Prevalence of Bovine Tuberculosis in Cattle in The Highlands of Cameroon Based On The Detection of Lesions in Slaughtered Cattle and Tuberculin Skin Tests of Live Cattle
Prevalence of Bovine Tuberculosis in Cattle in The Highlands of Cameroon Based On The Detection of Lesions in Slaughtered Cattle and Tuberculin Skin Tests of Live Cattle
Prevalence of Bovine Tuberculosis in Cattle in The Highlands of Cameroon Based On The Detection of Lesions in Slaughtered Cattle and Tuberculin Skin Tests of Live Cattle
ABSTRACT: Bovine tuberculosis (TB) is an important neglected zoonosis in Cameroon, where many communi-
ties depend on their livestock for livelihood and the incidence of human TB and TB-HIV/AIDS co-infection are
high and increasing annually. The aim of this study was to estimate the prevalence of bovine TB in cattle in the
highlands of Cameroon. The magnitude and trend of detecting TB lesions in slaughtered cattle (1994 to 2010)
and tuberculin skin tests (TST) in 2853 cattle (84 herds) of 39 livestock rearing communities were analysed. Of
129 165 slaughtered cattle inspected, 599 (0.46%; 95% CI: 0.43%–0.50%) showed suspected TB lesions among a
total of 983 (0.76%; 95% CI: 0.71%–0.81%) identified pathologies. The monthly TB detection rates ranged from
0.30% (95% CI: 0.20%–0.40%) to 0.81% (95% CI: 0.64%–0.98%) and annual rates from 0.04% (95% CI: 0%–0.11%)
to 1.46% (95% CI: 1.22%–1.69%). The rates were not affected (P < 0.05) by season and fluctuating peaks were
also recorded. The comparative TST revealed that bovine TB was widely distributed in live cattle (4.67%; 95%
CI: 3.89%–5.44%) and was higher (χ 2 = 17.50, P ≤ 0.001) in the Western highlands than Adamawa plateaux.
Comparative TST bovine TB reactors were higher (P < 0.05) in cattle managed in semi-intensive and beef pro-
duction systems compared to the others. Animals in small herds showed higher (χ2 = 4.283, P = 0.038) rates than
those in large herds. Bovine TB prevalence in exotic/upgraded cattle was comparable to that of the Red Bororo
zebu but higher than the rates in Guadali (χ2 = 4.971, P = 0.026) and White Fulani (χ2 = 5.6, P = 0.018) zebus.
Among the indigenous zebus, the rate was higher in Red Bororo than the Guadali (χ2 = 6.244, P = 0.012) and
White Fulani (χ2 = 6.568, P = 0.010). Sex did not influence (χ2 = 0.410, P = 0.522) bovine TB prevalence in this
study but diagnosis of the disease was higher (χ2 = 5.787; P = 0.016) among adult/older cattle than in younger
animals. Further analysis of the TST responses revealed that atypical mycobacterial infections was widespread
and 6.83% of tested animals showed positive reactions at both bovine and avian tuberculin injection sites and
a strong association (χ 2 = 2.512; P = 0.113) between skin responses to both tuberculins. The study confirms
that bovine TB is prevalent in live cattle and meat production abattoirs in Cameroon and we recommend strict
a interpretation of TST results for maximum diagnosis of the disease in the local environment. A need for
comprehensive investigation of the molecular epidemiology, zoonotic risks and the public health importance
of bovine TB in Cameroon cannot be overemphasised.
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Original Paper Veterinarni Medicina, 57, 2012 (2): 59–76
Tuberculosis (TB) is an important zoonosis culture of human sputa is only sporadically per-
caused by bacteria of the Mycobacterium tubercu- formed and then mainly for research purposes.
losis complex. M. bovis is virulent for cattle but can Awah-Ndukum et al. (2010) reported acid-fast
infect other animals and humans causing disease tubercle bacilli in 51% of suspected TB lesions in
and pathology similar to M. tuberculosis, which cattle based on mycobacterial culture and Ziehl-
is naturally pathogenic for man (Biet et al. 2005; Neelsen staining with microscopy and in 31% of the
Kaneene and Pfeiffer 2006; Thoen et al. 2006). The specimens based on direct smear microscopy with
prevalence of human TB in the Central African Ziehl-Neelsen staining without culture.
