Human enterobiasis in evolution: origin, specificity and

Article available at http://www.parasite-journal.org or http://dx.doi.org/10.1051/parasite/1999063201
HUMAN ENTEROBIASIS I N EVOLUTION:
ORIGIN, SPECIFICITY AND TRANSMISSION
HUGOT J.-P.*, REINHARD K.J.**, GARDNER S.L.*** & MORAND S.****
Summary:
Résumé
: H Y P O T H È S E S SUR L'ORIGINE E T LA SPÉCIFICITÉ DES O X Y U R E S
HUMAINS : LIENS AVEC LEUR M O D E D E TRANSMISSION
The co-evolutionary pathway seems to be the most plausible
hypothesis for the explanation of the origin of human pinworms.
Deux modes de contamination
Of the two modes of transmission of oxyurids among humans
l'enterobiosis
which have been documented, the direct oral/anal route is also
chez d'autres primates,
observed in other Primates and seems to have been favoured by
œufs en suspension
selection. As indirect air-borne transmission has also been shown
études de cophylogénie
for human enterobiasis, the question of "How this alternative to the
parallélisme
standard transmission method could have arisen" is examined. The
de leurs oxyures,
results of comparative studies of prevalence of Enterobius
résultat d'un phénomène
in human
humaine
ont été reconnus
: la voie oro-anale,
et la voie aérienne
ont d'outre part révélé l'existence d'un
si marqué entre l'arbre évolutif des Primates et celui
qu'il ne peut être expliqué
d'étroite
humains sont donc probablement
America, show that a higher prevalence of pinworms is correlated
des
with the lower total amount of air-exchange in caves relative to
génération
other structures. The air-borne route of transmission of pinworms
la voie oro-anale
animaux
savane,
pair. This mode of transfer could have been
en génération.
régulièrement
Or, si l'on distingue
nomades
et vivants dans des milieux
l'efficacité de la transmission
probablement
from a hunting-gathering to a more sedentary existence, initially
l'étude comparative
associated with cave habitats.
humains dans des séries
favorisé.
aisément
arborés ou de
de la prévalence
des œufs
de coprolites
d'oxyures
collectés sur plusieurs
comment ce mode de contamination
a pu être
des œufs est
beaucoup plus élevée sur les sites anciennement
des
vivants dans des villages,
chasseurs-cueilleurs
lorsque
occupés par des
que sur ceux occupés par
ou des agriculteurs
l'on compare les prévalences
sites
permettent de tenter
On observe en effet que la prévalence
agriculteurs
pourquoi
par voie aérienne est
du sud-ouest des Etats-Unis
d'expliquer
des parasites
transmis de
faible dans ces mêmes milieux. Les résultats de
néolithiques
Enterobius vermicuhris, E. gregorii, primates, pinworm, oxyurid,
coevolution, enterobiasis, habitation, prevalence, dust, coprolites, air-bornecontagion, air as a vector, archaeological material, parasites, helminths,
archeoparasitology.
Les oxyures
les descendants
a été favorisée par la sélection chez des
favoured during the time when humans changed their behaviour
KEY WORDS :
que comme le
coévolution.
ancêtres primates de l'Homme,
human/Enterobius
connue
dans laquelle des
dans l'air sont inhalés puis déglutis. Les
coprolites, in villages of Neolithic age of the arid west of North
among humans is interpreted as an innovation in the
dans
également
nomades.
De plus,
respectives de
villageois
MOTS CLES : Enterobius vermicularis,
E. gregorii, primates, oxyures, coévolution, vivants, soit dans des maisons construites en milieu ouvert, soit
enterobiosis, habitations, prévalence, poussière, coprolites, transmission par
dans des maisons troglodytes, on observe à nouveau une
voie aérienne, parasites, helminthes, palèoparasitologie.
différence significative : le taux d'oxyurose est environ deux fois
plus important à proximité
falaises
des habitations
construites au flanc des
et utilisant en partie des cavités naturelles de la roche. Il
semble donc que l'augmentation
humaines et les modifications
accompagné
expliquer
observées
de la densité des
le développement
de l'agriculture
totalement ce phénomène,
puissent
L'interprétation
observations
populations
de leur régime alimentaire
et que les différences
être en partie liées au type
que nous proposons
qui ont
ne puissent
d'habitat.
à partir de ces différentes
est la suivante : la transmission
par voie aérienne ne
peut être efficace que dans un milieu confiné où les courants
d'air
sont faibles,
abris aménagés
comme l'est l'atmosphère
* Muséum National d'Histoire Naturelle, Institut de Biosystématique
du développement
(FR 1541 CNRS), Nématologie Fondamentale et Appliquée, 55, rue
l'hypothèse
Buffon, 75231 Paris cedex 05, France; e-mail: [email protected].
