REVIEW OF RELATED LITERATURE

Distribution of Rodents

Rodents are dominant group of mammals. There are more than 2700 species of

rodents worldwide; in fact, 42% of all the mammal species on Earth are rodents, and

most of the rodents are found in Asia. Rodents occupy a wide range of natural habitats,

including forests and grasslands, as well as the human world agricultural landscapes,

villages and townships. Most rodents are prolific breeders and they often represent a

significant amount of the animal biomass in forest and other natural ecosystem (Aplin,

Brown, Jacob, Krebs and Singleton, 2003).

Diversity and Distribution of Rodents in the Philippines

The Philippine is extremely rich in biodiversity and is believed to have the highest

per-area level of mammalian in the world (Heaney, Balete, Louella Dolar & Ong, 1998).

The most diverse family mammals in the Philippines is Muridae (mice and rats), which

has at least 66 species described, 58 of which are endemic, and more species are regularly

being discovered (Balete, Rickart & Heaney, 2006).

Heany et al., 1998, says that the majority of rodent species live in natural forest

ecosystems, such as low land, montane, and mossy forest. Some species of rodents are

known to inhabit large areas of agricultural land that have replaced the natural habitat.

These species are often regarded as pests and are considered “non-native” in origin.
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Ecology and Biology

Ecological Importance of Rodents

Rodents play a crucial role in the balance of nature. Rodents play an important

role in the food web, both as consumers of plants and fungi, and as food resources for

larger predators. Rodents also play an important role as environmental engineers, helping

to spread pollen and seed and aerating the soil through their digging and burrowing

activities. Their network of burrows and diggings for roots and fungi influence the flow

of micronutrients and water at the scale of the landscape, and some of the larger rodents

have major impacts at the macro scale on water flow and bank stability along waterways

(Aplin et al., 2003).

Rodent as Pest Species

Rodents affect rural families in three main ways: they eat agricultural crops in the

field; they eat, spoil and contaminate stored food; and carry diseases of humans and

livestock (Aplin et al., 2003).

The losses caused by rodents to rice crops in Asia provide a graphic example of

their impact. Rodents typically cause annual per harvest losses to rice of between 5% and

10% of production. However, in some areas, episodic outbreaks of rodents cause heavier

losses or even the complete destruction of crops. Postharvest losses in some areas may

match or exceed the perharvest damage, and reports of 20% losses caused by rodents to

grain after harvest are not unusual (Aplin et al., 2003).

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Reproduction of Rodents

Breeding is the main reason why populations increase in size. This is especially

true of many rodents’ species that are capable of rapid population growth, especially

when conditions are favourable. Rapid population growth is generally due to the

combination of two factors, namely, a high reproductive potential and a short period of

maturation to sexual maturity. Rodents typically have short gestation periods, with high

litter sizes and an ability to fall pregnant again within a few days of delivery. These

factors alone would ensure a high reproductive potential. (Aplin et al., 2003).

Growth and Maturation of Rodents

The sequence and timing of maturation is very similar in all of the major pest

species of rodents. Pups of all species begin to take solid food brought into the nest by

adults from the end of the second week. However, weaning is generally not completed

until the end of week 3 or 4. After weaning, young rats and mice are effectively

independent from the mother, although in some species they may continue to inhabit the

same burrow complex for some time (Aplin et al., 2003).

Attainment of Sexual Maturity

. Many rodents attain sexual maturity at very early age, due mainly to rapid

growth during their first few weeks of life. In wild population of Rattus norvegicus,

ovulation (oestrous) cycles may start at any time from 40 days of age but with a mean age
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of around 100 days. In Rattus argentiventer, females show an open or perforate vagina at

a mean age of 33 days, and are pregnant at a mean age of 49 days. In laboratory mice

(Musmusculus domesticus), vaginal perforation occurs between 28-49 days, with a mean

of 35 days. Ovulation commences soon thereafter, but the first mating is often delayed by

one or two weeks. Male mice become sexually mature slightly later than females. The

particularly short period to sexual maturity of many murid rodents is one of the main

reasons why so many of the major agricultural pests belong to this one family of

mammals (Aplin et al., 2003).

