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REVIEW ARTICLE
Year : 2022 | Volume
: 59
| Issue : 1 | Page : 12-21
A review of public health important fleas (Insecta, Siphonaptera) and flea-borne diseases in India
V Rajamannar1, R Govindarajan1, Ashwani Kumar2, P Philip Samuel1
1 ICMR-Vector Control Research Centre Field Station, Madurai, Tamil Nadu, India
2 ICMR-Vector Control Research Centre, Puducherry, India
Correspondence Address:
P Philip Samuel
ICMR-Vector Control Research Centre, Field Station, Madurai, Department of Health Research, No.4, Sarojini Street, Chinnachokkikulam, Madurai-625002, Tamil Nadu
India
Source of Support: None, Conflict of Interest: None
CheckDOI: 10.4103/0972-9062.328977
Fleas (Insecta, Siphonaptera) are important vectors of plague and murine typhus in many parts of the world. Currently, about 2700 flea species were described in the world. The most common vector flea Xenopsylla cheopis is found throughout India, but X. astia, and X. brasiliensis are found less and limited in distribution associated with the domestic rats such as Rattus rattus, R. norvegicus, Mus musculus, and Bandicota bengalensis. Bubonic plague is a major flea-borne disease caused by the bacterial pathogen Yersinia pestis, transmitted from rats to humans via the rodent flea, X. cheopis. A major outbreak of plague and high mortality occurred in India. After 1966 with the 3 decadal intervals, plague cases occurred only during the year 1994 reported in 5 different states (Gujarat, Maharashtra, Karnataka, Uttar Pradesh, Madhya Pradesh and New Delhi and subsequently plague cases occurred during 2002 and 2004 after the one-decade interval in Himachal Pradesh (2002). Another outbreak of bubonic plague was reported in Dangud village, Barkhot tehsil, Uttarkashi district, Uttarakhand during October 2004. Ctenocephalides fleas are common in cats and dogs, which are the main vectors of bacteria rickettsiae, such as Rickettsia typhi, R. felis, R. conorii, and Bartonella henselae. Molecular and serological evidence also confirms the presence of R. typhi, R. conorii R. felis and B. henselae pathogens in cats and other fleas in India. Flea bites and flea-borne dermatitis are common in men and pet animals. Because of the re-emergence of the plague, updated information on fleas and flea-borne diseases are essential to control the flea vectors and flea-borne diseases in India. Hence, this comprehensive review updates the available information on fleas and fleas transmitted diseases in India.
Keywords: Flea vectors, Flea-borne diseases, India, Control of flea vectors and diseases
Fleas (Insecta, Siphonaptera) are small in size measuring 0.5 mm in length, but visible to naked eyes, and laterally compressed wingless hematophagous insects with backward directed spines on their legs and bodies[1]. Fleas are important vectors to plague and murine typhus in many parts of the world[2]. Fleas belonging to the family Pulicidae, and Ceratophyllidae, have medical and veterinary importance, distributed worldwide. In the world, currently, about 2700 species of Siphonaptera are described in 18 families[3], and modified after a phylogenetic classification[4]. In association with rodents and pet mammals, flea species of the genus Pulex, the genus Ctenocephalides and genus Xenopsylla act as vectors, found common in India play a vital role in the transmission of flea-borne diseases[5]. Humans are the only primate to be infected with fleas that are derived from other mammals and men become infected when they visit disease-endemic areas, through infected rodents and mammals[6]. Bubonic plague is a major flea transmitted disease.
