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STOLTE, H., WIEDERHOLT, M., FUCHS, G. & HIER­HOLZER, K. (1969). Pflilgers Archlv, 313, 252. THURAU, K. (1966). Ann. N.Y. Acad. Sci., 139, 388. THURAU, K. (1969). Circulation, 40, 739. THURAU, K. (1969). Proc. Renal Society, Jan., 1969. Nephroll, 6, 692. THURAt:, K. (1968). Proc. R. Soc. Med., 62, 1118. THURAU, K., DEETlEN, P. & KRAMER, K. (1960). PflUgers Archiv, 270, 270. THURAU, K., ScHNERMANN, J., NAGEL, W., HORSTER, M. & WAHL, M. (1967). Circulatioll Res., 21, Suppl. II, 79. TOBIAN, L. (1967). Fed. Proc., 26,48. VALTIN, H. (1966). 1. din. Invest., 45, 337. VANDER, A. J. (1968). Circulation Res., 23, 605. VANDER, A. J. (1968). Amer. 1. Physioi., 214, 218. WEEKS, J. R. (1969). CirClllation Res., 24, Suppl. 1, 123. WEITSEN, H. A. & NORVELL, J. E. (1969). CirclI­lalioll Res., 15, 535. WHITE, H. L. & ROLF, D. (I965). Amer. 1. Physiol., 108, 397. WIRZ, H., HARGITAY, B. & KUHN, W. (1951). Quoted by Gottschalk, C. W. (1964) in Amer. 1. Med" 36, 670. WOLGAST, M. (1968). Acla physiol. scaM., Suppl. 313. WOOSTER, M. J. (1969), Proc. Renal Society, Jan., 1969. N ephroll, 6, 691. ZEHR, J, E., JOHNSON, J. A., MOORE, W. W, (1969). Ama. 1. Physiol., 217, 1672.

Spurious Parasites recovered

from Stools and Urines In

Rhodesia

BY

1. M. GOLDSMID*

Deparlmelll of Medical Microbiology, University College of Rhodesia.

Spurious parasites are defined as species that have passed through the body of the apparent h 05t (usually the alimentary canal) without in­fecting that host (Belding, 1965). There are many records of such pseUdo-parasitic infections of man in the parasitological literature and many such pseudo-infections may easily be mistaken for true parasitic infections if due care is not taken to ensure the correct laboratory identification. In some cases also, one has to take measures to discover whether an apparent infection is a genuine one or whether it is merely a spurious infection (e.g., in the case of fascioliasis and false fascioliasis in humans).

" Th~s w?rk comprises part of the work accepted by the UniversIty of London for the degree of Doctor of Philosophy.

173

THE C.ENTRAL AF.lUCA.N ]OUR,:>{AL OF 1\h:oH . .:nn:.

During the course of stool examinations at Harare Central Hospital a number of these spurious parasitic infections have been recorded, many of which were reported as true parasitic infections by the microscopists in the routine laboratories due to their mistakenly identifying the spurious parasites as some parasitic species which they closely resembled.

METHODS

These spurious infections were recovered after routine examination of stool specimens by water centrifugation and NaCI flotation and by simple centrifugation of urine specimens.

RESULTS

Among the spurious parasitic infections reo corded were:

Trematoda Schistosoma mattheei

Eggs of this species of fluke are not uncom· monly recovered from stool and urine specimens at Harare Central Hospital and may usually be recognised by their characteristic morphology. In 1967 and 1968, of 4,735 African stool speci­mens from which eggs of Schistosoma spp. were recovered, 285 (6 per cent.) appeared to be eggs of S. mattheei. The species of these terminal spined cattle schistosome eggs is given here as S. mattheei as it is felt that the differentiation of eggs on the basis of size and shape in the cases recovered is not reliable enough to differentiate the S. mattheei type eggs from the S. bovis type, as has been proposed by Blair (1966), especially in view of the problem of hybrid species (S. haematobium/S. mattheei) as discussed by Pitch· ford (1965). It is felt that, in view of the work of Pitchford (1965), where a fair overlap was found, and in view of the fact that eggs re­covered from one patient at least varied from the bovis type to the mattheei type (using length, width and width 5011 from the non-spiked end as well as the presence or absence of shouldering and the position of the miracidium) (Figs. 1 and 2), it is best in this paper to use only the name S. mattheei. While infections of man with S. mattheei have been recorded in Rhodesia (Blackie, 1932; Blair, 1966), and while the recovery of viable and non·viable eggs of this species from the urines of patients at Harare hospital is de­finite evidence of infection, at least some of the cases in which non-viable eggs of S. mattheei have been found in human faeces are possible cases of spurious infection due to the ingestion of infected bovine and, to a lesser extent, sheep and goat livers and intestines.

