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6. Effects of disease on cattle productivity


Trypanosomosis and reproductive performance in village cows1
Interactions between experimental infections of Trypanosoma congolense and Haemonchus contortus2
Interactive effects between trypanosomal and trichostrongyle infections on health and productivity of young village cattle3


The productivity of cattle kept under traditional management conditions in Africa is adversely affected by harsh environmental conditions, nutritional deficiencies, seasonal labour constraints and rampant tropical diseases. Results presented in Chapters 4 and 5 have demonstrated that diseases are prevalent to varying degrees in the village production systems in The Gambia. Much of the variation in health and productivity of cattle among sites may have been attributable to differences in prevalence of trypanosomosis and helminthiasis. This chapter reports three studies conducted to ascertain the effects of disease on health and productivity of individual animals by comparing data from animals infected and not infected with a given parasite. Two studies extract data from the survey described in Chapter 4 to investigate, firstly, the effect of trypanosomosis on reproductive performance and, secondly, the interactive effects of Trichostrongyle and trypanosomal infections on the health and productivity of young cattle. The third is an experimental study, complementing the second study, to investigate the interactive effects of these diseases on the pathogenicity of each parasite.

Trypanosomosis and reproductive performance in village cows1

Introduction

Poor reproductive performance resulting from a combination of genetic, physiological, management and environmental factors is recognised as a major cause of low productivity among livestock in developing countries. Anoestrus is believed to be a primary cause of bovine infertility, which is often associated with poor nutrition, loss in body weight, lactational stress and poor body condition (Entwistle 1983; Lamond 1970; Mukasa-Mugerwa 1989; Richardson et al 1975).

In an analysis of data from cows in Gunjur, Pirang, Nioro Jattaba and Keneba, villages of zero or low trypanosomosis risk, Agyemang et al (1991d) demonstrated a 70-day shorter calving interval in cows that gained weight during the first four months post-partum compared with those that lost weight. In traditional village situations where animals lose weight because of feed shortages during dry seasons, reproductive impairment due to trypanosomosis is likely to be exacerbated. There are few published data on the effects of level of nutrition and body condition on responses to trypanosomal infection (Little et al 1990b) and most experimental infections with trypanosomes have been in growing animals (Dwinger et al 1992; Logan et al 1988). Simultaneous effects of body weight loss and trypanosomal infection on reproductive performance of East African zebu cattle have been demonstrated by Rowlands et al (1994b). In the present study, similar analyses are undertaken to assess the interactive effects of body weight loss and trypanosomal infection in cows in the village of Keneba, Missira and Bansang, sites with moderate to high prevalences of trypanosomal infections.

Aim

The aim of this analysis is to assess the possible interactive effects of changes in body weight and presence or absence of trypanosomes on reproductive performance.

Statistical analysis

Two hundred and ninety-four calving recodes were selected on the basis of body weights being available both one and four months post-partum and the cow remaining in the herd for at least 21 months following calving. The difference in body weight between one and four months post-partum was calculated and put into one of two groups:

Each record was also classified as to whether the cow was detected or not detected with trypanosomes up to four months post-partum.

Two measures of cow fertility were analysed: whether or not a cow calved again within 21 months, and, for cows that calved again, calving interval. Twenty-one months (or 640 days) was chosen, being approximately the weighted average calving interval for cows in these three sites.

The effect of post-partum body weight change and trypanosomal infection on fertility were assessed by least-squares models that also included parameters for site, calf viability to six months of age, season of calving (wet, July to October; dry, November to June), parity (1,2,>3) and their second order interactions. Year of calving (1986 to 1988) and herd were not included.

Results

Calving interval

The average calving interval was 620 (SD = 202) days. Assuming a gestation period of 280 days, and ignoring the possible occurrence of embryonic mortalities, the mean interval from calving to conception was therefore 340 days. With the exception of parity, all factors, namely, site, body weight change, trypanosomal infection status, calf viability and season of calving, had significant effects on calving interval (Table 34). Cows whose calves died during the first six months after birth calved again 174 days (33%) earlier than those whose calves survived longer than six months of age. Calving intervals resulting from calvings in the dry season (November to June) were 55 days (9.3% shorter than those resulting from calvings in the wet season. When adjusted for these other factors, cows that lost less than 5% of their body weight had a mean calving interval 99 days shorter (17.5%) than those that lost more than 5% of their weight. Cows which were not detected with trypanosomes up to four months post-partum had a 70-day (12%) shorter calving interval than those that were detected with trypanosomes.

Table 34. Least-squares means ( standard error) for percentage of cows calving again within 21 months of last calving and for calving interval in herds at Keneba, Missira and Bansang.
 