Plague is a major flea-borne disease caused by a bacterial pathogen Yersinia pestis of the family Enterobacteriaceae, transmitted in epidemics from rats to humans via the major rodent flea, Xenopsylla cheopis (oriental rat flea), which was originated in Egypt spread to all parts of the world resulting in millions of casualties worldwide during three plague’s pandemic out brakes[7],[8],[9],[10],[11]. Major outbreak cases of plague causality occurred in India at significant historical backgrounds[12]. After a period of three decadal intervals, a major outbreak of plague occurred in 1994 in 5 different states[13],[14],[15]. Subsequently, plague cases occurred during 2002 and 2004 after a decade interval in Himachal Pradesh (2002) and Uttarakhand (2004). In 2002, plague cases were reported from Himachal Pradesh[16], and the presence of Yersinia pestis in clinical samples indicated re-emerging plague pathogens in India[17],[18]. Another plague outbreak was recorded in Uttarakhand during October 2004, with eleven human cases and three deaths[18]. Even though the plague is controlled long back, it is still a re-emerging disease in India. Hence this comprehensive review updates the current knowledge of fleas and flea-borne diseases and the vector distribution pattern across India which will be very helpful for researchers and public health officials to make awareness about the prevalence of many plague vectors to initiate regular surveillance and control.
Material & MethodsLiterature review
The online database PubMed of National Library of Medicine, USA was used for the retrieval of references and abstracts subjected to “Fleas” and “flea-borne diseases” listed in life sciences and biomedical topics. MeSH terms and subheadings like Flea-borne diseases, the biology of fleas; and Flea-borne rickettsial infections were used for literature review. For the management of reference information, End Note Version 9.0.1©1998-2005 of Thomson, Mendeley Reference Manager Version 2.44.0©2020 of Mendeley Ltd was used. Journals, Books, Book Sections, Conference Proceedings, Web Pages, and local reports were the different types of documents used in the literature review.
Spot Map
Based on flea-borne diseases clinical data and outbreaks, spot maps were created by using the EpiMap in EpiInfoTM 7.2.2.6 website of CDC, Atlanta, USA.
Medical and veterinary important fleas in India
Oriental rat fleas
The oriental rat flea is the principal vector of the plague and murine typhus. It is most common on domestic rats and found to feed on humans and other domestic animals. Adult X. cheopis, otherwise called rat flea is abundant in India along with its associated rodent hosts in domestic and peridomestic areas, an important vector to the pathogen, Y. pestis for the outbreak of the plague disease. Xenopsylla cheopis is the only vector flea in India with pathogen Rickettsia typhi for the transmission of endemic (murine) typhus[19],[20]. In India, X. cheopis is abundant in the cold season and is found as ectoparasites on the rats, Rattus rattus and R. norvegicus. Xenopsylla astia and X. brasiliensis are widely distributed in India. Xenopsylla cheopis, X. astia and X. brasiliensis were recovered from the three rodent species of Rattus rattus, R. norvegicus and Bandicota bengalensis, from the shrew species Suncus murinus. Xenopsylla astia is most abundant on the bandicoot and Norway rat, while X. cheopis is more common on S. murinus. Except for X. cheopsis and X. astia, other fleas contributed less to plague transmission in India[21]. Xenopsylla astia was also collected from Indian antelope rats, Tatera indica[22].
Cat and dog fleas
The cat flea is found distributed worldwide and it is the most important flea of humans and domestic animals. The dog flea is less commonly found on domestic dogs in many parts of the world. Ctenocephalides felis is commonly found infested on the vertebrate host species in many places. Ctenocephalides felis is the known vector of Rickettsia typhi[23]. Ctenocephalides felis felis is found in cats and dogs everywhere except Antarctica[24], but C. felis orientis is found dominant on dogs distributed in many countries of Asia viz. Malaysia, Thailand, and India[25],[26]. Ctenocephalides felis is also an intermediate host for cysticercoid larvae of Dypidilium canium tapeworm[20]. Even though cat fleas were found in human beings, these fleas are considered inefficient vectors of Y. pestis and are not commonly found on rodents. Thus, they are unlikely to serve as bridging vectors or play a major role in plague epidemics[27],[28]. In India, C. canis is found dwelling in many animals like dogs, cats, rats, and other mammals in the temperate parts of India and also attack human.