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A UGUST, J 970

•

SPURIOUS PARASITES

LEFT COLUMN

T op: Schistosoma mallheei egg ( Fig. I).

Upper Middle : Schistosoma mattheei egg (Fig. 2).

Lower Middle : Fasciola gi­gal1 tica egg (Fig. 3).

Botto m: Capillaria hepatica egg (Fig. 4) .

THE: ( .. , ..... Tn ... L Ar-R1C.4.r.;

JOUR,""'''!.. OF' MWICI!'>l:

RIGHT COLUMN

Capillaria hepatica in liver section (Fig. 5).

Physaloptera sp. egg (Fig. 6).

Spiruroid egg (Fig. 7) . N ote: All eggs approx.

X 350.

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AUGllST, 1970 SPURIOUS PARASITES

.'

LEFT COLUMN RIGHT COLUMN

Top: Egg of unknow n Rhabditella sp. male adult species of nematode (Fig. 8). (npprox. x 100)

Upper Middle: Meloidogyne sp. egg-cleavage stage

(Fig. 9).

Lower Middle: MeloidogYlle sp. egg-fully developed

(Fig. 10) .

Bottom: Note: All eggs ap­prox . x 350.

(Fig. 11).

Anterior end of first stage larva of Rhabditella sp.

(approx. x 250) (Fig. 12).

Hymenolepis sp. egg (Fig. 13).

Mit e egg (Fig. 14 ).

Tilt CE::N'rJlA L AnUC,\N

JoUn:'iAT~ OF" },[EO{(.:t :\E

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AUGUST, 1970 SPURIOUS PARASITES THE Cr.NTRAL AFRJCA~ JOURNAL OF MEDICINE

Thus, of 131 cases of S. mattheei recorded at Harare hospital on single stool submissions, ] 5 (12 per cent.) proved to be passing viable eggs and 88 per cent. to be passing non-viable eggs. Allowing some of this 88 per cent. to be "burnt­out" infections, and allo,wing that some would prove to be true infections on repeat stool and urine examinations, it still seems probable that some are spurious infections, especially in view of spurious F asciala and Capillaria infections which have been proved at Harare Central Hos­pital to be due to the eating of infected liver. The fact that schistosome eggs can pass through the intestine and be recovered in a recognisable state was proved by feeding viable S. haema­tobium eggs to a young vervet monkey (Cerco­pithecus aethiops). Twenty-four hours after feeding this uninfected monkey with the eggs, faecal examination showed the presence of physically undamaged though non-viable eggs on centrifugation. It thus seems quite feasible that some at least of the human cases passing non­viable eggs of S. mattheei at Harare hospital were probably cas e s of pseudo-infection, especially in view of the high incidence of schisto­somiasis among Rhodesian cattle, Condy (per­sonal communication) finding that 92 per cent. of the cattle slaughtered at the Salisbury abattoir were infected with schistosomes.

Fasciola gigantica With this species, too, genuine cases of human in­

fection in Rhodesia have been recorded (Goldsmid, 1968), but when these large operculate eggs (Fig. 3) are recovered repeat examination of faeces must be carried out after about seven days with the patient on a liver-free diet as recommended by Faust and Russell (1964). Spurious infections with F. gigantica are not uncommon here, as evidenced by repeat specimens being negative for eggs, and this condition of "false fascioliasis" with this species and the related F. hepatica is well recognised throughout the world (Faust and Russell, 1964). In all cases of false fascioliasis recorded in Salisbury it has been possible to establish that the patient had recently eaten liver, and in view of the high incidence of liver fluke amongst Rhodesian cattle, such cases are only to be expected. In this respect Thornton (per­sonal communication) found that of 107,311 cattle slaughtered in Salisbury in 1966-67, 48 per cent. were infected with F. gigantica.

