A M ZOOLOGIST, 5:131-139 (1965).

HELMINTH LIFE CYCLES

JUSTUS F. MUELLER
Dept. of Microbiology, SUNY Upstate Medical Center, Syracuse

SYNOPSIS. Although classical work continues, particularly on the trematodes, for

the most part the basic life cycle patterns must be regarded as worked out. Helmin-
thologists are increasingly turning attention to the mechanics of the life cycle with
the result that parasitology is becoming an experimental science. Worms are now
under study from the biochemical, physiological, and behavioral points of view. As
a result, ideas of specificity have been altered, new physiological races of parasites

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discovered, and a number of new human helminthiases recognized, chiefly zoonotic
and involving larval forms. The number of parasitic worms successfully adapted to
laboratory propagation in animal hosts steadily increases, providing new and fruitful
models for investigation. Even more striking is the great breakthrough in the last
decade involving in vitro culture. Several cestodes and a variety of nematodes can
now be reared through various stages, if not their entire life cycle, in partially defined
media, and progress is being made with trematodes and acanthocephalans. Behavioral
studies are beginning to shed light on how parasites find their hosts and how they
locate each other inside the host. And in spite of long-held views to the contrary,
evidence increases that certain activities of helminths may be under hormonal control.

For "Is" and "Is-not" though with Rule and Line have been able to adapt to many different
And "Up-and-Down" by Logic I define. locations in the body of the host, whereas
Of all that one should care to fathom, I
Was never deep in anything but—wine. tapeworms, for example, are limited to the
Omar Khayyam small intestine. Certainly "age cannot
wither, nor custom stale, their infinite va-
In spite of Omar's modest disclaimer, he riety." Not only the Digenea but also the
seems to have enjoyed a certain reputation Monogenea represent currently active fields
as an astronomer and calendar maker. I, of research, and the larval forms of the
too, seem to have acquired some sort o£ latter are being described in increasing
reputation as a parasitologist. Yet I cer- numbers. Part of this interest in Mono-
tainly have never been deep in life cycles, genea is because their pronounced host
and why I was chosen to discuss this topic specificity is regarded as providing clues
is beyond me, unless it is to be regarded as to the evolutionary relationships of their
a sly tribute to my supposed ability at talk- fish hosts, a subject which is in a state of
ing my way out of a tight corner—or per- considerable confusion at the present time.
haps nobody else would take it. We have long been aware of such oddi-
For general purposes, the life cycles of ties of development as a miniature redia
the parasitic helminths have been worked telescoped inside of the miracidium, as in
out. Satisfactory accounts can be found in Parorchis acanthus, or of trematodes such
various reference works. And although the as Proterometra dickermani which attain
business of filling in the gaps still goes on, sexual maturity in the invertebrate host
and more species are constantly being added (Anderson and Anderson, 1963), apparently
to the list of those whose development is dispensing with the necessity of a verte-
understood, the essential features remain brate host, as seems also to be the case with
about as they were 25 or more years ago. Archigetes among the cestodes. Recently
Most of the newer information is detail James (1964) described a still more curious
that does not lend itself to summarization, form—a gymnophallid in which successive
and in any case is of interest only to spe- larval generations develop inside each other
cialists working in the various groups. from germ balls, and all stages look like
Chief objects in this continuing interest small copies of the adult.
in life histories are the trematodes. There One result of all this is Stunkard's (1963)
seem to be more of them, and as adults they recent conclusion that there is no clear-cut
131
132 JUSTUS F. MUELLER
distinction in life history between the
Monogenea and Digenea. He proposes to
go back to a scheme proposed by Burmeister
many years ago, with two subclasses: the
Pectobothridia (the present monogenes)
and the Malacobothridia (order Aspido-
bothrea and order Digenea), both based on
morphological features, but with names
derived from the character of the suckers.
On the other hand, Llewellyn (1963), on
the basis of the oncomiracidium of the
Monogenea, regards these forms as closer to
cestodes than to trematodes. Whether these
apparently divergent opinions can be har-
monized remains to be seen.
