An Abattoir Survey of Cattle Liver Infections with Fasciola Hepatica

Brit. vet. J. (1966),122,489

AN ABATTOIR SURVEY OF CATTLE LIVER INFECTIONS vVITH FASCIOLA HEPATICA By

J.

G. Ross

Veterinary Research Division, The Farm, Stormont, Belfast SUMMARY

An abattoir survey of fascioliasis in cattle livers is presented in which goo livers were examined over a 12-month period. Over 80 per cent of the livers were found to be infected. Immature infections were found from June to April with peak levels between October and December. The highest adult burdens were observed between January and March when roo to 200 flukes were present. Very high level adult infections were never seen and outside the peak period the mean adult burden was less than 50. The results are discussed and it is proposed that the optimum time for routine anthelmintic treatment of cattle is in the early months of the year. INTRODUCTION

It has long been recognized that cattle exhibit a degree of resistance to infection with Fasciola hepatica as compared to sheep and that acute fascioliasis is rare in this host (Taylor, 1949). Recent investigations of experimental infections in cattle have demonstrated the occurrence of inhibition of immature parasites in the parenchyma with increasing levels of infection and with challenge infections (Ross, 1965, 1966a). It was also demonstrated that a reduced take resulted in challenge infections and under certain circumstances that an "acquired self cure" of the primary infection resulted (Ross, 1966a, b). With high level metacercariae infections the numbers of flukes developing were reduced markedly and very few reached patency in the bile ducts (Ross, 1965). It was concluded from these investigations that while heavy metacercariae infections in cattle may produce decreased weight gains (Sazanov, 1961), the resistance mechanism demonstrated would render the probability of large numbers of mature flukes being present in the bile ducts of cattle unlikely and make the occurrence of a clinical anaemia rare, except in a very particular pattern and level of infection. In previous experimental infections it was shown that developing flukes produce consistent macroscopic lesions in the liver in cattle (Ross, Todd & Dow, 1966). Between the third and sixth week post-infection a red superficial tract is produced and from the seventh to ninth week localized red haemorrhagic plaque lesions develop. This results from localization of the parasite prior to entry to the bile ducts and it is in these plaque lesions, late haemorrhagic plaques, that flukes may become inhibited and eventually eliminated. On entry to the bile ducts, fibrosis of the duct wall and acinar hyperplasia results

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with recognizable calcification in the wall by the nineteenth week. Around the eighth week, small superficial haematoma lesions were observed and fine fibrinous strands were present on the parietal surface of the liver capsule. These lesions, together with red tracts, were evidence of recent infection. Inhibited flukes were found to survive in plaque lesions in the parenchyma for as long as one year and are not, therefore, necessarily indicative of recent infection. The above lesions have been used as a criteria of time and stage of infection in the present survey. Histological sections of lesions were examined at regular intervals to check on the validity of the criteria of assessment. MATERIALS AND METHODS

Examinations were made at two-weekly intervals of the bovine livers at the Belfast Abattoir over a 12-month period. Forty livers were normally examined at each observation but during the summer months, when succeeding observations were similar, only 20 livers were examined at a session. The presence of the various types of lesions were noted for each liver and a record made of whether the liver was fit for human consumption. Two condemned livers were collected at each observation. One liver was selected which showed chronic bile duct lesions and another selected which showed moderate lesions with evidence of immature infection if possible. These livers were treated as previously described (Ross, Todd & Dow, 1966), and the numbers and lengths of the flukes recovered were recorded. In all goo livers were inspected and 54 livers critically treated over the period from the 21st October, Ig64, to the 26th October, Ig65, when 27 observations were made. The following observations of lesions in each liver, from which a percentage incidence was calculated, was made at each inspection. (a) Numbers of livers: fit for human consumption; showing no lesions attributable to fluke; showing some degree of duct fibrosis; showing some measure of cirrhosis. From the percentage incidence of these four observations an assessment of overall infection level can be obtained. (b) Numbers of livers: showing severe cirrhosis; with calcified bile ducts. From these percentages an estimate of level of infection can be made. (c) Numbers oflivers: showing fluke tracts in the parenchyma; showing haematoma lesions; showing fibrinous strands on the capsule; showing early haemorrhagic plaques; showing late haemorrhagic plaques. From these percentages an estimate of the current infection level can be estimated. RESULTS

The results may be conveniently considered in two parts. Firstly, those observations which showed little seasonal variation. The percentage of livers passed for human consumption over the 12-month period was 24 per cent, ranging from 10 to 45 per cent between observations. The percentage condemnation rates for the same period compiled by the Bel-