être progressivement
** Department of Anthropology,
sorte que dans les circonstances
126 Bessey Hall, University of
des grottes ou des
sous roche, qui partout ont été utilisés au cours
des sociétés humaines ; nous
que le mode de transmission
favorisé au cours de ces périodes,
Nebraska-Lincoln, Lincoln, NE 48588-0568, USA.
de la densité des populations
*** H.W. Manter Laboratory of Parasitology, W-529, University of
d'un habitat particulièrement
Nebraska State Museum, University of Nebraska-Lincoln, Lincoln, NE
aérienne,
68588-0514, USA.
de façon considérable
**** Centre de Biologie et d'Écologie Tropicale et Méditerranéenne,
concernés.
l'ensemble
faisons
par voie aérienne
où une augmentation
a pu
de telle
importante
s'est accompagné de l'occupation
propice
à la transmission
de ces facteurs ail contribué
le taux de contamination
par vole
à augmenter
des groupes
Laboratoire de Biologie Animale (UMR 5555 CNRS), Université de
Perpignan, Av. Villeneuve, 66860 Perpignan, France.
Correspondence: J.P. Hugot.
Parasite, 1 9 9 9 , 6~, 2 0 1 - 2 0 8
Point de vue
201
HUGOT J.-P., REINHARD K.J., GARDNER S.L & MORAND S.
INTRODUCTION
A
shford & Crewe ( 1 9 9 8 ) noticed that, o f the
399 species o f parasites that have b e e n reported
from humans, more than 7 0 % are "adventi­
tious" species for which man is an incidental host and
only 16 % can b e considered "core" species, depen­
dent on man for their survival. Ashford ( 1 9 9 1 ) also
illustrated h o w parasites may b e c o m e parasitic in
humans by either host-transfer or coevolutionary path­
ways. C o m b e s ( 1 9 9 0 ) had observed this previously and
considered that most parasites o f humans originally
t r a n s f e r r e d t o m a n from n o n - p r i m a t e h o s t s . H e
explained this as a c o n s e q u e n c e o f the ecological cha­
racteristics o f humans. B e c a u s e o f our t e n d e n c y to
inhabit extremely varied environments and b e c a u s e o f
varied behavioural patterns exhibited by humans, w e
provide myriad opportunities for parasites to o c c u p y
n e w hosts. In other words, w h e n humans left the
natural habitat o f their primate ancestors and pro­
gressively c o n q u e r e d all available geographical ranges
on Earth, they also penetrated the territory o f different
parasites o f which s o m e host-switched successfully,
adapted, and speciated, b e c o m i n g host-specific human
parasites.
Here w e investigate the origins o f human pinworms
and the reasons w h i c h can explain their high speci­
ficity. This leads us to e x a m i n e and c o m p a r e the ways
o f transmission o f the pinworm parasites in different
host groups. For m a n y years the literature on pinw o r m e c o l o g y has r e c o g n i s e d the importance o f oral
ingestion as the primary m e a n s o f perpetuating infec­
tions o f t h e s e n e m a t o d e s within and b e t w e e n human
hosts. However, recent w o r k suggests that air-borne
transmission o f pinworm eggs may also b e important
in m a i n t e n a n c e o f their life-cycle. Air-borne trans­
mission o f p i n w o r m s a m o n g modern h u m a n s is dis­
cussed relative to the accumulating data sets o n the
p r e v a l e n c e o f parasites in coprolites from Neolithic
humans.
MATERIALS AND METHOD
A
sample o f 8 3 0 coprolites from the arid areas o f
North America allows to consider
Enterobius
vermicularis
infection in context with chan­
ging habitation patterns. T a b l e I summarises the dates
for most o f the locations in which positive coprolites
have b e e n discovered. T h e larger n u m b e r o f dates in
the AD range does not reflect m o r e sites studied from
later time periods. It simply indicates that pinworm
eggs are m o r e c o m m o n l y found at later sites. Table II
presents the locations which w e r e investigated for
human coprolites, ordered by habitation type, and
202
Locality
Date
8,000 BC
D a n g e r Cave, Utha
4,800-4,300 BC
Dirty S h a m e Shelter, O r e g o n
4,010-650 BC
H o g u p C a v e , Utah
AD 400
T u r k e y P e n C a v e , Utah
AD 600
Antelope House, Arizona
AD 500-1,200
C l y d e ' s C a v e r n , Utah
AD 920-1,130
Pueblo Bonito, New Mexico
AD 1,075-1,140
Antelope House, Arizona
AD 1.100-1,250
S a l m o n Ruin, N e w M e x i c o
AD 1,250-1,300
Inscription House, Arizona
T a b l e I. - D a t e s for Enterobius
vermicularis
finds from North A m e ­
rica.
tabulates the p r e v a l e n c e o f E. vermicularis
eggs.