Descriptive work on life cycles has for
decades been a basic part of parasitology,
and must remain so as long as it is necessary
to tell one organism from another, or to
assign it a logical place in the scheme of
things. However, the mere taking of in-
ventory, incomplete though it be, has
largely accomplished its purpose and para-
sitologists are increasingly branching out
in other directions. As a result, we are
beginning to look at life histories from a
new angle. Instead of being preoccupied
with a mere description of the life cycle,
the parasitologist wants to know the "how"
and "why" of it from the biochemical,
physiological, and behavioral points of
view. The present emphasis on health and
increased food production has stimulated
this trend in the search for more effective
ways to control parasites of medical and
economic importance.
The effect of all this activity may be
summed up under a few general headings.
First of all our ideas of specificity have
undergone some rude changes. Many spe-
cies are now known to be much more, and
others much less elastic in their choice of
hosts than formerly supposed. The common
ascaris of pigs, for instance, has recently
been grown to egg-laying maturity in rab-
bits (Berger, Wood, and Willey, 1961). And
the resulting eggs are capable of normal
development. Leland (1963a) has demon-
strated that the economically important
parasite of livestock, Trichostrongylus axei,
can mature in the gerbil. Dawes (1962) has
shown that the sheep liver fluke, Fasciola
hepatica, a giant among trematodes, can be
grown to maturity in mice. The advantages
for experimental purposes of growing such
important parasites in small laboratory ani-
mals are obvious. Trichinella spiralis, for-
merly thought to have little or no host
specificity as long as it got into a warm-
blooded mammal, turns out not to be quite
that simple. Nelson, Guggisberg, and Mu-
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kundi (1963) and Nelson and Mukundi
(1963) have shown that a strain of trichi-
nella in Africa exists with high infectivity
for the bush pig and certain wild carnivores,
but little or none for the domestic hog or
rat. On the other hand, Jordan (1964)
has shown that trichinella can infect a cold-
blooded animal, the Texas horned toad
(lizard), if the latter is kept at a sufficiently
high temperature.
Schistosoma japonicum, formerly thought
to be a homogeneous species, is now known
to be composed of at least four geographic
races differing markedly in their infectivity
for molluscan hosts and in their importance
as human parasites, some being mainly
zoophilic (Hsu and Hsu, 1956). Such find-
ings have important implications for hu-
man medicine. And just as we have become
aware of monkey malaria spilling over into
man once the human disease is eradicated,
just so are we becoming increasingly aware
of the extent to which the helminth para-
sites of lower animals, and especially their
larvae, may invade man now that the spe-
cifically human helminths are beginning to
come under control.
We have of course been aware for a long
time of such larval infections as trichinosis,
cysticercosis, and echinococcosis; during the
20's and 30's several others were added: cer-
carial dermatitis and creeping eruption.
But the last 15 years have seen many others
added to the list. Since 1950 various work-
ers have called attention to the prevalence
of human infection with the larvae of Toxo-
cara, the common ascarid of dogs and cats.
The infection, known as visceral larva mi-
grans, manifests itself primarily by an un-
explained eosinophilia, enlargement of the
spleen and liver, and at times a skin rash
(Lorentz, 1962). Contact with contaminated
soil and swallowing the infective eggs is the
 HELMINTH LIFE CYCLES
source of infection. The larvae may wan-
der for months or years in the viscera or
central nervous system, leaving granulo-
matous trails. Particularly serious conse-
quences result from the larva entering the
eye. There is a certain wry humor in re-
membering how, for a long time, man freely
used dogs, guinea pigs, and other animals
to work out the life histories of his own
parasites, without realizing that he might
in turn be serving equally well as an "ex-
perimental" host for the infective stages of
the parasites of his animal associates. The
appreciation of this fact is one of the most
important developments of the past 15
years.
