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Annu. Rev. Entomol. 1977.22:23-32. Downloaded from www.annualreviews.org Access provided by Technische Universiteit Eindhoven on 01/26/15. For personal use only.

Ann. Rev. Entomol. 1977. 22:23-32 Copyright © 1977 by Annual Reviews Inc. All rights reserved

CONTEMPORARY VIEWS ON

.6118

THE INTERRELATIONSHIPS BETWEEN FLEAS AND THE PATHOGENS OF HUMAN AND ANIMAL DISEASES

V. A. Bibikova Martsinovsky Institute of Medical Parasitology and Tropical Medicine, Ministry of Public Health, Moscow, USSR 119830

The fleas, like any other group of parasitic, bloodsucking arthropods, have been exposed to contact with various pathogenic agents throughout the protracted period of their existence. As a result of this association, the present interrelationships between the fleas and the pathogens of zoonoses and anthroponoses have evolved. Various indices are used to appraise the relationship between a vector and a causative agent (pathogen): the capacity of the causative agent to reproduce in the vector, the duration of their joint sojourn, the pathogenic effect, etc. However, these relationships most vividly manifest themselves in the mechanism of transmission that has evolved historically for the given disease. It is in the formation and realization of the mechanism of transmission that the maximal available adaptive possibilities between the pathogen and the vector are most vividly expressed, since the parasitic nature of the pathogen presupposes, as a condition of the existence of the species, the obligatory and multiple transmission from one host to another. Such a methodological approach to the assessment of the relationships between the vector and the causative agent of the transmissive disease stems from the recognition of the ecological principle of existence of natural foci (40) and the theory of the mechanism of transmission (28). For the time being the extent of our knowl­ edge of the peculiarities of transmission permits us to consider relationships of only six species of pathogens with the order Siphonaptera (Table I). 23

24

BIBIKOVA

Table 1 Peculiarities of transmission of certain pathogens by fleas Localization of pathogen in Disease and pathogen Myxomatosis, Fibroma·

the flea

Duration of existance

Main method of

effect on

pathogen

in vector

transmission

the flea

digestive tract

in flea

up to 100

virus myxomatosis Tularemia, Francisella

days digestive tract

several days

tularensis Murine typhus, Ricket·

Annu. Rev. Entomol. 1977.22:23-32. Downloaded from www.annualreviews.org Access provided by Technische Universiteit Eindhoven on 01/26/15. For personal use only.

mechanical

+

inoculation

c

me hanical inoculation

digestive tract

.+

tsia moosen

throughout lifetime

Murine trypanosomiasis,

digestive tract

+

throughout

digestive tract

+

up to 40

Trypanosoma lewin Salmonellosis,

lifetime

Salmonellll enteritidis Plague, Yersinia (Pasteurellll)

Pathogenic

Reproduction of

pestis

days digestive tract

+

from several months to

specific contamination specific contamination specific

+

inoculation specific

+

inoculation

more than a year

MYXOMATOSIS The Fibromavirus myxomatosis virus affects hares and rabbits in Australia, Europe, and South America and is transmitted by the fieas of these animals, Spi/opsyl/us cuniculi, or mosquitoes. The virus does not reproduce in fleas and is gradually excreted from the organisms. The long survival,up to 100 days,of the pathogen in the intestine and the mouth organs of the flea is noted only in cold temperatures (4, 22, 43). The virus is passed on through the contaminated mouth organs of the flea. Rather interesting conclusions about the reasons for inactive transmission of myxomatosis virus by the flea are given in the above-cited investigations. A remark­ able peculiarity of the rabbit flea is its almost immobile position on the ears of the rabbit,where,because of peculiarity of the blood circulation,they can rarely acquire the pathogen. When infected fleas have a blood meal on the ears of rabbits, the incubation period of the disease lasts 20 days instead of 2-3 days. Moreover, the ovaries of the fleas that had a blood meal from the sick rabbits develop abnormally. The evolution of the rabbit flea,according to Rothschild & Ford (43), was along the line of strictly local parasitizing and the reduction of contacts with the virus, since the mass destruction of the hosts is not favorable to the parasite. TULA REMIA

This disease is widespread in the Old and New Worlds. Fleas are capable of ingesting a large quantity of Francisella tularensis microbes (up to 100, 000); however,these do not reproduce and soon perish because they do not leave the digestive tract. There are no microbes in infected fleas after 2 months at a temperature of 4-7°C,and at IS-25°C they cannot be detected after 20 days (23). Although other investigators note longer periods of time (25, 45-47), they all agree about the absense of the reproduction of these microbes in the flea; thus the transmission of the tularemia microbe is purely mechanical. The efficiency of the transmission of tularemia by fleas is very low. For instance, out of 116 experiments (23), only six were positive.

