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Parasitic Bronchitis of Livestock in Japan

By HAKARU UENO

First Research Division, National Institute of Animal Health

From the viewpoint of livestock population ga1·bage in the dirty piggery on small farms. and economic damage, it can be said that the This might be due to the unclean environment major lungworm diseases of livestock in Japan produced by the utilization of garbage because ai·e substantially swine metastrongylosis and such environment is favorable for an increase bovine dictyocaulosis. in earthworms acting as intermediate hosts In Japan, lungworms of several species, for swine lungworms. which will be described below, cause parasitic On the other hand, the occurrence of bronchitis of animals, except swine and cattle. dictyocaulosis in calves is closely related to The combined infection of M etastrongylus climatic conditions, especially temperature, pudendotectus (Wostokov, 1905) and M. apri precipitation and humidity, and to the amount (Gmelin, 1790) is ve1·y common among wild of grass which is much influenced by these boars. conditions. Besides, the population density of Though several reports have been made on cattle has a great influence upon the severity the outbreak of dictyocaulosis caused by and spread of this disease in a herd. Dictyocaulus filaria (Rudolphi, 1809) among sheep, the sheep involved were exclusively Swine lungworm disease those imported from the United States or Australia into Japan. This is one of the most important diseases The parasitic with the small of the helminthic of piglets in lungworm, Muelle1·ius capillaris (Muller, 1889), Japan. Two species, M. civri and M. pudendo­ has rarely been recognized among sheep and tectus, have been known to be causal parasites goats. of this disease, but M. salmi (Gedoelst, 1923) Parasitic bronchitis in Cap-ricornis crisvus has . not been recorded. M. civ1'i is distributed (Temminck) , which is a natural monument, all over Japan but M. vuclendotectus is a less has recently been investigated owing to its important species which is distribtued locally. increased death rate among animals of this These two species induce a combined infection. species in which Protostrongylus sp., which Neither of them causes a single infection inde­ had not been reco1·ded in Japan, was detected pendently from each othe1·. from all the lungs examined. In general, the1·e is a direct or indirect Incidence relationship between feeding and management of livestock and the occunence of lungworm Statistics from slaughterhouses show that diseases. pigs were infected with this parasite at the The atomspheric temperature in Japan, rate of 60 to 70 per cent, and that the economic where such tempen,ture is quite variable by damage caused by this disease was very serious seasons, has no great influence on the occur­ up to about seven or eight years ago. Recently, rence of swine lungworm disease. In this this disease has been declining gradually in country, however, the frequency of occurrence severity owing to the technical improvement of this disease is rather high among pigs fed in pig enterprises, especially efficient manage- 236 JARQ Vol. 8, No. 4, l!l74 ment and the application of the very effective lus should be considered not only with the anthelmintic, tetramisole. The rate of infec­ direct pathogenicity of this parasite itself but tion of this disease is estimated to be about also with the symptoms of the combined in­ 20 to 30 percent at present. fection with this parasite and virus pneumonia (VP) 01· swine epizootic pneumonia (SEP). Life cycle and with the importance of transmission of swine influenza virus (SIV) . One species of earthworm, Eisenict f oetida, At present, nothing is known about worm­ is only one known intermediate host of toxin sec1·etecl by this parasite. Metastronyylus spp. in Japan. It is a common The pathogenicity of this pat·asite varies inhabitant in the porcine manure piled up with the number of parasites present. It is around the pigge1·y. When engorged by earth­ presented mainly as the functional insufficiency worms of this species, eggs of the pulmonary lobule and emphysema. The hatch in the body of the earthworms. After fo1·me1· is caused by the mechanical blockage the 1st and 2nd larval stages, 3rd-stage larvae in small and medium bronchi which control (infective la1·vae ) appear on the eighth to the function of lobules distributed in the tenth day after infection and are then