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Veterinary diseases review for mainland Japan, 2000-2010.

Zoonotic diseases and parasites infect animals and circulate in animal populations. They do not require a human host. Many debilitating and occasionally fatal zoonotic diseases are newly recognized threats to humans. Veterinary data are often unavailable for public health professionals, and their surveillance systems do not capture data from veterinary clinics. However, veterinary practitioners can report zoonotic pathogens to public health officials. Veterinarians are part of the first line of defense and detection (1) for many human pathogens. Veterinary facilities can provide potentially lifesaving data on the prevalence and local transmission of pathogens. They also give guidance and training to pet owners or public health officials on zoonotic diseases and risk management.

As an initial step in improving the surveillance of zoonotic diseases for US military bases in Japan, we conducted a physical audit and data analysis of all animal records at the US military veterinary care facilities in mainland Japan. The following report focuses on the major parasitic agents likely to infect humans or cause disease in military working dogs (MWDs). Veterinary clinic reviews could be useful for civilian public health organizations in monitoring zoonotic diseases.

METHODS

Military veterinary clinics in Japan maintain paper records on animals that were owned by both military personnel and civilians. Almost all animals that enter the country with incoming personnel are initially quarantined and examined by military veterinarians. We visited the veterinary care facilities at Camp Zama, Marine Corps Air Station (MCAS) Iwakuni, US Fleet Activities Sasebo, Misawa Air Base, Yokota Air Base, and Yokosuka Naval Base and manually reviewed more than 5,400 animal medical files to capture all reports of parasitic or pathogen activity reported in the last 10 years (2000 to 2010). Paper records were entered

into an electronic database, and each animal was given a unique identification number not tied to personal clinical records. Each record included species, animal name, arrival date, examination dates, and working dog status. All reports of parasites or infectious diseases were annotated in the computer database with the date the animal presented at the clinic.

The database was organized by military base. The US military bases in Japan with veterinary clinics include Camp Zama, Yokota Air Base, and Yokosuka Naval Base in the Kanto Plain region near the Tokyo metropolitan area. The veterinary clinics on these bases also serve neighboring military facilities without clinics. These include base housing areas, Atsugi Naval Air Station, Yokohama North Dock, Sagamihara Army Depot, and the US Embassy in Tokyo. Misawa Air Base is in Aomori Prefecture, one of the northernmost prefectures on Honshu Island. MCAS Iwakuni is located in southwestern Honshu in Yamaguchi Prefecture. US Fleet Activities Sasebo is in Nagasaki Prefecture on the southern island of Kyushu. Kadena Air Base on the island of Okinawa has a large veterinary facility that supports numerous military bases in Okinawa Prefecture. We did not review the records from Okinawa.

Data was analyzed using SAS version 9.1 (SAS Institute Inc, Cary, NC). Temporal analysis was not possible due to insufficient date denominator data, ie, when an animal tested negative, only year was available, not month. The frequency of positive test results by location and host was investigated.

RESULTS AND DISCUSSION

A total of 5,418 animals, predominately dogs and cats, were included in the database during the 10-year period for which data are available. Animals were tested 16,764 times. There were 91 unique working dogs.

The review focused on internal parasites and pathogens. While some external parasites such as fleas, mites, and ticks are potential vectors of zoonotic diseases, we do not discuss them. The majority of animals were cats and dogs, and results are summarized in Tables 1 and 2. The majority of parasites were unidentified worms followed by "Coccidia" (Figure 1).

Protozoons

Protozoan parasites are diverse and range from intestinal parasites with simple, direct life cycles to vectorborne agents that undergo complex life cycles. Parasitic protozoons cause some of the most significant zoonotic diseases worldwide. Several parasitic protozoons were reported from animals at the military veterinary clinics.

There are case reports of 2 dogs at the Camp Zama veterinary clinic infected with Leishmania infantum Nicolle, a visceral leishmania species. (2) The presence of L. infantum in military pets recently imported from southern Europe was not surprising but could be politically sensitive if a foreign disease were introduced into Japan.