FLEAS AND DISEASES

25

According to some authors (23, 39) transmission is obtained in the first 5 days. Mechanical contamination through the excrement of the infected fleas is of some importance. The significance of fleas in the epizootiology and epidemiology of tularemia is limited; the role of the main vector of tularemia belongs to other groups of Arthropoda.

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ENDEMIC OR MURINE EXANTHEMATOUS TYPHUS This disease is spread throughout the Old and New Worlds, especially in port cities in the subtropical and tropical zones. The causative agent of the disease is Rickettsia mooseri. Rats and mice contract the disease; sometimes humans do also. The fleas of rats, mice, and human dwellings are easily infected with rickettsiae, but the persistence of the causative agent in the flea is limited to the intestinal tract only. The flea is infected for life, and the pathogen does not harm the flea. The rickettsiae reproducing in the body of the flea, especially if it feeds regularly, are excreted with the feces over a long period of time (15, 16, 21, 37). Investigators note the high concentration and pathogenicity of rickettsiae in the feces of the vector. The effi­ ciency of infection of the warm-blooded host is the highest when the rickettsiae are implanted on the mucous membranes. In murine typhus there is no active mechanism of transmission of the pathogen directly to the blood of the animal, but this is compensated for by the stability of the rickettsiae despite unfavorable effects of the environment and their very high virulence. The infectious dose for a man is one fifth of a single excrement of the flea. The method of transmission of the pathogen is the specific contamination, deprived of deep mutual adaptation of the pathogen and the vector. MURINE TRYPANOSOMIASIS Trypanosoma lewisi is the causative agent of trypanosomiasis, which occurs in rats in almost all the comers of the world. The vectors of this disease are the fleas of rats, as well as fleas of human dwellings and of cats, dogs, and mice. The circulation of the causative agent is only within the intestine of the flea. The most detailed study of the life cycle of trypanosomes in fleas was made by Minchin & Thompson (36). Within the first 6 hr after entering the stomach of the flea with the blood, trypano­ somes apparently undergo some sort of physiological change. The confirmation of this is that, if the trypanosomes are administered to the rats during this period, they cannot induce the disease. After 6 hr they enter the epithelial cells of the stomach; each trypanosome acquires a pearlike form in the cell vacuole and reproduces through repeated divisions. The epithelial cells in which the trypanosomes accumu­ late finally break, making it possible for the parasites to get into the intestinal lumen. The intracellular phase lasts from 18 hr to 5 days and can be in any part of the stomach epithelium. The trypanosomes that emerge from the epithelial cells can again penetrate them, repeating the described process of reproduction. After this, they move to the posterior sections of the intestinal tract (into the anal and rectal intestine), where they change their structure and take on a crithidial form. The

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BIBIKOVA

investigators call this the rectal phase; it is characterized by polymorphicity-the formation of herpetomonad, crithidial, and trypanosome forms. Finally all these forms are excreted from the intestine to the environment. The majority of investiga­ tors consider that only small trypanosome forms can infect animals. Unlike the pathogens discussed before, trypanosomes not only reproduce in fleas, but also go through a certain cycle of morphophysiological changes. But during this too, the fleas do not transmit the causative agent through biting and only passively contaminate the environment or the skin of the animal. Susceptible animals contract trypanosomiasis while licking the flea excrements. The method of trypanosome transmission is typical specific contamination. SALMONELLOSIS Out of a very extensive group of salmonelloses we deal here only with the disease in rats cause by Salmonella enteritidis. The fate of this pathogen in the digestive tract of the murine fleas has been studied in sufficient detail (26). The salmonellae reproduce in the stomach of the flea and during defecation contaminate the environ­ ment to a great extent. It has been established that the exit portals for the pathogen are both the anus and the mouth. The pathogen does not exit immediately, but only after reproduction and a significant accumulation in the intestine of the flea. The salmonellae are accumulated in the proventriculus of the flea, which is situated before the stomach. This round, muscular organ is lined with chitin bristles, which in the normal state do not obstruct the passage of the blood to the stomach; during contraction they act as a barrier to the reverse flow of blood. The massive reproduction of the salmonellae apparently takes place in the an­ terior of the stomach; from here the microorganisms penetrate into the proven­ triculus and obstruct its normal function. They fill the gaps among the bristles, mechanically hindering the process of pulsation of the proventriculus, which leads to the free outflow of blood to the anterior sections of the intestine. Thus fleas transmit salmonellae not only by the method of specific contamination but also by specific inoculation, with the direct, active introduction of the pathogen into the blood of the animal, as is the case during the bloodsucking of a sand fly infected by Leishmania. However, besides the direct inoculation of the causative agent, the fleas themseleves suffer from this method of transmission. The same investigators note that disruption of the function of the proventriculus suppresses the vitality of the flea; the insects noticeably lose their tonus and elasticity of the intestinal canal, the esophagus expands abnormally and is displaced, and the fleas perish much earlier than they normally do. PLAGUE The plague is widespread in the desert and steppe zones of the world and its only specific vectors are among the Siphonaptera (29, 41, 42, 46, 47). The essence of the main, most effective method of transmission of the causative agent of plague by fleas lies in specific inoculation from an insect with a blocked intestinal track. This

Annu. Rev. Entomol. 1977.22:23-32. Downloaded from www.annualreviews.org Access provided by Technische Universiteit Eindhoven on 01/26/15. For personal use only.