Capillaria sp_ Capillaria hepatica, a nematode species related

to Trichuris trichiura, is recorded as a parasite of many mammals (including monkeys, dogs, lagomorphs and rodents). The adult worms live

176

in the liver of the infected host and soil con­tamination with eggs occurs after the death and decomposition of the infected host, or else eggs pass through the intestine of a carnivore which has eaten an infected animal, and soil contamina­tion occurs that way. These eggs (Fig. 4) then mature to the infective stage on the ground and are picked up by other animals and so infection occurs.

True human infections are recorded, mostly at autopsy, as in most cases of true infection eggs do not pass out of the host, but remain em­bedded in the liver (Fig. 5). Spurious human infections are not uncommon (Belding, 1965) and usually result from the eating of infected liver, the eggs passing through the alimentary canal. It is difficult to establish in these cases if infection will develop due to the possibility of some of the swallowed eggs being infective at the time of ingestion.

One such case of a spurious infection with Capillaria sp. has been found in Salisbury~ possibly the first recorded case from this country. This subject subsequently proved negative on repeated stool examination, and on questioning admitted to having recently eaten liver. However, Blackie (1932) recorded recovering eggs of lIepa­ticola hepatica from Rhodesia~a species now believed to be synonymous with C. hepatica.

The eggs of Capillaria resemble those of T. trichiura, but the polar plugs are less pronounced and the egg shell is conspicuously striated. With­out sufficient care being taken, these eggs (Fig. 4) could be taken for eggs of T. trichiura.

Physaloptera sp.

These eggs (Fig. 6) are not uncommonly re­covered from stool specimens in Rhodesia, and again true infections and spurious infections can occur (Faust and Russell, 1964). The presence of true human infection in this country has been established by continued recovery of eggs on repeated stool examination (,Blackie, 1932; Gold­smid, 1968) and by the recovery of adult worms after treatment with Thiabendazole (Mintezol) (Goldsmid, 1968).

A number of apparently pseudo-parasitic in­fections have been discovered at Harare hospital. repeat specimens after an initial positive examina­tion proving negative for eggs.

Spiruroid Eggs

Spiruroid nematodes are not uncommon in birds, and eggs resembling those of avian spiru­roid nematodes have been recorded from stool specimens by Blackie (1932) and Goldsmid (1968). These eggs resemble those of Physal-

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AI'miST, 1970 SPURIOUS PARASITES THE Cl::NTRAL AfRICAN JOtillNAL or J\.hmn::-.iJ;

optera sp" but are "narrower from side to side" (Blackie, 1932) (Fig, 7), It is probable that these eggs were merely "transit eggs" resulting from the ingestion of infected birds, The eggs are thick-shelled and contain a fully-developed

.... non-motile larva,

I

In one subject a spiruroid egg resembling that of Gongylonema ingluvicola as illustrated by Lapage (1962) was recovered, It too had a fully developed larva inside (Fig, 8),

Meloidogyne sp.

When plants (e.g., potatoes and carrots) in­fected with root-knot nematode are eaten, eggs of these plant parasitic nematodes may pass through the alimentary canal and out with the faeces. This type of spurious parasitic infection is well known in Africa, being recorded by Blackie (1932) (as Heterodera radicicola) in Rhodesia, Buckley (1946) (as Heterodera marioni) in Zambia, and in Durban, South Africa, by Elsdon-Dew and Freedman (1952) and Elsdon­Dew (1952). The latter authors found that in Durban 0.89 per cent. of 1,013 African stool specimens were infected with eggs of Meloidogyne spp., and Goldsmid (1968) in Rhodesia re­covered six cases (0.1 per cenL) from 5,545 African stool specimens examined in Salisbury.

The eggs of these nematodes may be found in the cleavage stages (Fig, 9) or in the fully­developed larval stage (Fig, 10).