Human flea
This flea feeds on humans and is capable of transmitting the pathogen. It parasitizes carnivores and sometimes pigs. Pulex irritans is the most studied species and all 7 species of the genus Pulex (Pulicidae) species are found in Europe[29]. Except for the Arctic region, this species was found all over the world, adapting to live in temperate climates[30]. Pulex irritans does not have genal or pronotalctenidia. Pulex irritans is a vector for diseases flea-borne spotted rickettsiosis, plague, and murine typhus. Bites from P. irritans are causing itching with a bright red appearance due to blood escaping from the punctured wound[31],[32]. It was recorded in India in very early days at Assam, Manipur, Jammu and Kashmir, and Mumbai[33] and in Juksam, Sikkim’ during April 15, 1982[34]. Pulex irritans were recorded more in cooler and temporal climate countries like France, Italy, and Greece[35].
Northern rat flea (Nosopsyllus fasciatus)
Northern rat flea is a common flea on a domestic rat. It can bite humans and can transmit several zoonotic pathogens. Nosopsyllus fasciatus has an elongated body, 3 to 4 mm in length. It has a pronotal ctenidium with 18 to 20 spines but lacks a genal ctenidium[36]. These species are rare in India but reported from buffalo (a female and a male) found in Bombay, India.
Sticktight flea (Echidnophaga gallinacea)
Sticktight flea is a sedentary flea. These species are commonly known as the hen fleas, sticktight fleas, which occur on a wide range of bird and mammal hosts. Stick-tight flea infestation in desi-chicken was also reported in Namakkal poultry, Tamil Nadu, India[37].
Flea-borne diseases
Plague
The most famous zoonotic bubonic plague is a pandemic disease, caused by Yersinia pestis a bacterial pathogen in the family Enterobacteriaceae, and transmitted through the main rodent fleas X. cheopis and X. astia, resulting in casualties of millions in parts of the Americas Africa, and Asia. Ctenocephalides fleas (fleas on cats) harbored this parasite in animal reservoirs of plague[38],[39],[40],[41]. The first plague pandemic began in 542 AD, known as the “Justinian plague” with 100 million deaths and the outbreak period was between the 6th and 7th centuries AD, second plague began in 1346 AD, known as the “Black Death”, lasted during three centuries (between 14th and 17th century AD)[42] and claimed 25 million deaths. The second pandemic killed many in the affected areas and the third pandemics began in 1894 and continued until the 1930s (between the late 19th and early 20th century AD)[43]. The transport of agricultural products led to plague incidence in India[5]. Cooler temperatures, higher humidity, and the monsoon season rains drove rats inside shelters such as burrows, houses, and warehouses, precipitating renewed outbreaks of plague in India[5],[44],[45]. During the third pandemic, between 1898 and 1918, 12.5 million people in India died[42]. The first authenticated plague epidemic in India occurred from 1895–96 onwards and reached a peak during 1907[46]. In India, plague cases/lakh population was decreased slowly from 6.88 to 0.0044 from the year 1939 to 1957, and the occurrence of plague diminished gradually[18].
During the first two decades of the Third Plague Pandemic in India that began in 1894, 25 million people were affected and died due to plague at a rate varying between 183 to 133 deaths per million per year, but during 1949–1958 the mortality rate dropped to 1.8 deaths per million per year [Figure 2] and [Figure 3][47]. Four epidemiological plague foci occurred in India[18] as Epizootic plague, Enzootic plague, Sylvatic plague, and Demic plague. The epizootic plague was caused by the commensal rodents found in domestic and peri-domestic areas of human habitats (R. rattus and R. norvegicus). In India, the enzootic foci of plague are present in four zones in the northern, central, western, and southern parts of India[18]. During 1970, serological evidence confirmed the presence of plague antibodies in the rodents collected such as R. rattus, T. indica, B. bengalensis, M. maltada, and Funumbulus palmarum, detected more in the enzootic foci of plague in India, by the NCDC after a plague outbreak[48]. NCDC reported plague outbreaks in 1966, 1969, 1971, 1983 in Tangnu and 1984 in the Jubbal area, Himachal Pradesh. Active enzootic foci were observed in Rohru tehsil and the other adjacent areas in Himachal Pradesh[17].