sub-region is high and increasing rapidly with the Conventional mycobacteriological methods
spread of the HIV/AID infection (WHO 2009, are often unsafe in inadequately constructed and
2010). For example, TB remains a common disease poorly equipped laboratories (Igbokwe et al. 2001),
in Cameroon, with a current annual incidence of common in most of Africa. Such methods are also
almost 200 cases per 100 000 of the population expensive, time consuming, laborious and not
(WHO 2009), especially among the economically practical for surveillance purposes (Strong and
active 21–40 age group (Noeske et al. 2004; Ane- Kubica 1985; Grange et al. 1996; Parsons et al. 2002;
Anyangwe et al. 2006). Extraordinarily high rates Warren et al. 2006). Further, the interpretation of
of TB-HIV/AIDS co-infection exist in Cameroon results is highly subjective and prone to errors such
and between 29% and 43% of TB cases of all ages as those possible when interpreting differences
are also positive for HIV/AIDS (Noeske et al. 2004; in colony morphology (Strong and Kubica 1985;
WHO 2009, 2010). Bovine TB is endemic in most Grange et al. 1996; Ameni et al. 2010). Though
of Africa (Ayele et al. 2004), and is under investi- also prone to inspector subjectivities and errors,
gated. Over 98.9% of all reported cases are in cat- meat inspection provides very significant insight
tle which is also a major source of animal protein into the prevalence of many infectious diseases and
(AU/IBAR 2006). An increasing human population plays vital roles in both the quality assurance and
and food shortage are some evident concerns in quality control systems for the gross inspection of
Cameroon. The keeping of livestock is integral to carcasses (Edwards et al. 1997; Hinton and Green
the socio-economic, cultural and religious activities 1997; Asseged et al. 2004). Major improvements in
of many communities in the country and close hu- animal and human health with regard to consumer
man-livestock interactions are common. M. bovis protection and eradication of epizootic TB in many
have been isolated from humans in parts of Africa developed countries was achieved when a drastic
including Cameroon (Cosivi et al. 1998; Kazwala reduction in relevant or suspicious lesions at meat
et al. 2001a; Niobe-Eyangoh et al. 2003; Cadmus inspection was strictly employed to provide the
et al. 2006; Zinsstag et al. 2006) and epidemiologi- quality and protection demanded for consumers
cal associations between bovine TB in cattle and (Grossklaus 1987; Hinton and Green 1997). The
human TB have been suggested (Cook et al. 1996; implementation of the post mortem detection of
Regassa et al. 2008). TB lesions in carcasses and during meat inspection
Post mortem detection of TB lesions in animal of slaughtered animals has been proposed (Corner
carcasses usually indicates the advanced stages of 1994; Edwards et al. 1997; Shitaye et al. 2006), and
bovine TB (Corner 1994; Shitaye et al. 2006). The continues to be the appropriate diagnostic and sur-
detection of lesions during the meat inspection of veillance tool in many developing countries where
slaughtered animals is the basis for indicating the bovine TB is endemic.
occurrence of the disease in Cameroon (Doufissa TST are the best procedures available interna-
1993; Awah-Ndukum et al. 2005). TB lesions are tionally for the field diagnosis of bovine TB in
common pathologies identified in slaughtered cat- live animals (de la Rua-Domenech et al. 2006a, b).
tle in the country and rates ranging from 0.18% There are recommended cut-off points for increas-
to 4.25% have been recorded (Awah-Ndukum es in skin thickness for a tuberculin test to be posi-
et al. 2005, 2010). However, there are only a few tive (OIE 2009), which are the basis for eliminating
reports of the bacteriological isolation and mo- positive reactors in eradication programmes (Good
lecular genotyping of TB in Cameroon (Njanpop- 2006). However, political and socio-economic con-
Lafourcade et al. 2001; Niobe-Eyangoh et al. 2003). straints as well as a lack of attention in developing
Mycobacteriological diagnosis of bovine TB in ani- and poor countries like Cameroon are significantly
mals is practically unknown in Cameroon and the hampering routine tuberculin testing and the elimi-
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Veterinarni Medicina, 57, 2012 (2): 59–76 Original Paper
nation of infected cattle, which has proved very ef- conducting ante mortem of live animals and post
fective in eradicating bovine TB in most developed mortem examinations of slaughtered cattle.
countries (Gilbert et al. 2005; Abernethy et al. 2006; After obtaining consent from the relevant au-
Good 2006). There are scant reports approximat- thorities, members of the research team liaised
ing the prevalence of bovine TB based on the TST with the abattoir veterinarians, assisted in meat
of live cattle in Cameroon (Merlin and Tsangueu inspection from March 2008 to December 2010
1985; Tanya et al. 1985; Martrenchar et al. 1993; and also collected the required data. The relevant
Nfi and Ndi 1997; Muchaal 2002). The epidemiol- data (daily, monthly and yearly) retrieved from
ogy of bovine TB and its implications on livestock the records were the number of slaughtered and
productivity and risks to human health are largely inspected cattle carcasses, and the number with
unknown. Bovine TB is neglected in Cameroon and suspected TB lesions. The slaughter and meat in-
zoonotic TB is increasingly becoming a source of spections were based on procedures legislated by
concern to practitioners of veterinary and espe- the law regulating Veterinary health inspection
cially human medicine in the country because TB and notification of contagious animal diseases in
is the most common opportunistic disease affect- Cameroon (MINEPIA 2002). Briefly, the procedure
ing HIV/AIDS patients in Cameroon (Noeske et al. employed visual examination, palpation and inci-
2004). The apparent risks of exposure and trans- sion of the lungs, liver and kidneys, lymph nodes
mission of bovine TB in cattle and humans war- of the thoracic and head regions, the mesenteric
rant comprehensive investigation of the prevalence lymph nodes, other lymph nodes and organs of the
of bovine TB in cattle, especially in high risk and body. For condemnation, the Veterinary inspector
cattle-producing areas. would seize the whole carcass if generalised TB was
A more serious focus on bovine TB status as well detected; otherwise only the parts drained by the
as accurate estimation of the magnitude and dis- affected lymph nodes and affected organs were con-
tribution of bovine TB in cattle are essential for demned (Corner 1994; FAO 1994). There were no
appropriate intervention strategies. This study was pre-slaughter TB testing schemes at the abattoir but
carried out to ascertain the magnitude and trend of ante-mortem inspections for general examination
detection of TB lesions in slaughtered cattle at the of health were carried out. Animals that showed
Bamenda city abattoir of the Western highlands of signs of ill-health were usually not slaughtered but
Cameroon over a period of more than seventeen kept for further appraisal before slaughter could be
years. The study also reports the estimated preva- recommended at a later date.