FASCIOLA HEPATICA IN CATTLE

49'

fast Abattoir Authorities (Gracey, personal communication) ranged between 50 and 60 per cent. These latter figures are based on weight of liver condemned and include parts of livers where the remainder was passed for human consumption. Seventy-seven per cent of the livers during the year showed some measure of duct involvement (range 55 to 90 per cent), while only 12 per cent of the livers inspected had no lesions (range 3 to 35 per cent). A slight decrease in the numbers of livers showing duct changes and an increase in livers with no lesions was observed between March and August 1965. In over 83 per cent of the livers some measure of cirrhosis was present, the incidence following the same trend as the duct fibrosis. Calcified ducts were observed in 48 per cent (range 27 to 65 per cent) of the livers and while between observations variations occurred there was no evidence of seasonal variation. Late or healing haemorrhagic plaques were of a similar incidence throughout the year confirming experimental evidence that inhibited parenchymal flukes can persist for very long periods of time (Table I). Marked seasonal variations were observed in those lesions associated with migrating immature flukes, and in the numbers of immature flukes and mature flukes recovered from the livers examined in detail. Details of the percentage incidence of fluke tracts, haematoma and fibrinous strands on the liver capsule will not be presented as the other data gives an accurate and similar account of variations. They will, however, be referred to where they supplied additional information. To eliminate inevitable variations between observations the results are presented on a moving average of three mean consecutive observations (Table II). Migrating immature flukes were present in the livers from October 1964 to May 1965 and again from July 1965 to October 1965. The numbers of immature flukes present and the percentage oflivers carrying immature infections rose from July to October. The percentage of livers with immature infections fell from November to May and the numbers of immature flukes recovered from livers fell from March to May. The mean length of the immature flukes was constant from October to April and slightly less from August to October. The numbers of adult flukes recovered rose from September 1964 to March 1965, fell from March to April to a plateau before a second rise occurred between June and August 1965. The maximum number of adult flukes recovered from a liver was 278 in June. This was not typical of this season of the year as prior and subsequent observations had few adults recorded. Consistent high level adult infections of between 100 and 200 were recorded between January and March. To assist in the discussion of these results, fluke incidence forecast values ("Mt." values, Ollerenshaw & Rowlands, 1959), based on the meteorological data from a meteorological station situated in Northern Ireland, are shown in Table III. The Mt. values are based on rainfall and transpiration figures for the months of May to October and from these estimates can be made of the probable incidence of disease in late summer and spring. The sum of Mt. values from May to October 1964, which predict the summer infection for 1964, is 433, and of the August to October 1964 and May and June 1965, which predict the

TABLE I

Observations

Passed,

% Mean Of27 observations

24

No Duct lesions, Cirrhotic, fibrosis,

%

% 12

Extensive cirrhosis,

%

83

Calcified Tracts, duc ts, 0/

%

% 20

77

48

~ );)

27

MEAN VALUES OF

OBSERVATIONS

Number Mean length mature mature .Number lv!ean length flukes flukes, Immature Immature mm. flukes flukes, mm.

I Early P aques, pi Haematoma, 0/ aques, 0/

/0

/0

%

/0

14

72

25

II

17.8

67

9·3

31

OJ

::t' .... >-l ....

[J}

::t:

TABLE II MOVING AVERAGE VALUES OF LESION AND FLUKE NUMBERS FROM

Months

Observation number Early plaque lesions, % Immature flukes number Mature flukes number

Oct.-Dec. 1964

2

Jan.-Feb. 1965

27

OBSERVATIONS FROM OCTOBER

March-April 1965

May-June 1965

1964

TO OCTOBER

July-Aug. 1965

5

6

7

8

9

10

II

12

13

14

15

16

17

18

19 20 21

40 46 37 39 23 . 38 34 53

33

34

15

2

6

6

6

0

0

0

3 20 28

35

5 48

2

35

19 12

48

17

15

13

13

0

0

0

0

7

64 65 51

83

128 81

65

74 67

72

45 59 43

28

3

4

77

130 101

35

12 3 108

22

~

1965

t'Il

Sept.-Oct. 1965

23

24 25

26

::t' ....

27

~

25 23 30 63 76 7 8 8 20 67 117

\-0

24 34 35 53 49

t'

24

o c:

~

);)

~);)

TABLE III FLUKE INCIDENCE FORECAST VALUES

Month

Mt. values Sum ofMt.

