POSSIBLE EXTRAHUMAN RESERVOIRS OF THE …phthiraptera.info/Publications/41600.pdf · taxonomic entity, Borrelia recurrentis (Le- ... including ornitho- dorid ticks ... guide to the

SECTION C � ECOLOGY OF LOUSE-BORNE INFECTIONS � WALTON 117

Un nouveau reservoir de virus

pour Rickettsia prowazeki: les animaux domestiques et leurs tiques. Doctoral thesis, University de Paris. 1957.

26. ��. Nouveaux isolements de R. prowazeki a partir d’animaux domestiques et de tiques. Bull Sac Pathol Exot 54:284-97, 1961.

27. ��. The isolation of Rickeilsia prowazeki and mooseri from unusual sources. Am } Trop Med Hyg 15:943-49, 1966.

_

28. ��andF>CROCE. The susceptibility of lambs for the experimental infection with Rick-

013e<5(- Gerald A. Walton,1 Possible extrahuman

reservoirs of the relapsing fever spirochete Borrelia recurrentis.

Introduction

The magnitude of exploring possible extrahuman reservoirs of epidemic and endemic relapsing fever Borrelia on a world scale borders on the impossible. When I was preparing this contribution I was unaware of the recent review published by Dr. Oscar Felsen- feld which contains 750 references (28). That list of references omits many contained in the references that appear at the end of this paper, a list that must of necessity be restricted. Consequently, a fully comprehen- sive review would entail the inclusion of at least 1,000 references. Under the circum- stances I have taken the liberty of extracting a small number of references from Dr. Felsenfed’s study because we both, inde-

pendently, reach the same conclusion, which is backed by the opinions of a number of eminent authorities (33, 37, 54. 80). It would seem, from this weight of opinion, that despite all the work done on some 30 "species" of Borrelia implicated in relapsing fevers, these are but strains of a single taxonomic entity, Borrelia recurrentis (Le- bert 1874), which has an exceedingly wide range of animal hosts and a bewildering variety of antigenic properties (27, 28, 31, 52. 55).

] Department of Zoology, University College, Cork, Ireland.

etisia prowazeki. G. Batteriol Virol linmunol 64:144-54, 1971.

29. VARELA, G., and R. VELASCO. Nuevos aspectos de la epidemiologia del tifo: exploraci6n serologica de animales domesticos. Rev Inst Salubr Enferm Trop 25:171-75, 1965. r

30. WALTON, K. W., and P. J. SCOTT. Estima-

tion of the low density (beta) lipoprotein of serum in health and disease using large molecular weight dextran sulfate. / Clin Pathol 17:627-43, 1964.

To emphasize this concept I quote Zuck- erman (83), who refers to the classical isolation of a Borrelia from a wild Pana- manian monkey (14) and its passage to

mice, rats, guinea pigs, other monkeys, and man: "Here then is a disease without very definite boundaries in the mammalian world," No species name was ever given to the Borrelia involved. A more recent reference to the possible evolution of the epidemic louse-borne form of Borrelia (34) ("The parasite presumably changes its antigenic composition during this hypothetical evolution: its name changes from B. crocidurae to B. duttoni and finally to B. recurrentis in the louse-borne form") is a gentler way of putting the point. The real question posed by the title of

this contribution is: Can any of the borreliae found in wild hosts and vectors con- vert to the devastating form transmitted by human lice? Conversely, could that epidemic form return "underground" to the wild reservoirs? The answer is difficult since much funda-

mental work was carried out before this century or in its early days and involves translation. Thus, the reader who takes this thesis seriously should read it in conjunc- tion with that of Pelsenfeld (27) and his contribution to this Symposium (28).