har­ marginal parts of the lung. Piglets hal'boring bored by the earthworms. numerous parasites of this species are affected When a pig is expel'imentally fed earth­ with dyspnea and show retarded growth. worms harboring infective-stage larvae, it is MacKenzie ( 1963) s, t·eportecl that the com­ easily infected with lungworm disease. The bined infection of VP and Metastrongylus author has proved, however, that no pig is, caused severe and more extensive pneumonitis at least positively, fond of capturing earth­ than the single infection of either of the two wot·ms, though there may be a few chances agents. Shope (1941 ) 12 > and Kammer & Hanson for it to capture them. (1962)., suggested the possibility of this pa1·a­ As a result of their experimental study, site to be the carl'ier of SIV masking this Ueno et al. (1965) ,., revealed an interesting virus. biological phenomenon that infective larvae It is very intel'esting to study 'l'oxovla.sma ha1·bored in the alimentary tract of earth­ gondii in future since this pathogen may be wot·ms finally came out in the lumen of the transmitted by Metastl'ongylus parasites them­ tract, from piercing through the wall, and selves and theil' eggs and 3rd-stage larvae. were mixed with feces to be discharged from The author has some experience in this the body little by little. Encysted larvae show problem. When piglets were infected with 3rd­ a strong resistance to environmental sensiti­ stage larvae of Metastrongylus released from zation. They may be transmitted to pigs pepsinated earthwot·ms collected from a dil'ectly or by some mechanical intermediary. pigge1·y contaminated with Metastrongylus and Toxoplasma, most of them showed a Experimental typical symptom of toxoplasmosis unexpectedly. Intermediate host ------··-> Final host The sera of these infected piglets showed an (Earthworm) (Pig) ...... l' extraordinarily high antibody titer when ex­ Naturally discharged amined by the dye test. 3rd-stage larvae in feces or earthworm Natural Clinical symptoms and diagnosis Fig. 1. Mode or Metastrongylus infection in pigs When infected, adult pigs manifested no Pathogenicity specific clinical symptoms, except coughing, but piglets show frequent coughing, increment The pathogenicity of the genus Metastrongy- in respiration, and dyspnea after subjected 237 to a sudden fo!'ced movement. They gradually with 50,000 r, guinea pigs were conferred a become thin, suffel'ing from anemia. strong immunity against reinfection with the The exact diagnosis of this disease can be parasite. made when eggs of Metastrongylus are de­ tected from feces. Generally speaking, an Treatment and prophylaxis animal harbors much more parasites of this species than it is expected to do from the Tetramisole was developed by Thienpont 13 number of eggs detected from it. It may be et al. (1966) > as a wide-spectrum anthel­ considered that when a fecal sample contains mintic against parasites. It was 100 epg ( eggs per gram) , it is estimated reported to be a very effective agent against to keep 60 to 100 parasites. swine lungwo1·ms. After that, its efficacy was Though Metastrongylus eggs can be floated confirmed by Ueno et al. (1967) •~> and other on a solution saturated with sodium chloride workers. or sucrose, Bello (1961) •> found a saturated When a close of 7.5 to 10 mg/ kg of this MgS0,1 solution to be most suitable for this compound is administered to infected piglets, purpose. it is so effective as to remove nearly completely An ecological diagnosis is made to know the lungwol'ms of all the stages covering from extent of infestation with swine lungworms seven-day-old larvae to adult worms. on a given hog farm. It is made by detecting It is the most effective mode of adminis­ developing-stage larvae of lungworms from t1·ation of this agent to mix the agent with the body of intermediate hosts collected around feed. There is no significant difference in the piggery. In this method, such part of the efficiency between subcutaneous and intramus­ earthworm body as called "the heart" is ex­ cular injection. posed anatomically in the 10th to 12th segment In a few minutes after the administration of the earthwo1·m. It is solely disposed between of this compound, the pig being to suffer two pieces of sli de glass to be pressed and from transitory coughing and its l'espiration examined for the existence of larvae under increases in rate for a while. There is a trend the microscope at a low-power magnification. that