A review of the published literature on the phlebotomine sand flies in Japan revealed that they do not feed on mammals. (3)

Numerous gastrointestinal protozoan parasites were reported from animals. For example, Giardia lamblia was detected by fecal flotation or with ELISA SNAP tests (IDEXX Laboratories, Ontario, Canada) from both cats and dogs. Giardia lamblia (Stiles) is one of the more common zoonotic protozoa and has a relatively stable encysted stage that remains infectious in water or wet soil. (4) Both acute and cryptic cases occur in humans and animals. The taxonomy of Giardia spp is somewhat convoluted, with a variety of serotypes recognized. (4,5) Not all serotypes cause clinical illness in humans, and they are indistinguishable in fecal flotations. G. lambia was the most frequently reported parasite of MWDs. The infected MWDs were from Misawa Air Base and Camp Zama. The reservoir of the infections remains an unknown potential threat to human health. In addition to dogs and cats, several fecal samples from water birds on Camp Zama were tested for G. lamblia, but all were negative.

Coccidia, gastrointestinal protozoa, were reported in 18 animals including dogs, cats, a rabbit, and a military working dog from Camp Zama. Unfortunately, the term coccidia is inclusive of many parasitic protozoa. Based on conversations with veterinary staff, some coccidia were Isospora spp. One sample was positively identified as an Isospora sp from a dog at Misawa Air Base. In general, Isospora spp do not infect humans. However, several other parasitic protozoa such as Cryptosporidium spp and Toxoplasma gondii (Nicolle and Manceaux) might be mistaken as a "coccidia." One of the animals with coccidia was a cat, which could shed T. gondii. Toxoplasma gondii was detected by the veterinary staff in some animals from a petting zoo adjacent to Camp Zama (unpublished data).

A dog in Sasebo was reported to harbor Cryptosporidium canis Fayer, Trout, Xiao, Morgan, Lai, and Dubey. This gastrointestinal protozoon has a wide distribution throughout the world, (6) including Japan. Like other species of Cryptosporidium, an infected animal can present with diarrhea. This parasite has some zoonotic potential, but the taxonomy of Cryptosporidium is unclear and humans are not susceptible to all species. (7)

Nematodes

Nematodes are some of the most diverse and common parasites throughout the world. These worms range from commensal internal associates, to near-mutualists, to blood-sucking and life-threatening parasites. Numerous nematodes from veterinary clinics were identified as "worms" and nematodes. Based on interviews with the veterinary staff, most of these nematodes were ascarids.

The veterinary clinics captured data on one species of filarial nematode, Dirofilaria immitis (Leidy) (heartworm). Both pet owners and veterinarians are aware of the risks of heartworm disease. This explains the frequent sampling and subsequent detection of this parasite. Dirofilaria immitis is transmitted by mosquitoes and vector populations on most installations, and are significant during the summer and fall. (8) Stray dogs are rare on most installations, however, wild tanuki (Nyctereutes procyonoides viverrinus Temminck) (Figure 2) are susceptible to D. immitis (9) and live on bases. The zoonotic risk of D. immitis is low, as most human infections do not progress. However, larvae can die in the lungs and superficially resemble tuberculosis or cancer. (10) Heartworm was the most commonly reported parasite of dogs seen at US military veterinary care facilities in mainland Japan. A single feline case was reported from Yokosuka. There were no infections in MWDs, but they are regularly treated with preventive drugs.

The primary diagnostic tests for heartworm are serologic and detect adult antigens. Identification of microfilaria in blood smears was rare, however, blood smears were performed on some animals. Microscopic examination of blood smears will detect other filarial nematodes, Babesia, etc. There are several species of Dirofilaria in wildlife, and animals from Europe pose the risk of arriving with Dirofilaria repens (Railliet and Henry). The serologic ELISA SNAP tests (IDEXX Laboratories, Ontario, Canada) for heartworm will not detect infections with species other than D. immitis.

There were numerous other species of parasitic worms that develop in the gastrointestinal tracts of animals. Unfortunately, the majority of records on parasitic worms were recorded as nematodes or worms. Poorly identified parasites and recordkeeping present a consistent problem in veterinary data from clinics. Interviews with the veterinary staff allowed some to be identified, but incomplete data reduce the value of veterinary clinics in disease surveillance. We summarize the worms that were identified to at least the genus level.