Progress in achieving an understanding of the probable dynamic nature of the problem stems from _^he elusive characteristics of the strains of borreliae causing endemic relapsing fever both in man and in their vectors. This spirochete can lurk undetected

118 SESSION I � CURRENT STATUS: PROBLEMS AND CONTROL MEASURES

in man on a vast scale. For example, 25,000 dwellings of Africans were infested by Ornithodoros porcinus domesticus (Wal- ton 1962) in the Tanzanian Usambara mountain range when only three human cases of relapsing fever were reported in

1952. The ticks were shown to be infected, although the borreHae could be detected in them only after the fourth brain passage in rats inoculated with the emulsified ticks (76, 79). This is, in all probability, due to high levels of immunity in the human population, a feature apparently present also in Central and South America (summary item 12 in 16). The complexity of the kind of manipu- lations needed to recover borreliae of tick vectors is emphasized (.20). Another factor obstructing progress is the limited range of animals usually available in most labora- tories for transmission studies or the failure to appreciate the efficacy of newborn or infant media (9, 20). The global range of relapsing fever borreliae is indicated by Tarizzo (72) and a map is available (.1).

Complexity o( Borrelia ecosystems

Borreliae have been isolated from wild

monkeys and an ape in West Africa {14, 39), and from monkeys in East Africa (33) and the neotropics (14). Fiennes (29) states that "many simian species have been found infected in the wild with spirochaetes or relapsing fever," but of note was the

finding of both Ornithodoros talage and

A rgas refiexus on a single monkey (71). The West African B. pithed (Theroux & De- fougere 1919) was assumed to have been transmitted by argasid ticks (39). The presence of the louse Pediculus on gorillas and chimpanzees may need confirmation, but the origin of the human louse (Pediculus hu- manus on the thousands of neotropical ceboid monkeys in the vast tracts of South American forests is open to conjecture (63). Old World monkeys are infested by the

louse Pedicinus (44) and the louse-borne

epidemic "recurrently’ form of Borrelia can be adapted to it (33).

Since the dog tick Rhipicephalus sangu- ineus is capable of retaining borreliae for as long as three months (27, 69), other ixodid ticks should be suspect vectors; quite bizarre cycles of transmission, presently unsus-

pected, may be in operation. Specialized ixodid ticks infest the nostrils of man in

chimpanzee forests (78) and creep’into-and attach to the human anus (A. J. Haddow, personal communication). A single tree may harbor an incredible

variety of possible hosts and vectors. Those mentioned by Hoogstraal (41), and others inhabiting a Dalbergia tree at Lahore, India (42), included Argas abdussalami, white

vultures, parakeets, mynahs, pigeons, doves, crows, Sfurnus vulgaris (the cosmopolitan starling), and a squirrel. Had the tree been subjected to an exhaustive examination,

many other hosts and vectors might have been added to the list, including ornithodorid ticks, cimicid bugs, reptiles, and

arboreal rodents, as well as bats and monkeys.

Carnivores (dogs, jackals, and foxes) were infested in Asia (32, 68, 69), and the Chiroptera are included (46, 61). The first Borrelia to be isolated from a wild host came from an insectivore Croddura (48).

Hedgehogs (Er’maceus) are also incrim- inated (27), as were marsupials (Didel- phus, the opossum) (14), together with

armadillos among the edentates. Borreliae were also isolated from calves and a horse

in Panama (14). Seals (Pinnepedia) have echidnothiriid sucking lice (44, 60) and come on land near penguins infested by 0. capensis (56, 57). Since epidemics among sea birds are known in southern oceans (17) to involve infections by borreliae, it is quite possible, however remote it may seem, to envisage reservoirs in Antarctica, Borreliae

may be preserved alive for years at �76°C (27, 81). Consequently, while it is con-

jectural, the possible presence of reservoirs


of borreliae in the brains of mammoths and other animals preserved in the permafrost should not be unduly rejected. Bovine borreliae (B. theileri) are transmitted by ixodid ticks (Boophilus microplus, B. decolomtus, B. annulatus, and Rhipicephalus everts!) in Africa, the U.S.S.R., and Australia (2, 3, 6, 65). Although we are here concerned with ecology, it should be mentioned that transovarial transmission of borreliae is involved.