No. of cows

Percentage calving within 21 months

No. of cows calving again

Calving interval (days)

Mean

294

40.46.6

262

61628

Site

 

***

 

***

Keneba

165

51.37.8

148

56531

Missira

55

47.28.4

38

54235

Bansang

74

22.78.1

40

74236

Post-partum body weight change                                                                  *

>5%

101

30.910.8

74

66646

<5%

193

50.07.5

152

56729

Trypanosomal infection status                           *                                           *

Uninfected

251

48.86.7

194

58128

Infected

43

32.08.9

32

65137

Season of calving                                          *                                            *

Wet

128

33.48.4

101

64435

Dry

166

47.46.6

125

58927

Calf viability

 

***

 

***

Survived >6 months

275

19.84.7

211

70320

Died <6 months

19

61.011.8

15

52949

Parity

1

90

36.68.0

66

636 32

2

67

45.19.8

52

61141

>3

137

39.68.5

108

60236

*** = P<0.001; * = P<0.05.
Decrease in body weight from one to four months post-partum as a percentage of body weight one month post-partum.
No infection detected during the first four months post-partum.

The interaction between body weight change and trypanosomal infection status was not significant. Cows losing body weight and simultaneously infected with trypanosomes had a calving interval 169 days longer than those not infected and gaining or maintaining their body weight (Table 35).

Table 35. Least-squares means (± standard error) for percentage of cows calving again within 21 months of last calving and for calving interval related to loss in body weight post-partum and detection or not with trypanosomes.

Post-partum body weight change

Trypanosomal infection status

Infected

Uninfected

 

Percentage calving within 21 months

5%

25.4 ± 13.3 (20)

< 5%

38.5 ± 11.5 (23)

 

Calving interval (days)

5%

700 ± 55 (15)

631 ± 50 (59)

< 5%

602 ± 46 (17)

531 ± 27 (135)

See footnote to Table 34.
Numbers in parentheses are numbers of records.

Ability to calve again within 21 months of calving

Table 34 shows that the ability to calve again differed significantly among sites, with season of calving and with calf viability. When adjusted for these factors, trypanosomal infection significantly decreased the percentage of cows calving again. Forty- nine percent of cows that were uninfected calved again within 21 months, compared with 32% of cows infected with trypanosomes. There was also a greater proportion of cows (50%0) calving again within 21 months and losing less than 5% of body weight post-partum than of those (31%) which lost more body weight (P=0.08).

Discussion

The essence of the data summarised in Table 34 and 35 is that, after correcting for other factors affecting reproductive performance, both body weight loss and incidence of trypanosomal infection over the four-month period post-partum significantly impaired conception and lengthened calving interval. The lack of an interaction between these factors indicated their independence in impairing reproductive performance.

The association between post-partum body weight gain and superior reproductive performance is consistent with many other studies (Richardson et al 1975; Patil and Deshpande 1981; Rowlands et al 1994b; Ward 1968). A deleterious effect of trypanosomal infection on oestrous activity has been demonstrated in artificial challenge experiments involving two-year-old, well-fed Boran and N’Dama heifers (Lorenzini et al 1988). Trial et al (1990) showed that, under ranching conditions, mean calving interval for cows infected with trypanosomes was 68 days (14%) longer than that for uninfected cows. In village cattle in Ethiopia trypanosomosis was found to significantly affect calving and abortion rate (Rowlands et al 1994b).

The results of this analysis have implications for the management of cow reproduction under traditional husbandry systems in The Gambia. Frequency distributions of the calving intervals of cows in each herd demonstrated a bimodal distribution (as shown in Figure 11 in Chapter 5) which indicated that cows that failed to become pregnant between October and April tended not to conceive until the following year. Although it is difficult to avoid animal contact with tsetse under communal grazing and cropping practices, extreme body weight losses occurring during the post-partum period can be prevented by appropriate feeding strategies. A number of experiments were undertaken to assess nutritional supplementation. One of these, supplementing lactating cows with groundnut cake to reduce body weight loss during the dry season, doubled mean conception rate within 12 months from 36 to 64%. The results of this experiment are described in Chapter 7.

Improved nutrition might also reduce the reproductive impairment caused by trypanosomal infections themselves, which tended to occur more frequently in lactating than non-lactating cows (Agyemang et al 1992). For example, at Missira, where the mean monthly prevalence of trypanosomal infections in cows was 8.4% (Chapter 5, Table 27), mean calving interval was approximately 140 days shorter than at Bansang, where the prevalence of trypanosomal infections was 3.6%. The Missira region provides more abundant dry season pasture by virtue of its location in a seasonally-flooded enclave of The Gambia River. Post-partum body weight loss in cows is less than that in cows at Bansang; this may have contributed to the superior reproductive performance of cows at Missira.

