Redescription, deposition of life-cycle stage specimens of Sarcocystis bovifelis Heydorn, Gestrich, Mehlhorn and Rommel, 1975, and amendment to Sarcocystis hirsuta Moulé, 1888

Abstract

There is considerable debate concerning the life cycles and taxonomy of Sarcocystis species in cattle. Of the 8 species of Sarcocystis named from cattle, 2 (Sarcocystis cruzi and Sarcocystis heydorni) are morphologically distinctive because their sarcocysts are microscopic and the sarcocyst wall is thin (<0.5 μm thick). The sarcocysts of the remaining species (Sarcocystis hirsuta, Sarcocystis hominis, Sarcocystis bovini, Sarcocystis bovifelis, Sarcocystis sinensis, Sarcocystis rommeli) have thick (5–8 μm) walls indistinguishable by light microscopy, alone. To provide needed clarity, I herein review the history, nomenclature and life cycle of S. bovifelis (originally named by Heydorn and associates from Germany), redescribe it and deposit specimens of its various life-cycle stages at a museum for future reference. I also provide means to distinguish this parasite from S. hirsuta. Cats are the definitive hosts for both S. bovifelis and S. hirsuta. The sarcocysts of S. bovifelis are microscopic, its sarcocyst wall is type 10g, it has 2 schizogonic stages in blood vessels and sarcocysts are formed between 25 and 30 days post-inoculation in striated muscles, but not in the heart. Sporulated oocysts are 17.1 × 12.7 μm and sporocysts are 12.8 × 8.4 μm. The sarcocysts of Sarcocystis hirsuta are macroscopic, up to 7 mm long, its wall is type 18. Nothing is known of the development of S. hirsuta in cattle tissues and in cat intestine. Size of its oocysts and sporocysts is uncertain.

Keywords: Amendment; Sarcocystis bovifelis; Sarcocystis hirsuta; cat; cattle; history; life cycle.

Graphical abstract

Fig. 1.

Development of first-generation schizonts of Sarcocystis bovifelis in mesenteric arteries of calves. (A) A sporozoite (arrow) in a leucocyte in mid-lumen of a mesenteric artery of calf no. 597, day 7 p.i. The leucocyte nucleus (arrowhead) is out of focus. BF, HE. (B) Cross-section of an artery in mesentery of calf no. 597, day 7 p.i. Note an early schizont (arrow). The infected endothelial cell is protruding in the lumen. The endothelial cell nucleus (arrowhead) is slightly out of focus. BF, PASH. (C) A schizont (arrow) protruding in the lumen. Note nuclei (arrowheads) of the schizont. BF, IH. (D) Maturing schizonts protruding (arrows) in lumen of artery in mesentery of calf no. 487, day 10 p.i. HE. (E) Immature schizont (arrow on the left) with vesicular nuclei (arrowheads) and an adjacent mature schizont (arrow on the right) with few longitudinally cut merozoites (opposing arrowheads). BF, IH.

Fig. 2.

Second-generation schizonts and a free merozoite in calf no. 599, day 16 p.i. Scale bar applies to all panels. (A) Immature narrow serpentine multinucleated immature schizont (arrow) in myocardium; arrowheads point to its ends. BF, HE. (B) Small immature schizont with 8 nuclei in the myocardium. BF, HE. (C) Multinucleated schizont (arrow) in an ocular capillary. HE. (D) Immature schizont with 22 nuclei (arrowheads); compare the size of the parasite nuclei with the size of an erythrocyte (double arrows of the capillary). HE. (E) Ruptured schizont with spilled merozoites (arrows). BF, HE. (F) An extracellular merozoite (arrow) in smear of buffy coat of blood from a jugular vein. Arrowheads point to thrombocytes. Methanol, Giemsa's stain.

Fig. 3.

Transmission electron micrograph of an intracellular S. bovifelis merozoite in the myocardium of calf no. 599, day 16 p.i. Note a conoid (co), micronemes (mn), dense granules (dg), a nucleus (nu) and absence of rhoptries.

Fig. 4.

