17 - Trypanosome infections and other factors influencing PVC in livestock

G.D.M. d'IETEREN, K. AWUOME, K. BOKOVI, S. CHEMA, C. COLARDELLE, L COULIBALY, A. DEFLY, A. FERON, G. GRUNDLER, M. HANDLOS, P. HACKER, P. ITTY, O. KAKIESE, S.G.A. LEAK, J.H.H. MAEHL, S.H. MALOO, K. MAWUENA, M. MINENGU, G. MORKRAMER, F. MUKENDI, W. MULATU, M. MULUNGO, S.M. NAGDA, C. NANKODABA, S. NGAMUNA, C. ORDNER, R.W. PALING, J.M. RARIEYA, A. SCHUETTERLE, M. SHERIA, W. THORPE, G. TIKUBET, J.C.M. TRAIL and G. YANGARI

Introduction
Materials and methods
Results
Conclusion
References

Introduction

Anaemia is one of the most important clinical signs of trypanosomiasis. It has now been definitely established that the measurement of PCV gives a reliable indication of the disease status of trypanosome infected cattle (Murray, 1979). PCV has also been shown to be a reliable index of anaemia as no evidence of haemodilution has been found in trypanosome infected cattle (Dargie et al., 1979). Therefore PCV has been widely used in the research protocols within the ATLN (ILCA, 1986a). Feron et al. (in press) suggested from their preliminary results that PCV may also be a useful indicator of livestock performance in trypanosomiasis infection.

Resistance to trypanosomiasis is determined by at least three main characteristics, namely, the ability to control parasitaemia, the ability to develop an effective immune response and the ability to resist the development of anaemia (Murray, see article 15 of these Proceedings).

A significant linkage between parasitaemia and PCV in cattle, sheep and goat populations has been reported by ILCA in 22 species/breed/site situations studied. These data show an average 1.3% increase in trypanosome prevalence for each 1% drop in PCV (ILCA/ILRAD, 1986b). Preliminary findings from ILCA (1986b) also indicated that the repeatability of the monthly PCV in cattle ranged from 0.25 to 0.39, justifying further work to estimate the heritability of PCV. Trail et al. (see article 41 of these Proceedings) are evaluating the phenotypic relationships between parasitaemia, anaemia control and daily liveweight change. The many factors influencing PCV need to be identified and their effects evaluated within the environments where these studies are conducted. This paper updates and reviews some of the important factors influencing PCV value in livestock in six Network sites.

Materials and methods

A comprehensive description of the sites where these results were obtained (Avetonou, Togo; Boundiali and Tengrela, Cote d'Ivoire; OGAPROV, Gabon; and Kolo and Mushie, Zaire) has been given by ILCA/ILRAD (1986a). Each month the darkground/phase contrast, huffy coat technique was used to detect the presence of trypanosome and for quantification of parasitaemia, while the anaemia situation was indicated by measuring PCV. Other genetic and environmental factors which may interact with trypanosome infections and affect PCV were considered, including other anaemia producing diseases. Protocols and methodologies have been described in detail elsewhere (ILCA/ILRAD, 1986a). The analyses used data from the period January 1984 to December 1986; in Boundiali most data came from the latter part of that period.

The PCV values were measured on dams and their progeny and relate to defined periods around a parturition: dam average PCV during gestation, average PCV during lactation, progeny average PCV pre-weaning, average PCV post-weaning. Gestation was defined as nine and five months pre-partum, and lactation and weaning as eight and four months post-partum in cattle and sheep, respectively.

The effect of trypanosome infection was estimated by trypanosome species and the number of months in which trypanosomes were detected. Other factors included in the models were the fixed effects of herd, breed, year/season of parturition/birth, dam age and birth type, as appropriate to the trait and the animal group being studied. In preliminary analyses, two factor interactions between trypanosome infection and the other major effects were fitted and retained if they approached significance.

