Effect of Cassava (Manihot esculenta) Foliage Supplementation to Calves on the Viability and Egg Count of Haemonchus contortus Nematodes

American Journal of Animal and Veterinary Sciences 2 (4): 93-98, 2007
ISSN 1557-4555
© 2007 Science Publications
Effect of Cassava (Manihot esculenta) Foliage Supplementation to Calves on the Viability
and Egg Count of Haemonchus contortus Nematodes

1Juan López, 2Esteban Machín, 2Arturo Zentella, 3Victor Vázquez, 4Irma Tejada, 5Armando Shimada
and 1David Sánchez
1Campo Experimental de Huimanguillo, Instituto Nacional de Investigaciones Forestales, Agrícolas y
Pecuarias (INIFAP), Huimanguillo, Tab., México
2Ingeniería en Zootecnia, Universidad Popular de la Chontalpa, Cárdenas, Tab., México
3Centro Nacional de Investigación en Parasitología Veterinaria-INIFAP, Jiutepec, Mor., México
4Posgrado en Ciencias de la Producción y la Salud Animal, Universidad Nacional Autónoma de México
(UNAM), Cuautitlán-Izcalli, Méx., México
5Laboratorio de Rumiología y Metabolismo Nutricional (RuMeN), Facultad de Estudios Superiores
Cuautitlán-UNAM, Juriquilla, Qro., México

Abstract: Thirty early-weaned 5±3 month-old calves with an average body weight of 96±23 kg were
used; 24 were artificially infested with 90 larvae (L3), of H. contortus per kilogram body weight.
Calves grazed on African Star Grass (Cynodon plectostachyus) from 0600 to 1300 hours. Grazing was
supplemented with lucerne hay (Medicago sativa) or cassava foliage (Manihot esculenta), and 500 g?1
head?1 day?1 of a commercial feed containing 16% crude protein and trace-mineralized salt, offered
during the time spent in confinement. Five treatments were compared: (1) infested, supplemented with
lucerne; (2) as treatment (1), drenched; (3) infested, supplemented with cassava; (4) as treatment (3),
drenched; (5) non-infested, supplemented with cassava. Each treatment had three replicates of two
calves. Those that were drenched orally received 7 mg kg?1 albendazole on day 21 after being infested.
The experiment lasted until 35 days after infestation. The response criteria were number of nematodes
in the abomasum and egg count per gram of feces, both taken at weekly intervals. Numerical data were
analysed as a completely randomized design, including the effect of sampling week for egg counts and
feed intake. The average number of nematodes found in the abomasums did not differ between
treatments (P<0.05), the observed values being from 200 to 496 H. contortus. Regarding the egg count
in feces, the highest figure (822 g?1) was observed in the undrenched control treatment and the lowest
(115 g?1) in the cassava-albendazole treatment. In general, there was a 50-85% reduction in egg counts
when cassava foliage was used; the response seemingly being improved when the nematicide was
administered. Dry matter intake was lower (P<0.05) for the cassava treatments. In conclusion, cassava
foliage could be used for controlling and reducing the infestation of cattle by H. contortus.

Key words: calves, Manihot esculenta foliage, Haemonchus contortus eggs

INTRODUCTION
sheep, cattle and other ruminants and has been

reported to be the most common nematode in the

Beef cattle operations, especially those
tropical regions, because of the favourable climatic
based on grazing systems, are constantly faced with
conditions that facilitate its development and survival
diseases caused by different etiological agents
[1].
(viruses, bacteria, parasites) that not only affect the

animals’ health, but also their productivity. Parasites,
Although nematode control strategies such as the use
in general, can cause their hosts to suffer from
of
anthelmintic
drugs
(benzimidazoles,
anemia, edema, undernutrition, weight loss, slow
imidazothiazoles and macrocyclic lactones) are in
growth, gastritis, and in acute cases, even death.
use, the problem has not been satisfactorily solved
Within parasitic diseases, those caused by helminths
and, in some regions, it has even worsened due to the
are the most relevant, and the one with the highest
mismanagement of the drugs. To date there is no
incidence is by Haemonchus spp., which affects
method which is efficient, practical and sustainable,
Corresponding Author: Shimada, A. PMB 23-141; 413 Interamerican Boulevard WHI; Laredo, TX 78045; USA. Tel: + 52 419 292 0415
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American J. Animal & Vety. Sci., 2 (4): 93-98, 2007

that is, which does not present toxicity risks for both
All feedstuffs were analysed for dry matter, crude
animals and humans, and for the environment [2].
protein and iron, according to the methods suggested
An alternative would be the use of plants with
by Tejada [7]. Free and reactive condensed tannins
nematicidal properties such as those which contain
(CT) in forages were determined as described before
condensed tannins (CT). These are secondary
[3]. M. esculenta had 55.5±4.0 g CT kg?1 of dry
metabolites that in the tropics can be found in fodder
matter. Neither M. sativa nor C. plectostachyus had
crops such as Leucaena leucocephala, Gliricidia
detectable levels of CT.
sepium, Manihot esculenta [3]. The metabolic role of