Another such parasitosis which we might
mention is eosinophilic meningitis (Alicata,
1962; Rosen et al., 1962) caused by invasion
of the human body and particularly the
meninges, by the rat lungworm, Angio-
strongylus cantonensis. This disease has
now been recognized in a number of Pacific
islands and in China, and appears to be
acquired from accidentally eating slugs
which carry the infective larvae. Another
example (Van Thiel, Kuipers, and Roskam,
1960) is herring worm disease, which seems
to be limited to Holland. This is contracted
by eating raw herring which are frequently
infected with large anisakid nematode lar-
vae coiled in their flesh. These worms
normally mature in fish-eating birds or
mammals, and since they are marine in
origin, up to a few years ago would have
been regarded as harmless to man. How-
ever, when liberated in the human small
intestine, the worms attack the mucosa and
set up an intense inflammation in the af-
fected segment of bowel. This may result
in blockage and necessitate surgical inter-
vention.
Several larval tapeworms deserve men-
tion. The mystery of the aberrant forms of
echinococcus cyst has been cleared up with
the recognition of at least three separate
species of these worms, each with its own
characteristic geographic area and preferred
natural reservoir hosts (Rausch, 1956;
Rausch and Nelson, 1963). Still another
tapeworm larva which has come in for in-
creasing attention is the pseudophyllidean
133
Spirometra. Up to 1950 only two cases of
this infection (sparganosis) were known
for the United States, although the parasite
was known to be widespread in its animal
hosts: water snakes and cats, throughout the
eastern United States. Its life cycle is such
that man must certainly be exposed to in-
fection throughout this area. As of the
present date 36 cases (Short and Lewis,
1964) have been reported from a region ex-
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tending from Buffalo, N. Y., to the southern
Mississippi Valley, Gulf Coast, Florida, and
the eastern seaboard. And another unre-
ported recent case from Florida is known to
the author, making 37. This parasite lives
in tissues, causing itching and at times mi-
grating nodules under the skin; without
doubt the current cancer consciousness of
the public with its stress on having any
unexplained "lump" examined accounts
for the sudden increase in the number
of reported cases.
Filarial worms have long been known as
parasites of man, and at least Wuchereria
bancrofti, the commonest cause of elephan-
tiasis, is as far as we know, specific for man.
Brugia malayi, on the other hand, which
also causes elephantiasis, is now known to
cause a zoonosis, the worm commonly oc-
curring in various monkeys or in the cat,
from which it is transmitted to man by
mosquitoes (Laing, Edeson, Wharton, 1960;
and others). The common heart worm of
the dog, Dirofilaria immitis, has now been
found in other animals, and 12 cases of
this or a very similar parasite have been
reported in man from various regions of
the United States (Welty, Ludden, and
Beaver, 1963). For years a condition known
as tropical eosinophilia, eosinophilic lung,
etc. (Beaver, 1961), characterized by a cloud-
ing of the lungs on x-ray examination,
cough, asthma, and eosinophilia, has been
a medical mystery. It now seems clear that
this is an "occult filariasis" (Lie, 1962)
again caused by various zoonotic filariae,
transmitted to man by mosquitoes. For
reasons not entirely clear, but possibly hav-
ing to do with some disproportion in the
size of the micronlariae and the diameter
of the capillaries, or perhaps the allergic
constitution of the individual, the embryos
134 JUSTUS F. MUELLER
do not appear in the circulating blood, but
remain in the capillary bed of the lungs
causing the characteristic congestive reac-
tion. Filaricidal drugs cure the condition
and thus serve as one means of retroactive
diagnosis. In both visceral larva migrans
and occult filariasis, no stage of the worm is
present in either the blood or discharges,
and the disease can be diagnosed only by
indirect means.
If I may be permitted an "aside" at this
point, I am associated with several hospitals
in Syracuse as staff parasitologist, and am
also consultant to the City Laboratory.
Physicians have long associated eosinophilia
with intestinal parasites, and formerly,
when no other diagnosis was forthcoming,
they would always order a stool examina-
tion for ova and parasites.* When we
couldn't find any they would become in-
sistent, and frequently get rather nasty, and
sometimes they would send the stool to
Tulane, or some other place where they had
more competent personnel. Visceral larva
migrans has now changed all this. In these
obscure cases I now tell the physician that
in all probability we are dealing with a case
of visceral larva migrans, and I suggest that
he do a laparotomy and get me a piece of
liver about 2 x 1 X 1 cm> ar>d we will fix
and section it and look for granulomatous
trails, or perhaps even find larvae. It is
astonishing how quickly his interest in a
positive diagnosis cools!