Interactions between experimental infections of Trypanosoma congolense and Haemonchus contortus2

Introduction

The major constraint to cattle production in tsetse-infested areas is repeatedly reported to be trypanosomosis (Shaw and Hoste 1987). Consequently, when anaemia is detected among cattle in these areas it is mainly attributed to trypanosomal infections. However, there are other important anaemia-causing pathogens such as gastrointestinal helminth infections (Chiejina 1986; Kaufmann and Pfister 1990). As shown in Chapter 4, trypanosomosis was apparently not a major limiting factor to production except possibly in Missira and Bansang. However, moderate to high prevalences of helminth infections were detected at some sites. Towards the end of the rainy season, Fula herders often find that calves, particularly those that have been weaned, are weak and display rough coats and pale mucosa membranes. High worm burdens (predominantly Haemonchus contortus, Bonostomum phlebotomum and Oesophagostomum radiatum) were found in the gastrointestinal tract of such calves at necropsy (Kaufmann et al 1990). These findings were generally accompanied by severe anaemia, emaciation and hypoproteinaemia.

Immunosuppression is a phenomenon which has been associated with trypanosomosis. Thus, T. brucei, superimposed on a Nippostrongylus brasiliensis infection in rats, resulted in eliminating the self-cure response and enhancing pathogenicity of the nematode (Urquhart et al 1973; Murray et al 1974). Although various researchers have found pancytopaenia following trypanosomal infections (e.g. Murray and Dexter 1988), very little is known about the interactions between trypanosomal and nematode infections in cattle. Experiments were therefore conducted using young N'Dama bulls to investigate these interactions.

Aim

An experiment was undertaken to investigate the interactions between experimental infections of trypanosomosis (T congolense) and helminthiassis (H. Contortus) in N’Dama bulls and to determine whether pathogenicity was affected when one infection was superimposed on the other.

Experimental design

Thirty-eight healthy bulls, two years of age and reared under traditional management conditions, were purchased from farmers and randomly allocated to four groups (eight to group 1, 10 each to groups 2, 3, and 4) according to body weight, packed red cell volume (PCV) and absence of anti-trypanosomal antibodies by the immunofluorescent antibody test (Katende et al 1987). All animals were vaccinated against clostridial infections, haemorrhagic septicemia and anthrax, and dewormed with fenbendazole (Panacur®, Hoechst A G; 7.5 mg/ kg).

For the artificial T. congolense infection, ITC 50, a clone derived from T. congolense IL Nat 3.1, was used after one passage in mice. Bulls in groups 1, 2 and 4 were inoculated intradermally at five sites with a total of 5 104 T. conoglense. An H. contortus strain, isolated from local N’Dama bulls, was used for the experimental helminthiasis infection. Bulls in groups 2, 3 and 4 were infected orally with 10,000 ineffective third stage larvae (L3) followed by four doses of 5000 L3, administered on consecutive days following the first infection.

The eight animals in group 1 were treated every three weeks with fenbendazole throughout the study. They were also treated with diminazene aceturate (Berenil® Hoechst AG; 3.5 mg/ kg) at four-week intervals until they were infected with 5 104 T. congolense in week 9. The ten animals in group 2 were treated at four-week intervals with dimiinazene aceturate until they were infected with 5 104 T. congolense in week 9. They were also treated every three weeks with fenbendazole until infection with 30,000 L3 H. contortus in week 10. The ten animals in group 3 were treated with diminazene aceturate every four weeks throughout the study. In week 5 they were infected with 30,000 L3 H. contortus. The ten animals in group 4 were treated at four-week intervals with diminazene aceturate until they were infected with 5 104 T. congolense in week 9. In week 5 these animals were also infected with 30,000 L3 H. contortus. A layout of these interventions in the four groups is shown in Table 36.

Table 36. Design of experiment for evaluating interactions between experimental infections of T congolense and H. contortus in two-year-old N'Dama bulls.

Group

Number of bulls

Week of experiment

1

2

3

4

5

6

7

8

9

10

11

12

13

14

15

16

17

18

19

1 (T)

8

BFt

—

—

F

B

—

F

—

T

F

—

—

F

—

—

F

—

—

B

2 (TH)

10

BF

—

—

F

B

—

F

—

T

H§

—

—

—

—

—

—

—

—

BF

3 (H)

10

BF

—

—

—

BH

—

—

—

B

—

—

—

B

—

—

—

B

—

F

4 (HT)

10

BF

—

—

—

BH

—

—

—

T

—

—

—

—

—

—

—

—

—

BF

B: animals treated with 3.5 mg of diminazene aceturate (Berenil)/kg body weight; F: animals treated with fenbendazole.
T: animals inoculated with 5104 T..congolense.
§H: animals infected orally with 10,000 L3 H. contortus on day 0 followed by 5000 administered on each of days 1–4.