CT in plants is not well known, but it has been
To remove all internal parasites, calves were
observed that they provide them with protection
subcutaneously medicated with Ivermectine (Iverfull,
against microbes, insects and even large herbivores.
Aranda) at doses of 0.2 mg kg?1 live weight. After 35
Controlled-condition studies on their anthelmintic
days, they were orally given 10 mg kg?1 live weight
effect on larvae and adult parasites of both sheep and
of Fenbendazol (Actuol, Senosiain). Six days
cattle suggest that they could be considered as
thereafter, a McMaster analysis of faeces [8],
alternatives against gastro-enteric parasites, although
indicated that all animals were parasite-free.
their presence in the diet could affect its digestibility
Although the oral anthelmintics are supposedly
and therefore its nutritive value. Concentrations of 60
eliminated within 72 h after their application, a
g kg?1 in feed improve the utilization of protein by
further period of 72 h was allowed before starting the
ruminants, although higher levels may depress
experiment proper. During this time, animals were
voluntary intake [4, 5].
adapted to the consumption of the supplemental

forages and concentrate.
The objective of this experiment was to evaluate the

anthelmintic effect of cassava foliage (M. esculenta)
A sample of faeces from a steer, orally infested with
in calves infested with H contortus, raised in a
H contortus and free from other nematodes, was
restricted grazing system.

used. Starting at 2 weeks post-inoculation, the animal
MATERIALS AND METHODS
was sampled to detect for the elimination of eggs.


The experiment was conducted in the Huimanguillo
Larvae were extracted with the Baermann method,
Experimental Station of the Instituto Nacional de
which is based on their ability to migrate within a
Investigaciones Forestales Agrícolas y Pecuarias,
semi-liquid substrate, through positive hydrotropism.
located in the State of Tabasco (17°50 N; 20 m
Feces were covered with cheesecloth and placed in a
above sea level). The predominant climate of the
funnel with distilled water. After a 12–24 h period,
State is classified as warm–humid (AmW), the
the larvae migrated, along with some escaped feces.
temperature varies from 24 to 34°C, and the annual
The larvae-containing sediment was then centrifuged
rainfall is 2,123 mm, 70% of which falls between
3 min at 3,000 rpm, washed with a glucose solution,
May and November [6].
and the supernatant was siphoned and discarded. Two

to three drops of the sediment were observed through
Thirty predominantly Brown Swiss X Zebu crossbred
a microscope to check the developmental stage and
calves, weaned at 5±2 months and with an initial
viability of the larvae; 1 mL of the sediment was then
weight of 96±23 kg were used. All animals were
placed in refrigeration. The collected larvae were
maintained on an African Star Grass (Cynodon
identified, quantified and the dosages calculated
plectostachyus) subdivided pasture, with 5-day
according to each animal’s weight [9]. Twenty-four
grazing periods, and 25 days of rest. Calves grazed
calves were infested with approximately 90 larvae
from 0600 to 1300 hours and the rest of the time they
(L
were confined and supplemented with lucerne
3) of H. contortus kg?1 live weight.
Five experimental treatments were tested: (1) infested
(Medicago sativa) hay or chopped cassava (Manihot
esculenta) foliage. The amount of forage offered was
with H contortus, supplemented with Lucerne; (2) as
adjusted daily, allowing for 5% refusal. The lucerne
treatment (1), drenched with albendazole; (3)
was commercially purchased. The cassava used was
infested, supplemented with cassava; (4) as treatment
of the “Sabanera” cultivar (MPan 51), planted as a
(3), drenched with albendazole; (5) non-infested,
fodder crop with 25 cm spacing between plants and
supplemented with cassava. Each treatment had three
30 cm between rows, and the foliage was harvested
replicates of two animals. The experiment lasted 35
daily. In addition to the forage, each animal was
days. On day 21 after infestation, treatments (2) and
offered 500 g of a 16% crude protein concentrate and
(4) received 7 mg kg?1 live weight of a commercial
25 g of a trace-mineralized formula daily.
nematicide (Albendazole [methyl 5-6 propyl thio-1H-

benzimidazole-2yl carbamate]; Lavet Laboratories).