Hunter-gatherer sites were o c c u p i e d by small groups
o f p e o p l e (less than 5 0 ) w h o subsisted o n wild plants
and animals. Agricultural sites w e r e o c c u p i e d by large
groups o f p e o p l e (several hundred) w h o subsisted in
part on cultivated plants and in part on wild plants and
animals.
Parasite remains have b e e n r e c o v e r e d from coprolites
( d e s i c c a t e d faeces) for 2.5 d e c a d e s in North America
(for review s e e Reinhard, 1 9 9 0 ) . Paleoparasitological
methodology was established by Samuels ( 1 9 6 5 )
w h e n he d e v e l o p e d the rehydration and sedimenta­
tion technique for extracting parasite eggs from copro­
lites. Since that time, relatively little variation has
o c c u r r e d other than the introduction o f n e w equip­
ment and adaptation to available materials. Consis­
tency in technique is essential for comparing data col­
lected by several researchers o v e r a 25-year period:
the fact that the t e c h n i q u e o f Samuels ( 1 9 6 5 ) was fol­
l o w e d with minor variations by all North American
coprolite researchers until present supports the vali­
dity o f comparative analysis. T o further evaluate the
c o n s i s t e n c y o f results, R e i n h a r d ( 1 9 8 8 ) a n a l y s e d
coprolites from Antelope House, o n e o f Fry's main
study sites. No statistical difference in recovery o f eggs
o f E. vermicularis
or larvae was found. Therefore, w e
b e l i e v e that, with regard to E. vermicularis,
the data
sets from different researchers may reliably b e c o m ­
pared.
Relative preservation o f the remains b e t w e e n sites is
also a significant factor w h e n considering the reliabi­
lity o f intersite c o m p a r i s o n s . In the c a s e o f t h e s e
coprolites, the eggs s h o w excellent preservation, except
for those from Pueblo B o n i t o which w e r e poorly pre­
served. For the rest o f the sites, the eggs w e r e well
preserved and the larvae w e r e sufficiently robust to
allow them to b e s q u e e z e d out o f the egg. However,
even for the site which exhibited relative poor pre­
servation, the eggs w e r e still recognisable and identi­
fiable.
Point de vue
Parasite, 1 9 9 9 , 6, 2 0 1 - 2 0 8
H U M A N E N T E R O B I A S I S IN
Studied
Positive
Site
Cave
Dwelling,
Hunter
EVOLUTION
Analyst
gatherer
100
0
Dust D e v i l C a v e
Reinhard
50
0
Love Lock Cave
Heizer a n d N a p t o n
16
1
Danger Cave
Fry
50
4
Hogup Cave
Fry
32
0
Frightful C a v e , C o a h u i t a , M e x i c o
Fry
13
1
Dirty S h a m e R o c k S h e l t e r
Hall
35
0
Bighorn Cave
Reinhard
326
6 (1.8 % )
Cave
sites
stone
walled
villages/Agricultural
0
Glen Canyon Anasazi
Fry
10
0
Glen Canyon Fremont
Fry
40
0 (0 % )
Stone
1
without
30
12
walled
Villages/Agricultural
S a l m o n Ruin
5
9
0
Kin K e t s o
Reinhard
15
4
Pueblo Bonito
Reinhard
Reinhard
132
13 ( 9 . 9 % )
ISO
•w
20
2
B i g h o r n S h e e p Ruin
Gardner
56
4
Hoy
Stiger
17
3
1
Inscription
Stone
20
283
walled
Antelope
Villages
in
Caves/Agricultural
House
Reinhard
House
House
Fry
Step House
Samuels
54 ( 1 9 % )
Unknown
Construction
in
Caves/Agricultural
24
7
Turkey Pen Cave
Reinhard
25
4
Clydes Cavern
Hall
49
11 ( 2 2 % )
T a b l e II. - T a b u l a t i o n s o f Enterobius
vermicularis
finds b y h a b i t a t i o n a n d s u b s i s t e n c e t y p e .
As in the following w e use the prevalence o f Entero­
bius eggs in stools as an indicator o f the prevalence
o f infection, the question arises o f h o w both indices
are related. Frequently Enterobius
eggs prevalence in
stools is relatively low as c o m p a r e d with the preva­
lence o f other helminth eggs (Chieffi et al, 1974; Haswell-Elkins et al, 1987). This can b e considered a
c o n s e q u e n c e o f the peculiar behaviour o f female pinworms which release their eggs outside where they get
stuck around the anus. This also explains that the pre­
valence o f Enterobius
eggs in stool samples is g e n e ­
rally highly inferior to the rate o f infested individuals
in the s a m e population. Another characteristic o f pinworm infections is that a great amount o f the worms
are aggregated in a small fraction o f the population and
that certain households contain aggregations o f hea­
vily infected individuals (Haswell-Elkins et al, 1987;
Hugot, unpublished). This suggests that w h e n consi­
dering egg prevalence in stools w e are probably under­
estimating the prevalence o f infection, not the contrary.