Many new forms have been added to
those whose life histories can be successfully
propagated in the laboratory, both in natu-
ral and in substitute hosts. Several of these
forms have already been mentioned. Pin-
worms of rodents have long been used as
substitutes for investigations on their hu-
man counterparts. The cotton rat filariid
Litomosoides and the rodent nematodes
Nippostrongylus and Nematospiroid.es are
other examples. The dog hookworm and
whipworm have long been used as models.
We have had Hydatigera of the cat, and
Hymenolepis of rodents as cyclophyllidean
tapeworm models. Until recently however
• "Parasitology is the last refuge of the diagnos-
tically destitute."
we had no laboratory model of a pseudo-
phyllidean tapeworm for experimental pur-
poses. Such has now been provided with
the development of means to cycle Spiro-
metra mansonoides in a completely con-
trolled system (Mueller, 1959a, b). Since
these are primitive tapeworms with striking
differences from cyclophyllideans in mor-
phology and physiology (the eggs develop
only under aerobic conditions, for instance),
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and since they have more life history stages
and require more hosts, it is obvious that a
lot of "information" must be locked up in
such a life cycle. Recently means have been
developed for the serial passage in labora-
tory rodents of the larval stages of both
forms of Echinococcus, eliminating the need
for dealing with the dangerous adult form
in dogs (Schwabe et al., 1964). The avail-
ability of all these models is of importance
not only for purposes of basic research, but
also in pharmacology, since certain host-
parasite combinations are much more useful
than others for screening drugs intended for
human use (Berberian and Freele, 1964).
Another feature of current research is the
study of helminthic behavior and response.
While worms which spend so much of their
lives inside a host are not ideal subjects for
studies of behavior, such are nevertheless
being undertaken. We want to know how
the parasites get there; what stimuli guide
them on their journeys through the body.
We are all familiar with the programming
and feed-back mechanisms which guide the
flight of rockets, and the difficult problem
of effecting a rendezvous in space. When
we regard a parasite as an organism pro-
grammed to rendezvous with another or-
ganism (the host) in time and space, not
only once, but several times in its life his-
tory, and arrive at the precise region in
the host best fitted to provide it with food
and shelter, we can see that the stored
information and cybernetic problems of
satellites are by comparison relatively sim-
ple. It is generally supposed that the pro-
lific reproductive potential of many para-
sites is a compensation for the hazards of
their existence, with survival depending so
largely upon chance. Baer (1952) however
disputes this and feels this is only a response
 HELMINTH LIFE CYCLES
to the nutritional abundance of their en-
vironment. However this may be, parasites
certainly do not depend upon chance alone.
Campbell (1961), Etges and Decker (1963)
and Maclnnis (1963) have produced evi-
dence that larval trematodes find their snail
hosts by responding to chemical attractants.
While Chernin and Dunavan (1962) and
others dispute this, they have demonstrated
that miracidia are remarkably efficient in
scanning their immediate environment for
the presence of snails. McCue and Thorson
(1964) have tested various helminths in a
thermal gradient and find a positive re-
sponse. It is defective, however, in that
unlike free-living worms similarly tested,
the parasites move into the region of ther-
mal damage and death, apparently lacking
any mechanism for reversal of the response.
These authors have shown also that the rate
of movement into the thermal stimulus fol-
lows a daily rhythm and that young worms
migrate more rapidly than old.
It appears that female ascaris are at-
tracted to the males, and that at times of
sperm depletion they develop a genital
girdle at the vulvar level to facilitate copu-
lation (Beaver and Little, 1964). At other
times the girdle is absent. The probing
movements of the female in seeking out
the looped or coiled tail of the male perhaps
account for the tendency of these worms to
enter the appendix or bile duct on occasion
(Beaver, 1964). If the association of the
genital girdle with "estrus" can be substan-
tiated, it would indicate that in worms, too,
certain types of behavior and development
are under endocrine control. Thorson finds
that in Nippostrongylus also the females
seek out the males, and are even attracted
to cotton soaked in ground up males (per-
sonal communication). In hookworms,
however, the males seem to be attracted to
the females, and there seems to be some
connection between the sex ratio and the
amount of mucosal laceration and blood
loss. Anemia is least when the two sexes
are balanced or when males alone are pres-
ent, and most severe when female worms
greatly outnumber the males (Beaver,
Yoshida, and Ash, 1964). Thus it appears
that hookworms, like human beings, tend
135
to compensate for emotional frustration by
overeating. And perhaps the day is not far
distant when papers on the psychiatric
problems of helminths will be included in
our program.