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American J. Animal & Vety. Sci., 2 (4): 93-98, 2007

Weekly feces collections from all animals were
elimination of parasites, while in more recent papers,
analysed as described above, to measure the effect of
others do not agree [13], possibly reflecting an
the treatments on H. contortus egg yield. Blood was
increasing resistance of the parasites to the drugs.
collected in vaccutainer tubes and the serum
Table 2 shows the weekly numbers of H. contortus
separated [10]. Its iron content was determined by
eggs per gram of faeces from grazing calves
indirect atomic absorption (Nova 10 Analyzer).
supplemented with Lucerne or cassava, untreated or
Hemoglobin was measured in EDTA-added blood.
drenched with albendazole. From the first to the
Thirty-five days following medication, animals were
fourth week of the experiment, there was a gradual
slaughtered according to Mexican laws [11]. The
increment in the number of parasite eggs present in
extracted abomasums were placed in plastic bowls
the calves’ faeces, with no significant difference
and cut open, collecting their contents in a separate
between treatments (P>0.05). Eight days after
container; the mucosa was washed with tap water.
drenching (week 5), animals from the medicated
The collected volume was brought to 1–3 L, mixed,
treatment groups had significantly fewer eggs
and a 10% aliquot saved. Live parasites were placed
(P<0.05). By week 6, all treatments except the
in a saline solution, and refrigerated for later
control showed a significant reduction in egg counts
identification and quantification.
(P<0.05). The results are similar to those reported in

cattle [14] and in goats [15], when fed tanniferous
The response criteria were: abomasal parasite yield
forages.
and sex; egg numbers at weekly post-infestation

periods; blood hemoglobin and serum iron at the start
It has been reported that the mode of action of CT is
of the experiment, 21 days post-inoculation, and at
to either bind specific nutrients, and thus inhibit their
slaughter; weekly supplemented forage intake.

availability for the larvae, or to interfere with their
The numbers of larvae were analysed as completely
metabolism through a disruption in the oxidative
randomized designs, with data transformed to their
phosphorylation process, causing a reduction in egg
square roots; the other parameters were analysed as
yield or death [16]. It has been reported [14] that CT
measurements repeated over time. A SAS [12]
have a negative effect on the fecundity of female
statistical package was used.
nematodes. Moreover, it has also been informed that

CT and synthetic anthelmintic drugs have similar
RESULTS AND DISCUSSION
effects on egg yield [17].


Anti-nutritional factors: Parasite numbers present
Likewise, CT could have modified the rumen
inside the abomasums of calves infested with H.
microbial digestion processes [18, 19] as it is known
contortus and supplemented with lucerne or cassava,
that the amount and quality of the diet, as well as its
unmedicated or drenched with albendazole, are
shown in Table 1. The total number of larvae in the
fermentation pattern, can have adverse effects on the
abomasums did not differ significantly between
development and establishment of the parasites,
treatments (P>0.05) and varied from 200 to 496, with
intensifying the effect of the anthelmintic drugs [20].
no differences between the sexes. When we
Iron concentrations in blood serum from grazing
previously [5] fed confined Pelibuey sheep ad libitum
calves supplemented with Lucerne or cassava,
amounts of tanniferous forages, the parasite yields
untreated or drenched with albendazole, are shown in
were reduced 70–94%; however as our calves were
Table 3. There were no significant differences in
on pasture, they could have been naturally re-
serum iron values between treatments (P<0.05), and
infested.
the observed values were much lower than those

considered normal (100–170 µg 100 ml?1) [21]. It has
Table 1: Haemonchus contortus numbers in the abomasums of
been demonstrated that hematophagous parasites,
grazing calves supplemented with lucerne or cassava,
such as Haemonchus, consume daily up to 0.05 mL
untreated or drenched with albendazole (mean ± SEM)
of blood, which is enough as to induce anemia in the
Treatment
Total


Lucerne, untreated
255±229
147±123
108±108
host animals [22]. The observed blood serum iron
Lucerne, drenched
496±205
264±110
232±097
values showed that the calves were anemic
Cassava, untreated
466±229
245±123
221±108
throughout the experiment; therefore they were not
Cassava, drenched
200±229
88±123
112±108
able to overcome the damage suffered before the
Cassava, non-infested
407±265
223±142
184±125
initial medication. Furthermore, the effect was

prevalent regardless of the adequate levels of dietary
The drenched treatments were not 100% effective.
iron provided: cassava (200 mg kg?1), lucerne (249
However the literature also contains conflicting
mg kg?1), protein concentrate (185 mg kg?1), trace-
information, with some early authors reporting that
mineralized formula (513 mg kg?1); their daily
the use of benzimidazoles result in the total
requirement being 50 mg kg?1 [23].