lence of bovine TB based on the TST of live cattle in
the wider agro-ecological highlands of Cameroon.
Tuberculin skin tests in cattle: Study area
and selection of herds
MATERIAL AND METHODS
The cattle populations in the Western highlands
Location of the abattoir and post mortem (5°–7°N and 10°–11°E) and Adamawa plateaux
detection of tuberculosis lesions (6–7°30’N and 12°30’–14°E) of Cameroon were
sampled from March to September 2009 to ana-
The present study reports on the prevalence lyse responses to tuberculin skin tests (TST) us-
of tuberculosis lesions in cattle in the Bamenda ing both avian (AT) and bovine (BT) tuberculin
municipal abattoir of the Western highlands of purified protein derivates (Lelystad Biologicals,
Cameroon (5°–7°N and 10°–11°E) between 1994 Lelystad, the Netherlands) as part of a bovine
and 2010, with reference to the variations which TB prevalence study. A single intradermal TST
occurred over time. The abattoir is the largest in (SIT) bovine TB prevalence rate of 26% recorded
the region and was selected based on its geographic in the peri-urban areas of Bamenda, Northwest
proximity to the largest cattle markets and main Cameroon (Muchaal 2002), was used to estimate
trade routes. The abattoir was under the super- the number of cattle required to detect ≥1 infected
vision of MINEPIA (Ministère de l’Elevage, des animal with a desired 95% confidence and preci-
Pêches et des Industries Animales – Ministry of sion of ≥ 5% as previously described (Thrusfield
Livestock, Fisheries and Animal Industries) and 2007). The selection of cattle herds was done by
qualified veterinarians served as meat inspectors the random-number generation method of cattle-
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Original Paper Veterinarni Medicina, 57, 2012 (2): 59–76
keeping communities, cattle owners and locations the increase in the skin thickness at the AT site
of herds from records of annual livestock vaccina- of injection. Thus, the skin response for SICCT-
tion campaigns (contagious bovine pleuropneu- BT was given by [(BT72–BT0) – (AT72–AT0)] and
monia, pasturellosis, black quarter) at the Regional SICCT-AT by [(AT72–AT0) – (BT72–BT0)]. BT0 and
Delegations of MINEPIA. The selection procedure AT0 are the measures of skin fold thickness prior to
took into consideration costs, season and road ac- injecting BT and AT. BT72 and AT72 are the meas-
cessibility (including distance and time to trek to ures 72 h after injecting BT and AT. For SIT-BT and
herds) and local cultural beliefs because a farmer’s SIT-AT, a reaction was considered positive if the in-
willingness to participate was never guaranteed. crease in skin-fold thickness at the specified tuber-
All animals within the chosen herds were tested culin site of injection [(BT72–BT0) or (AT72–AT0)]
except for recently calved cows (within two months was ≥ 4 mm, negative if the increase was ≤ 2 mm,
post-partum) and calves less than six months old and inconclusive if the increase was between
because of immuno-suppression in lactating cows > 2 mm and < 4 mm.
and high maternal antibodies in calves which de- The animals in this study were reared tradition-
sensitise them to tuberculin (Costello et al. 1997; ally with or without transhumance, as well as in
Shirima et al. 2003). Placed ear tags and skin tattoos semi-intensive and intensive systems. They were
were used to identify test animals and herdsmen composed of the indigenious zebus, upgraded and
had also memorised features for each animal under exotic breeds. The purpose of the study was ex-
their care (e.g., vocals, body markings, manner- plained to the farmers with the assistance of local
isms). However, the right horn or horn bud were veterinarians, community leaders and trusted in-
also marked with red cosmetic nail varnish to guar- termediaries. A herd was tested after an informed
antee that all tested animals were presented when consent was given by the owner. Apart from the in-
the results were being read. Other information re- tradermal injections of AT and BT and procedural
lating to the location, husbandry practices, breed, restraining manipulations for safety purposes, the
sex and age of the animal were noted. The ages and animals were not subjected to suffering.