Figure 1: Vector fleas: 1.Ctenocephalides canis; 2. C. felis; 3. C. orientis; 4. Echidnophaga gallinacean; 5. Pulex irritans; 6. Tunga penetrans; 7. Xenopsylla astia; 8. X. brasiliensis; 9. X. cheopis; 10. Ceratophyllus fasciatus
Figure 2: Fading of plague mortality in India from 1898-1968. Decadal decrease of deaths from 1898–1958 and localized deaths during 1959–1968
Figure 3: Localized plague outbreak cases and deaths in India (1969–2004). Discontinued outbreaks in the selected areas.Since 1980, only small, isolated bubonic plague outbreaks have occurred in Andhra Pradesh, Gujarat, Himachal Pradesh, Tamil Nadu, Bihar, Maharashtra, Karnataka and Uttarakhand[49]. These outbreaks had low case fatality rates, and most patients suffered only a mild illness, all indicative of a minimally virulent plague strain[50]. In Himachal Pradesh, pneumonic plague erupted in 1983, infecting 22 and killing 17 people[16],[50]. On September 23, 1994, 460 pneumonic plague cases were reported in Surat, Gujarat[14],[15],[51],[52]. This received national and worldwide attention, causing over 200,000 Indians and foreigners to flee the states of Gujarat and Maharashtra[53].
From Surat, pneumonic plague diffused across the local region (termed ‘expansion diffusion), remaining within 40 km of Surat before October 1994, but once people panicked and fled by train from Surat, plague jumped across India in a manner known as ‘relocation diffusion[51]. Once the pneumonic plague had relocated to Delhi, Mumbai, and Kolkata, it again diffused locally in a manner referred to as ‘hierarchical diffusion’, moving from regional centers to local market towns to villages[51]. Although over 200,000 fled Gujarat and Maharashtra, only 693 plague cases were reported across India, with 56 deaths[54]. The distribution of flea vectors & flea-borne diseases reported in India is furnished in [Figure 1] and [Table 1]. Plague outbreaks in India at various localities and different years are presented in [Table 2] and [Figure 2] and [Figure 3]. The decreasing trend of plague cases (fading of plague cases) occurred from 1898 to 1958 (in 60 years) and the mortality rate decreased from 183.3 mortality/ 1 lakh population (1898) to 1.8 mortality / 1 lakh population (1958). Very low cases with 0.2 mortality/1 lakh population occurred after 1959–1968[46]. No case after and some localized outbreak occurred at Surat, Gujarat (1994), Himachal Pradesh (2002), and Uttarakhand (2004) [Figure 2] and [Figure 3] and [Table 2].
Table 2: Plague out-break in India year wise, important hosts and flea vectors (1898–2004)Murine typhus or rat-flea typhus
Murine typhus is a febrile Zoonotic disease spread by Rickettsia typhi pathogen maintained in nature by a flearat-flea transmission cycle[30]. This disease is distributed globally except in the Antarctic region[30],[55]. Murine typhus infection is clearly associated with indoor communal rat populations such as R. rattus (or) R. norvegicus throughout the world, and the fleas X. cheopis, X. astia, and X. brazilliensis play major role[19],[53]. In India, very few cases were confirmed by passengers who traveled during international travels from India[56]. An increase in temperature of 3°C (25–28°C) reduced the hatchability time, pupation, and development in Xenopsylla flea species[57], which lead to an increased flea population density correlated to an increased human risk of infection by Rickettsia species. Ctenocephalides fleas are also main vectors to Rickettsia typhi, R. felis, R. conorii and B. henselae[58], and C. felis felis harbored R. typhi[19]. Rickettsia felis alone contributes mainly to the transmission of cat flea rickettsiosis[59].