A dog at the Sasebo clinic was diagnosed with Strongyloides stercoralis (Bavay), presumably during a fecal analysis. Strongyloidiasis was found throughout Japan, and recent data indicate it can be locally common. (11) Strongyloides stercoralis, a zoonotic nematode, readily infects humans and companion animals, causing strongyloidiasis. (12) There are several morphologically similar species of Strongyloides in dogs and cats. Humans and companion animals are generally infected when nematode larvae in the soil pierce their skin, invade the circulatory system, and move into the body. However, S. stercoralis can autoinfect or reinfect a host. (13)

Eggs of unidentified hookworms were occasionally reported from dogs at Camp Zama but not other veterinary clinics. This probably represents a sampling anomaly or variation in the diagnostic abilities of the veterinary staff. Larval hookworms are infectious as free-living worms in the soil. They have a life cycle similar to that of S. stercoralis and can penetrate the skin of humans and dogs. Humans are accidental hosts to these worms. In humans, the larval worms usually die near the point of exposure, but occasionally the migration tract of the larval worm becomes infected and inflamed. (14) The resulting cutaneous larval migrans (usually from Ancylostoma sp) may last weeks to months and at times causes intense itching, but the condition is self-limiting.

Both wildlife and cats harbored hookworms. Some tanuki on base were infected with Ancylostoma kusimaense Nagayosi or a related species. Two were removed from the intestine of a dead tanuki on Camp Zama. These worms are reported to infect domestic dogs. (15) A cat from Yokota harbored hookworms. Based on a review of the Japanese parasitological literature, this worm was most likely Ancylostoma tubaeforme (Zeder), which is the primary hookworm of domestic cats reported near this region of Japan. (16) Exotic worms could be introduced in pets, but local acquisition of A. tubaeforme is probable. Symptoms from infestations with A. tubaeforme can range from asymptomatic to a serious disease in cats.

Trichuris vulpis (Froelich) is a whipworm of canids. It infects the intestine, but in humans and aberrant hosts it can infect other organs. (17) Human infections are rare. (17) Adult worms can live for years if an animal is untreated, although most animals with low level infestations are asymptomatic. Heavy infestations can cause rectal prolapse or bloody diarrhea. Eggs are shed in the feces and are somewhat environmentally resistant and remain infectious in the soil, allowing reinfection. (18) They resemble the eggs of most other whipworms and could be misidentified. Eggs from T. vulpis were discovered in 3 dogs in the last 10 years, one each at Yokosuka, Iwakuni, and Zama veterinary facilities. The one dog at Camp Zama was repeatedly seen at the clinic for over 8 months in 2008 and continued to be actively infected despite repeated treatments.

Dog and cat roundworms (Toxocara canis (Werner)/T. cati (Zeder)) were occasionally reported in fecal samples. In addition, numerous unidentified nematodes from the clinics were probably Toxocara spp. Both dog and cat roundworms are mildly zoonotic geohelminths. (19) The eggs are environmentally stable and infectious in soil contaminated by animal feces. (18) When the eggs are consumed, the infectious larvae invade host tissues and can cause visceral larval migrans. (19) In rare cases, visceral larval migrans is fatal. (19)

Toxascaris leonina (von Linstow) was reported from 2 cats at the Sasebo and Iwakuni veterinary facilities. The adult worms live in the intestine like other ascarids. Eggs are shed in the feces and are infectious to cats. (20) This worm is not a zoonotic parasite, but it can infect dogs. (20)

In addition to the Toxocara species found in domestic animals, there are numerous species in wildlife. Several feral animals were necropsied at veterinary clinics. Two adult T. tanuki Yarnaguti were removed during the necropsy of a dead tanuki on Camp Zama. Exotic North American raccoons live on base, and these animals can harbor other ascarids.

The feline lungworm, Aelurostrongylus abstrusus (Railliet), was reported from 2 cats from the same household at MCAS Iwakuni. Lungworms have a wide geographic range and occur in up to 22% of cats in some surveys. (21) Many cats are asymptomatic when infected. These worms are not a zoonotic threat.

One rather cryptic handwritten note in a record of a military working dog at Camp Zama seems to imply that there were worm eggs in the urine. The notes were not complete and cannot be fully interpreted. The only worms likely to infect the bladder are Capillaria or Dioctophyma spp. (22,23) The notes later mention the presence of tapeworm proglottids in the same urine sample. The urine sample was probably contaminated with fecal material or with tapeworm proglottids that crawled into the wrong orifice as they moved out of the anus. Yet, based on the incomplete data, there was no way to rule out Capillaria or Dioctophyma spp.

