**F**FII*G"**+*t**IGL'SIS*****IGL*SIs**S******8*******
D.nihonkaiense-2
*+A’F**GF**Ft*FII*G******tIGL*SIS**IGL*SIS**S******S*******
S.erinacei-1 S.erinacei-2 S.proliferum D.nihonkaiense-1 D.nihonkaiense-2
***h**t*****t****t********t*****t***,***v**********IG*** ***,~********C******t****t*t*****t*********V*,*********G***
104 104
CFS~TYFSLLVFFVIFDLEISLLLNMPEQGLLFSNFIYYFIFLLLLGVSFLG ***,~*********tV*************N****G******L~*II*SLG*VS ***n+*t***+*+tV***********r*N**N****G******L**II*SLG*VS
104 104 104
S.erinacei-1 S.erinacei-2 S.proliferum D.nihonkaiense-1 D.nihonkaiense-2
***]J**********L**** ***];***t******L**** EVLWGYVRWGYWSNWLGYC **+rr*******+~* l **'t**A***f*K*
52
52 52
12-j 12-3 123 118 118
Fig. 2. (A) Nucleotide sequences of ND3 gene from S. prolifemm and those of pseudophyllidean cestodes. An asterisk indicates a nucleotide that is identical to S. proliferum. ATG (bold) indicates the initiation codon and TAA and TAG (bold) code for the stop codon. (B) Comparison of the amino acid sequences of ND3 predicted from the nucleotide sequences of S. prolifemm and pseudophyllidean cestodes. An asterisk indicates an amino acid that is identical to .S. prolifemm.
was higher than the value between S. proliferum and D. nihonkaiense. Compared with the tRNA coding regions, much divergence was found in nucleotide sequences of non-coding regions (Fig. 3). 4. Discussion The taxonomy of S. prokferum has been controversial since its first identification in 1905 [l]. For instance, in 1967, ophthalmic sparganum budding in a manner suggestive of S. proi’ifeferumwas reported as abnormal Spargunum mansoni, namely S. erinacei [191. In 1972, Iwata and others had reported branched, proliferative larvae morphologically similar to the plerocercoid stage of S. erinacei as S. prolifencm [20]. In recent years, it was shown that serum from a patient with proliferative sparganosis reacted with S. erinacei antigens by immunoelectrophoresis 11171.These reports indicate that S. proliferum and S. erinucei are closely related or an identical species. However, no definitive conclusion on .the relationship between them has been obtained up to present. In this study, we have investigated nucleotide sequences of ND3 and mt tRNA genes of two
different isolates of S. prolifemm and other pseudophyllidean cestodes to clarify the phylogeny of S. proliferum. One isolate of S. proliferum was obtained from the second Japanese case [5,6] and the other from a Venezuelan patient 1131. The two cases were reported as having similar clinical courses and prognosis, the chief complaints were cutaneous swellings on the breast and abdomen in both cases [5,6,13]. To our surprise, these different isolates of S. proliferum had completely identical ND3 and mt tRNA nucleotide sequences, although it is possible to suggest that some genetic variants, as observed in genus Echinococcus [27], might be found in the other isolates of S. proliferum. From nucleotide sequence comparison, it was shown clearly that S. proliferum is not identical with S. erinucei. Based on nucleotide sequences of ND3 genes and tRNA sequences, we have constructed phylogenetic trees to identify the phylogeny of S. prolifencm among these cestodes. As shown in Fig. 5, S. proliferum is closely related to S. erinucei. The same result was obtained from the tRNA sequences, which also correspond well with the morphological observations. Garey and Wolstenholme had reported that F.
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primerA * TGT+ACGTTAAGMGGAGT-A’GGTTCTACAAACGTATC-TT +**~+***+*++**r+++T* --tAtt*tt*tt*t**tttT-f+ ***~++**++++**T*A+TGAGAG+TA++rC**.C**TG***G**~**
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46 (1997)
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Lys)
CTCATATATCTM-TTTAAGTGCAGGGTTCTTACCCCTGTGATGTGTTTT
*************, I~**t*t**tt***,****f*t*******tt T”*.‘“*A*‘**OC**“‘***********“‘*”t**CA******.A*
S.proliferum S. erinacei D.nihonkaiense
B S.proliferum S.erinacei D.nihonkaiense tRRA(Trp) S.proli feran S.erinacei D.nihonkaie,nse
CAAATTMGTTMGTTAGACTAAO~;TTTTCAAAATACTATTT
*t******tt*********t******t*****t~****~****~*****~*~~ **C*******tt*t*-**t**t**t*t*tt**tt*~t~*********c****A*****G*A-
co1 S.proliferttln S, erinacei
,Zi:$rz
D.nihonkaiense
-A************
Fig. 3. Sequences of tRNA coding regions upstream (A) of, and downstream (B) of the ND3 gene. Sequences of S. prolifemm, S. esnacei-2, and D. n&o&z&se-2 arc shown. An asterisk indicates a nucleotide that is identical to S. prolifemm. The tRNA coding regions are indicated by an open box Dashed boxes with an arrow in (B) indicate the 5-bp stem of hairpin sequence.
tRNAS”’ between ND3 and tRNATrP [34]. Same type of secondary structure which lacks D-loop has been reported in many other metazoan mt tRNA [41-431. However, such a structure was not found
hepatica
code
structurally
bizarre
all cestodes in this study. Instead, a 5bp hairpin-loop structure (Fig. 3B) was commonly observed. The function of this sequence is not clear at present. In conclusion, our results clearly showed that
for
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(b)S.erinacei
T-G G-C A-T T-G T-A T-A T
GOT C-G
T-A
T-A T
G
GGG
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.