All rickettsial diseases including murine typhus were documented in India since the 1930s, and the first murine typhus case was recorded at Jabalpur in Madhya Pradesh and later in the Kashmir area[60],[61]. Some clinically suspected cases of murine typhus fever were recorded in Mumbai, acquired during short-term urban travel and the serological evidence confirmed the presence of pathogens in the fleas. Serological and molecular evidence also confirmed the presence of Murine typhus pathogen, Rickettsia typhi in the fleas responding to the transmission of the disease to human[62] in India. The presence of Murine typhus pathogen was also observed as a cross-sectional survey, conducted in Vellore, Tiruvannamalai, and Salem districts, of Tamil Nadu state, at three different geographical areas such as urban, rural plains, and rural hill areas[63].
Flea-borne spotted fever or cat-flea typhus
Ctenocephalides fleas can transmit Rickettsia felis a new pathogen found in human[19],[64]. In India, this disease was common in cats and dogs, confirmed in animals in hilly regions, western Himalayas, and Mumbai, Lucknow, and Pune cities[65],[66]. An outbreak caused by the rat flea-borne (C. fasciatus) human Rickettsiosis in the sub-Himalayan region of Himachal Pradesh showed the role of a Rickettsia sp. spread by rat fleas in the human population which has public health importance. The rat flea vector C. fasiatus, detected with Rickettsial species (R14) observed feeding on captured rats and mice and found in human dwellings and animal shed. A high prevalence of febrile illness was recorded among the people residing indoors in mud houses like women and children compared to men who go out for jobs where repeated flea-bites led to higher doses of pathogen inoculation with a higher rodent population[65].
Bartonellosis
Bartonellosis is a zoonotic disease caused by the bacterial genus Bartonella through cat fleas C. felis[67], which is common in mammals. There are 45 species described so far in the Bartonella genus[68]. By the scratches or bites of C. felis infected cat, one type of species flea-borne B. henselae, was first isolated[69],[70],[71]. A study in North India showed Bartonella infection and B. henselae infection and the clinicians suggested considering practicing differential diagnosis of febrile illness and chronic diseases[72].
Tungiasis
Tunga penetrans, a small-sized jigger flea or sand flea can cause Tungiasis a neglected parasitic skin disease by the permanent penetration into the skin[73]. They can expel hundreds of eggs for two to three weeks[74]. A clinical case of Tungiasis from Maharashtra was recorded, as the first report from India[75].
Flea allergy dermatitis, flea bites, and other infections
Ctenocephalides felis sometimes affect small ruminants, causing flea allergy dermatitis and iron deficiency anemia[76],[77]. In Puducherry, molecular detection of the flea rickettsial pathogen observed from domestic pet animals confirmed fleas as vectors of rickettsial disease transmission[78]. Human cases were also reported in India by the infected fleas[79]. Flea bites are common to the entire host animals while fleas feed on the blood of the host. Flea allergic dermatitis (FAD) is caused by flea saliva during flea bites as a biochemical disorder and causing allergy to the skin[80]. Pet animals and men are affected by flea bites, which are causing a nuisance to humans worldwide[81].
There is a definite correlation with every plague epidemic. The widespread ecological changes created by the earthquake in September 1993 resulted in the gradual growth of rat population and flea nuisance followed by bubonic plague in Beed and other districts. Topi River brought more dead rodents attributed to the unhealthy sewerage conditions and the residents who made crowds during a festival season came into contact with dead animals infected with this disease during 1994. In Uganda, the site of the plague outbreak was a densely populated area inhabited by rats and gerbils found nearby human dwellings. This must be the reason for the appearance of human plague resulting from an epizootic among synanthropic rodents. In the USA, rapid urbanization resulted in increased numbers of people living in or near active plague foci. Plague is thus transmitted between rodents and other animals via rodent fleas, cannibalism, or contaminated soil. On every continent there is a favorable climatic condition prevail for the high and stable number of rodent reservoirs and flea vectors[82].