A group of nine bulls, kept in a privately owned herd nearby, acted as external control and they were monitored for body weight. The bulls were kept in the same grazing area but were neither treated nor artificially infected. All the experimental animals were herded together during the day and tethered at night in a fenced paddock.

The animals infected with T. congolense (groups 1, 2 and 4) were treated with diminazene aceturate and those infected with H. contortus (groups 2, 3 and 4) with fenbendazole at the end of the experiment (week 19). A feed supplemement of 1 kg/ day of groundnut cake and a subcutaneous application of 100 mg/kg iron (Ferrovet®, Chassot and Cie, Koniz, Switzerland) was administered to the bulls to assist with their convalescence.

All animals were monitored weekly and the following measurements made: faecal egg counts using a modified McMaster technique (Boch and Supperer 1983), PCV, haemoglobin, red cell counts and level of parasitaemia (dark ground buffy coat method, Murray et al 1977), leucocyte counts and differentiation (Plonait 1980) and serum albumin (Abbott VP Bichromatic analyzer, Abott Diagnostic Division, South Pasadena, California). Body weights were determined monthly using an electronic weighing scale (Barlo Instruments, Australia).

Results

Trichostrongyle egg excretion

The percentages of animals detected with a positive faecal egg count at different times following H. contortus infection is shown in Figure 12. All infected animals excreted eggs but the prepatent period varied markedly between the three groups. In the group 2 bulls infected firstly with T. congolense and secondly with H. contortus, eggs began to be detected in the faeces 11 days after infection. By 17 days following infection all bulls were excreting eggs in their faeces. In contrast, the group 3 and 4 animals, first infected with H. contortus, began to excrete eggs 14 days following infection (1 bull) but it was not until 42 days after infection that all bulls were excreting eggs in their faeces.

.Figure 12. Percentages of two-year-old N'Dama bulls with detectable faecal eggs following H. contortus infection (See Table 36 for description of groups 2, 3 and 4).

Increases in overall faecal egg counts among animals in groups 2, 3 and 4 are shown in Figure 13. Bulls, first infected with T. congolense, and followed by H. contortus (group 2), showed the sharpest rise in faecal egg count reaching a mean 5575 epg eight weeks following infection. Bulls in groups 3 and 4 had similar faecal egg counts until three weeks following the infection with T. congolense in week 9 (group 4). Thereafter, a more rapid increase occurred among animals in this group, reaching 4275 epg in week 18, whereas faecal egg counts in group 3 animals, which were not infected with T. congolense, reached a maximum of only 2411 epg in week 17, significantly lower than in the other two groups (P<0.05).

Figure 13. Faecal egg output in groups of two-year-old bulls infected with H. contortus (See Table 36 for description of groups 2, 3 and 4).

These results showed that the prepatent period of H. contortus superimposed on a T. congolense infection was reduced from an average of three to less than two weeks. Further, H. contortus egg output was significantly increased by a superimposed or a preceding T. congolense infection.

Trypanosomal parasitaemia

Group 1, 2 and 4 bulls infected with T. congolense had mean parasitaemia scores following infection that were similar in pattern for the three groups (Figure 14). Trypanosomes were first detected in the peripheral blood six to seven days following infection and reached a maximum score of about 4 (between 104 and 5 105 trypanosomes/ml blood; Murray et al 1983) between 10 and 16 days post infection. Parasitaemia score then decreased to between 1 and 2 (102 to 104 trypanosomes/ml) over the remainder of the experiment. None of the infections appear to have been self-cured as is often observed in N'Dama cattle by 10 weeks following T. congolense infection (Dargie 1980)

Figure 14. Levels of parasitaemia in three groups of two-year-old bulls at different days after infection with T. congolense (See Table 36 for description of groups 1, 2 and 4).

Infection with H.contortus did not affect the pattern of the T. congolense parasitaemia in the present experiment, neither in bulls with a preceding H. contortus infection, nor in those with a subsequent H. contortus infection.

Haematology

Decreases in PCV were significantly greater in animals simultaneously infected with T. congolense and H. contortus (P<0.01) than in those infected with only one pathogen (Figure 15). Packed cell volumes in bulls with a single trypanosomal infection fell by 0.99% per week (group 1) compared with 1.5% per week in animals also infected with H. contortus (group 2). These animals in group 2 were very anaemic by the end of the experiment, when they had a mean PCV of 15.8%.

Figure 15. Changes in PCV in groups of two-year-old bulls infected with H. contortus and/or T. congolense.

The PCV in calves first infected with H. contortus (groups 3 and 4) decreased slightly between week 5 and week 11 (0.71 and 0.88% units per week, respectively). Thereafter, a more pronounced decrease occurred in group 4, following infection of bulls in this group with T. congolense, than in group 2.