breeds of the animals were provided by the farmers,
or otherwise were determined as described earlier
(Blench 1999; Turton 1999; MINEPIA 2002). Management of data and statistical analysis
The single intradermal comparative TST (SICCT)
and single intradermal TST (SIT) were performed Slaughter and meat inspection records of approx-
on a total of 2853 cattle from 61 herds (33 village imately 129 165 mostly Zebu cattle originating from
communities) in the Sudano-guinea Western high- the Western highland regions were scrutinised. The
lands and 23 herds (seven village communities) in proportion of carcasses with suspected TB lesions
the Vina area of the Guinean savannah Adamawa of the total slaughtered cattle and the standard er-
plateaux. TST were carried out in the selected ror were calculated and the Mann-Whitney test
cattle by intradermal injections of 0.1ml each of was used to compare seasonal observations as
AT (2500 IU/dose) and BT (3000 IU/dose) in two previously described (Greiner and Gardner 2000;
sites, at 12 cm apart in the right neck region. A Thrusfield 2007).
correct intradermal injection was confirmed by The existence of bovine TB had been established
palpating a small grain-like swelling at each injec- in the country (Doufissa 1993; Martrenchar et al.
tion site. Skin thickness was measured prior to and 1993; Muchaal 2002; Awah-Ndukum et al. 2005),
72 h after injecting the tuberculins using a digital and the diagnostic accuracy of the tuberculin tests
calliper. The OIE-recommended ≥ 4-mm cut-off was assumed to be constant across the regions.
point of increase in skin fold thickness (OIE 2009) However, due to the lack of TST accuracy data for
was assessed for TST reactor status. Briefly, for the exact Cameroon environments, the sensitivity
the SICCT-BT test, a reaction was considered to [100% (95% CI: 59.8–100%)] and specificity [90.9%
be positive if the increase in skin thickness at the (95% CI: 69.4–98.4%)] of the findings obtained by
BT site of injection was ≥ 4 mm greater than the Ameni et al. (2000) in similar tropical conditions in
reaction shown at the site of the AT injection. The Ethiopia were used to correct the observed rates of
reaction was inconclusive and negative if the in- SICCT-BT reactors. The data (90% for specificity
crease in skin thickness at the BT site of injection and 86.4% for sensitivity) obtained by Pollock et al
was from 1 to 4 mm greater and < 1 mm less than (2003) was also used to adjust the observed rates of
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Veterinarni Medicina, 57, 2012 (2): 59–76 Original Paper
SIT-BT reactors. These rates were corrected using 0%–0.11%) to 1.46% (95% CI: 1.22%–1.69%). Over
the Rogan-and-Gladen formula and the 95% con- 60.94% of all pathologies that warranted partial or
fidence intervals calculated (Greiner and Gardner whole carcass condemnation were due to TB le-
2000; Thrusfield 2007). sions. High detection rates of TB lesions in March,
All observed data were initially entered into April, June and August and several fluctuating an-
Excel 2007 (Microsoft Corporation, USA) and nual peaks (Figure 2) were recorded. However, no
exported to the SigmaPlot 11.0 (Systat Software difference (Mann-Whitney Statistic = 4588; P =
Inc., Richmond, USA) for further analysis. The 0.927), was observed between the rates for wet
Chi-square test was applied to compare rates of season (0.46%; 95% CI: 0.32%–0.59%), and dry
individual and herd TST reactors in the groups of season (0.33%; 95% CI: 0.25%–0.41%). The regres-
variables studied. The odds ratio, relative risks and sion model revealed a weak positive gradient (Y =
regression analysis were used to assess the strength 0.0529X–0.0978; R2 = 0.5262), suggesting stagna-
of association of different factors with the preva- tion or a mild increase in the trend of TB lesion
lence of bovine TB (Thrusfield 2007). occurrence in the Bamenda municipal abattoir.