Life Span and Menopause

Even when reared under optimum conditions, most rodents have a maximum life

span of only 2-3 years. Females of Rattus norvegicus and Musmusculus domesticus top

ovulating (i.e. enter menopause) altogether between 12-18 months of age, although

average litter size declines well before this age. Under natural conditions, very few

individuals are likely to survive to such advanced ages (Aplin et al., 2003).

Rodents Pest Species of Rice in the Philippines

Four non-native rodent species are known to inhabit the Philippine

agroecosystem: Rattus tanezumi (Temminck), Rattus argentiventer (Robinson & Kloss),

Rattus exulans (Peale), and Rattus norvegicus (Berkenhout) (Singleton, 2003). These
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species are regarded as serious pests of rice in the country. The major rodent pest species

are R. tanezumi in Luzon and R. argentiventer

Rattus tanezumi (Rattusrattus mindanensis) (Philippine rice-field rat)

It is one of the two major species found in rice fields. Geographically, it is the

most widely distributed and attributed as the principal pest of most food crops other than

rice. This species is the major rice field rat in Luzon and the Visayas. It is largely

commensal in Mindanao and sympatric to R. argentiventer in Mindoro (Sumangil, 1990).

Rattus argentiventer Robinson and Kloss (Field rat)

R. argentiventer is the major rodent species in rice agro-ecosystems in Mindanao

Island; constituting 95% of all rats caught in the rice fields. In Mindoro Island, this

species coexists with R. tanezumi but its distribution is restricted (Barbehenn, 1973).

Rattus norvegicus Berkenhaut (Norwegian rat)

Previously, R. norvegicus was reported only in cities, but in recent years, they

have been found in rice fields in the vicinity of major cities. They have now replaced

populations of R. tanezumi in Iloilo City paddy habitats (Cuaterno, 2008).

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Rattus exulans Peale (Polynesian rat)

R. exulans is an important pest of upland rice in the Philippines. It occasionally

coexists with the R. tanezumi in Central Luzon, but it appears to be a weak competitor. R.

exulansis a major pest in granaries and around houses (Cuaterno, 2008).

Parasites of Rodents and their Zoonotic Implications

Rodents are responsible for transmitting various agents, including a number of

helminths parasites, to human and domestic animals. Infection in human generally occurs

directly through contact with rodent excrement, ingesting food contaminated with their

fur, feet, urine or fecal dropping, rodent’s bites and indirectly through bites from

ectoparasitic vectors such as flea and ticks. Wild rodents serve as reservoir host and have

greater ability to harbor a number of endoparasitic agents that play important role in

human and livestock health (Pakdel, Naem, and Chalehchaleh, 2013).

All parasites recorded from R. novergicus and R. tanezumi listed below. Species

transmissible to humans are also presented in some detail as to their biology, transmission

and zoonotic potential (Eduardo, Domingo & Divina, 2008).

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Trematode

Artyfechinostomum malayanum (Leiper, 1911) Mendheim, 1943

It has been known to exist in Asian countries but has been lately recorded in field

rats (Eduardo and Lee, 2006), and recently in humans in the Philippines (Belizario et al.,

2007). Eggs produced by the adult worms are passed out with the feces. The eggs must

reach freshwater to hatch to miracidium, which actively seeks suitable first intermediate

snail hosts (Indoplanor bisexustus), and where it develops into various intramolluscan

stages (sporocysts, redia, and cercariae), multiplying by polyembryony, however in the

Philippines, the first snail are not yet known (Eduardo, 2001).

All snails are the source of infection for rats and pigs, which maintain the cycle in

nature. Prepatent period in rats is 14–18 days (Lie, 1963).