Archaeological results are only as useful as dating
procedures are accurate. In the case o f the coprolite
data, dating the coprolites is b a s e d on stratigraphic
association, radiocarbon analysis, and dendrochronological dates.
Parasite, 1 9 9 9 , 6, 2 0 1 - 2 0 8
RESULTS
T
h e l o w e s t p r e v a l e n c e o f E. vermicularis
is
observed at hunter-gatherer cave sites (2 % )
and in agricultural peoples living without stone
Fig. 1. - Result o f an A N O V A p e r f o r m e d o n e g g s p r e v a l e n c e values,
transformed in arsinus ( p r e v a l e n c e
1 7 2
) in o r d e r to n o r m a l i s e residuals
(Zar, 1 9 8 4 ) . 1: c a v e d w e l l i n g h u n t e r gatherer; 2: s t o n e w a l l e d villages
agricultural; 3: s t o n e w a l l e d villages o r u n k n o w n c o n s t r u c t i o n s
in
c a v e s , agricultural.
Point de vue
203
HUGOT J.-P., REINHARD K.J.. GARDNER S.L & MORAND S
walled villages (0 % ) ; the latter sites have maize and
o t h e r d o m e s t i c a t e d c r o p s but lack villages. S t o n e
walled agricultural villages not associated with caves
have a prevalence o f 10 %. T h e highest prevalences
( 1 9 % and 22 % ) are observed a m o n g coprolites o f
agricultural p e o p l e s living in villages or constructions
in c a v e s . A N O V A (Fig. 1) r e v e a l e d a significant
influence o f habitat/subsistence types on prevalence o f
eggs (P = 0 . 0 1 4 ) . However, only egg prevalence in
cave dwelling hunter/gatherer was significantly lower
than egg prevalence in agricultural caves (Scheffe's post
hoc test, P < 0 . 0 1 4 ) .
DISCUSSION
H O S T - T R A N S F E R O R COEVOLUTIONARY PATHWAY?
P
inworms occur in most families and genera o f the
order Primates. Host specificity is extreme in the
pinworms, with each species o f nematode occur­
ring in a specific host (Hugot, Gardner & Morand,
1996). Cameron ( 1 9 2 9 ) first suggested a close corres­
pondence between phylogenetic histories of both Oxyurids and Primates: "The examination o f the fomis ... ( o f
pinworms found in Primates) ... suggests ... that the
parasite has evolved with the host. If o n e assumes the
existence o f a pre-enterobius
form in the
pre-simian
host, then the modifications o f the parasite should
a c c o m p a n y the generic difference o f the host. O n e will
expect to find forms more closely related to the human
parasite in apes, while those in old World m o n k e y s
would b e closer to E. vermicularis
than those in n e w
World m o n k e y s and the lorises but not so close as in
apes". Later, Sandosham ( 1 9 5 0 ) and Inglis ( 1 9 6 1 ) , and
finally B r o o k s & Glen ( 1 9 8 2 ) using cladistic analysis,
gave additional arguments for coevolutionary rela­
tionships a m o n g Primates and their oxyurid parasites.
Recently, b e c a u s e they share derived characters, most
m e m b e r s o f the Oxyuridae Cobbold, 1 8 6 4 , parasitic in
Primates have b e e n grouped into a n e w subfamily: the
Enterobiinae Hugot, Gardner & Morand, 1 9 9 6 . T h e
results o f a cladistic analysis o f the E n t e r o b i i n a e
(Hugot, in press) extensively supports the hypothesis
Fig. 2. - T r e e r e c o n c i l i a t i o n "parasite c l a d e s v e r s u s h o s t families". H o s t t r e e after Purvis ( 1 9 9 5 ) m o d i f i e d . Parasite t r e e after H u g o t (in p r e s s )
E T = E t h i o p i a n ; AS = Asiatic.
204
Point de vue
Parasite, 1 9 9 9 , 6, 2 0 1 - 2 0 8
H U M A N E N T E R O B I A S I S IN E V O L U T I O N
o f Cameron in its aspect o f "coevolution + c o s p e c i a tion" o r "association b y descent" as defined by B r o o k s
& McLennan ( 1 9 9 1 ) . As e x p e c t e d by Cameron ( 1 9 2 9 ) ,
the closest relative to the human parasites,
vermicularis
Enterobius
(Linneus, 1 7 5 8 ) and E. gregorii
1983, is the parasite o f the c h i m p a n z e e s : E.
pitheci
Hugot,
sugars by bacteria and protistans living in the caecum.