There is a severe lack of information about the involvement of 16 entire groups of arboreal animals ranging from flying squirrels, tree shrews, civits, kinkajou, and tree hyrax to scaly anteaters, two-toed anteaters, sloths, dormice, tree mice, and rats. The study of night rests by Lumsden (57) used by monkeys may be mentioned here. Nineteen bat species are listed as hosts of 0. batuensis in Malaysia (4). Caves have been fairly well surveyed, but cliffs, mines, and monuments have been neglected. There are specialized rats (Graphiurus) in South Africa with flattened skulls and elastic ribs as adaptations to rock crevice habitats (.11). Since rodents, and especially rats and mice are of major importance as reservoir hosts of endemic borreliae, references to lists of

species are mentioned here (7, 11, 25). They suggest that wild rodent reservoirs may be almost universal. The least known area must be that containing arboreal animals linking reservoirs of borreliae in the forest canopies with those in the epigeum.

Independent summations of the relation- ship between small animals (especially rodents) and the Ornithodoros ticks associated with them were made in 1968 and 1969 (6, 35, 50). This concentrated effort at a

similar moment may represent a conceptual turning point in this extremely complex issue. Additional detail may be gleaned from other references cited (,3, 70). The whole of America, Africa, Southern Europe, and Asia is involved in this small mammal sub- reservoir. Once east of Wallace’s line, however, there seem to be very few examples of

these small mammal-argasid tick microreser- voirs and there is no record of relapsing fever in New Zealand (L. J. Dumbleton, personal communication). In fact, foci of endemic relapsing fever are rare east of 100° longi- tude (25). No borreliae appear to have been recorded from Madagascan mammals, and argasid ticks on lemurs are unrecorded (G. Uilenberg, personal communication), which suggests that the adaptation of borreliae to simians is a recent event in geologic terms.

The unique niche of argasid ticks

Microreservoir niches are filled by many species of Ornithodoros. Not only do they live for many years (31, 77) and withstand prolonged starvation, but they also conserve borreliae over long periods (20). Frequency of taking blood meals and avidity for a wide range of preferred hosts assures borreliae of a homeostatic parasite habitant and transfer to new hosts. Resistance to adverse climate is high, e.g., 0. capensis at �35°C about the Aral Sea (46), 0. foleyi within the Saharan 30°C isotherm (40). Moreover, transmission of borreliae is aided by transstadial and transovarial transmission (10).

It has been customary to name borreliae as "species" as and when each new tick/host association has been found. These "species" names are avoided in this communication as far as possible because their use is not only taxonomically unsound (52), but is also confusing and contrary to the opinion of

many leading authorities. I would like to regard them all as strains of a single symbi- ont (21).

Over 30 species of Argas have been de- scribed. They are primarily parasites of

birds and transmit avian borreliae (62) which show "banding," a character noted in borreliae of simians (14, 33). Knowledge of the role of these ticks is limited and their study is at the exploratory stage. Mammals


are bitten, however, in the absence of normal hosts.

Transmission

The role of Omithodoros ticks and small rodents as reservoirs of endemic borreliae has been stressed. Numerous strains are

produced in the ticks (35), whereas no such antigenic instability appears to be produced in lice. It is extremely difficult to sort out strains of borreliae when the antigenic properties vary with each relapse (27, 28, 31, 36, 66, 79) in infected hosts, and there is little to be gained from the literature as a guide to the antigenic fate of different relapse strains when they cycle in the tissues of different species of Ornilhodoros or in different sexes and stages of their life cycles. Certainly quite remarkable differences have been found in the transmissibility of some so-called "species" (10, 18, 19, 75).

Strains of the human louse-borne epidemic borreliae have been transmitted to squirrels, rats, mice, infant rabbits, monkeys, and apes (27). It is clear that infant animals are susceptible (9, 81), and further work is needed in which argasid ticks are fed on these hosts. Other vectors should be tested and different routes of infection investigated using repeat passage methods (27).

While it is a fact that louse-borne borreliae infect man through skin abrasions and mucus membranes, this route seems to have been strangely neglected during investigations of the endemic borreliae. The red and brown layers of accumulated

blood and bodies of engorged ticks, bedbugs, and lice, thumb-squashed against the wall near beds in East African huts, as I witnessed during the 1950’s, highlighted the elective route of the spirochete through abrasions and mucus membranes of man. Legge (49) provides a classical reference to infection in man resulting from mere contami- nation with squirrel blood. Figure 1 shows a Kikuyu girl who was eating lice in the

now nonexistent Nyeri focus of endemic relapsing fever in Kenya. Figure 2 shows a blood-spattered cook preparing a South American monkey for a stew. The ease with which transmission could occur during the rough-and-tumble of animals during play, fighting for mates, mating, preening, grooming, and desperate escapes from predators is emphasized.