(a) (b)
Figure 1. Cattle tissues showing incised tuberculous lesions detected at slaughter/meat inspection in the Bamenda
city abattoir; (a) lung and lung lymph nodes; (b) various lymph nodes (and enlarged kidney)
63
64
Table 1. Prevalence of single intradermal comparative cervical tuberculin skin test (SICCT) responses in cattle according to location, breed, sex, age group, management
system and herd sizes in the highland regions of Cameroon
Animals tested SICCT-AT positive reactors* Doubtful SICCT-BT reactors SICCT-BT positive reactors
Variable Label
(n) n % (95%CI) n % (95%CI) n % (95%CI)
Original Paper
Total all animals 2853 81 2.84 (2.23–3.45) 203 7.83 (6.84–8.81) 121 4.67 (3.89–5.44)
Sudano-Guinea
2126 67 3.15a (2.41–3.89) 172 8.90a (7.69–10.11) 104 5.38a (4.42–6.34)
Agro-ecological (Western Highlands)
Regions Guinean savannah
727 14 1.93a (0.93–2.92) 31 4.69b (3.15–6.23) 17 2.57b (1.42–3.72)
(Adamawa plateaux)
Graded/Exotic 368 11 2.99a (1.25–4.73) 36 10.76a (7.60–13.93) 26 7.77a (5.04–10.51)
Guadali 1317 20 1.52a (0.86–2.18) 82 6.85b (5.49–8.21) 45 3.76b (2.73–4.79)
Breed Namchi 33 0 0 0 0 1 3.03
b a a
Red Mbororo 487 35 7.19 (4.89– 9.48) 56 12.65 (9.70–15.60) 32 7.23 (4.93–9.53)
a b
White Fulani 648 15 2.31 (1.16–3.47) 29 4.92 (3.26– 6.59) 17 2.89b (1.60–4.18)
female 2212 66 2.98a (2.27–3.69) 172 8.55a (7.39–9.72) 97 4.82a (3.93–5.72)
Sex
male 641 15 2.34a (1.17–3.51) 31 5.32a (3.58–7.06) 24 4.12a (2.58–5.66)
young (age ≤ 4) 1481 48 3.24a (2.34–14) 94 6.98a (5.68–8.28) 49 3.64a (2.69–4.59)
Age (years)
adult (age > 6) 1372 33 2.41a (1.59–3.22) 109 8.74a (7.25–10.23) 72 5.77b (4.54–7.01)
extensive 1510 44 2.91a (2.07–76) 85 6.19a (4.98–7.41) 58 4.23a (3.21–5.24)
intensive 138 2 1.45ac (–0.54–3.44) 15 11.96b (6.54–17.37) 5 3.99a (0.72–7.25)
Management system semi-intensive 1205 35 2.90bc (1.96–3.85) 103 9.40b (7.76–11.05) 58 5.30a (4.03–6.56)
a a
beef herds 2357 73 3.10 (2.40–3.80) 146 6.81 (5.80–7.83) 109 5.09a (4.20–5.97)
dairy herds 496 8 1.61a (0.50–2.72) 57 12.64b (9.72–15.57) 12 2.66a (1.25–4.08)
Herd sizes (animals animals ≤ 40 1325 32 2.42a (1.59–3.24) 81 6.73a (5.38–8.07) 69 5.73a (4.48–6.98)
per herd) animals > 40 1528 49 3.21a (2.32–4.09) 122 8.78b (7.36–10.20) 52 3.74b (2.79–4.70)
0.8
0.6
0.4
0.2
0.0
1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010
Year
Figure 2. Annual prevalence of tuberculous lesions in slaughtered cattle recorded at the Bamenda municipal abattoir,
Cameroon
positive reactors (Table 3) [OR = 121.17 (95%CI: those in large herds. The rates were significantly
83.02–176.85); RR = 4.42 (95%CI: 3.50–5.58); χ2 = higher for the upgraded and exotic cattle than the
1499.942; P ≤ 0.001]. The trend of typical and Guadali (χ2 = 4.971, P = 0.026), and White Fulani
atypical mycobacterial infection in cattle was of (χ 2 = 5.6, P = 0.018) zebus. However, among the
co-occurrence and their rates were not significantly indigenous zebus, the disease was more prevalent
different (χ2 = 2.512; P = 0.113) in the studied re- in the Red Mbororo breed than the Guadali (χ2 =
gions. Overall, 6.83% of tested animals responded 6.244, P = 0.012), and White Fulani (χ2 = 6.568, P =
positively to both SIT-BT and SIT-AT (Figure 3). 0.010). Comparable rates were noted between the
The rates of SICCT-BT reactors were signifi- upgraded / exotic and local Red Mbororo breeds.
cantly higher in cattle managed in semi-intensive Sex did not seem to influence the prevalence rate
and beef production systems compared to the other of bovine TB (χ 2 = 0.410, P = 0.522). The trend
systems (P < 0.05). However, more cattle in the was towards a higher detection of positive reactors
intensive and dairy production systems showed (χ 2 = 5.787; P = 0.016), and more doubtful cases
significantly higher doubtful reactions (P < 0.05). among adult/older cattle than in younger animals
The animals in small herds (≤ 40 animals), showed (Figure 4).