This is also a very efficient w a y for the packaged and
non-invasive parasite eggs to b e ingested. In humans
and other Primates, swallowing eggs implies different
mechanisms.
antbropo-
Gedoelst, 1916. T h e sister-group for these three
T H E ANAL CONNECTION
species includes the parasites o f the apes (orang-utan
Descriptions of enterobiasis as reported by Moule
and gorilla), and old World monkeys
(1911) prove that the ancient Greeks and Latins already
(baboons,
m a c a q u e s and g u e n o n s ) . A tree reconciliation «para­
had recognised human pinworms and discovered pre­
site s p e c i e s versus host species» p e r f o r m e d
gnant female nematodes crawling around the ano-
using
TREEMAP ( P a g e , 1 9 9 5 ) g a v e 6 4 % o f c o d i v e r g e n c e
genital area during the night. Nocturnal
( s u p e r i m p o s a b l e n o d e s ) b e t w e e n the trees; however,
accompanied by a strong pruritus is common in ente­
w h e n considered at the level o f "parasite clades vs.
robiasis. This explains why anal swabs remain the best
host families" the c o n g r u e n c e e x t e n d e d to 8 4 % o f
and simplest way for diagnostic. This also explains why
superimposable
pinworm eggs have such a high prevalence on chil­
n o d e s (Fig. 2 ) . T h e probability for
such a high percentage to o c c u r by chance, as revealed
egg-laying
dren's hands and fingernails (Chieffi et ai, 1974; Ryang,
by a Markovian test, is p = 0 . 0 0 1 . Thus the co-evolu­
1975). This method of transmission has also been
tionary pathway s e e m s to b e the most plausible hypo­
observed
thesis for explanation o f the origin o f human pin-
common trait for the whole order.
in other Primates and is likely to be a
worms.
Cameron ( 1 9 2 9 ) asked the question: "why and h o w
such a high specificity?" and h e speculated that "the
life history o f primate pinworms tends to m a k e them
parasites o f the individual b e c a u s e . . . their eggs d o not
tend t o b e broadcast as d o those o f other helmint h e s . . . " This c a n probably b e e x t e n d e d to the w h o l e
order Oxyurida in which Maupas & Seurat ( 1 9 1 6 ) a n d
Seurat ( 1 9 1 6 ,
1 9 2 0 ) demonstrated
that the infestive
larval stages (L3) develop within the egg, which makes
these larvae unable to actively search for a n e w host.
In addition, most o f the oxyurids parasitic in mammals
have their eggs either grouped into a p o u c h as the
parasite o f domestic rabbits (Hugot, Bain & Cassone,
1982), stuck together with an adhesive secretion o f the
female as the oxyurids o f the p o r c u p i n e s
(Hugot,
1 9 8 2 ) , or they occasionally stay e n c l o s e d inside the
female cuticle after its death (Seurat, 1916). This nondissemination o f the eggs reduces the c h a n c e s for a
n e w host to b e infected and transmission may b e
assisted by a special behaviour.
T H E AIR-BORNE
Another method
CONNECTION
of transmission
is suggested
for
human enterobiasis. When sampling house dust, fur­
niture, bed-clothes, etc., in schools, nurseries
orphanages, Enterobius
and
eggs were encountered eve­
rywhere (Nolan & Reardon, 1939; Gieryng & Pietron,
1981) and were more frequent than eggs of other para­
sites such as Trichuris,
ai,
Ascaris
and Taenia
(Chieffi et
1974; Chung, Chang & Horng, 1978; Engelbrecht
& Berendt, 1991). These authors also observed that the
larger the space for children's activity, the lower the
prevalence of eggs. This relationship between
volume, space, and abundance
air
of eggs was also
reported by Engelbrecht & Berendt (1991). In addition,
Irgashev, Babaeva & Daidaliev (1974) and Babaeva &
Saidaliev (1975) observed that: "All dust samples taken
from the bedding and flooring of houses in a hamlet
near Samarkand, Uzbek SSR, contained Enterobius
ova
and occasionally ascarid and taeniid eggs. Of the many
thousands of Enterobius
ova collected, between 6 5 . 5
and 8 5 . 5 % w e r e viable. The average number of
CAECOTROPHY
AND PINWORM
TRANSMISSION
ova/g o f dust was 7.7 to 13.1" (our emphasis). These
In the Rodentia a n d Lagomorpha, infestation is pro­
reports clearly show that Enterobius
bably facilitated b y both grooming and c a e c o t r o p h y
high prevalence in air and dust in human environments
eggs can reach a
(sensu Morot, 1882 = p s e u d o rumination sensu Taylor,
and that a great number of those floating eggs remain
1 9 4 0 ) : during intervals o f resting, the animals produce
viable or infective. This show that, in particular condi­
special droppings (the c a e c o t r o p h s , after Morot, 1882).
tions, air-borne transmission can be considered an
T h e y swallow these small faeces pellets b y arching
alternative to oral infestation for human enterobiasis
their b a c k until they are able to collect them up at the
(Smyth, 1994).