Investigation is needed into the effects on borreliae of cannibalism and predation among the argasid ticks themselves (59). Cannibalism is recorded of 0. tholowni, I. verrucosus, 0. capensis, and 0. coniceps (30), and in ticks of the subgenus Ornitho- doros (76). Startlingly, one small 0. coniceps was observed to consume a larger Argas persicus (itself capable of harboring Borrelia for 40 days) and, by transovarial

ECOLOGY OP LOUSE-BORNE INFECTIONS � WALTON 121

Figure 2. Cook preparin9 South American in key for

transmission, to conserve Borrelia for 25 to 30 years (58), reducing it to an empty skin during a single night. Not only does this raise the question of

the fate of avian borreliae in such transmissions, as, in any case, there is a need for reinvestigation into their mode of transfer (5), but also it suggests innumerable new transmissive pathways for study in the future. There is also a suggestion that borreliae introduced into tick hemocoeles di-

rectly, when one tick feeds on another, may result in higher levels of infectivity (76), Indeed, Wagner-Jevseenko (,35) records transfer of borreliae from male to. female "0. moubata" during spermatophore transfer. Human seminal fluid and menstrual fluid may contain Borrelia (27) and con-

genital infection in man is known (.34). Skrynnik (46) is said to have infected a guinea pig by feeding it infected 0. lahoren- sis, which is a natural nonvector incapable of transmitting by bite.

The virulence of Borrelia strains is en- hanced by passage from host to host but the

number of passages varies in mice from five (22) to 10 (33), but naturally virulent strains occur which have been known to kill mice on day 3 or 4 following infection (62). The bedbug Cimex, and presumably a

wide range of the Cimicidae, which frequently share microhabitats with argasids, is capable of retaining Borrelia for at least a month without altering the antigenic state (81). Monkeys were infected with blood from crushed Cimex (24, 74). Thus, the bedbug could assume vector importance on its resurgence during malaria eradication programs (64).

Study of simple mechanical transfer of borreliae on the mouthparts of bloodsucking arthropods (e.g., Tabanus, Chrysops, Glos- sina, fleas) disturbed during meals and when biting another host, or when these, or even the scavenging ectoparasites containing fresh blood, are crushed on abrasions, has not received the attention it might deserve.

Opinions differ about the ability of mites to transmit borreliae. Unidentified mites from infected pygmy gerbils (Dipodillus) and Dermanyssus mites (36, 82) were nega- tive but the rat mite Liponyssus remained infective for 12 days (27).

Despite all that has been said, there appears to be no evidence in support of conversion of any endemic borreliae to the louse-borne epidemic "recurrentis" form. If such a conversion is possible, then the most probable place to suspect would be the

arboreal cycles in the most ancient forest canopies, the evergreen forest of Africa, which are one of the world’s most stable features (53). In it, and around its fringes, man would have evolved. Simian borreliae are present and so are squirrels, small rodents, monkeys, and apes, all susceptible to the borreliae of epidemic human louse- borne relapsing fever. In the next section a series of events in the possible evolution of the "recurrentis" type of Borrelia will be traced in an attempt to expand on and bridge over the five stages proposed by Nicolle and


Anderson in 1927 which seem strangely prophetic today. I read the original in 1947, but here quote from Moursund (55):

1. An infection of small mammals transmitted by ectoparasites which are pos- sibly, though not necessarily, species of Ornilhodoros.

2. The intervention of ticks of the genus Omithodoros which obtain the germ and conserve it and which require large mammals for the maintenance of their adult stages ["may require" would have been more appropriate. G.A.W.].

3. The intervention of human beings infected by the ticks, more as an occasional accident than as a necessity.

4. The intervention of the louse by the adaptation to it of the spirochete which is nevertheless still transmissible by the tick.