higher (χ2 = 4.283, P = 0.038) bovine TB cases than The different predicted variables for SICCT–
BT outcomes (Table 4) showed that sex, age and
breed served as good indicators of bovine TB in
the study. Female cattle, adult/older animals, up-
graded/exotic and Red Mbororo breeds were more
likely to test positive for SICCT-BT than male
cattle, younger animals, Gudali and White Fulani
cattle, respectively. Although the rates of SICCT-
BT positive reactors was significantly higher in
the Western highland regions compared to the
Adamawa plateaux (χ 2 = 17.50, P ≤ 0.001), the
different study sites on their own seem to pose
little or similar risks [OR = 0.0; RR = 0.97 (95%CI;
0.96–0.98)]. The detection of SICCT-AT positive
reactors was also not influenced by the differ-
ence in regions [OR = 0.0; RR = 0.92 (95%CI:
0.91–0.94); χ2 = 0.0145, P = 0.904)]. Classification
Figure 3. Neck of cattle showing Tuberculin skin test of herds with at least one test positive SICCT-BT
response to bovine tuberculin (red arrow) and avian and SIT-BT reactor and showing major differ-
tuberculin (orange arrow) purified protein derivatives ences between study sites and husbandry manage-
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Original Paper Veterinarni Medicina, 57, 2012 (2): 59–76
Table 2. Distribution of single intradermal tuberculin skin test (SIT) reactors according to location, breed, sex, age
group, management system and herd size
Agro-ecological Sudano-Guinea (WHC) 2126 208 9.78a (8.52–11.05) 230 14.03a (12.55–15.51)
Regions Guinean savannah (ADP) 727 42 5.78b (4.08–7.47) 39 6.89b (5.05–8.73)
Graded/Exotic 368 40 10.87a (7.69–14.05) 53 18.72a (14.73–22.71)
Guadali 1317 102 7.74b (6.30–9.19) 114 11.20b (9.50–12.90)
Breed Namchi 33 1 3.03 1 3.03
a ab
Red Mbororo 487 65 13.35 (10.33–16.37) 61 16.26 (12.99–19.54)
b
White Fulani 648 42 6.48 (4.59–8.38) 40 7.95b (5.87–10.03)
female 2212 212 9.58a (8.36–10.81) 222 13.01a (11.60–14.41)
Sex
male 641 38 5.93a (4.10–7.76) 47 9.47a (7.20–11.73)
young 1481 112 7.56a (6.22–8.91) 114 9.94a (8.42–11.47)
Age
adult 1372 138 10.06a (8.47–11.65) 155 14.66b (12.78–16.53)
extensive 1510 125 8.28a (6.89–9.67) 120 10.27a (8.74–11.80)
intensive 138 16 11.59bc (6.25–16.94) 18 16.94ab (10.68–23.20)
Management c
semi-intensive 1205 109 9.05 (7.43–10.67) 131 14.10b (12.13–16.06)
system
beef herds 2357 192 8.15a (7.04–9.25) 208 11.42a (10.14–12.70)
dairy herds 496 58 11.69b (8.87–14.52) 61 15.97b (12.74–19.19)
animals ≤ 40 1325 110 8.30a (6.82–9.79) 123 12.02a (10.27–13.77)
Herd sizes
animals > 40 1528 140 9.16a (7.72–10.61) 146 12.38a (10.72–14.03)
Table 3. Association between individual responses to Avian PPD and Bovine PPD*
*positive and negative reactions were defined as skin indurations of ≥ 4 mm and < 4 mm, respectively; OR = 121.17 (95%CI:
83.02–176.85); RR = 4.42 (95%CI: 3.50–5.58); χ2 = 1499.942; P ≤ 0.001
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Veterinarni Medicina, 57, 2012 (2): 59–76 Original Paper
14
3.11
12
10 3.43 8.72
8.76
8 7.98
6 5.56
4
6.14 5.41
2 3.23 3.93
3.93 6.14 5.41
3.23
0
Age ≤ 2 2 < Age ≤4 4 < Age ≤ 6 Age > 6
(1.73 ± 0.47) (3.46 ± 0.05) (5.46 ± 0.05) (8.42 ± 1.05)
Years
one million inhabitants of the city, peri-urban a few parts (e.g., horn and hooves), almost all
areas and its neighbouring villages (rural areas). the other parts and organs of a carcass are ed-
Cattle slaughtered at the abattoir were mainly ible in Cameroon if passed at slaughter and meat
of the Zebu type and originated from within inspection. Retrospective analysis showed that
the Western highlands. With the exception of tuberculous lesions were the most often detected
67
Original Paper Veterinarni Medicina, 57, 2012 (2): 59–76
Positive herds
Herds
Variable Label SICCT-BT SIT-BT
tested
n % (95%CI) n % (95%CI)
60.24 83.33
Total all herds 84 46 70
(50.73–69.76) (75.36-91.30)
Sudano-guinea 68.53a 86.89a
61 38 53
Agro-ecological (Western Highlands) (57.94–79.12) (78.41–95.36)
Regions Guinean savannah 38.26a 73.91a
23 8 17
(Adamawa plateau) (20.21–56.32) (89.80–51.60)
75.01a 88.64a
extensive 44 30 39
(63.38–86.64) (79.26–98.01)
55.01b 75.00b
intensive 4 2 3
(10.69–99.32) (19.40–99.40)
Management 42.78c 77.78a
semi-intensive 36 14 28
system (28.09–57.47) (64.20–91.36)
63.77a 84.06a
beef herds 69 40 58
(53.47–74.08) (75.42–92.70)
44.00b 80.00b
dairy herds 15 6 12
(21.17–66.84) (95.70–51.90)
58.93a 80.36a
animals ≤ 40 56 30 45
(47.22–70.65) (69.95–90.76)
Herd sizes
62.86a 89.29b
animals > 40 28 16 25
(46.60–79.13) (99.10–76.50)
SICCT-BT = single intradermal comparative cervical tuberculin skin test to detect bovine TB
SIT-BT = single intradermal tuberculin skin test to detect bovine TB
a–c
different letters in a class of labels are significantly different (P < 0.05)
pathologies and the main cause of condemnations differences could be explained by many factors in-
at the abattoir. Awah-Ndukum et al (2005, 2010) cluding differences in the disease status in the ani-
had recorded higher rates of bovine TB in slaugh- mal populations, the degree of implemention of the
tered cattle in other parts of the country ranging disease control programme and various environ-
from 0.67%–4.28%. They also observed that tuber- mental influences. The association noted between
culous lesions were 3–5 times more frequent than the increase in TB lesion detection rates in recent
other lesions in abattoirs in the western highland years (especially from 2002–2010), could be associ-
and littoral regions of Cameroon. Bovine TB is ated with an increase in the number of slaughtered
therefore endemic in Cameroon since the cattle cattle (due to increasing public demands for meat),
slaughtered in these abattoirs are from the main but it coincided with the additional recruitment
cattle-producing regions of the country including of personnel and enhanced efficiency of meat in-
both highland regions in this study. Compared spectors. Thus, the increasing trend recorded may