Rhabditidae

The presence of Rhabditella axe; in urines has been reported in the past from China (Feng and Li, 1950) and the first record of this in Rhodesia is the report of Goldsmid (1967a). It is possible that this latter infection resulted from the habit of African females of using plant bulbs as vaginal dilators or their use of plant roots, etc., inserted into the vagina as a cure for sterility, nematodes of the family Rhabditidae being commonly

~ found in plant debris and humus. It would thus be possible for these worms to establish them­selves and then pass through a number of genera­tions in the human body as temporary parasites, as has been discussed in detail by Goldsmid (l967a).

Members of the genus Rhabditis are also reo _~ corded as temporary residents of the human

intestine, infection resulting from ingestion of contaminated food and water. Such infections are not uncommon during routine stool exami· nations in Rhodesia and have also been recorded in other parts of the world by Joyeaux and Baer (1942), Sasa et al. (1958). Shinohara (1960). Faust and Russell (1964).

177

In the case of the urine found containing these helminths, adults (Fig. 11), eggs and larvae were recovered, but in all cases of infected faeces only larvae were seen.

These larvae are extremely active and have a long thin whip-like tail. On detailed examination they can be distinguished with certainty from the rhabditiform larvae of the hookworm species, Ternidens deminutus, Strongyloides spp. and Oesphagostomum spp. by the presence of an extra oesophageal bulb or pseudo-bulb (Fig. 12). In most cases these larvae have been identified as larvae of Strongyloides sp.

When using culture techniques (e.g., the Harada·Mori test tube cultivation technique of Sa sa et al. (1958), Hsieh (1963) and Goldsmid (1 967b ), species of Rhabditis and Rhabditella may also be picked up.

Cestoda Hymenolepis sp.

Goldsmid (1968) reported the presence of eggs of Hymenolepis sp. in stools of two Africans at Harare Central Hospital. These eggs re­sembled the eggs recovered by Buckley (1946) and which he believed were eggs of the avian cestode Hymenolepis lanceoluta which had been accidentally ingested. However, while being morphologically similar to the eggs of H. lanceo­lata, the present eggs were much larger, being 91p. x 60,). as discussed by Goldsmid (1968). Superficially these eggs could be taken for eggs of H. nana, having polar filaments like the latter species, but they differed in their much greater size and the presence of an extra envelope as can be seen in Fig. 13.

Arthropoda Mite Eggs

It is not uncommon to recover mite eggs in the faeces of Africans in Rhodesia, and in the past these have been variously identified ts "hookworm" eggs or, more commonly, eggs of Trichostrongylus sp. They tend to be large in size (about 120p. x 60p.) and have a rough shell (as can be seen from Fig. 14). On squashing, a typical mite larva can often be found.

Miscellaneous.

Cysts of free-living species of protozoa are common in faeces, probably as a result of the drinking of contaminated water. When such stool specimens are allowed to stand it is not uncom­mon for the protozoa to excyst. A fairly safe rule is that the finding of active protozoan tropho­zoites in an old faecal specimen is suggestive of a coprozoic species of protozoan, and some of

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AUGUST, 1970 SPURIOUS PARASITES THE CENTRAL AFRICAl'f JOUttNAL OF .MEDlCI Nt.:

the ciliates found may resemble Balantidium coli superficially. In a freshly collected stool specimen trophozoites are more likely to belong to human commensal or parasitic species.

DISCUSSION AND SUMMARY

It can thus be seen that a wide range of easily recognisable spurious parasitic infections of man are recovered from African stool specimens in Rhodesia. Of these, caution is needed in the interpretation of some results where both true parasitic and spurious pseudo-infections with "transit eggs" can occur. In these latter cases re-examination after periods of controlled diet can help establish whether the infection is real or spurious before treatment is contemplated.

Of course, the whole problem of spurious para­sites (mainly "transit eggs") in stool specimens is intimately tied up with the incidence of these species in the food material eaten and the methods of food preparation and cooking prac­tised by the African people.

As mentioned earlier, discussion with the De­partment of Veterinary Services confirmed the high incidence of many of the potential human spurious parasites amongst food animals in Rho­desia and further talks with African doctors, students and medical assistants revealed that liver and intestine (the source of many helminth eggs) are commonly eaten by Africans. It appears that such food, especially in the reserves, is often not very thoroughly cleaned prior to cooking and thus many eggs (especially schistosome eggs in intestinal walls) must be ingested.