Cestodes and Trematodes

Like nematodes, flatworms are some of the most diverse and commonly reported endoparasites of domestic animals. There are 2 primary groups of parasitic flatworms: the flukes (trematodes) and tapeworms (cestodes). The eggs of most parasitic species are shed in the host's feces. These are often detected by fecal flotation and microscopy. Unfortunately, for surveillance purposes, the eggs of most flukes do not float on the frequently used solutions, but tapeworm and nematodes eggs do. There were no reports of trematodes in any animals despite the fact that the intermediate host snails and crustaceans live on several bases.

Although tapeworms were reported at every clinic, the vast majority (85%) of them were not identified. Molecular techniques or serologic techniques are required for some identifications. At least 65 animals were diagnosed with unidentified "tapeworms." The majority were from dogs, however, some cats were infected. One case was noted in a military working dog from Camp Zama. Based on additional information from the veterinary staff, many of the infections were Dipylidium caninum (Linnaeus), the dog tapeworm.

The most significant tapeworm of public health concern in Japan is Echinococcus multilocularis (24) This worm is known to infect dogs in northern Japan, with sporadic cases in the Tokyo area. (25) Unlike the majority of the detected zoonotic parasites which are mildly debilitating and not life threatening, an infection with E. multilocularis is likely to be fatal. (26) The eggs of E. multilocularis are almost impossible to differentiate from Taenia spp. (27)

The similarity between Taenia and Echinococcus was a problem when a dog from Misawa was reported to shed eggs from a Taenia sp. However, the eggs are morphologically identical to E. multilocularis (Leuckart). (27) Echinococcus multilocularis was reported from pet dogs in the Tokyo area in 2005 and 2009 and is regularly reported in Hokkaido near Misawa AB. (25) A 2009 survey of endoparasites in dogs and cats in Saitama, Japan, indicated that E. multilocularis could be as common as D. caninum in some pet populations. (16) Identification and treatment of E. multilocularis in dogs are critical for the prevention of hydatid disease in humans. People are infected with larval tapeworms when they accidentally consume the eggs (26) by allowing their dogs to lick their face, which is a route of exposure. The lack of identification of tapeworms in animal feces is a failure to protect the public's health.

Two additional species of zoonotic tapeworms were identified from dogs. A dog from Yokota Air Base was positive for Diphyllobothrium latum (Linnaeus) in a fecal float. D. latum, the broad fish tapeworm, is one of the best studied and broadly distributed species in the genus throughout Asia. (28) These tapeworms use fish as intermediate hosts and infect fish-eating mammals. Based on published surveillance, humans in Japan are infested with D. latum from eating fish. (29) Dogs are susceptible to this worm if they eat raw fish. This tapeworm does not cause major diseases in dogs. However, it can cause serious anemia in some humans, and the detection of the worm indicates infected fish were available to the pet. Sushi is a popular food in Japan and could be the source of the parasite.

One of the most frequently reported tapeworms was D. caninum, the double-pored dog tapeworm. It is a zoonotic parasite transmitted by arthropods (30) but rarely is a serious problem. Tapeworm larvae develop in invertebrates and are not a health threat. Humans are susceptible to infection if they eat infected lice or fleas. Young children are most likely to be infected when playing with infected animals. (31) Dog tapeworms were reported from dogs and cats at almost all installations. In addition, a large proportion of the unidentified tapeworms were probably D. caninum.

Veterinary clinics maintain records on zoonotic diseases and parasites. Our review of veterinary data indicates that there is a wide range of zoonotic parasites and pathogens circulating in the environment on military bases. This information is helpful for public health officials and could serve as a model for civilian public health agencies to determine which threats are present.

ACKNOWLEDGMENTS

We thank the veterinary staff at the veterinary care facilities for their assistance with record reviews and SGT D. Lewis, SGT C. Utter, and Mrs J. Spencer for assistance with record reviews and database management. A portion of this research was supported by the Global Emerging Infections Surveillance and Response System Operations Division of the Armed Forces Health Surveillance Center. The views expressed in this article are those of the authors and do not reflect the official policy or position of the Department of the Air Force, the Department of the Army, the Department of Defense, or the US Government. This research was supported in part by an appointment to the Postgraduate Research Participation Program at the US Air Force School of Aerospace Medicine administered by the Oak Ridge Institute for Science and Education through an interagency agreement between the US Department of Energy and the School of Aerospace Medicine. Distribution A: Approved for public release; distribution is unlimited. Case Number: 88ABW-2012-2210.