Echinostoma ilocanum (Garrison, 1908) Odhner, 1911

In the Philippines, this species was first described as a human infection before it

was reported in animals, and it is being cause of human echinostomiasis in the

Philippines (Eduardo, 2001). Adult worms are found in the intestine of the definitive

hosts (man, dog, rats, etc.).Gyraulus phrasadi and Hippeutisum bilicalis are snail hosts as

the first intermediate hosts in the Philippines; Pilaconica (kohol) is a freshwater snail

serve as second intermediate hosts. The latter is the most important source of human

infection because this snail is consumed by Filipinos (Cross and Basaca-Sevilla, 1986).
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Echinostoma lindoense Sandground& Bonne, 1940

E. lindoense also cause of human intestinal echinostomiasis. It was first described

and reported as a human infection in Indonesia and later in other Southeast Asian

countries (Indonesia, Malaysia, and Thailand). It has been recently re-described and

figured by Eduardo and Lee (2006) based on specimens from field rats in the Philippines.

Human infection results from ingestion of viable metacercaria contained in the second

intermediate hosts. Human infections have long been recorded in Indonesia (Lie, 1968).

Paragonimus westermani (Kerbert, 1878) Braun, 1899

Paragonimus westermani also known as “oriental lung fluke,” is the main cause

of human paragonimiasis in the Philippines. Definitive hosts include dogs, cats, field rats,

other rodents, and humans. Cercaria emerges and seeks a suitable second intermediate

host which, in the Philippines, is the crustacean mountain crab, Sundathelphusa

philippina, where it encysts as metacercaria. The definitive host becomes infected by

ingesting raw or partly cooked infected crabs. Following ingestion, the metacercaria

excysts in the duodenum. The young worm then penetrates the intestinal wall to the

peritoneal cavity, wanders and embeds itself on the abdominal wall for several days. It

then returns to the peritoneal cavity, traverses the diaphragm to the pleural cavity, and

penetrates the lungs to grow into adulthood (Belizario & Malte, 2004).
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Plagiorchis muris Tanabe, 1922

This species is an intestinal parasite of rats. Eggs are passed out with the feces of

the definitive hosts. Eggs must reach freshwater to hatch to miracidium. The miracidium

then seeks a suitable snail intermediate host where the various intramolluscan stages

develop and multiply by polyembryony. The definitive host becomes infected through

ingestion of second intermediate hosts harboring metacercaria. Prepatent period is 7–9 d

(Baker, 2007). Infection results from ingestion of viable metacercariae from infected

second intermediate hosts. No human infection has been reported yet in the Philippines

(Eduardo et al., 2008).

Plagiorchis philippinensis Sandground, 1940

This fluke was first described and reported in 1937 in the Philippines as a human

infection. The life cycle, including the intermediate hosts of this species, has yet to be

established. Human infection can occur through ingestion of infected intermediate host

(Eduardo., et al 2008).

Plagiorchis potamonides (Tubangui, 1946) Yamaguti, 1958

Tubangui (1946), described the first species in the Philippines on the basis of

specimens recovered from experimentally infected laboratory white rats fed with

metacercaria from the crab Sundathelpusa philippina. The species was subsequently

recovered from naturally infected brown and field rats (Eduardo & Lee, 2006).
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The snail intermediate host is not yet known. Rats serve as important reservoir

hosts. Although no human case has been reported, the potential of human infection exists

as the second intermediate host is an edible crab, the same intermediate host of

Paragominus westermani, which is endemic in certain provinces in the Philippines.

Human infection can result through ingestion of improperly cooked or raw crabs infected

with metacercariae of this species (Eduardo et al., 2008).

Schistosoma japonicum Katsurada, 1904

Also called “oriental blood fluke,” Schistosoma japonicum is endemic in China,

Philippines, and Sulawesi, Indonesia. The members of the family Schistosomatidae are

unique among trematodes because the sexes are separate. Adults are primarily parasites

of the portal veins and their branches. Compared with the other three species of human

schistosomes, S. japonicum is regarded as a true zoonosis. It affects 46 species of

mammals, including rats and humans (McGarvey et al., 2006). It is the cause of

schistosomosis japonica in humans.