time they are discharged by the anus. This special
behaviour w a s first described from the Lagomorpha
and has b e e n later recorded in most families o f Rodent
SPECIFICITY AND MECHANISMS O F TRANSMISSION
T h e Oxyurida are unique a m o n g the parasitic forms
( K e n a g y & Hoyt, 1980). It is interpreted as a w a y for
in the Nematoda being the only group that was able
recycling cellulose after it has b e e n transformed into
to c o l o n i s e and u n d e r g o a spectacular diversification
Parasite, 1 9 9 9 , 6, 2 0 1 - 2 0 8
Point de vue
205
H U G O T J.-P., REINHARD K.J.. GARDNER S.L. & MORAND S.
in both invertebrates (cockroaches and millipedes prin­
cipally) and vertebrates. In mammals, the Oxyurida
succeeded primarily in the Primates, Rodentia, and
Lagomorpha in which every host genus (and in some
cases every host species) has its specific pinworm. The
gregarious and sedentary life history of the invertebrate
hosts of the Oxyurida explains that new hosts could
easily be infected with eggs and coprophagy is pro­
bably an important method of transmission in these
hosts. In mammals the mechanisms described above
result in a very short or almost non-existent free living
stage for the parasite. For this reason and because
interspecific interactions are rare, a close correspon­
dence between phylogenetic histories of the oxyurids
and their specific hosts can be observed. With nonsedentary hosts such as Primates, it is easy to unders­
tand that the "anal/oral connection" may be appro­
priate, and then favoured by selection since Primates
and their pinworms are living close together. Conver­
sely the "air-borne connection" appears as an ineffi­
cient method of transmission among wandering hosts,
living either on trees, or in open savannas. Thus a
question must be asked: How this.alternative to the
standard way of transmission could arise? The disco­
very of various different levels of prevalence of Enterobius eggs in human coprolites from Northern Ame­
rica allows speculation on how air-borne transmission
can influence the prevalence of enterobiasis.
VISITING "UNHEALTHY" CAVES
The earliest discovery of E. vermicularis is from Danger
Cave, Utah, deposited about 8,000 years ago and the
dates for the later sites are in the thirteenth century
AD: before Europeans invaders first arrived in Ame­
rica. These ancient dates suggest that E. vermicularis
entered the Americas with the first migrations of
humans and was not introduced later with trans­
oceanic contact. Therefore, the parasite has great anti­
quity in the New World and the variation in prevalence
of E. vermicularis through time is not a result of recent
introductions, but rather of behavioural characteristics
of indigenous peoples.
It is apparent that two aspects of human behaviour
affect the prevalence of E. vermicularis in humans,
including: subsistence type and dwelling type. These
two aspects are not independent; hunter-gathering
subsistence limits numerical group size of populations
to no more than about 50 people. Especially in arid
lands, carrying capacity prevents the development of
large numbers of hunter-gatherers. Also, because
hunter-gatherers must frequently move from one area
to another to find food, the development of perma­
nent structures among such cultures is unknown and
these factors ultimately define the nature of huntergatherer parasitism (Reinhardt, 1988). The development
206
of agriculture had significant impacts on habitation type
and numerical density of populations. A dependable,
storable food supply led to the increase of populations
such that hundreds to thousands of people lived toge­
ther. The need to store food, and need to defend
arable land, necessitated the establishment of perma­
nent villages. These aspects of agricultural life led to
an impressive change in the nature of human parasi­
tism as documented by studies of coprolites (Reinhard,
1988). In the arid west of North America, many of the
permanent villages were established in caves, often as
a defensive, measure. Each of these stone walled vil­
lages (Salmon Ruin, Kin Kletso, and Pueblo Bonito),
is a large, multi-storied complex containing between
200 and 500 rooms. They represent the largest villages
built in the Southwest before 1300 AD.
Thus, the increase in pinworm prevalence in coprolites
as compared to agricultural people and hunter gathe­
rers may be presumed to be related to numerical den­
sity of the human population, due to the increased pro­
bability of transmission of pinworms in larger
populations. However: i) the results of investigations in
Glen Canyon (Table I) suggest that pinworm prevalence
among agricultural peoples was not greater than huntergatherers, if agriculturists did not live in village or
constructions, it) there is also a remarkable increase in
pinworm positive coprolites in villages within caves.
Point i) suggests that diet alone did not affect preva­
lence. Analyses of room patterns between cave villages
and open villages suggest that the basic organisation of
open villages was the same as in caves. This means that
it is unlikely that populations of humans were larger
or more concentrated in caves. Thus, point ii) indicates
that numerical density of the population is not the only
variable that led to increased pinwonu infection. The­
refore, there must be some other factor involved.