The most important development of the
last ten years is the number of break-
throughs on the culture front. An increas-
ing number of life cycles can now be dupli-
cated, at least in part, in vitro. Up to a
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few years ago only a few nematodes, free-
living forms, or parasites of insects, so little
modified that there is some question as to
whether they should be regarded as true
parasites or not, had been cultured in vitro.
Glaser and Stoll (1938) reported the devel-
opment in vitro under sterile conditions of
the sheep stomach worm, Haemonchus con-
tortus, up to the fourth stage larva. Smyth
(1947, 1950), and before him others, suc-
ceeded in obtaining differentiation and
maturation of certain large pseudophyl-
lidean larvae in vitro (Schistocephalus,
Ligula), but in these cases there is an abun-
dance of stored energy, and no real growth
is involved. In fact, Baer (1952) stated, "So
far no single true culture of any parasitic
helminth can be claimed." This has now
changed. Weinstein and Jones (1956),
Douvres (1962), Douvres and Tromba
(1962), and Leland (1963b) have succeeded
in culturing several nematode parasites of
rodents, sheep, and cattle in vitro up to
the egg-laying stage. Fairbairn (1961) has
worked out a system for the mass hatching
of ascaris eggs in vitro, something previously
supposed to occur only inside the alimen-
tary canal of the host. Voge and Berntzen
(1961) have hatched Hymenolepis eggs in
vitro. More remarkable, Berntzen (1962)
has succeeded in growing gravid adults of
Hymenolepis diminuta and H. nana in vitro
from cysticercoids removed from flour
beetles. Mueller (1959) cultured the plero-
cercoid of Spirometra from the procercoid.
The rate of growth compares favorably with
that which occurs in the mouse host, and
the cultured plerocercoids produce perfect
adult worms when fed to cats. Berntzen
and Mueller (1963) have grown young
adults (strobilated, but not yet egg-bearing)
in culture from both mouse-reared and
136 JUSTUS F. MUELLER
culture-reared spargana. The trematodes
seem to have lagged somewhat, but progress
has been made toward maintaining if not
actually culturing several forms (Williams,
Hopkins, and Wyllie, 1961; Senft and Senft,
1962). And Chernin and his associates are
working on the in vitro culture of larval
schistosomes in snail tissues, and appear to
be on the verge of success. At least a start
has been made on the Acanthocephala
(Jensen, 1952).
The above work has been done for the
most part with enriched media containing
such things as blood serum or chick embryo
extract, so that we cannot claim to have
denned the nutritional requirements of
these various worms as yet,1 and much of
it has been done by trial and error methods.
Nevertheless, anyone who has seen these
cultures cannot doubt that we have come
a long way from the time when the in vitro
culture of these large organisms was re-
garded as a hopeless task.
Several years ago I asked Ben Dawes
whether he had attempted to culture the
liver fluke and he replied that we weren't
ready for that yet, since we didn't know
nearly enough about the biochemistry of
the fluke to attempt to culture it. I then
asked him whether he didn't think we
might have to culture the fluke before we
learned much about its biochemistry?
Although much biochemical work is be-
ing done on parasites, so far at least no new
principles have emerged, nor is it clear that
parasites, aside from their faculty for an-
aerobiasis, differ in any fundamental chemi-
cal way from their hosts. In fact, I have
come to think of the parasitological bio-
chemists as our new taxonomists. Their
preoccupation with description and detail
is necessary, but so far at least unexciting.