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American J. Animal & Vety. Sci., 2 (4): 93-98, 2007

Table 2: Number of Haemonchus contortus eggs per gram of faeces from grazing calves supplemented with lucerne or cassava, untreated or
drenched with albendazole, measured weekly (mean ± SEM).
Treatment/ Week
1
2
3
4
5
6
Lucerne, untreated
nd
112a±48
304a±89
773a±176
921a±210
822a±117
Lucerne, drenched
nd
80a±43
225a±79
471a±158
237b±188
220b±104
Cassava, untreated
nd
50a±48
288a±89
484a±176
431a±210
215b±117
Cassava, drenched
nd
50a±48
192a±89
356a±176
147b±210
115b±117
Cassava, non-infested
nd
50a±55
306a±102
504a±204
337a±243
383b±135
Values with different superscripts are statistically significant.
nd = not detected.

Table 3. Iron (Fe) and haemoglobin (Hb) concentrations in blood serum from grazing calves supplemented with lucerne or cassava, untreated or
drenched with albendazole (mean ± SEM).
Sample
Initial
When eggs appear
Final
Treatment
Fe
Hb
Fe
Hb
Fe
Hb
Lucerne, untreated
83.7±13.03
9.05±0.70
82.5±7.9
9.05±0.44
78.7±9.5
8.83±0.54
Lucerne, drenched
80.0±11.65
8.88±0.63
76.2±7.1
8.70±0.39
95.2±8.5
9.65±0.48
Cassava , untreated
81.3±15.04
9.20±0.70
86.3±9.2
8.62±0.44
86.0±10.9
9.05±0.54
Cassava , drenched
86.5±13.03
8.81±0.70
74.7±7.9
8.74±0.44
82.2±9.5
8.59±0.54
Cassava , non-infested
81.3±15.04
8.85±0.81
86.3±9.2
9.22±0.50
86.0±10.9
9.27±0.63


Table 4. Weekly supplement intake of grazing calves supplemented with lucerne or cassava, untreated or drenched with albendazole, kg (mean ±
SEM).
Week

Treatment
1
2
3
4
5
6
Lucerne, untreated
6.4±1.2
7.9±1.3
9.0±1.2
11.4±1.8
11.4 a±1.2
9.9ª±1.0
Lucerne, drenched
9.1±1.1
9.1±1.1
10.8±1.1
13.4±1.7
13.4 a±1.1
11.8 a±0.9
Cassava, untreated
5.5±1.2
5.6±1.3
6.9±1.2
8.9±1.8
6.4b±1.2
6.0 b±1.0
Cassava, drenched
5.9±1.2
6.7±1.3
6.9±1.2
7.3±1.8
6.6 b±1.2
5.9 b±1.0
Cassava, non-infested
7.3±1.4
8.1±1.5
7.3±1.4
7.2±2.1
6.8 b±1.4
6.2 b ±1.2
Values with different superscripts are statistically significant.


Table 3 also shows the hemoglobin concentrations in
dietary DM do not affect the intake or nutritive value of
blood from grazing calves supplemented with lucerne
the diet in sheep [27, 15], it has been suggested that about
or cassava, untreated or drenched with albendazole.
60 g of CT kg?1 of DM, could decrease consumption,
There were no significant differences between
due to its astringency having an adverse effect on
treatments at any sampling time (P>0.05). Nevertheless
palatability [4, 28] and digestibility. In a previous
the values fell within the lower limits of what would be
experiment with confined sheep, we did not observe
considered as normal (8–15 g dl?1) [24] and were also
any differences in voluntary intake [5], but calves could
inferior to those previously observed in sheep [25].
have a lower threshold value [28, 29].
Whereas it appears that infestation with nematodes

decreases blood haemoglobin levels [26], the quality of
CONCLUSIONS
the diet could exert a synergistic effect [20].


1. Supplementation of pasture-raised sheep with M.
The weekly supplement intake of grazing calves, with
esculenta decreases faecal H. contortus egg counts.
lucerne or cassava, untreated or drenched with
2. Blood serum iron levels were lower than normal,
albendazole, is summarized in Table 4. There were no
probably due to the parasites.
significant differences between treatments in
3. Condensed tannins had an adverse effect on
supplement consumption during the first 4 weeks of the
voluntary feed intake.
experiment (P>0.05); however, the intake in the

lucerne, but not the cassava treatments, had gradually
ACKNOWLEDGMENTS
increased and therefore by the fifth week, the difference

between forages had become significant (P<0.05).

This work is part of the Baccalaureate theses of the
Although the supplemented cassava contained 56 g of
second and third authors and was financed by
CT kg?1 DM, and levels of 50–80 g of CT kg?1 of
CONACYT-SAGARPA (Project C01-1464). The

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American J. Animal & Vety. Sci., 2 (4): 93-98, 2007

English of the manuscript was revised by Nancy M.
13. Montalvo, A.X.G., 2003. Determinación de
Boston.
nematodos
gastroentéricos
resistentes
a
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improvement of blood nutritional indicators in

half-bred zebu cows. Livestock Res. Rural Dev. 14(5).

http://www.cipav.org.co/lrrd/lrrd14/5/copp145.htm












































98

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