One distinct difference between caves and open vil­
lages is the fact that air flow is limited within the
confines of a cave. This allows air-borne particles to
remain in the air column for a longer period of time
which in turn increases the probability that humans
living in the cave will encounter these particles. It has
been shown that E. vermicularis eggs are infective via
inhalation and may abound in the air environment of
humans when living in confined and sedentary habi­
tats. Therefore, the still air of caves enhances the
potential for human infection with pinworms. Thus, for
agriculturists who built their villages in caves, the
interplay of larger population combined with the
reduced air circulation in caves may explain the remar­
kable increase of E. vermicularis infection which is
reflected by greater numbers of coprolites that are posi­
tive for eggs.
In conclusion, the oral/anal mode of transmission
which results in a very short or almost non-existent free
Point de vue
Parasite, 1 9 9 9 , 6, 2 0 1 - 2 0 8
HUMAN EN FEROBIASIS IN EVOLUTION
living stage for the parasite allowed the Primates a n d
CHIEFFI P.P., MORETTI I.G., FOIZER A.CM., NAKAGAWA E. (S:
their pinworm parasites t o live an "idyllic and unin-
GOMES A.C Studies on the epidemiology of enteroparasi-
terrupted romance", p r o b a b l y from the time o f origin
toses in a closed population. II. Mechanisms of transmission. Revista da Sociedade Brasileira de Medicina Tropical,
1974, 8, 87-91.
CHUNG W.C., CHANG K.C & HORNG S.H. Epidemiology of Enterobius vermicularis infection among orphans in orphanages in Taipei City. Chinese Journal of Microbiology,
1978, 11, 30-36.
o f the hosts themselves. As the air-borne transmission
cannot reliably b e c o n s i d e r e d advantageous for transmission a m o n g wandering hosts, living either o n trees,
or in o p e n savannas, as w e r e the primate ancestors o f
humans, w e argue that this different m o d e o f transmission could b e an innovation o f the h u m a n / E n t e r o bius
pair. This different m o d e o f transfer could have
b e e n favoured during the time w h e n humans b e c a m e
m o r e sedentary, which initially associated with cave
habitats. In addition,
during h u m a n s
progressively
settled and d e v e l o p e d denser populations they also
a c q u i r e d a m o r e a n d m o r e sophisticated
language
which tended to substitute for grooming. This in turn
could result in a reduction o f b o d y contacts and a
decreasing efficiency o f the o r o / a n a l m o d e o f transmission.
However, s o m e questions remain w h i c h presently w e
are unable to response. First, did the capacity for eggs
to float in air and to remain viable and infective appear
in the h u m a n / E n t e r o b i u s pair, or, is this m e t h o d o f
transmission potentially available to other related species, but reveals to b e inefficient d u e to the different
way o f life o f the hosts? Solely experimental investigations could evidence if other Enterobius
eggs c a n b e
transmitted in air a n d if human forms resist desicca-
ENGEI.BRECHT H. & BERENDT H. Investigation of house dust for
eggs of Enterobius vermicularis. I. Methods. Angewandte
Parasitologic, 1991, 32, 15-19.
GEDOELST L. Notes sur la faune parasitaire du Congo Belge.
Revue de Zoologie Africaine, 1916, 5, 24-27.
GIERYNG R. & PIETRON W. Detection of the eggs of parasitic
nematodes in the rural environment by the method of
Kaledin and Romanienko. Wiadomosci Parazytologiczne,
1981, 27, 591-597.
HASWELL-ELKINS M.R., ELKINS D.B., MANJULA K., MICHAEL E. &
ANDERSON R.M. The distribution and abundance of Ente-
robius vermicularis in a South Indian fishing community.
Parasitology, 1987, 95, 339-354.
J.P. Sur le genre Wellcomia (Oxyuridae, Nematoda),
parasite de Rongeurs archaïques. Bulletin du Muséum
National d'Histoire Naturelle, Paris, 1982, 4, 25-48.
HUGOT
Enterobius gregorii (Oxyuridae, Nematoda), un
nouveau parasite humain (Note préliminaire). Annales
de Parasitologic Humaine et Comparée, 1983, 58, 403404.
HUGOT J.P.
tion better. As the parasites o f man are considered to
HUGOT J.P. Primates and their pinworm parasites: the
b e t w o different species (Hugot, 1 9 8 3 ) , another interesting question w o u l d b e to determine if any special
Cameron hypothesis revisited Systematic Biology, 1999, 48,
(in press).
adaptation for air-borne transmission d e v e l o p e d either
HUGOT J.P., BAIN O. & CASSONE J. Insémination traumatique
in Enterobius
vermicularis
or E.
gregorii.
et tube de ponte chez l'oxyure parasite du lapin domestique. Comptes-rendus de l'Académie des Sciences, Paris,
1982, 294, 707-710.
REFERENCES
HUGOT J.P., GARDNER S.L. & MORAND S. The Enterobiinae fam.
ASHFORD R.W. The human parasite fauna: towards an ana-
nov. (Nematoda, Oxyurida), parasites of Primates and
Rodents. International Journal for Parasitology, 1996, 26,
147-159.
lysis and interpretation. Annals of Tropical Medicine and
Parasitology, 1991, 85, 189-198.