A pronounced decrease in eosinophil counts occurred in animals in group 4 following T. congolense infection. This contrasted with the normal eosinophil counts maintained in group 3 animals which were not infected at this time. A decrease in total leucocyte counts from approximately 9000/µl to 6000/µl-occurred in groups 2 and 4 following T. congolense infection, and this was due mainly to a decrease in lymphocyte counts.

Serum albumin

Decrease in serum albumin concentrations occurred in all groups during the course of the experiment (Figure 16). However, the decrease was more pronounced in calves infected with both T. congolense and H. contortus (respectively 0.5 and 0.4 g/1 per week in group 2 and 4 calves) than in calves infected with H. contortus only (0.2 g/1 per week) (group 3). From week 12 onwards the decrease in albumin concentration was significantly greater (P<0.05) in calves infected with H. contortus only (group 3) than in calves infected with T. congolense only (group 1). Thus, the combined infections appeared to have had a greater effect than the single infections on reduction in serum albumin concentration. Furthermore, a single H. contortus infection resulted in a reduction in albumin concentration greater than that following a single T. congolense infection.

Figure 16. Changes in mean serum albumin concentrations in groups of two-year-old bulls infected with H. contortus and/or T congolense.

Body weight loss and mortality

Mean body weights of the bulls in the four groups are summarised in Table 37 together with those in the external control group. N'Dama calves with a single T. congolense infection (group 1) gained 7 kg on average during the 18-week experiment whereas animals with a single H. contortus infection lost 1.3 kg. Infections with both T. congolense and H. contortus resulted in body weight losses of 13.9 kg in group 2 and 10.6 kg in group 4. Although a single T. congolense infection appeared to suppress the weight gain of N'Dama calves compared with that of the external control, the bulls nevertheless still gained weight. The other three groups lost weight.

Table 37. Mean body weights (kg) of four experimental groups of two-year-old N'Dama bulls and one control group kept in a privately owned herd nearby.
 

Group

Week

1 (T)

2 (TH)

3 (H)

4 (HT)

Control

2

102.8

109.7

94.3

107.6

100.4

10

106.2

99.0

91.2

96.6

121.6

18

109.8

95.8

93.0

97.0

129.3

Change from week 2 to 18

+7.0

–13.9

–1.3

–10.6

+28.9

See footnote to Table 36.

Deaths of bulls during and after the experiment are shown in Table 38. Mortality was highest in group 2 in which four bulls died following the end of the experiment. Two bulls died in group 4 during the same period. No animal died in group 1. These results indicated that the animals were able to survive a single T. congolense or single H. contortus infection better than when infected with both parasites.

Table 38. Mortality of N'Dama bulls during 18 weeks of experiment and 10 weeks after completion of experiment when administered with different combinations of T. congolense and H. contortus infections.

Group

Number of bulls

Deaths

Up to 18 weeks

From 19 to 28 weeks

Total

1 (T)

8

0

0

0

2 (TH)

10

1

4

5

3 (H)

10

1

0

1

4 (HT)

10

1

2

3

See footnote to Table 36.

Discussion

The most important finding of the present experiment was the markedly reduced prepatent period of H. contortus, from an average of approximately three weeks to two weeks, and the increased pathogenicity of H. contortus superimposed on a primary T. congolense infection. Likewise, a T. congolense infection given to an animal already infected with H. contortus resulted in higher faecal egg counts, more severe anaemia and high body weight loss compared with animals not infected with T. congolense. High mortality, low PCV and increased weight loss in goats have also been reported due to concomitant experimental infections with T. congolense and H. contortus (Griffin et al 1981).

The increased egg output, reduced prepatent period, increased decrease in PCV and serum albumin concentration and increased weight loss and mortality observed for the infection regimen of T. congolense followed by H. contortus infection suggested that this regimen was the most pathogenic. Packed cell volume decreased more rapidly in bulls in groups 2 and 4 infected with both T. congolense and H. contortus than in bulls infected with either, and there was also an apparent increase in death rate in these groups. The bulls therefore appeared to tolerate individual H. contortus or T. congolense infections better than when both infections occurred together.

It has been shown that suppression of the immune response by one pathogen prevents the host from mounting a normal response against a second (Goodwin et al 1972; Longstaffe et al 1973; Murray et al 1973, 1974), although studies of this phenomenon in cattle are few (Scott et al 1977; Rurangirwa et al 1983). Immunosuppression caused by T. congolense infection was probably responsible for the increase in pathogenicity of the existing H. contortus infection in group 4 animals. The fall in eosinophils at the same time in this group may also be associated with this immunosuppression. A decrease in eosinophils after trypanosomal infection has also been reported by Naylor (1971) and Maxie and Valli (1979).

