The embryonic development of Schistosoma mansoni eggs: proposal for a new staging system

  • Arnon D. JurbergEmail author
  • Tiana Gonçalves
  • Tatiane A. Costa
  • Ana Carolina A. de Mattos
  • Bernardo M. Pascarelli
  • Pedro Paulo A. de Manso
  • Marcelo Ribeiro-Alves
  • Marcelo Pelajo-Machado
  • José M. Peralta
  • Paulo Marcos Z. Coelho
  • Henrique L. LenziEmail author
Original Article


Schistosomiasis is a water-borne parasitic illness caused by neoophoran trematodes of the genus Schistosoma. Using classical histological techniques and whole-mount preparations, the present work describes the embryonic development of Schistosoma mansoni eggs in the murine host and compares it with eggs maintained under in vitro conditions. Two pre-embryonic stages occur inside the female worm: the prezygotic stage is characterized by the release of mature oocytes from the female ovary until its fertilization. The zygotic stage encompasses the migration of the zygote through the ootype, where the eggshell is formed, to the uterus. Fully formed eggs are laid still undeveloped, without having suffered any cleavage. In the outside environment, eight embryonic stages can be defined: stage 1 refers to early cleavages and the beginning of yolk fusion. Stage 2 represents late cleavage, with the formation of a stereoblastula and the onset of outer envelope differentiation. Stage 3 is defined by the elongation of the embryonic primordium and the onset of inner envelope formation. At stage 4, the first organ primordia arise. During stages 5 to 7, tissue and organ differentiation occurs (neural mass, epidermis, terebratorium, musculature, and miracidial glands). Stage 7 is characterized by the nuclear condensation of neurons of the central neural mass. Stage 8 refers to the fully formed larva, presenting muscular contraction, cilia, and flame-cell beating. This staging system was compared to a previous classification and could underlie further studies on egg histoproteomics (morphological localizome). The differentiation of embryonic structures and their probable roles in granulomatogenesis are discussed herein.


Schistosoma mansoni Egg Embryo Development Platyhelminth 



The authors acknowledge the staff of the Laboratório de Patologia-IOC/Fiocruz and of the Laboratório de Esquistossomose-CPqRR/Fiocruz for technical assistance, Mr. Bruno Eschenazi from the Setor de Produção e Tratamento de Imagens-IOC/Fiocruz for the schematic drawing of S. mansoni egg embryonic development, Dr. Jane Arnt Lenzi from the Laboratório de Patologia-IOC/Fiocruz and Dr. John R Kusel from the Glasgow University for critical review of the manuscript, and Dr. Jennifer Rowland from the Laboratory of Patterning and Morphogenesis-Instituto Gulbenkian de Ciência for the English review. ADJ and TG received fellowships from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)—Brazil. TAC and ACA de M received fellowships from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)—Brazil. The work was supported by the Fundação Oswaldo Cruz (Fiocruz).

Supplementary material

427_2009_285_MOESM1_ESM.doc (30 kb)
Supplementary methods (DOC 30 kb)
427_2009_285_MOESM2_ESM.doc (27 kb)
Supplementary results (DOC 27 kb)
427_2009_285_Fig9_ESM.gif (62 kb)
Fig. S1

Interaction plots between each evaluated main effect. a Egg maturation stages at its source. b Egg source at its maturation stage. The nonparallel nature of lines connecting the mean area at levels of one main source put into a hierarchy by the levels of the other main source suggests interaction, as mentioned in the text. (GIF 62 kb)

427_2009_285_Fig10_ESM.tif (19 kb)
High-Resolution Image (TIFF 18 kb)
427_2009_285_Fig11_ESM.gif (41 kb)
Fig. S2

Model good fitting diagnostics. a Plot of residual quantiles against theoretical normal quantiles (Q–Q norm plot) shows a moderate tail and about 97% of data fitting the straight line, which suggests its normal distribution. b Box plot of padronized residuals shows a median value equal to null and a symmetric interquantile range (box), also suggesting a normal residual distribution. (GIF 47 kb)

427_2009_285_Fig12_ESM.tif (14 kb)
High-Resolution Image (TIFF 13 kb)
427_2009_285_Fig13_ESM.gif (47 kb)
Fig. S3

Distribution of the main effect levels of egg estimated areas during maturation. a Box plot of estimated areas of eggs for the source main effect levels, cultivated and isolated. Cultivated eggs are significant bigger than those eggs isolated from the murine host (P = 0.00017). b Box plot of estimated area of eggs for the maturation stage main effect levels, ordered in roman numerals(I to V). Eggs increase in size as embryos develop. (GIF 40 kb)