FLEAS AND DISEASES

27

phenomenon of blocking the intestinal tract is so important and interesting that it needs special consideration and detailed analysis. The block was first described by Bacot & Martin (5),and then by other investigators (10,17,25,29,34,35,38,41, 46). The reproducing bacilli, Yersinia pestis, occupy the anterior position in the stomach and form a viscous accumulation, which wholly closes the lumen of the flea proventriculus. Usually the fleas, which take numerous blood meals, fail in their next attempt to feed because the blood that is ingested into the esophagus comes up against the bacillary block in the proventriculus and cannot go further. After many futile muscular efforts, the blocked flea, during the blood meal, regurgitates the content of the frontal sections of the esophagus together with the plague bacilli. Such fleas remain hungry and constantly attempt to bite and feed, which raises the possibility of numerous transmissions of the pathogen. The poor state of the fleas is apparently aggravated by poisoning with the products of the vital activity of the microbes--endotoxins, exotoxins, and metabolic products. Soon (an average of 5-10 days after the blocking) the exhausted and starved insect perishes. During this period, the blocked flea can infect dozens of animals, which in turn infect new fleas, and thus the usual cycle of maintenance of the pathogen in the natural plague focus continues to exist. In addition to other methods of transmission of the plague microbe by fleas, there is specific contamination. This occurs when the body of the warm-blooded host or the environment is contaminated by the flea excrement and also when the flea is crushed. But because of the biological features of the flea and the pathogen and the level of reactivity of rodents, this method of infection is obviously of secondary importance. Lately there has been a lively discussion of the method of mechanical inoculation of the causative agent of plague through flea mouth organs that are contaminated by bacilli (during the first days after the insect is infected). The American investiga­ tors (17,31) consider this method of transmission to be especially important at the time of acute epizootics. Until recently, it was unclear how an assessment could be made of the quantitative and qualitative preservation of the microbes outside and inside the mouth organs. However, it is obvious that, without the proof of contami­ nation and of at least relatively short survival of the bacilli on the proboscis of the flea, we cannot uphold the possibility of the mechanical transmission of the causative agent, since one intake during the first day after an infective feeding does not exclude other ways of transmissions. Experiments with direct contamination of the probos­ cises and investigations of the vitality of the bacilli contained in periodic washings from them conducted with a special apparatus for dosed feeding (11) showed that under moderate temperatures the bacilli remain viable for only 3 hr. Since the overwhelming majority of flea vectors do not feed again within this period of time, they consequently cannot carry out mechanical inoculation of the bacilli. The role of mechanical inoculation was obviously greatly overemphasized. The significant element in plague transmission is still the specific inoculation of the pathogen through the bite of a blocked flea. This method of transmission is ensured by a whole complex of adaptations of the pathogen to the organism of the flea: the change of the optimum temperature for the plague bacilli in relation to the

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28

BIBIKOVA

optimum temperature of the corresponding species of vectors, the possibility of selection of bacilli varying in virulence during the reproduction in the flea, and the occurrence in the plague bacilli of biological properties that ensure the effective development of the block in the digestive tract of the flea (3, 9, 13, 17, 24, 29, 31, 34, 35, 38, 42, 44). The frequency of blocking depends not only on the species of fleas and the environmental conditions but also on the properties of the plague bacillus strain. Formerly, however, the influence of biological properties of the pathogen strain on the efficiency of blocking was not taken into consideration. The assessment of this influence was greatly facilitated after discovering the determinants of virulence in Y. pestis strains and developing the methods used in their discovery (19, 30). One determinant of virulence is the ability of bacilli to grow in the form of pigmented colonies in a culture medium with gemine (determinant P). Jackson & Burrows (30) pointed out the dense consistency of pigmented colonies, which did not give homogeneous suspension in phosphate buffer (the majority of bacilli remained glued together in the form of very dense flakes). At the same time, the colonies of nonpigmented variants were distinguished by soft consistency, and in phosphate buffer they formed homogeneous suspension. This peculiarity of p+ and P- colonies indicates a tendency ofP+ variants to give compact growth in the presence of gemine due to forces of adhesion among bacilli. In the intestinal tract of the flea, the protein component of hemoglobin is disrupted under the influence of proteolitic ferments, releasing the blood pigment with subsequent formation of gemine or closely related ferrous compounds. It seems that the plague bacillus strain, capable of compact growth in the form of pigmented colonies in the medium with gemine-determinant of virulence of P+, according to Burrows (19)-

Contemporary views on the interrelationships between fleas and the pathogens of human and animal diseases.

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