Further, while the most common method of cooking is boiling and while this boiling is often very prolonged, in many cases the intestinal material is rolled into balls and the inner por­tions may thus often be rather undercooked. However, experiments with Schistosoma haema­tobium eggs showed that they could be boiled in water for 30 minutes or longer and still be recovered physically undamaged (although ob­viously non-viable) on centrifugation and thus eggs protected in muscle, etc., must be able to survive disintegration for long periods of cook­ing. The eating of raw liver does occur, although not commonly, and even then it appears that only small amounts are eaten; and as regards other methods of meat preparation, gr,jj]ing may be used for liver and intestine, in which case, too, the centre portions may be undercooked. How­ever, the latter practices appear to be uncommon amongst adults, being mainly indulged in by small boys.

In all, spurious trematode, cestode, nematode, arthropod and miscellaneous protozoa and rotifer

178

"infections" have been found, many of which have been in the past reported as infections of some parasite which is superficially similar. Spurious parasites recorded from African stool specimens at Harare Central Hospital included:

Trematoda: Schistosoma mattheei eggs. Fasciola gigantica eggs.

Cestoda: Hymenolepis sp. eggs.

Nematoda: Capillaria sp. eggs. Physaloptera sp. eggs. ? GongylOllema ingillvicoia eggs. Unidentified spiruroid eggs. Meloidogyne gp. eggs. Rhabditella axei adults, eggs and larvae. Rhabditis sp. larvae.

Arthropoda: Unidentified mite eggs.

Miscellaneous: Unidentified protozoa, etc.

It can thus be seen that it is very necessary to train microscopists to recognise not only true parasite species and their products, but also basically similar pseUdo-parasitic species to im­prove the diagnostic efficiency of the laboratory and to ensure reliable laboratory reports for the physician.

REFERENCES BELDING, D. L. (1965). Textbook of Paristology, 3rd

Ed. N.Y., Appleton-Century-Crofts. BLACK IE, W. K. (1932). Memoir Ser. 5, London, Sch.

Hyg. trop. Med. BLAIR, D. M. (1966). C. Afr. J. Med., 12, 103. BUCKLEY, J. J. C. (1946). 1. Helminth, 21, 111. ELSDON-DEW, R. (1953). S. Afr. med. J., 27, 140. ELSDON-DEW, R. & FREEDMAN, L. (1952). S. Afr. J.

clin. Sci., 3, 59. FAUST, E. C. & RUSSELL, P. C. (1964). Craig & Faust's

Clinical Parasitology, 7th Ed. London, Kimpton. FENG. L. C. & LT, F. (1950). Peking nat. Hist. Bull., 18,

195 (Abs. No. 712 from Helminth. Abs. 1950, 19). GOI.DSMJD, J. M. (l967a). J. Helminth, 41, 305. GOLDSMID, J. (1967b). c. Afr. J. Med., 13, 54. GOLDSMJD, J. M. (1%8). Trans. R. Soc. trop. Med. Hyg.,

62, 619. HSIEH, H. C. (1%3). Wid. Hitll. Org. tech. Rep. Ser. 255. JOYEAUX, C. & BAER, J. G. (1942). Marseille med., 2,

676 (Abs. No. 1070 from Helminth. Abs. 1%5,28,303). LAPAGE, G. 0%2). Monnigs Veterinary Helminthology

and Entomology, 5th Ed. London, Bailliere, Tindall and Cox.

PITCHFORD, R. J. (1965). Bull. Wid. Hlth. Org., 32, 105. SASA, M., HAYASHI, S., TANAKA, H. & SHIRASAKA, R.

(1958). Japan J. expo Med., 28, 129. SHIN OHARA, T. (1960). J. KUTlIme Med. Ass., 23, 2777

(Abs. No. 2237 from Helminth. Abs. 1%2, 31, 403.

Acknowledgment

I should like to thank Mr. Hugh Hudson for his invaluable help with the taking of the photo­micrographs.

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