to data recorded elsewhere in Africa, the rate re- not have been an actual increase of the disease
corded in this study was higher than 0.052% re- state but is probably due to improved diagnostic
ported by Shitaye et al. (2006), but lower than other awareness of the disease and intensification of the
findings ranging from 0.49% to 11.3% (Du-Sai and slaughter/meat inspection procedure. Edwards et al
Abdullahi 1994; Ankugah 2002; Ameni and Wudie (1997) have stated that while in need of modifica-
2003; Asseged et al. 2004; Diguimbaye-Djaibe et al. tion, meat inspections still play an important role
2006; Muller et al. 2008; Biffa et al. 2009; Cadmus in meat safety and quality assurance for consum-
and Adesokan 2009; Ngandolo et al. 2009). These ers, and should also be based on the identification
68
Veterinarni Medicina, 57, 2012 (2): 59–76 Original Paper
and analysis of risks. Indeed, limited progress with techniques, along with the intensification of meat
bovine TB eradication schemes in some industri- inspection and tracing of infected/suspicious cases
alised countries and the increasing involvement of to the herds of origin would be necessary for ef-
non-tuberculous mycobacteria in mycobacterial ill- fective surveillance of TB in the studied regions
nesses in animals and humans (Edwards et al. 1997; and the whole of Cameroon. However, the im-
Biet et al. 2005), justify the continued maintenance portance of this study cannot be underestimated
of intensive post mortem examination of carcasses considering the zoonotic implications of bovine
(Edwards et al. 1997). TB. Furthermore, most farmers shared the same
The wide fluctuations and numerous peaks of TB micro-environments with their animals, thereby
lesion occurrence in this study could be associated increasing the risk of exposure and spread of the
with an unchecked course of bovine TB in live cat- disease from infected to uninfected or “clean” herds
tle in the environment. There is no active control of and people in the community.
the disease in animals in Cameroon. Also, animals
presenting poor symptoms of health and production
characteristics are usually among the first to be re- Prevalence of bovine tuberculosis based
moved from herds and slaughtered for meat produc- on tuberculin skin tests
tion. Natural and arbitrary (human) selections of live
animals could have determined the detection rates The TST showed that bovine TB was widespread
of bovine TB in slaughtered animals and its semi- in cattle in the studied regions and the prevalence
natural course in herds and rearing communities in rates were comparable irrespective of the manage-
the studied regions. The improved meat inspection ment system employed. This finding is in agree-
team from 2002 was more thorough and detected ment with Inangolet et al. (2008), who suggested
cases which otherwise would have been missed by high levels of infectiousness of bovine TB under
the former setup. However, the possibility of un- the common cattle management practices and hu-
der-recording and under-detection remains. For ex- mid tropical conditions. However, inefficient close
ample, it was not uncommon to note questionable contact between diseased and healthy animals in
summary meat inspection reports when compared extensive systems, dairy herds and large herds, and
to the crude abattoir registers. Poor clinical meat possibly a decrease in virulence and transmission
inspection records, which could not be relied upon, capacity of the causal strains due to adverse weather
have been reported in Cameroon (Awah-Ndukum et (Oloya et al. 2006), and low infectiousness of the
al. 2005; Awah-Ndukum et al. 2010). The findings of local zebu cattle (Ameni et al. 2006, 2007; Inangolet
this study agree with earlier reports that post mor- et al. 2008), were also characteristics in the study
tem surveillance through the detection of bovine TB environments. A better resistance or adapted toler-
lesions depend on the work load, time and diligence ance to bovine TB infection of some local breeds
of the inspector conducting the examination (Corner have been suggested (O’Reilly and Daborn 1995;
et al. 1990; Edwards et al. 1997; Shitaye et al. 2006). Ameni et al. 2008), and could have been the reasons
The detection of TB lesions in slaughtered cattle for the lower prevalence rates recorded among the
can be affected by infections other than M. bovis, Namchi, Guadali and White Fulani compared to
parasites, non-specific reactions (Corner 1994; the Red Mbororo cattle. The reasons underlying
Shitaye et al. 2006), and other irregularities of the differences in bovine TB prevalence between
abattoir meat inspections (FAO 1994; Edwards et the local breeds in this study remain unclear and
al. 1997), and lesions may be confused with those require further investigation. However, continuous
caused by Nocardia, Corynebacterium and other close contact between animals (due to increasing
granuloma-causing organisms (Blood and Radostits animal and human population densities and lim-
1989; Gracey and Collins 1992; FAO 1994; Grist ited pasture for grazing), also played roles in the
2008). Thus, for meat inspection to offer an effec- higher prevalence rates recorded in the western
tive means of monitoring the level of bovine TB in highlands. The lower SICCT-BT prevalence rate
cattle, all predilection tissues and organs should in the Adamawa plateaux (2.57%) is in agreement
be thoroughly examined for detection of a single with Martrenchar et al. (1993) who recorded 2.7%
or multiple lesions (Grossklaus 1987; Hinton and in a trial in the neighbouring Northern and Far
Green 1997). The introduction of confirmatory Northern regions of Cameroon. The Adamawa
mycobacteriological and other modern diagnostic plateaux and Northern regions of Cameroon are
69
Original Paper Veterinarni Medicina, 57, 2012 (2): 59–76
70
Veterinarni Medicina, 57, 2012 (2): 59–76 Original Paper
study location, age and breed of cattle. For both intensive managements were significantly affected.