The shorter prepatent period of H. contortus following a trypanosomal infection may necessitate more frequent anthelmintic treatments where both pathogens are prevalent. Furthermore, the increased egg excretion of animals infected also with a trypanosomal infection may result in increased environmental contamination and increased risk of helminth infections. The interactions between trypanosomal and helminth infections may have important implications for the strategic control of these two diseases.

Interactive effects between trypanosomal and trichostrongyle infections on health and productivity of young village cattle3

Introduction

The experimental study described in the previous section demonstrated that an H. contortus infection superimposed on a T. congolense infection, or a T. congolense infection superimposed on a H. contortus infection, produced a more pathogenic response in the animal than when either infection occurred alone. It thus appeared pertinent to investigate whether the same effect could be detected in the field data collected in the survey described in Chapters 2 to 5. At the same time the database was used to investigate whether presence of Trichostrongyle infestation in turn increased susceptibility to trypanosomosis. Although concomitant infections of trypanosomes and gastro-intestinal nematodes have been shown to reduce body weight gains of sheep and goats in Mozambique (Specht 1982), there appears to have been no similar study in cattle.

Aim

The aim of the analysis was to assess from field data the effects of trypanosomal and Trichostrongyle infections on PCV and body weights of cattle up to 48 months of age and whether animals infected with Trichostrongyles were more predisposed to infection with trypanosomes than those without Trichostrongyle infection.

Animal selection

Three groups of animals were selected from those used in the field survey described in Chapter 4 for the purpose of studying the interactive effects of trypanosomal and Trichostrongyle infections on PCV and body weight. The three groups were: pre-yearlings (<12 months of age), yearlings (12–24 months of age), and young adults (24–48 months of age). These were selected from cattle at Gunjur, Pirang, Keneba, Missira and Bangang.

All calves with known birth dates and born between October 1985 and December 1989 were selected for the pre-yearling group. Body weights and faecal and blood sample results were assembled from those collected from birth to 12 months of age. Six hundred and seventy two calves with at least four samplings of blood and faeces and a body weight recorded at least from 10 months of age, in addition to those recopied earlier in their life, were available for analysis. Extrapolated or interpolated 365-day (or 12-month) body weight was calculated for each calf from the daily weight gain calculated from birth to the last recorded body weight. Birth weight, 12-month body weight, growth rate to 365 days of age and mean PCV from birth to 12 months of age were analysed. Records of calves which did not survive to 365 days of age and were known to have died accidentally or of an infectious disease were investigated for any links with Trichostrongyle infections.

Animals which survived to 24 months of age were selected for the yearling group. As for pre-yearlings, extrapolated or interpolated 730-day body weight was estimated from the daily weight gain calculated from 365 days to the body weight recorded closest to 24 months of age. Four hundred and fifty-five animals with at least four samplings of blood and faeces during this period, and a body weight recorded between 22 and 24 months of age, were available for analysis.

Animals born between 1982 and 1987 were selected for the group of young adults. All body weights and faecal and blood sample results recorded from 24 months to 48 months of age for these animals were assembled. For each animal, the calendar year when it attained 24 or 36 months of age was noted; females were omitted from the analysis once they became pregnant (estimated from the subsequent calving date). Mean PCVs and body weights were calculated between 24 and 36 and between 36 and 48 months of age for those animals recorded throughout the period. Records were assembled for 887 animals.

Records of 369 animals monitored between July 1988 and June 1989 were also studied to determine both the influence of Trichostrongyle infestation on susceptibility to trypanosomal infection and the effect of trypanosomal infection on Trichostrongyle faecal egg count.

Statistical analysis

A moderately high degree of infestation was defined as being more than 500 epg of Haemonchus and a low degree of infestation as being less than 500 epg (Skerman and Hillard 1966). Six  trichostrongyle/trypanosomal classifications were then defined as follows (see Table 39):

Table 39. Effects of trichostrongyle and trypanosomal infections on mean PCV and body weight in three age groups of cattle selected from Gunjur, Pirang, Keneba, Missira and Bansang

Trichostrongyle status

Trypanosomal status

Pre-yearlings

Yearlings

Young adults (2–3 years of age)

No. of animals

Mean PCV1–12 months of age (%)

Body weight at 12 months of age (kg)

Growth Rate (g/d)

No. of animals

Mean PCV13–24 months of age (%)

Body weight at 24 months of age (kg)

Growth rate (g/d)

No. of animals

Mean PCV (%)

Mean body weight (kg)

0

No

160

27.5

77

166

138

23.6

135

154

183

27.3

176

Low

No

204

27.3

74

160

251

24.2

132

149

354

26.8§

164

High

No

279

26.7

73

156

56

23.7

128

139

263

26.1§

153§

0

Yes

8

27.1

76

159

—

—

—

—

—

—

—

Low

Yes

12

26.9

80

175

10

24.0

119

126

40

26.1§

164

High

Yes

9

25.9

62

126

—

—

—

—

47

25.3§

158§

Low: 100–500 epg; high: >500 epg on at least one occasion during 12-month period.
Yes: trypanosomes detected at least once during 12-month period; No: not detected.
§Significantly different from control (negative for both trichostrongyles and trypanosomes) (P<0.05 at least).
(—) Very few records.