Results

Effect of trypanosome infection on PCV

Sheep

Table 1 presents results from Boundiali. PCV levels of Djallonke sheep with one, two, or more parasitaemic months during gestation or lactation had significantly lower PCV levels than those of uninfected ewes. Note that the PCV mean of lactating ewes was lower than that of gestating ewes and that during gestation two or more infections were necessary to induce a marked PCV decrease.

Table 1. Effect of number of months with trypanosome parasitaemia on PCV in Djallonke sheep, Boundiali.

No. of parasitaemic months	Ewe average PCV during gestation (%)			Ewe average PCV during lactation (%)
	No.	Mean	s.e.	No.	Mean	s.e.
0	263	27.5	0.32	190	26.0	0.46
1	82	27.3	0.46	74	24.7	0.54
2 or more	38	25.7	0.63	68	23.8	0.54
Significance		*			***

*P<0.05
***P<0.001

Similar results were reported by Defly et al. (see article 25 of these Proceedings) for Djallonke sheep maintained under village conditions around Avetonou. In the Boundiali sheep population, one T. congolense parasitaemia depressed PCV during gestation more than one or two T. vivax or mixed parasitaemias, but the reverse was true during lactation (Table 2). During both gestation and lactation, three parasitaemic months resulted in the lowest PCV. A further analysis showed that a high compared to a low mean score of a single T. vivax parasitaemia did not depress PCV further.

Table 2. Effect of period of parasitaemia and trypanosome species on PCV in ewes, Boundiali.

No. of parasitaemic months	Trypanosome species	Average PCV during gestation (%)			Average PCV during lactation (%)
		No.	Mean	s.e.	No.	Mean	s.e.
0		222	27.7	0.39	219	27.3	0.36
1	T. congolense	11	25.2	0.91	18	26.7	1.54
1	T. vivax	41	26.5	0.52	44	25.9	0.76
1	Mixed	17	26.8	0.76	18	25.7	0.97
2	T. vivax	6	26.1	1.21	18	25.8	1.54
2	Others	15	25.7	0.80	38	25.4	1.10
3		10	24.6	0.94	30	23.1	1.10
Significance			***			**

**P<0.01
***P<0.001

In the analysis of PCV in both the Avetonou and Boundiali sheep populations, two factor interactions between trypanosome infection and other effects were not significant.

Table 3 shows an interaction which did not reach statistical significance but which illustrates the approach to estimating any residual effects of trypanosome infection. The ewes uninfected pre-partum but infected during lactation suffered twice the depression of PCV of the ewes that had been infected pre-partum. PCV was highest for those that were uninfected both pre- and post-partum.

Table 3. Effect of number of months with trypanosome parasitaemia Are- and post-partum on ewe average PCV during lactation, Boundiali.

No. of parasitaemic months during lactation	Number of parasitaemic months during gestation
	0			1			>1
	No.	Mean	s.e.	No.	Mean	s.e.	No.	Mean	s.e.
0	147	26.8	0.41	31	25.6	0.61	12	25.5	0.90
1	48	25.0	0.55	15	24.7	0.82	11	24.4	0.98
>1	35	22.9	0.63	23	24.3	0.72	10	24.2	1.00
Significance	P<0.09

Cattle

The trypanotolerant cattle breeds, N'Dama and Race Locale (West African Shorthorn) maintained in Avetonou had significantly depressed PCV when infected with T. vivax, while a higher parasitaemia score generally resulted in a lower PCV (Defly, see article 25 of these Proceedings). The two breeds had the same PCV and gave the same response to trypanosome infection.

A more comprehensive comparison of the effects of trypanosome parasitaemia on PCV in cattle was possible in Boundiali where infections of T. vivax and T. congolense were frequent. Table 4 shows that in Boundiali, one parasitaemic month depressed the PCV of cows and post-weaners, but not pre-weaners, by 1.5 percentage units. Additional parasitaemia did depress PCV in pre-weaners and caused further depression of PCV in the older animals.