Systematic sentinel surveillance of vectors, reservoirs, and other hosts must be undertaken. This is to collect dead rodents for laboratory analysis after die-offs and rat falls is a simple method to monitor and examine for plague infection. It is required to map and periodically check the rodent colonies in an area to inspect for dead animals and to inspect for infected fleas. Rodents should be systematically trapped to know the difference in abundance in an area. Wonder traps can be used to collect more live animals in trap[83]. Rodent sera can be collected for Y. pestis isolation. Flea species can be collected to estimate human flea infection.
ConclusionThere is a need to maintain close epidemiological surveillance of fleas and flea-borne diseases in India, due to the abundance of flea vectors in the commensal rodents and the re-emergence of the flea-borne disease in India, especially in endemic or enzootic areas. Molecular and serological evidence confirms the circulation of bacterial pathogens in fleas[78]. Transport of rodent hosts from foreign cargo ships traveling from plague endemic countries may be the source for plague outbreaks. Hence, severe quarantine should be made for controlling the pest rodents and associated vectors in the port and railways. This review indicates different flea-borne typhus fevers reported in India. Molecular and serological evidence also confirms the presence of R. typhi, R. felis, R. conorii and B. henselae pathogens in fleas which may lead to an outbreak of flea-borne diseases[62]. Hence, flea control is very much essential. Infected pet animals should be taken care of against fleas, which are the main sources for the multiplication of fleas.
In India, domestic and wild fleas prefer to live in warm-blood hosts, adapted to various topographical regional climates. Most of the fleas are species-specific, but some are adapted to survive in different hosts. Xenopsylla cheopis, X. astia, C. canis, C. felis, and Stivalius aporus are adapted to live in warm blood animals of domestic and peridomestic areas, and to live in the Indian climate as X. cheopis is more abundant in India. Indian climate also favors other vector fleas such as X. cheopis, X. astia, C. canis, C. felis which are involved in plague transmissions. The pest rodent species R. rattus, R. norvegicus and B. bengalensis are reservoirs of plague pathogen at plague endemic areas, which are normally called urban rats; the gerbil T. indica, an important agricultural pest rodent, the Indian field mouse M. budooga, and the squirrels F. pennanti and F. palmarum were found positive for plague in various foci. These rodents should be controlled in the plague endemic areas using multiple live traps (wonder trap) available[83].
The widespread ecological changes created by earthquake, high rainfall, resulted in floods attributed to unhealthy sewerage conditions, and the crowding of residents during a festival came into contact with dead animals infected with this disease. The plague outbreak was reported in a densely populated area inhabited by rats and gerbils found nearby human dwellings. Rapid urbanization resulted in increased numbers of people living in or near active plague foci. The aforementioned especial ecological disasters play a major role in the transmission of these fleas-borne diseases[82].
In India after the third pandemic era, from the year 1939 to 1957, plague cases decreased slowly and some localized outbreaks occurred in Surat (Gujarat) during 1994 and very minor cases in the Himalayan states (Himachal Pradesh and Uttarakhand) during 2002 and 2004. Efforts should be concentrated to improve the awareness among community and health officials and to enhance capacity building to detect sporadic cases to curtail possible future epidemics. There was a change in human habitation; change of life pattern, environmental sanitation, and the safest food storage patterns controlled the prevalence of rodent hosts and related plague vectors in India and thus cases decreased. Agricultural development in rural areas, changing ecological patterns and urban development controlled the composition of rodent populations which may be the key reasons for its present condition. The emerging and re-emerging flea infections reported in this world showed the shifting and expanding nature of these vectors. This publication reviews the extent of damage caused by this disease in India and its public health burden will be a prerequisite for the health officials to undertake necessary intervention measures. Thus, it is emphasized that there should be a need for the establishment of a permanent flea surveillance system with improved flea-borne disease diagnostics to initiate effective vector control efforts to stop the transmission of flea-borne diseases in the future.
Conflict of interest: None
AcknowledgementsWe are thankful to the Secretary, Department of Health Research, Ministry of Health & Family Welfare, and the Director-General, ICMR for financial support. We want to express our deep gratitude to our Director, ICMR-VCRC, Puducherry.
References
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