May

June

1964

1964

34 Summer 1964 Winter 1964/ 65 Summer 1965

68 433 390 481

(MT. VALUES)

MAY

1964

TO OCTOBER

1965

July

August

September

1964 66

1964

October

1964 100

May

1964 71

1965

July

August

1965

1965

September

1965

43

82

100

1965 100

94

June

100

October

1965 56

FASCIOLA HEPATICA IN CATTLE

493

winter infection for 1964/65, is 390. the values indicate an average incidence of fluke infection for these periods. The sum of Mt. values from May to October 1965 which predict the summer infection for that year is 48 I, suggesting an above average incidence of the disease. DISCUSSION

In a survey of this nature it is not possible to form concrete conclusions but merely to observe trends and associate these with theoretical predictions based on experimental evidence. It is not known how many cattle in Northern Ireland are treated for fascioliasis and to what extent this alters the eventual burden of parasites. Inquiries have, however, indicated that many of the large beef producers routinely treat in October only and that very few of the smaller farmers treat at all, unless clinical disease is present. Cattle would not be treated immediately prior to slaughter so that the October treatment would affect the adult fluke numbers in only a percentage of those animals slaughtered from January onwards. The two livers selected at each observation, from which the numbers of mature fluke were calculated, were normally the severest affected, and therefore must give a higher mean value than would be present overall for each observation. This would tend to counteract the effect of reduced numbers due to treatment, although it would not alter any trend resulting from treatmeht. Eighty-eight per cent of the cattle had at some time been infected with fascioliasis and between 55 and 90 per cent had lesions sufficiently severe to warrant condemnation of the liver. Forty-eight per cent of the cattle had been subjected to heavy infection levels. The presence ofhaemorrhagic plaque lesions in the majority of the livers throughout the year and of early haemorrhagic plaques in 25 per cent for nine months of the year substantiates experimental evidence that localized lesions of this type containing inhibited or disintegrating flukes may persist in the liver for a considerable period of time. The predicted infection level Mt. values for 1964 and 1965 summer infections indicated that infections in 1965 would be higher than in 1964. The considerably higher levels of immature parasites present in October 1965 as compared to October 1964 suggest that this was in fact the case. All the livers examined were from cattle which would normally have experienced at least two infection seasons. From experimental evidence one would expect two features to arise. A drop in the numbers of metacercariae becoming established, associated with increasing numbers of inhibited immature flukes and an "acquired self cure" of adult bile duct stages as a result of challenge infection (Ross, 1966a, b). This will result in a decrease in the numbers of duct stages, a spread of the season when immatures will be found in the parenchyma ;md a decrease in the numbers of duct stage as a fresh infection period arises. The probability of a limited life span of adult flukes in cattle will also reduce the number and duration of these stages (Dixon, 1964). Not all cattle will be subjected to infection each season, consequently trends rather than dramatic changes can be expected from data o(this nature.

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BRITISH VETERINARY JOURNAL, 122,

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The maximum number of adult parasites was recorded in May 1965 and 278 were recovered from one liver. This was not, however, typical of this period and mean maximum numbers of between 100 and 150 adults were observed between February and March. These levels are less than that necessary to produce anaemia in cattle (Ross, Todd & Dow, 1966) and this supports prior contentions that levels associated with anaemia in cattle would only occur in particular circumstances. There are several important findings revealed by this investigation. Firstly, the incidence of infection is very high and it is apparent that the majority of cattle in Northern Ireland experience infection at some time. Levels of infection resulting in severe liver lesions are common but levels of adult duct infections sufficiently high to produce anaemia are apparently rare. It is, however, relevant that while the levels of around 100 adult flukes observed may not produce anaemia they may produce subclinical disease and treatment might be beneficial. Peak adult fluke levels were present between J anuiry and April. At other times of the year adult burdens were low apart from odd livers. It therefore appears that treatment of cattle for Fasciola hepatica with the anthelmintics at present available, which are only effective against mature flukes, is indicated only in the first three months of the year except in animals experiencing first infections, when earlier treatment may be indicated. It is doubtful if the current practice of treatment of cattle in October is indicated and whether it significantly alters the overall burden except in cattle carrying high burdens from the previous season. ACKNOWLEDGEMENTS

I am grateful to Professor H. G. Lamont for permission to publish and to Messrs. Close, O'Hagan and Kenny for their most excellent technical assistance. I also wish to acknowledge the facilities and assistance given by Dr.J. F. Gracey and Mr. R. Roddy at the Belfast Abattoir. REFERENCES

J. Helminth., 28, 203. (1959). Vet. lUc., 71,957. & ROWLANDS, W. T. (1959). Vet. Rec., 71, 591. Ross, j. G. (1965). Nature, Lond., 208,907. Ross, j. G. (19660). Nature, Lond., in press. Ross, j. G. (1966b). Br. vet. J., 122,209. Ross,j. G., TODD,j. R. & Dow, C. (1966). J. compo Path.,,ct, 67. SAZANOV, A. M. (1961). Sbonik Tekh. In! Inst. Gelm., No. 7/8,53. TAYLOR, E. L. (1949). Rep. 14th Int. Vet. Gongr., 2, 81. DIXON, K. E. (1964). OLLERENSHAW, C. B. OLLERENSHAW, C. B.

(Accepted for publication 8 July 1966)