Table 4. Effect of number of months with trypanosome parasitaemia on PCV of cattle, Boundiali

No of parasitaemic months	Cow average PCV during gestation (%)			Cow average PCV during lactation (%)			Calf average PCV pre-weaning (%)			Calf average PCV from 9 to 15 months (%)
	No.	Mean	s e.	No.	Mean	s.e.	No.	Mean	s.e.	No.	Mean	s.e.
0	113	32.3	0.32	64	31.1	0.55	66	31.1	0.54	91	82.2	0.43
1	44	30.8	0.54	33	84.4	0.74	25	31.2	0.6,	33	28.2	0.74
2	24	29.5	0.69	23	28.4	0.76	17	29.8	0.89	37	26.9	0.62
>2	-	-	-	12	25.0	1.26	15	28.8	0.90	-	-	-
Significance	***			***			P < 0.08			***
Mean	181	30.9	0.34	132	28.5	0.46	123	30.2	0.48	161	28.3	0.38
CV (%)	10.1			9.9			10.2			12.

*** P<0.001

The independent comparison of number and species of trypanosome parasitaemia was also possible in Boundiali. T. congolense depressed the average cow PCV during lactation more than T. vivax, but in a subsequent analysis there was no indication that a high score (mean 3.3) depressed PCV more than a low score (mean 1.5) for T. congolense parasitaemia nor for T. vivax (4.4 and 3.3, respectively).

These results were confirmed in Mushie where the PCVs of N'Dama cows and pre-weaning calves were depressed more by T. congolense than by T. vivax (Table 5). Further T. congolense parasitaemic months did not depress PCV more than the first parasitaemia The effect of intensity of infection could not be estimated as the majority of the parasitaemia scores were low (less than 3).

Table 5. Effect of species and number of trypanosome parasitaemia months on PCV of N'Dama cattle. Mushie.

Species and number of parasitaemic months	Cow average PVC during gestation (%)			Cow average PVC during lactation (%)			Species and number of parasitaemic months	Calf average PVC pre-weaning (%)
	No.	Mean	s.e.	No.	Mean	s.e.		No.	Mean	s.e.
0	183	34.5	0.28	082	34.3	035	0	178	35.3	029
1 T congolense	55	31.9	0.49	55	31.2	0.51	1 T congolense	26	33.4	0.89
1 T vivax	26	34.1	0.69	34	33.6	0.63	1 T vivax	46	34.7	0.48
2 or more T congolense	25	31.5	0.70	51	30.7	0.53	2 or more T congolense	13	33.2	0.99
2 or more others	16	31.8	0.88	35	30.5	0.63	2 or T vivax	20	34.1	0.74
							2 or more T congolense + T vivax	11	33.6	1.02
Significance	***			***				P < 0.08
Mean	305	32.8	0.32	357	32.1	0.36		294	34.1	0.35
CV (%)		13.3							10.2

*** P<0.001

Clearly trypanosome infection from natural tsetse challenge depressed PCV in cattle and in sheep in these field studies, whether the infection was T. vivax in trypanotolerant cattle and sheep in Avetonou, or T. congolense and T. vivax in N'Dama cattle in Zaire or in trypanotolerant cattle and sheep in Cote d'Ivoire. T. congolense depressed PCV more than T. vivax, but responses to a higher intensity of infection were variable. One parasitaemic month did not depress the PCV traits used in this study, but two or more parasitaemic months did.

Other factors affecting PCV

Several factors were significant sources of variation. For example, sex of progeny affected its PCV pre-weaning (Table 6), with female progeny consistently having higher PCV.

Table 6. Average PCV pre-weaning of male and female progeny at three Network sites.