Figure 1.Paragunimus spp. egg. (Retrieved from Garcia L. S. 2016)

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Cestodes

Hymenolepis diminuta (Rudolphi, 1819) Weinland, 1858

Hymenolepis diminuta, also known as “rat tapeworm,” inhabits the anterior

intestine of mice, rats, other rodents, and primates, including humans. Gravid posterior

segments detach from the main body, disintegrate, and release eggs, which are passed out

with the feces. The parasite eggs are ingested by insect intermediate hosts (beetles, moth,

or the rat flea), hatch, and develop into larvae called cysticercoids. The definitive host

becomes infected by ingestion of the infected intermediate host. After ingestion, larvae

are liberated in the small intestine, evaginate, and attach themselves to the intestinal

mucosa to grow into adults. The prepatent period is 19–21 d (Baker, 2007). Humans

become infected through accidental ingestion of infected intermediate hosts. The

prevalence rate of human infection in the Philippines is less than 1% (de Leon, 2004).

Rodentolepis nana (von Siebold, 1892) Spasskii, 1954

This species occurs in the anterior intestine of rodents, including rats and mice.

The life cycle is either direct or indirect, and autoinfection can occur. In the former,

gravid segments detach from the main body of the worm, disintegrate, and eggs are

released and passed out with the feces. Eggs are ingested by the definitive host (direct

cycle) and hatch in the intestine where the embryo penetrates the intestinal villi to
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develop to cysticercoids in 4–5 d. Cysticercoids re-enter intestinal lumen, attach to the

mucosa, and grow into mature worms in 10–11 d. In the indirect mode, intermediate

hosts are required. Eggs that are passed out are ingested by intermediate hosts such as

beetles (grain, flour) and fleas (Pulexirritans, Ctenocephalidesfelis, and

Xenopsyllacheopis) where they develop into cysticercoids (Baker, 2007). Humans

become infected accidentally through ingestion of infected intermediate hosts. Human

infection in the Philippines is more common in poor communities where rats abound (de

Leon, 2004).

Raillietina madagascariensis (Davaine, 1869) Fuhrmann, 1924 (R. garrisoni)

This tapeworm was first described from an adult Filipino as Raillietina garrisoni,

which is now considered a junior synonym of R. madagascariensis. The adult form

inhabits the intestine of the definitive hosts (rats). Gravid segments are passed out with

the feces and are ingested by flour beetles (Triboliumconfusum) as intermediate host

where cysticercoid larva develops. Infection of definitive hosts results from ingestion of

infected intermediate host. Human infection occurs through accidental ingestion of

infected flour beetles. Several cases of infection with Raillietina spp. have been reported

in the Philippines, majority of which involved children (De Leon, 2004).

Taenia taeniaeformis (Batsch, 1786) Wolffhügel, 1911

Eggs released through the feces of the definitive host and are ingested by the

intermediate hosts. Larvae are released in the intestine and migrate through the intestinal
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wall and to the liver to develop into a larva called Strobilocercusfasciolaris. The cat

becomes infected through ingestion of infected rat liver where the larva is released in the

intestine and attaches to the mucosa to grow to maturity (Baker, 2007). The cat is the

definitive host for this tapeworm where adults are found in the intestine. Rodent and

rabbits serve as intermediate hosts for the larval stage which is found in their liver.

Infection in humans can result from ingestion of raw or improperly cooked liver of

infected rodents. No case of human infection with this tapeworm has been reported in the

Philippines (Eduardo et al., 2008).