the larger the number of swine lungworms harbored by a pig, the more frequently these Immunity symptoms appear in the pig. It is rather difficult to contl'OI swine lung­ It has been proved by the hemoagglutination worm infection. Establishment and practice test and CF test that antibody exists in the of a control program of swine lungworm infec­ sera of pigs inf ected with swine lungworms. tion are dependent on the rearing environment Some pigs were exposed to reinfection after of swine. they had been freed from infection with swine The economic loss caused by tbis infection lungworms by some anthelmintic treatment will be blocked at a minimum level if sufficient and allowed to stand for about three weeks. attention is paid to the following points: Others were inoculated subcutaneously or (1) An effective anthelmintic must be applied intramuscularly with the physiological saline periodically not only to piglets but also to emulsion of adult lungworms. No immunity, fu ll-grown pigs in a piggery contaminated however, was produced in any pig of either with the parasite. (2 ) No manure heap is group to prevent it from reinfection with this made around the piggery. (3) Ditches around parasite. the piggery must be drained well and kept 91 10 On the other hand, Onishi ( 1968 , 1973 >) always clean to prevent feces from being reported that when inoculated perorally 01· scattered. parenterally with 3rd-stage larvae of Meta­ strongylus partially inactivated by inadiation 238 J ARQ Vol. 8, No. 4, 1974

Bovine parasitic bronchitis Life cycle (Bovine dictyocaulosis) D. vivivarus is parnsi tic to the trachea and This disease is caused by the infection of bronchi of cattle and deposits embryonated Dictyocaulus vivivarus. It is commonly called eggs in these organs. These eggs come up by "husk" or "hoose" and is a serious parnsi tic coughing and are swallowed. They pass disease which is usually fo und among calves through the alimentary trnct of cattle and in many European countries. hatch out to be first-stage larvae, which are It is well known that when infected once discharged with the excretion of feces on the with this parasite spontaneously or experi­ pasture ground. These larvae grow into infec­ mentally in the field, cattle can acquire a tive (3rd-stage) larvae in four or five days, strong resistance to the reinfection. On the and infect cattle when ingested with grass. basis of this fact, a unique vaccine has been Infective larvae are so resistant to environ­ developed in the domain of . mental conditions, especially cold weather, that they can live over winter even in the northern Incidence part of the J apanesc mainland and in Hokkaido. First-stage larvae, however, a1·e so sensitive Although bovine parasitic bronchitis has to environmental conditions that only ten per­ occurred in several pastures in Japan, the cent of them can reach the 3rd stage, or become substantial damage of cattle is rather small infective larvae. because major yearling calves are kept in The migratory course of this parasite inside cowsheds. the body of the host animal was reported in Even if yearling calves are placed in the detail by Jarrett et al. (1957) 3 >, Poynter et al. pasture, the pasturing period is limited to (1960) "), and Douvres & Lucker (1958) •> in a few months. Recently, however, the conven­ cattle 0 1· guinea pigs. tional manner of rearing has been transformed When ingested by cattle with grass, infec­ into pasturing. The establishment of a large­ tive larvae take off their sheath, pass through scale pasture and the expansion of the existing the wall of the small intestine and the pasture have been encournged. mesenteric lymph node to the lymph vessel, Consequently, several pastures have already and attain the lung at the end of 24 hours been contaminated by the etiological parasite after infection. spread by yeal'ling calves infected subclinically The prepatent period of this parasite is with the parasite (carriers) and introduced about 25 to 27 clays. The largest number of from a pasture contaminated with the parasite 1st-stage larvae appears about 85 days after into a newly established pasture. the infection. Then the larvae in feces begin It is possible to recognize the pattern of to decrease graduall y in number, reaching a outbreak of this disease in the field ; that is, minimum around the 45th to 50th day after clinical symptoms usuall y appear over a period the infection. from late su mmer to early autumn and usuall y Most of the parasites in the lung disappear disappear within two or three months. within two months, when no reinfection occurs In numerous pastures where no effective successively. countermeasures have been taken immediately after the occurrence of this diseases, about Pathog-enicity 30 to 47 per cent of calves have died suffering from husk, and the growth of surviving calves Since D. vivi1)arus is more strongly patho­ has been retarded distinctly to cause great genic than any other helminth, it causes an economic damage. infection in a herd of cattle which may result 239