Sarcocysts of S. bovifelis. (A) Sarcocyst in gluteal muscle of calf no. 595, 30 days p.i. Arrow points to 2 metrocytes in a parasitophorous vacuole. BF, HE. (B, C) Longitudinal section of immature sarcocyst in gluteal muscle of calf no. 617, day 42 p.i. Note thin sarcocyst wall (opposing arrowheads). HF, HE. (D, E) Longitudinally cut immature sarcocyst (arrow) in tongue of calf no. 485, day 62 p.i. HF, HE. Note thickness (opposing arrowheads) of the sarcocyst wall. (F) Longitudinally cut immature sarcocyst (arrow) in gluteal muscle of calf no. 523, day 88 p.i. This is the longest sarcocyst observed in sections. BF. HE (G) Section of a mature sarcocyst in oesophagus of calf no. 523, 88 days p.i. Note thickness of the sarcocyst wall (opposing arrowheads). HF, HE.

Fig. 5.

Comparison of mature sarcocysts of S. bovifelis from the study in the USA and in Germany. HE. Opposing arrows point to thickness of the sarcocyst wall. Note metrocytes (me) and bradyzoites (br). Scale bar applies to all panels. Longitudinal (A) and cross-section (B) of sarcocysts in calf no. 386, 89 days p.i. from the present study in the USA. Longitudinal (C) and cross-section (D) of sarcocysts in calf no. 12, day 98 p.i. from the study in Germany (Gestrich et al., 1975a).

Fig. 6.

Sexual stages of S. bovifelis in sections of small intestine of cats. Scale bar applies to all panels. (A)–(H) are sections from a kitten orally inoculated with free bradyzoites; the epithelial brush border is oriented up towards the intestinal lumen. The host cell nucleus (arrowheads) is misoriented and indented. (I)–(M) are from the same HE-stained section of small intestine of a cat fed with S. bovifelis-infected meat. (A) Bradyzoite (arrow) in lumen, adjacent to a goblet cell. PASH. (B) A binucleate microgamont. Note vesicular nuclei (arrows). HE. (C) Immature microgamont in a goblet cell with 6 nuclei (arrow). (D) Mature microgamont with peripherally arranged microgametes (arrows) and a large residual body (rb). (E) A rupturing microgamont with 2 gametes (arrow) in lumen around a residual body (rb). Giemsa. (F) A macrogamont (arrow) in a goblet cell. (G) An elongated macrogamont (arrow) in a goblet cell. HE. (H) A near mature macrogamont (arrow) in a goblet cell. PASH. (I) An immature oocyst with 2 polar nuclei (arrows). (J) An oocyst with 2 sporocysts (arrows). HE. (K) An oocyst with 2 sporocysts. Arrows point to microgamete-like structures. (L) A sporulated sporocyst (arrow) with 4 sporozoites. (M) A sporocyst with 2 sporozoites (arrow) in focus.

Fig. 7.

Transmission electron microscopic views of sarcocysts of Sarcocystis hirsuta in a naturally infected cow from the USA. am, amylopectin granules, br, bradyzoites, co, conoid, dg, dense granules, edg, electron-dense granules, edl, electron-dense layer, gs, ground substance layer, me, metrocytes, mc, micronemes, mp, micropore, mt, microtubules, mct, mitochondrion, my, myocyte, nu, nucleus, pvm, parasitophorous vacuolar membrane, rh, rhoptries, cw, sarcocyst wall, se, septa, vp, villar protrusions. (A) Low magnification of sarcocyst showing vp butted against my. Also note folded vp, relatively smooth gs and numerous br. (B, C) Sections of pedunculated vp, attached to gs by a narrow stalk (double arrows). The pvm is highly folded, is lined by edl and has blebs (triple arrows). The vp contains numerous criss-crossing mt and edg (arrowheads). (D) Sections of me (arrows) below gs and se. Note numerous am, and a large nucleus. Also note section of br with many micronemes and dg. (E) Longitudinal section of a br (double arrowheads) butted against the smooth gs. Note numerous mc, a group of dg, an elongated (mct), numerous am and a terminal nu. (F) Anterior (conoidal) end of a br. Note a co, numerous mc, a micropore (triple arrows) and 2 rh.