Figure 2. Anatomy of egg Taenia spp. (Retrieved from Garcia L.S., 2016)

Nematodes

Angiostrongylus cantonensis Chen, 1935

Adult Angiostrongylus cantonensis inhabits the pulmonary artery and lungs of rats

and other rodents, thus the name “rat lungworm.” The life cycle of this roundworm is

eggs from adult worms in the lungs are lodged in small pulmonary vessels. They
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embryonate and hatch to larvae. Larvae are coughed up, swallowed, and expelled out

with the feces. Rats do not spit unlike humans. Larvae are ingested by obligate

intermediate hosts, which include aquatic and terrestrial snails and slugs. Development to

the infective larva takes about 17 d in the molluscan hosts. In the rat, larvae migrate to

the brain and stay in the parenchyma for up to 1 week, then move to the subarachnoid

space and reach the pulmonary artery and lungs via the vein system, where they become

adults (Anderson, 1992).

Humans are accidental hosts. Infection results from ingestion of infective larvae

frequently through the paratenic hosts which are eaten raw and whose juices are used in

the preparation of local dishes or ingestion of vegetables contaminated with larvae from

infected obligate intermediate hosts (Anderson, 1992). In the Philippines, two cases of

ocular angiostrongyliasis have been diagnosed in the College of Public Health, University

of the Philippines Manila (Belizario and Trinidad, 2004).

Figure 3. Angiostrongylus cantonensis egg. (Retrieved from Archer C.E.

et al.,2011)
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Calodium hepaticum (Bancroft, 1891) Moravec, 1982

This species resides in the liver of a wide range of definitive hosts worldwide. It is

common in rodents, especially wild rats, and also occurs in many other mammals (Spratt

and Singleton, 2001). The life cycle of C. hepaticum is unique among helminths of

mammals because it requires host death for transmission. Unembryonated eggs in the

liver tissue are released only when the host dies and when the infected liver or host is

eaten by another host, thus liberating the eggs which are passed out with the feces. With

rodents, the main route of liberation is through cannibalism or necrophagy. Eggs need to

mature (embryonation) on the outside to be infective, which takes about 5–7 week in

tropical conditions. Following ingestion of embryonated eggs by the definitive host,

larvae hatch in the intestine, penetrate the intestinal mucosa, and reach the liver, via the

portal circulation, where they reach maturity and lay eggs in rats after 21–33 d. Male

worms disappear afterward and only females with eggs remain (Baker, 2007).

Human infection results from ingestion of released and embryonated egg through

contaminated soil (most infections are in young children) and not through ingestion of

raw infected liver. There have been no reports of human infection in the Philippines

(Eduardo et al., 2008).

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Figure 4. Eggs of Calodiumhepaticum in stool and liver tissue. A. In human

stools, B. In peccary liver tissue, C. Indogfeces (Retrieved from
ResearchGate)

Acanthocephala (Thorny-headed worms)

Moniliformis moniliformis (Bremser, 1811) Travassos, 1915

This species occurs in rats worldwide and is common in tropical and subtropical

regions (Eduardo et al., 2008). The life cycle is indirect. Adults are found in the intestine

of the definitive hosts (rats, mice, hamster, dogs, and cats). Eggs are passed out with the

feces and are ingested by arthropod intermediate hosts (cockroaches). Larvae called

acanthor are released in the gut of the cockroach and penetrate the gut wall and finally

develops into acanthella or cystacanth cysts (infective form) in the hemocoel in 7 wk.

Rodents acquire infection by ingesting an infected cockroach. Following ingestion,

acanthella escapes from the cyst and grows to an adult in the small intestine in about 31–

38 d (Baker, 2007).

Infection in humans occurs when an infected cockroach is accidentally ingested.

No record of human infection in the Philippines exists (Eduardo et al., 2008).

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Figure 5. Moniliformismoniliformis egg. (Retrieve from biolualberta.ca at

August 11,2018)

Rodent-borne Zoonotic Diseases

Hantaan virus (Haemorrhagic fever)

There is a group of Hantaviruses that has been detected in urban populations of

rodents in many parts of the world. The virus is passed from host to host via infected

saliva, urine and feces. Some strains have little effect on humans; others cause major

illnesses with a wide variety of symptoms (Aplin et al., 2003).