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Will K. Reeves, PhD

MAJ Kimberly Yore, VC, USA

MAJ Robert Paul, VC, USA

Laurel Lloyd, MPH

Dr Reeves is an Entomologist with the Epidemiology Consult Service, US Air Force School of Aerospace Medicine, Wright-Patterson Air Force Base, Ohio.

MAJ Yore is a graduate student at Colorado State University, Fort Collins, Colorado.

MAJ Paul is a Preventive Medicine Instructor, US Army Public Health Command District - Fort Belvoir, Virginia.

Ms Lloyd is an Oak Ridge Institute for Science and Education Fellow at the Epidemiology Consult Service, US Air Force School of Aerospace Medicine, Wright-Patterson Air Force Base, Ohio.

Table 1. Positive results in dogs from all mainland military
veterinary clinics in Japan 2000-2010.

                                       Location

Parasite                     Zama                   Sasebo

Nematode

Dirofilaria immitis          13                      6
Trichuris vulpis              1 *                   --
Toxocara spp                  3                      2
Nematode (no further ID)     --                      7 ([dagger])
Strongyloides stercoralis    --                      1
Aelurostrongylus abstrusus   --                     --
Capillaria/Dioctophyma sp     1 ([double dagger])   --
Hookworm                      5                     --

Tapeworm

Unidentified tapeworm         2                      3
Dipylidium caninum            2                      1
Taneia sp                    --                     --
Diphyllobothrium latum       --                     --
Protozoa                     --                     --
Giardia                       4 **                  --
Coccidia                      5 **                  --
Cryptosporidium canis        --                      1
Isospora                     --                     --

                                           Location

Parasite                     Iwakuni   Misawa    Yokota    Yokosuka

Nematode

Dirofilaria immitis             6        17         3          8
Trichuris vulpis                1        --        --          1
Toxocara spp                   --         8        --         --
Nematode (no further ID)       --        --         5          1
Strongyloides stercoralis      --        --        --         --
Aelurostrongylus abstrusus     --        --        --         --
Capillaria/Dioctophyma sp      --        --        --         --
Hookworm                       --        --         1         --

Tapeworm

Unidentified tapeworm           3         6         3         15
Dipylidium caninum              1        --        --         --
Taneia sp                      --         1        --         --
Diphyllobothrium latum         --        --         1         --

Protozoa                       --        --        --         --

Giardia                         2        --        --          3
Coccidia                        1         2        --         --
Cryptosporidium canis          --        --        --         --
Isospora                       --         1        --         --

* Tested positive 4 times.

([dagger]) Two military working dogs included in the total.

([double dagger]) Military working dog.

 ** One military working dog included in the total.

Table 2. Positive results in cats from all mainland military
veterinary clinics in Japan 2000-2010.

                                         Location

Parasite                       Zama       Sasebo      Iwakuni

Nematode

Dirofilaria immitis             --          --          --
Toxocara spp                    --          --          --
Nematode (no further ID)        --           7          --
Aelurostrongylus abstrusus      --          --           2
Hookworm                        --          --          --
Toxascaris leonina              --           1           1

Tapeworm

Tapeworm                         1           5           2
Dipylidium caninum               2           1          --

Protozoa

Giardia                          2          --          --
Coccidia                         2          --          --

                                         Location

Parasite                      Misawa      Yokota     Yokosuka

Nematode

Dirofilaria immitis             --          --           1
Toxocara spp                     1          --          --
Nematode (no further ID)        --           5           1
Aelurostrongylus abstrusus      --          --          --
Hookworm                        --           1          --
Toxascaris leonina              --          --          --

Tapeworm

Tapeworm                         9           7           9
Dipylidium caninum               3          --          --

Protozoa

Giardia                         --          --          --
Coccidia                         2           2           2

Figure 1. The overall percentage each taxon contributed to the sum
of all pathogens reported by veterinary clinics of US military
bases in Japan from 2000 to 2010.

Coccidia                  (8.0%)
Unidentified Nematode     (8.0%)
Dirofilaria immitis       (26.3%)
Unidentified Tapeworms    (30.5%)
Dipylidium caniunum       (5.2%)
Ascaridae                 (7.5%)
Unidentified Hookworms    (2.8%)
Giardia                   (6.6%)
Other Worms               (5.2%%)

Note: Table made from pie chart.
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Author:Reeves, Will K.; Yore, Kimberly; Paul, Robert; Lloyd, Laurel
Publication:U.S. Army Medical Department Journal
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Date:Jan 1, 2013
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