5. The complete adaptation of the louse and the consequent spread from Africa throughout the Old World [italics added. G.A.W.].

Symbiotic echelons

Since the reader will have by now appre- ciated how all possible vector-host, vector- vector, and host-host associations concerned with transmissions of borreliae are almost too intricate to envisage, the idea of time- successive evolutions of host-vector-Bor- relia ecologic communities is introduced as a conceptual framework for future reference. As each association arises in time, it con-

tinues in a modified form to the present and beyond; each stage successively overlaps the next. Seven of these episodes, or "echelons," are postulated in an attempt to put

’ the problem of evolution into perspective. A diagram of projected flow of borreliae through these echelons is provided (Figure 3).

Echelon 1

Vmto-Borrelia are transmitted by evolving argasid ticks (the potential ornithodorid lines, both of which may have the same chromosome number (2n = 26); larvae of some species of both genera are indistin-

guishable (15, 43) to terrestrial amphibians, reptiles, mammal-like reptiles, pterodactyls, and birds. Over 14 species of Omithodoros now infest toads and reptiles. Pmto-Argas and borreliae adapt to homeothermic birds during the Eocene and, towards the Oligo- cene, borreliae adapt via the evolving Omi- thodoros to homeothermic mammals,

Echelon 2

Dnring the Oligocene, louse-infested simians evolve in extensive forest canopies accompanied by Argas ticks of, and borreliae of birds, removed from epigean borreliae of mammals in burrows, cliffs, and caves. Bats evolve, forming a potential interconnecting link. Lemuroids groom with specifically evolved and modified lower incisor teeth. Madagascar is of interest since borreliae appear to be absent from the indigenous animals, although sucking lice are numerous. Argasid ticks are absent from lemurs but are present on reptiles, insectivores, tenrecids, and, of course, on birds and bats (G. Uilen- berg, personal communication).

Echelon 3

There were two significant episodes. In the first, "baboons" descended, about 10 million years ago, from forest canopies to contact epigean reservoirs of borreliae. Their grooming is highly effective (38). Apes evolve and proliferate, accompanied by their lice. Australopithicines and hominines (47) (Figure 4) came into contact with epigean reservoirs of borreliae, perhaps in caves

(53). It has been suggested that these

large, clumsy, and hairy primates were "no less adept than hairless men in removing ectoparasites" (23), but I would prefer to disagree and suggest that they had great difficulty in effectively grooming. Infesta- tions of lice could have been severe, and resulted in epidemics caused by borreliae adapted to these hominid lice over a period of more than 2 million years (47). These vital reservoir hosts became drastically re-

duced, along with the apes, and widely scat- tered consequent to predation by evolving man, who ate raw brains of "lesser" primates and thus may have been immunized to these neurotrophic borreliae; by changing climatic conditions resulting from prolonged arid periods during the interglacials; and by possible epidemics of louse-borne relapsing fever. Apes survive in isolated forest "islands" and the borreliae survive, in modified form, in the cercopithicine monkeys of the forests, having reached them from the moninids during this echelon.

Echelon 4

Stone Age to neolithic man (/6) forms settlements (12 adults, 18 children) (12, 73) and domesticated animals. Argasid ticks invade man’s dwelling ipsefacts (5), and lice increase as man replaces body hair by

clothing ipsefacts (5). Grooming becomes increasingly complex. Many commensal animals accompany man from the cave to his new ipsefacts (13). This echelon was ex- tensively investigated in Africa (79); endemic relapsing fever became virtually extinct in Kenya and Uganda as a result of the introduction of improved living conditions which eliminated ticks of the "0. moubata" group and severed the link with the wild reservoirs of borreliae. Now, in Tan- zania, the process continues; "in several

places in Tanzania this disease has prac- tically disappeared, in others it is more and more fading" (R. Geigy, personal communication).