Least-squares analyses of variance were carried out on PCV and body weight with terms for site, sex, either month and year of birth (pre-yearlings and yearlings only) or year and age (24, 36 months of age) (young adults only), level of trichostrongyle infestation, presence or absence of trypanosomal infection and interaction between trichostrongyle infestation and trypanosomal infection.

Possible associations between incidences of trypanosomal infections and trichostrongyle infestations in individual animals were analysed by c2 tests.

Results

Monthly prevalences of trypanosomal and strongyle infections in young adult cattle

As shown previously in Chapter 4 (Figures 6 and 10) there was a seasonal pattern in the prevalence of trichostrongyles in cattle between two and four years of age at Gunjur, Pirang, Missira and Bansang. There was a rise in mean trichostrongyle egg counts from July to September/October reaching a maximum of about 70% of animals infested. Mean numbers of trichostrongyle egg counts detected in cattle at Keneba, which were also included in this analysis, were lower than in cattle at the other four sites with fewer than 10% of animals detected with trichostrongyles in any one month. The majority of these had low egg counts (less than 200 epg), and only a small proportion (approximately 5%) of animals were ever detected with more than 1000 epg.

As previously shown in Chapter 4, average monthly prevalences of trypanosomal infection varied from 0 to 20% with the highest prevalences tending to be recorded mostly at the end of the dry season (April to June), and occasionally in Missira at the beginning of the dry season in November and December.

Effect of trypanosomal and trichostrongyle infection on PCV, body weight and mortality

There was no significant effect of trichostrongyle or trypanosomal status on PCV, growth rate or final body weight of pre-yearlings and yearlings (Table 39). Comparison of the causes of mortality in calves up to 12 months of age showed that whilst 48% of deaths due to infectious disease (27/56) occurred in animals infested with trichostrongyles, only 17% of deaths due to trauma or accidents were so associated (c2 = 31.2, P<0.001).

In contrast to these younger animals, the effect of trichostrongyle and trypanosomal infection significantly reduced PCV of young adults (P<0.01; Table 39). Trichostrongyle infestation also reduced body weight (P<0.01). The magnitude of the reduction in body weight appeared to be less in two- than three-year-old animals (P<0.05; Table 40). Thus, the mean body weight of two-year-olds with high faecal egg counts of trichostrongyles and also trypanosomes was 9 kg lower than that of uninfected animals, whereas the corresponding difference in three-year-olds was 28 kg.

Table 40. Effect of trichostrongyle and trypanosomal infections on mean PCV and body weights of two and three-year-old village cattle.

Trichostrongyle status

Trypanosomal status

Two-year-olds

Three-year-olds

No. of animals

PCV (%)

Body weight (kg)

No. of animals

PCV (%)

Body weight (kg)

0

No

127

26.5

148

56

28.0

204

Low

No

236

26.3

144

118

27.3

185

High

No

203

26.0

135

60

26.2

171

0

Yes

Low

Yes

13

25.8

142

27

26.3

187

High

Yes

29

25.4

139

18

25.1

176

†,‡See footnotes to Table 39.
(—) No data.

Effect of trichostrongyle infestation on susceptibility to trypanosomosis

Sixty-seven of the 369 animals used for studying the association between incidence of trypanosomal infections and occurrence of trichostrongyle infestations were detected with trypanosomes. Of these, 45% were associated with T. congolense, 42% with T. vivax, 3% with T. brucei and the remaining 10% were mixed infections. Sixty-two of these 67 animals shed trichostrongyle eggs at least once during the 12-month period compared with 237 of 302 animals not infected (c 12= 7.04, P<0.01). The 67 animals were detected positive with trypanosomes a total of 92 times. Of these 92 individual infections, 50 coincided with detection of trichostrongyles in the same month, 16 were associated with trichostrongyles having been detected in the previous month, and 5 with trichostrongyles having been detected two months previously. When the data were classified by site, representing areas of low, medium and high tsetse challenge, all trypanosomal infections in the higher tsetse-challenge areas coincided with trichostrongyles detected in the same or previous month. These results indicate associations between the presence of trichostrongyle and the onset of trypanosomosis.