427_2009_285_Fig14_ESM.tif (26 kb)
High-Resolution Image (TIFF 25 kb)
427_2009_285_Fig15_ESM.gif (92 kb)
Fig. S4

Statistical analysis of egg growth. a, b Only the biologically relevant relationships were plotted, i.e., M-I:M-II, M-II:M-III, M-III:M-IV, and M-IV:M-V, where M is the maturation stage in roman numerals (according to Vogel and Prata's classification). a Simultaneous 95% confidence intervals for comparing estimated mean areas of cultivated eggs during growth under in vitro conditions (RPMI-1640 medium). b Simultaneous 95% confidence intervals for comparing estimated mean areas of isolated eggs during growth in the murine host. The overlapping of confidence intervals with the vertical dotted line at abscissa 0 indicates no pairwise difference between maturation stages at a level of confidence set as 0.05. Positive significant mean differences are higher than 0 for the lower intervals, while negative significant mean differences are lower than 0 for higher intervals. See details in the text. c Box plot of egg area during different stages of maturation (M) in regard to egg source (S). S1 refers to eggs obtained from the host and S2 refers to eggs maintained in culture. d Simultaneous 95% confidence intervals for comparing estimated mean areas of each matching stages for both sources (isolated and cultivated), i.e. M-I:M-I, M-II: M-II, M-III:M-III, M-IV:M-IV, and M-V:M-V. (GIF 92 kb)

427_2009_285_Fig16_ESM.tif (68 kb)
High-Resolution Image (TIFF 67 kb)
427_2009_285_Fig17_ESM.gif (70 kb)
Fig. S5

Oogram technique by bright field and confocal microscopies. a, b Bright field micrographs of compressed fragments of S. mansoni-infected mouse intestines. a Classical oogram. Three mature eggs are shown. b Compressed intestinal fragment stained with hydrochloric carmine analyzed by BM. It is difficult to identify the stages of maturation in each egg. ce Confocal laser scanning microscope images of carmine-stained fragments of compressed intestines. c Sagittal section of two mature eggs (stage 8) and a third egg in an oblique view. nm, neural mass; np, neuropile; lg, lateral glands; gc, germinal cells. d Stage 2 egg, with the developing embryo (em). The stereoblastula and the yolk are visible. e Stage 3 egg, with an elongated embryo (em) and some yolk (yk). Scale bars 100 µm (GIF 69 kb)

427_2009_285_Fig18_ESM.tif (962 kb)
High-Resolution Image (TIFF 962 kb)
427_2009_285_MOESM3_ESM.doc (29 kb)
Supplementary Table 1 Number of eggs counted per each Vogel and Prata's stage. The eggs were obtained from S. mansoni-infected mice and from culture. (DOC 29 kb)
427_2009_285_MOESM4_ESM.doc (170 kb)
Supplementary Table 2 Estimated mean areas (µm2) during S. mansoni egg growth in mice (isolated) and under in vitro conditions (cultivated). (DOC 169 kb)
Video S1

Schistosoma mansoni embryo at stage 3 (MPG 3670 kb)

Video S2

Schistosoma mansoni embryo at stage 6 (MPG 5014 kb)

Video S3

Schistosoma mansoni embryo at stage 8 (mature miracidium) (MPG 3080 kb)


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Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Arnon D. Jurberg
    • 1
    Email author
  • Tiana Gonçalves
    • 1
  • Tatiane A. Costa
    • 1
  • Ana Carolina A. de Mattos
    • 2
  • Bernardo M. Pascarelli
    • 1
  • Pedro Paulo A. de Manso
    • 1
  • Marcelo Ribeiro-Alves
    • 3
  • Marcelo Pelajo-Machado
    • 1
  • José M. Peralta
    • 4
  • Paulo Marcos Z. Coelho
    • 2
  • Henrique L. Lenzi
    • 1
    Email author
  1. 1.Laboratório de PatologiaInstituto Oswaldo Cruz (IOC)/Fundação Oswaldo Cruz (Fiocruz)Rio de JaneiroBrazil
  2. 2.Laboratório de EsquistossomoseInstituto René Rachou (CPqRR)/FiocruzBelo HorizonteBrazil
  3. 3.Centro de Desenvolvimento Tecnológico em Saúde (CDTS)/FiocruzRio de JaneiroBrazil
  4. 4.Instituto de Microbiologia/Universidade Federal do Rio de JaneiroRio de JaneiroBrazil

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