ASHFORD R.W. & CREW W. The parasites of Homo sapiens.- an
annotated checklist of the protozoa, helminths and arthropods for which we are home. Liverpool: Liverpool School
of Tropical Medicine, 1998, 128 p.
BABAEVA R.I. & SAIDALIEV T. Survival times of Enterobius ova
on household items. Aktual'nye Problemy Meditsinskoi
Parazitologii, 1975, 2, 82-84.
IRGASHEV I.K.H., BABAEVA R.I. & DAIDALIEV T. The survival of
BROOKS D.R. & GLEN D.R. Pinworms and primates: a case
MAUPAS E. & SEURAT L.G. Sur les mécanismes de l'accouple-
study in coevolution. Proceedings of the Helminthological
Society of Washington, 1982, 49, 76-85.
ment chez les Nematodes. Comptes-rendus des Séances de
la Société de Biologie, Paris, 1916, 79, 607-611.
Phytogeny, ecology and behaviour. Chicago Univ. Press, Chicago, 1991, 434 p.
CAMERON T.W. The species of Enterobius Leach, in Primates.
Journal of Helminthology, 1929, 7, 161-182.
COMBES C. Where do human parasites come from? Annales
de Parasitologic Humaine et Comparée, 1990, 65, 59-64.
BROOKS D.R. & MCLENNAN D A .
Parasite, 1 9 9 9 , 6, 2 0 1 - 2 0 8
INGLIS W.G. The oxyurids parasites (Nematoda) of Primates.
Proceedings of the Zoological Society, London, 196l, 136,
103-122.
Enterobius ova in dust. Trudy Uzbekskogo Nauchno Issledovatel'skogo Veterinamogo, 1974, 22, 38-40.
KENAGY G.J. & HOYT D.F. Reingestion of feces in rodents and
its daily rhythmicity. Oecologia, 1980, 44, 403-409.
C. Des pelotes stomacales des Léporidés. Mémoires
de la Société centrale de Médecine vétérinaire, 12, sér. 1,
Paris, 1882.
MOROT
MOULÉ L. La Parasitologic dans la littérature antique. II. Les
parasites du tube digestif. Archives de Parasitologie, 1911,
15, 353-383.
Point de vue
207
HUGOT J.-P.. REINHARD K.J., GARDNER S.L. & MORAND S.
M. & R E A R D O N L. Distribution of the ova of Enterobius vermicularis in household dust. Journal of Parasitology, 1 9 3 9 , 25, 1 7 3 - 1 7 7 .
NOLAN
R.D. Parallel phylogenies: reconstructing the history of
host-parasite assemblages. Cladistics, 1 9 9 5 , 10, 1 5 5 - 1 7 3 .
PAGE
A. A composite estimate of primate phylogeny. Philosophical Transactions of the Royal Society, London, B ,
PURVIS
1 9 9 5 , 348,
405-421.
Cultural ecology of prehistoric parasitism on
the Colorado Plateau as evidenced by coprology. American Journal of Physical Anthropology, 1 9 8 8 , 7 7 , 3 5 5 - 3 6 6 .
REINHARD
K.J.
REINHARD
K.J.
rican Journal
Archaeoparasitology in North America. Ameof Physical Anthropology, 1 9 9 0 , 82, 1 4 5 - 1 6 2 .
Y.S. Enterobius vermicularis infection in school children and environmental contamination with Enterobius
eggs. Korean Journal of Veterinary Public Health, 1 9 7 5 , 12,
RYANG
108-114.
A.A. On Enterobius vermicularis (Linnaeus, 1 7 5 8 )
and some related species from Primates and Rodents.
Journal of Helminthology, 1 9 5 0 , 24, 1 7 1 - 2 0 4 .
SANDOSHAM
SAMUELS
R.
Parasitological study of long dried fecal samples.
American.
Antiquity,
1965,
31,
175-179.
L.G. Sur les Oxyures de Mammifères. Comptes-rendus
des Séances de la Société Biologique, Paris, 1 9 1 6 , 7 9 , 6 4 -
SEURAT
68.
L.G. Histoire naturelle des Nematodes de la Berbérie.
1. Morphologie, développement et affinités des Nematodes.
Imp. S. Stamel, Alger, 1 9 2 0 , 2 2 1 p.
SEURAT
J.D. Introduction
to Animal Parasitology,
Cambridge University Press, 1 9 9 4 , 5 4 9 p.
SMYTH
3d edn.
ZAR J . H . Biostatistical Analysis, 2nd edn. Prentice-Hall, Inc.,
New Jersey, 1 9 8 4 , 7 1 8 p.
Reçu le 1 6 septembre 1 9 9 8
Accepté le 2 6 avril 1 9 9 9
208
Point de vue
Parasite, 1 9 9 9 , 6, 2 0 1 - 2 0 8