Echelon 5

Urbanized man enters the technosphere accompanied by his lice, but is once more

124 CURRENT STATUS: PROBLEMS AND CONTROL MEASURES

F;9ure 4. Australopithicine.

removed from reservoirs of borreliae. 0. kellyi invades man’s dwellings in New York City (.20) and 0. concanensis invades

dwellings in Kansas (45), however. Al- though a point of controversy, Pediculus is introduced to neotropical arboreal ceboid conquistadors (63), thereby creating a vast reservoir of borreliae. The reader is referred to the opening remark in this section and is asked to conjecture a microhabitat of small rodents, ticks, and bedbugs in a dwelling or monument in delapidation or, to a tree-hole in a forest. There is an interesting epide- miologic model based on a study of Cimex distribution in English towns. While unexpected, the study indicated there was a tenfold "increase" in Cimex infestation in the larger towns compared with the smaller. This is interpreted by the mathematical law of collisions. When the number of events is increased by a given factor, e.g., the num-

ber of vectors or hosts increases, the contacts (blood meals or transmissions of borreliae) increase by the square of the number of vectors or hosts. Thus, in a given condition favorable to vectors or hosts, which results in multiplication, Borrelia transmission and antigenic change can, theoretically, take place with unexpected suddenness.

Echelon 6

Man adopts a wide variety of commensal animals, frequently of exotic origin, as his "pets" (S) and once more forms a link with reservoirs of borreliae within his dwelling and zoological garden ipsefacts. The epitomy was "Africa, U.S.A.," a zoo at

Boca Raton, Florida, where 350 African animals roamed 480 hectares infected by the Borrelia vector tick R. evertsi (67).

Echelon 7

Towards A.D. 2000, "doomsday" world overcrowding (12) forces man against re- maining reservoirs of borreliae in the "World Natural Parks" and "monuments." Orni- thodoros ticks remain in these retreats and Pediculus survives on the outcasts, a with- drawn class of the lower-ranking hierarchies �an extension of the heavily tick-infested "loner" baboons observed in the Sudan (38).

Epilogue

The existence of extensive Borrelia reservoirs on a worldwide scale is supported by massive evidence, but whether all the strains could alter to infect man, especially as

epidemic relapsing fever, is not always known. For example, infection is rare in Australia and South Africa, where arboreal cycles are rare and associated wild primates few or absent. The great 1921 louse-borne epidemic of relapsing fever started in Upper Guinea (37). Who, one might ask, was in those great lowland evergreen forests (53) to witness a possible prodromal epidemic of wild anthropoids? Fiennes (29) wrote:

SECTION C � BCOLOGY OF LOUSE-BORNE INFECTIONS � WALTON 125

"The natural vector, a tick which as its name implies, is primarily a bird parasite, suggests the possibility that this disease may be derived from an arboreal cycle in which birds and simian primates are involved." I quote from Eiton (26) a stanza from Adam Mickiewicz’s Pan Tadeusz:

The hunter can but skirt our forest bed and he

Beholds its outward form and features, these alone;

To him its inner heart and secret are unknown.

Further attention might be given to the study of B. harveyi (33), which was said to show "avian" characteristics. Communi- cation of ideas being urgent, there is regret at the printing of only 2,200 copies of

Balashov’s Soviet monograph on bloodsucking ticks, while Hopkins’ work on hosts of lice (44) is amost unobtainable (Teresa Clay, personal communication). A direc- tive suggesting the printing of 5,000 copies of such monographs would seem appropriate.

ACKNOWLEDGEMENT

Help given during synthesis of the massed data used in this contribution is acknowl- edged. Thanks are extended to Prof. D. S. Bertram; John Breen, B.Sc.; W. Burgdorfer; L. J. Dumbleton; Prof. P. C. C. Gamham; J. H. S- Gear; Prof. R. Geigy; Dr. N. Filip- pova; Dr. H. Hoogstraal; Tom Kelly, B.Sc.; Prof. J. F. O’Rourke and the President of University College, Cork, for permission to

attend the Symposium; Mr. Rawley for preparing illustrations; and G. Uilenberg and M. G. R. Varma for suggestions. Special thanks are extended to Prof. J. R. Busvine for his exceptional kindness and help with some very difficult references, and Mrs. Lydia S. Lisann for the same reasons. Data requested from other authorities had not come to hand at the time of compilation.

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