Progeny sex	Sheep						Cattle
	E Boundiali			Avetonou			Boundiali			Mushie			Kolo
	No.	Mean	s.e.	No.	Mean	s.e.	No.	Mean	s.e.	No.	Mean	s.e.		No.	Mean	s.e.
Male	150	28.0	0.78	90	28.2	0.56	52	29.8		163	34.2	0.29		211	34.3	0.19
Female	148	29.0	0.82	88	28.6	0.57	71	30.6		136	34.9	0.31		221	35.5	0.18
Significance	**			NS			NS			*				***

*·P<0.05
**P<0.01
***P0.001

Lambs born as singles rather than as twins had a higher average pre-weaning PCV.

Cows failing to wean a calf had a higher average PCV during the lactational period (Table 7), a result consistent with lactation causing a depression in PCV and the reported lower PCV of lactating compared to gestating cows.

Table 7. Average PCV during lactation of cows weaning or not weaning a calf

Weaning status	Boundiali			Mushie			Kolo
	No.	Mean	s.e.	No.	Mean	s.e.	No.	Mean	s.e.
No calf weaned	25	28.8	0.69	54	33.1	0.53	98	38.6	0.30
Calf weaned	107	28.2	0.48	307	31.0	0.26	455	37.2	0.15
Significance	NS			***			***

***P<0.001.

Where more than one breed was maintained in the same environment, breed comparisons were possible. N'Dama and West African Shorthorn in Avetonou and N'Dama, Baoule and crossbreds in Boundiali all had similar mean PCV values.

Coulibaly et al. (see article 12 of these Proceedings) did not find evidence that other parasites depressed PCV values significantly in cattle and sheep in the Boundiali area, whereas trypanosomes did. Interaction between the parasites was unimportant for both PCV and growth.

There was a large variation in PCV between year-season and between herds. No biologically consistent pattern of seasonal variation emerged.

Despite the large year-season and herd variations, interactions between trypanosome infection and these effects were not significant, perhaps because the proportion of animals with infection was too low for any to be detected.

Conclusion

Statistically significant interactions between parasitaemia and ether environmental and genetic factors were not found. Further data will have to be built up to evaluate their possible importance.

Within a particular situation it is clear that several factors must be simultaneously taken into consideration when analysing the effects of trypanosome infection on PCV. If PCV levels are to be used as a criteria for trypanotolerance, then the data on which to base decisions must be derived from contemporary comparisons, i.e. in the same place, at the same time with the same management and must be adjusted for the factors identified as important. Individual factors have not necessarily the same importance in all situations; thus each situation needs to be considered separately.

Trail et al. (see article 43 of these Proceedings) have indicated from their preliminary investigations that there are promising possibilities for PCV traits to be used in selection programmes. This justifies the further work being undertaken on the identification and quantification of the effects of environmental factors on PCV in given situations.

References

Dargie, J.D., P.K. Murray, Max Murray, W.R.I. Grimshaw and W.I.M. McIntyre. 1979. Bovine trypanosomiasis: the red cell kinetics of N'Dama and Zebu cattle infected with Trypanosoma congolense. Parasitology. 78: 271-286.

Feron, A., G. d'Ieteren, P. Itty, H. Maehl, M. Mulungo, S. Nagda, R. Paling, M. Rarieya, M. Sheria, W. Thorpe and J. Trail. Can PCV be used as an indicator of trypanosomiasis and production level in cattle? 19th Meeting of the International Scientific Council for Trypanosomiasis Research and Control (ISCTRC) 1987, Lome, Togo, 30 March-3 April. In press.

ILCA/ILRAD. 1986a. The ILCA/ILRAD Trypanotolerance Network. Situation report, December 1985. Proceedings of a Network Meeting held at ILCA, Nairobi. June 1986. ILCA, Addis Ababa, Ethiopia.

ILCA/ILRAD. 1986b. The African Trypanotolerant Livestock Network. Indications from Results. 1983-1985. December 1986. ILCA, Addis Ababa, Ethiopia.

Murray, Max. 1979. Anaemia of bovine African trypanosomiasis: An overview. In: Pathogenicity of Trypanosomes. G. Losos and Amy Chouinard, eds. IDRC No. 132e. pp. 121-127.