Tick typhus (Rickettsia conori)

The principal reservoir for this disease is the dog, but rodents are also important

reservoirs. The disease in human results from a bite from an infected tick. The tick

particularly involved in transmission is found throughout Asia (Aplin et al., 2003).

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Scrub typhus (Orientiatsu tsugamushi)

A variety of rodents throughout Asia are the principal reservoir for this disease,

which is transmitted by larval trombiculid mites called ‘chiggers’. Mortality rates in

humans are low if treatment is sought early. Murine typhus (Rickettsia typhi): reported

throughout Southeast Asia, this disease is spread by flea bites or contact with infected

feces or crushed fleas. The disease causes a wide range of symptoms in humans, but the

mortality rate is low (Aplin et al., 2003).

Leptospirosis

Caused by a variety of spirochetes, leptospirosis is one of the most prevalent

zoonotic diseases carried by rodents in rice fields. Almost all rodent species in Southeast

Asia can act as hosts. Human infection occurs when an open wound contact with water,

moist soil or vegetation contaminated by rat urine. The mortality rate is low for most

strains. The symptoms are similar to influenza and last from several days to three weeks.

Symptoms of leptospirosis can be confused with those of malaria and dengue fever, and

many cases are probably misdiagnosed. People working in rodent infested plantations or

fields are most at risk (Aplin et al., 2003).

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Rat bite fever (Spirillum minor)

Caused by a spirochaete, this disease is transmitted by rodent bites and is found

throughout the world. Incubation takes several weeks and symptoms usually appear after

the wound has healed (Aplin et al., 2003).

Plague (Yersinia pestis)

Bacterial disease that can be treated with antibiotics if diagnosed early. The cycle

of this disease is mammal to flea to mammal, with rodents as the primary host. Whilst

advances in medical science make it unlikely that plague will erupt again in global

pandemic, as it did on various occasions through history, it still presents a serious

healthproblem in many parts of the world. The last major epidemic of plague in Asia and

Australia occurred in the first decade of the 20th century (Aplin et al., 2003).

Salmonellosis

Salmonella bacteria infect humans worldwide, usually through ingestion of water

or food contaminated by feces of an infected animal but also through eating incorrectly

prepared foods. There are many strains with variable severity of impact (Aplin et al.,

2003).
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Toxoplasmosis

Caused by a coccidian Toxoplasmagondii, for which the domestic cat is the

primary host. Many other mammals, including rats and mice, may act as intermediate

hosts (Aplin et al., 2003).

Impact of Rodent Diseases in Humans

In the Philippines, the most commonly reported and frequently studied rat-borne

infection is leptospirosis. The symptoms are flu-like and can easily be mistaken and

neglected in the rural areas until serious clinical damage has occurred. If left untreated,

patients can develop kidney damage, meningitis, liver failure and respiratory distress

(Singleton et al., 2003). Moreover, rats are significant carriers of several human diseases

such as leptospirosis, typhus, and human plague, otherwise known as the “Black Death”

(Gratz, 1994).

Factors that Influence the Parasite Intensity and Prevalence

Host gender was considered to be one factor when it comes to parasite differences

in prevalence and intensity which has been reported in several studies (Zuk and McKean,

1996; Poulin, 1996; Hughes and Randolph, 2001; Tschirren et al., 2003; Ferrari et al.,

2004; Morand et al., 2004; Hoby et al., 2006; Matthee et al., 2010). Males and females

can constitute different environments for parasites. Factors like immune-competence,

mobility, body size; home range and dispersal rates differ between sexes and hence
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render male and female hosts different habitats for parasites with their own constraints

and characteristics. This may be attributable to the fact that male rodents were more

active and can travel significantly farther than females; making them more likely to infect

by parasites, their broad diet makes them adaptive to travel longer distances (Heaney et

al, 1999; Soliman et al, 2001b)