in an epizootic, bring about a high fatality, Since these symptoms are manifested in the and affect weight gain seriously. case of this disease, it is not always difficult In a newly infected calf, the tissue reaction to make a clinical diagnosis of the disease. of the lung to this parasite begins to appear The most correct diagnosis may be made when about ten days a.fter the infection. As one 1st-stage larvae are detected from feces. It of the specific pathological changes of this is widely utilized for this purpose to isolate reaction in its initial stage, alveloar collapse 1st-stage larvae by means of the Bermann's mostly occurs in the diaphragmatic lobe. apparatus. Infiltration with eosinophils, macrophages and Ueno (1968 a & b) ••>."> established the fol­ giant cells can be recognized as a histopath­ lowing technique to make the detection of ological change. 1st-stage larvae easy by using no special With the progress of the disease, a distinct equipment in the field. contraction is seen between a normal and a (1) A 3 g fecal sample is put on a piece consolidated pulmonary lobule. Such contracted of gauze ( I OxI O cm) . area spreads to the anterior part of the lung. (2) The four corners of this piece of gauze Dull plum-colored irregular areas of consoli­ are gathered to one point which is drawn up. dation appear in the apical lobe most conspicu­ (3) With the gathered comers held up­ ously and in the intermediate lobe to a lesser ward, the sample wrnpped with the piece of extent. A violent cellular response also occurs gauze is put into a pointed centrifuge tube in them. about 50 ml in capacity. In the second-half stage of disease, or ( 4) The gathered corners are fixed at the classical husk pneumonia, the features of opening edge of the tube, into which faucet edema and emphysema can be observed micro­ water is poured. All the tubes are allowed to scopica.Ily. These pathological lesions exist stand overnight 01· for 24 hours to make larvae for a fairly long time, even after the removal migrate into the water and settle at the bottom of this parasite. of the tube. Although the cause of fog fever is yet un­ (5) The sediment is collected by the aid known, the fever may be an allergic reaction of a pipette, the tip of which has a relatively induced under a singular immunological condi­ large oepning. tion between this parasite and cattle. (6) The pipetted sediment is dropped on There has been a cattle disease of unknown a slide glass for microscopic examination at a etiology called "kiri yoi" (fog inebriation) low-power magnification. in the mountainous Chubu region of Japan (7) The number of larvae per gram of contaminated with the infestation of D . vivi­ feces (LPG) can be determined by dividing parus. The symptoms of this disease agree the number of detected larvae by three. well with those of fog fever clinically and immunologically. Immunity and X-in-adiated larval vaccine Clinical symptoms and diagnosis It has been proved by many researchers that A calf suffering from this disease breathes a moderate infection caused in calves by the forcedly through the mouth, with the head ex­ significant attack of this parasite or by experi­ tended. It is obliged to continue respiration mental inoculation with a controlled number with an extremely hard effort. Therefore, it of infective larvae results in an acquisition cannot afford to any other activity, such as of solid immunity against reinfection. feeding. Moreover, it is almost impossible for Jarrett et al. (1958, 1959, 1960) •>.s>.o > of the animal to eat, respiratory count often ex­ Glasgow University made an attempt to ceeding the pulse rate. develop an X-itTacliated larval vaccine on the 240 JARQ Vol. 8, No. 4, 1974 basis of this fact. The vaccine is utilized bovine dictyocaulosis may be reduced lo the practically at present. It contains larvae minimum thl'oughout the pasturing period. partially inactivated by inadiation with X-rays at 40 KR, and is given orally twice at References a two-week interval before the pasturing of calves. Calves administered with this vaccine 1) Bello, T . R.: Comparison of the fl otation suffer from mild dictyocaulosis, which confers of Metastrong-ylus and Ascaris eggs in 3 them immunity to the probable succeeding different leviation solution. A mer. J. Vet. Res. 22, 597-600 (1961) . infection. 