(I am heavily insured and worth more dead
1 certain tapeworms (Coenurus, Echinococ-
1 myself have long been of the opinion that
such absolute parasites as tapeworms probably lack
certain enzyme systems, and that in consequence
the> are dependent upon the enzyme systems of the
host, at least to initiate certain processes. These en-
zymes are perhaps the essential elements supplied
In such substances as serum and thick embryo ex-
tract. If this is the case, then "defined media" in
the usual sense will never be possible for these
forms.
than alive, otherwise I would not dare make
this statement.)
It has long been known that cestodes are
influenced in their development by the en-
docrine physiology of their host. In the
monogenetic trematodes Polystoma integer-
imum and P. stellai we have forms which
are potentially dimorphic. Attaching to the
gills of very young tadpoles, they may be-
come mature on the gills, but normally
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they pass to the urinary bladder at the time
of metamorphosis, and arrive at sexual ma-
turity only when the amphibian host itself
matures (Stunkard, 1959). In this case
again we seem to have an example of the
physiology of the parasite being regulated
by the endocrine system of the host. But
whether this is a direct or indirect effect is
an unsettled question. Baer (1952) flatly
states, "There is so far no single clear case
of a vertebrate hormone affecting an in-
vertebrate, as the latter do not possess the
necessary receptor cells." However this may
be, we know that plant parasitic nematodes
are capable of producing hormone-like sub-
stances which cause the host tissue to pro-
liferate (Krusberg, 1962). Fisher (1963) has
given an excellent review of the literature
on hormonal alteration of plant and ar-
thropod hosts by endocrine substances pro-
duced by their parasites. And recently
Mueller (1963) has shown that the larva of
Spirometra produces an insulin-like sub-
stance which causes infected mice to gain
weight at an accelerated rate as compared
with controls.
Many problems remain to be solved.
What is the correct cytological interpreta-
tion of the larval asexual generations in
Digenea? Of the telescoping of several gen-
erations inside each other in Gyrodactylus?
Are these cases of polyembryony or some-
thing else? Is the larval reproduction of
cus) comparable? What is the meaning of
the extensive proliferation of larval tissue
seen in the body of the plerocercoid of
Spirometra, or of the strobilocercus of Hy-
datigera, only to be sloughed off at matura-
tion? If tapeworms are self-fertilizing, as
commonly stated, by what mechanism do
they keep variation under control without
 HELMINTH LIFE CYCLES
constant exchange of genetic material
(Jones et al., 1963)? Which is the head end
of a tapeworm? Where is its endoderm, if
indeed it has any (Ogren, 1953)? And is
it an individual or a colony (Stunkard,
1962)?
To what extent is the ability of a parasite
to infect a host determined by genetic fac-
tors? There is considerable evidence that
the ability of snails to support development
of larval trematodes is a genetic character
which differs from strain to strain within
the species. And we have already seen that
there are several races of Schistosoma japon-
icum differing in their biological characters.
There is strong evidence from my own
work, as yet unpublished, that suscepti-
bility of copepods to coracidia of Spiro-
metra is a genetic trait.
We have neglected the Acanthocephala
in our discussion. They are a monotonous
group, and few people seem inclined to
work with them. Nevertheless, they too
pose interesting problems of organization,
physiology, and development as do the ces-
todes, and their systematic position still
remains uncertain.
Unlike flatworms, the nematodes, both
free-living and parasitic, form a homogene-
ous group. The parasitic forms are not
greatly modified and show few peculiarities
which cannot be reconciled with their free-
living relatives. Hence they present fewer
puzzles and are in a sense less interesting
than such degenerate and absolute parasites
as tapeworms or Acanthocephala.
It is a sign of the healthy state of para-
sitology and its recognition as a major bio-
logical science that there has recently ap-
peared volume 1 of a new series "Advances
in Parasitology" edited by Ben Dawes,
wherein the several subdivisions of our
subject will be periodically reviewed by
experts. This should make refresher courses
like the present one unnecessary, and should
also be a help to the specialists, since para-
sitology today has grown to the extent where
it is difficult even for the expert to keep up
with what his fellow experts are doing.
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Baer, J. G. 1952. Ecology of animal parasites. 224
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Beaver, P. C. 1961. Toxocarosis (visceral larva
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-, and M. D. Little. 1964. The genital girdle
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