When animals detected with trichostrongyles over the 12-month period were compared in cattle infected or uninfected with trypanosomes, there was a slightly higher proportion of infected (58%) than uninfected (45%) animals detected with high faecal egg counts, though this difference was not significant (c12= 3.24). Mean faecal egg counts recorded in samples detected with trichostrongyles were on average similar between trypanosomal infected and uninfected animals (Table 41).

Table 41. Comparison of frequencies of infestation and levels of trichostrongyle egg burdens in cattle infected or uninfected with trypanosomes over a 12-month period between July 1988 and July 1989.

Trichostrongyle status

Trypanosomal status

Uninfected

Infected

No. of animals

Samples with faecal eggs (%)

Mean epg

No. of animals

Samples with faecal eggs (%)

Mean epg

Low

130

38

203

26

46

216

High

107

65

498

36

75

513

See footnotes to Table 39.
Percentage of samples detected with trichostrongyles over 12-month period.

Discussion

Trichostrongyle infestations were prevalent throughout the year under these traditional management conditions in The Gambia. Highest faecal egg counts occurred between July and September (wet season) which confirms previous findings from one of the study sites (Kaufmann and Pfister 1990). Although no larval differentiation of tricho-strongyloides was done in this study, results published elsewhere indicate that H. contortus is a predominant species in village cattle in The Gambia (Kaufmann et al 1990).

Peak trypanosomal prevalence rates in the different villages tended to occur either in November or December (early dry season) or in April to June (late dry season). The percentages of animals detected with trypanosomes during one year were, however, small, ranging from approximately 3% in pre-yearlings and yearlings to 10% in young adults. Neither trichostrongyle infestation nor trypanosomal infection significantly affected 12-month PCV or growth rate of calves up to 24 months of age. The long periods over which these calves suckled their dams as demonstrated in Chapter 4 may have had an important influence in reducing the effect of infection in the calf on its health and productivity.

In contrast to the younger animals, there were significant effects of trichostrongyle infestation on PCV and body weight of young adults, and, in a separate analysis in cows, an effect of trichostrongyle infestation on milk offtake was also indicated (Agyemang et al 1993b). Again trypanosomal infection had no effect on mean PCV or body weight measured over the 12-month period. Presumably, animals compensated for any temporary reduction in PCV or loss in body weight at the time of infection. However, there were some indications of interacting effects of helminthiasis and trypanosomosis in the present study since a higher percentage of animals infected with trichostrongyles developed trypanosomosis compared with animals not infected with trichostrongyles over the 12-month period. These results could indicate either that those animals more tolerant than others to helminth infections are also more tolerant to trypanosomal infections, or that animals shedding trichostrongyle eggs are more predisposed to trypanosomal infections. The experimental results with infections of T. congolense and H. contortus described in the previous section of this chapter showed that a T. congolense infection given to an animal already infected with H. contortus resulted in higher faecal egg counts. These observations were not confirmed by the field data although there was an indication that animals infected with trypanosomes were detected more frequently with trichostrongyles.

The implications of our results are that anthelmintic treatment of two- to three-year-old village cattle at strategic times of the year may have a beneficial effect on their body weight gains and possibly also their susceptibility to trypanosomosis. Anthelmintic treatment of grazing heifers in Sri Lanka, for example, was shown to increase growth rate and reduce the age at first service (de Rond et al 1990).

In contrast to the observations on trichostongyle infestation, there was no apparent constraint of trypanosomosis on growth when averaged over all sites, and, in cattle under 24 months of age, no significant reduction in average PCV. Similar conclusions were drawn from zebu cattle in Ethiopia exposed to drug-resistant trypanosomes and under a treatment regimen of 3.5 mg/kg diminazene aceturate when detected parasitaemic and with PCV<26% (Rowlands et al 1994a). Although the prevalence of trypanosomal infections in these zebu cattle was higher, any effect of trypanosomal infection on growth was temporary since animals later compensated for poor periods of growth. As shown earlier in this chapter, the effect of trypanosomosis on the reproductive performance of N'Dama cows was greater than on growth, and Agyemang et al (1990a) also demonstrated a significant reduction in milk offtake due to trypanosomosis. These authors found that the mean daily milk extracted for human consumption from uninfected cows was proportionally 0.26 higher over a six-month period than that extracted from infected cows. In financial terms the loss of milk extracted for human consumption due to trypanosomal infections amounted to an average of about 12 Dalasi (6.7 Dalasi = 1 US $ in 1988) per month per cow.

Thus, there was evidence that the strains of trypanosomes found in cattle in The Gambia were pathogenic, and this adds credence to the conclusion drawn in Chapters 4 and 5 that the high mortality in cattle at Missira, and to a lesser extent at Bansang, was likely to have been largely attributable to the presence of trypanosomosis. In the western half of The Gambia, however, trypanosomosis was not a major limiting factor to cattle production. Here, poor nutrition was a primary factor and this is discussed in the next chapter.

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