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C-GA T-A A-T GOT T-A
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217
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46 (I 997) 271-279
G G
T GG
Fig. 4. Deduced secondary structure of tRNAR” gene. Similar clover-leaf secondary structures were commonly deduced from all the other three tRNA genes in all three cestodes.
Diplogonoporus grandis, another pseudophyllidean
cestode (Miyadera, unpublished observation). In order to further confirm that S. prolifentm belongs to pseudophyllidean cestode, we are currently investigating cytochrome c oxidase subunit I (COI) sequences of S. prolifenrm and other pseudophyllidean cestodes in comparison with those of cyclophyllidean cestodes.
S. erinacei
D. nrhonkarense
Lb----
f. hepatrca
H 0.02
Fig. 5. The unrooted phylogenetic tree based on nucleotide sequences of ND3 gene, depicting relationships between S. proliferum and pseudophyllidean cestodes. The actual genetic distance between F. hepatica and D. nihonkaiense is 0.4569. The bootstrap value of this tree based cn the generation of 1000 trees was lOGO.
the phylogeny of S. proliferum is not identical with that of S. erinacei but is very close to each other, which implies that S. proliferum may belong to pseudophyllidean cestodes. This was confirmed by the fact of high similarity of ND3 nucleotide sequence between 5: proliferum and
Acknowledgements
We acknowledge to Drs M. Kamiya, K. Hirai, M. Sano, M. Niimura, Z. Kawamura and Y. Kawakami for supply of specimens of pseudophyllidean cestodes. We are also grateful to Drs M. Hasegawa and T. Hashimoto for useful comments and discussions. This work was supported partly by Grants-in-Aid for Scientific Research on Priority Areas (no. 08281103 and 08281105) from the Ministry of Education, Science, Sports and Culture of Japan for SK. and K.K., respectively. References [I]
Ijima, I. (1905) On a new cestoda larva parasitic in man prolifer). J. Coll. Sci., Imperial Univ. Tokyo 20, l-21. (Plerocercoide~
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[2] Stiles, C.W. (1908) The occurrence of a proliferating cestode larva (Sparganum prolr@um) in man in Florida. Hyg. Lab. Bull. 40, 7-18. [3] Gates, H. (1908) Larval tapeworm in human flesh. South. Med. J. 1, 351-367. 141 Gates, H. (1909) Larval tape-worm in human flesh, or Sparganum prolifencm gatesius (Stiles). Gulf States J. Med. Surg. Mobile Med. Surg. J. 15, 543-553. [5] Yoshida, S.O. (1914) On a second and third case of infection with Plerocercoides prolifer Ijima, found in Japan, Parasitology 7, 219-225. [6] Usui, R. (1909) Plerocercoides prolifer Ijima. Igakuchuou-zasshi 7, 79-84. [7] Akanuma, S. (1920) Pathologic,aI and anatomical study on plerocercoides prolifer. Iji-sbimbun 1039, 129-141. [8] Tashiro, K. (1924) Clinical, pathologic-anatomical and experimental studies on ‘Plerocercoides prolifer Iijima’ (19051, ‘Sparganum prolifemm Stiles’ (1906). Mitt. Med. Fak. Kaiserliches Kyushu Univ. 9, l-42. [9] Morishita, K. (1972) Rare human tapeworms reported from Japan. V. Sparganum p,‘-olifencm (Ijima, 1905). Progr. Med. Parasitol. Jpn. 4, 45’8-488. [lo] Connor, D.H., Sparks, A.R., Strano, A.J., Neafie, R.C. and Juvelier, B. (1976) Dissemi.nated parasitosis in an immunosuppressed patient. Arch. Pathol. Lab. Med. 100, 65-68. [ll] Lin, T.P., Su, I.J., Lu, SC. and Yang, S.P. (1978) Pulmonary proliferating sparganosis. A case report. J. Formosan Med. Assoc. 77,467-472 [12] Beaver, P.C. and Rolon, F.A. (1381) Proliferating larval cestode in a man in Paraguay. A case report and review. Am. J. Trop. Med. Hyg. 30, 625637. [13] Mouhnier, R., Martinez, E., Torres, J., Noya, O., Noya, B.A. and Reyes, 0. (1982) Human proliferative sparganosis in Venezuela: report of a case. Am. J. Trop. Med. Hyg. 31,358-363. [14] LaChance, M.A., Clark, R.M. and Connor, D.H. (1983) Proliferating larval cestodiasis: report of a case. Acta Trop. 40, 391-397. [15] Liao, S.W., Lee, T.S., Shih, T.P., Ho, W.L. and Chen, E.R. (1984) Proliferating sparganosis in lumbar spine: a case report. J. Formosan Med. Assoc. 83, 603-611. [16] Lo, Y.K., Chao, D., Yan, S.H., Liu, H.C., Chu, F.L., Huang, C.I., Chang, T. and Liu, H.C. (1987) Spinal cord proliferative sparganosis in Taiwan: a case report. Neurosurgery 21, 235-238. [17] Nakamura, T., Hara, M., Matsuoka, M., Kawabata, M. and Tsuji, M. (1990) Human proliferative sparganosis: a new Japanese case. Am. J. Chn. Pathol. 94, 224-228. [18] Iwata, S. (1934) Some experimental studies on the regeneration of the plerocercoid of Manson’s tapeworm, Diphylfobothrium erinacei (Rudoplhi), with special reference to its relationship with Spaq:anumprolifenm Ijima. Jpn. J. Zool. 6, 139-158. [19] Tanaka, H., Yamashita, S., Endo, H., Kane, R., Komatsuzaki, K. and Kawashima, J. (1967) Two cases of human
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[25] 1261 [27] [28] [29]
[30] [31]
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[33]
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