2) Douvres, F. W. & Lucker, J. T. : The T he disadvantages of this vaccine in field morphogenesis of the parasitics stages of use are the early expiration date, necessity of the cattle lungworm, Dictyocault1s vivi1,cirus, double vaccination, and difficulty in the mainte­ in cxpcl'imentally infected p;uinca pigs. nance of its activity during transportation. .J. L'arasit. 11 4, 28-29 (1958) . 3) J an·ett, W. F. H. et al.: The pathology of Many problems may have to be solved, there­ experimental bovine bronchitis. ./. Pcithol. fore, before the vaccine is applied pl'actically !Jcicteriol. 73, 183-193 (1957). in the field, except in fairly well Ol'gan ized 4) Jal'l'Ctt, W. F . H. et al. : A fi eld trial of regions. pa!'asitic bronchitis vaccine. V el. llec. 70, 451-454 (1958) . 5) Jal'rett, W. F. H. ct al.: Immunological Treatment and prophylaxis studies on Dictyocaulus vivi7>cw11s infection calves-double vaccination with itTadiatccirus infection, however, is rather li mited because of the dis­ l mmunity J)l'oduced by the administration advantages mentioned above. As effective or inadiatccl larvae. hnmmwloyy 3, 145- 151 anthelmintics against swine lungwol'ms, ( 1960) . diethylcarbamazine, cyanacethydrazide, as­ 7) Kammer, H. & Hanson, R. P .: Studies on the transmission of swine influcn;m vil'us caridole-santonin aerosol and methylridine with Metastrongylus species in specific have been reported so fat· by many reseal'chers. pathogens-free swine. J. Infect. Dis. 110, Practically, they do not always bl'ing about 99-102 (1962) . satisfactory resu Its. 8) MacKenzie, A.: Experimental observations Tetramisole is also very effective against on lungworm infection together with virus pneumonia in pigs. Vet. Rec. 75, 114- 115 bovine Dictyocaulus, showing a mal'ked efficacy (1963) . in the extermination of swine lungworms. In 9) Onishi, T.: Immunological studies on Japan, the field application of this compound M etastronyylus ci1wi infection. I. Immuniz­ has been studied not on ly to eliminate the ing activity produced by the administration parasite in the lung but also to confer acquired of X-irl'adiatecl larvae to guinea pigs. Jav. ./. Pcirnsi.tol. 6, 516- 524 (1968). immunity to calves exposed to natural in­ JO) On ishi, T.: Immunologica l studies on M elci­ fection. slronyyhri infection. II. Immunizing Although no conclusion has yet been drawn activity of various oral dosages of la l'val from these studies, the following l'ecommen­ vaccine between oral and subcutaneous in­ oculation. Jci7>. J. Vet. Sci. 35, 507-513 clation may be made under the actual pastul'ing (1973) . conditions of yearling calves in Japan: 11) Poynter, R. ct al.: Recent cxpel'iences with Calves should be administered with tetra vaccination. Vet. Rec. 72, 1078- 1090 (1960). misole twice at a 40-day interval after the l 2) Shope, R. E.: The swine lungworm as a initial administration, which is performed one rcsel'vation and intermecliale host fol' swine influenza virus. II. The transmission of week after the recognition of an outbreak of swine influenza virus by the swine lung­ this infection. By this step the damage of worm. J. Exv. Mell. 711, 49- 68 (L94l). 241

13) Thienpont, D. et al.: Tetramisole (R 8299) . Quart. 7, 65-73 (1967). A new potent broad spectrum anthelmintic. 16) Ueno, H.: A simple method for detection of Nat?we 209, 1084-1086 (1966) . first-stag·e larvae of Dictyocaiilus vivi7)arus 14) Ueno, H. et al.: Spontaneous liberation of from feces. I. Procedure and fundamental infective larvae from the earthworm, Eisenia tests. J. Jap. Vet. Med. Ass. 21 , 210- 213 . foetida, infected with Metast1·ongylus a7n•i. (1968") . Nett. Inst. Anim. Hlth Qua1·t. 6, 89-100 17) Ueno, H.: A simple method for detection (1966). of first-stage larvae of Dictyocau.lus vivi­ 15) Ueno, H. et al.: Anthelmintic evaluation of pan,s from feces. II. Comparison with other tetramisole against the swine lungworm, methods and field application. J. Jap. Vet. Me/,astrongylus apri. Nat. Inst. Anim. Hlth Mecl. Ass. 21, 255-259 (1968b).