tests, the disease was more severe in the Western However, SICCT-BT involving the injection of BT
highlands compared to the Adamawa plateaux; age and AT at separate sites in the skin of the neck would
was a more significant risk factor than sex, and give more specific results than SIT-BT using only BT
upgraded / exotic and Red Mbororo cattle showed (Monaghan et al. 1994), and interpreting SICCT-BT
the highest prevalence rates. Age and sex (Ameni at a cut-off point of less than 4mm could have im-
et al. 2003, 2007; Oloya et al. 2006; Inangolet et proved the bovine TB detection rates in this study.
al. 2008), herd size and body condition (Ameni et Though not statistically significant, the observed
al. 2003), husbandry system and breed (Ameni et prevalence of SICCT-AT reactors was higher in
al. 2006, 2007), have been extensively reported as young cattle and SICCT-BT doubtful reactors
important risk factors influencing individual bo- increased with age and were higher among adult
vine TB prevalence rates. However, Ameni et al. and/or old cattle. This finding is in agreement with
(2003) and Oloya et al. (2006) suggested that sex Chacon et al. (2004) who reported that cattle were
was a weak risk factor similarly to this study where very susceptible to M. avium infection and that the
non-significantly more female than male animals young were most affected. The rearing of poultry
were affected. The chronic nature of bovine TB, and small ruminants (sheep and goats) which are the
low transmissibility of the disease in an extensive/ natural and suitable reservoir hosts of the M. avi-
transhumance system and delayed onset of tuber- um complex (Biet et al. 2005), was common among
culin positive response in adult and old animals the farmers. Infected free range poultry could have
has been attributed to the long incubation period contaminated the animal and human microenvi-
of the disease, pre-allergenic status, and acquired ronments, pastures and watering points by shed-
and maternal immunity (Kazwala et al. 2001b; ding atypical mycobacteria in their faeces. Large
Oloya et al. 2006). These factors were also noted groups of goats and sheep frequently shared the
as important risk factors in this study. Differing same grazing and drinking environments with cattle
SICCT-BT and SIT-BT observations were noted and could have also served as additional sources of
for husbandry practices (herd size, management infection. Bias in the SICCT-AT test was linked to
and type of production systems). The introduction environmental mycobacteria and non-specific im-
and propagation of bovine TB in large herds in the mune responses to other mycobacterial agents in
studied regions were favoured by the potential for the animal environments (Philips et al. 2003; Biet et
more contacts and other conditions favourable for al. 2005; OIE 2009). The shift from the more positive
the transmission of the disease between infected SICCT-AT in the young animals (or in early years)
and uninfected (susceptible) animals. to the more doubtful SICCT-BT status in adults and
In this study, widespread SICCT-AT and SIT-AT re- old animals (or later years) was also in accordance
actors were recorded and the proportions in some ar- with Lauzi et al (2000; cited by Oloya et al. 2006)
eas and herds were comparable to those of SICCT-BT who reported that non-specific immune responses
and SIT-BT, respectively. The influence of environ- induced by atypical mycobacteria towards BT over-
mental mycobacteria and non-specific responses on came the effect of contamination by the M. avium
TST in the diagnosis of bovine TB have been widely complex with an increase in age.
reported (Philips et al. 2003; Biet et al. 2005; de la Anergy has been reported to cause false TST
Rua-Domenech et al. 2006a; Oloya et al. 2006; OIE negative reactions but the reasons are still poorly
2009). Indeed, Lesslie and Herbert (1975) and Lesslie understood (Inangolet et al. 2008). However, re-
et al (1975a, b), recorded hypersensitivity responses cently infected cattle, cattle under stress due to
to AT that were equal to or higher than responses malnutrition, gastrointestinal parasitoses and other
to BT in cattle naturally infected with M. bovis and concurrent infections and cattle with generalized
presenting visible lesions at slaughter. The nature of TB would be anergic and fail to react to TST (Ameni
the tuberculin is vital in non-specific skin test re- and Medhin 2000; Inangolet et al. 2008). The tuber-
sponses for the diagnosis of bovine TB, and the use culin skin screening in this study coincided with the
of M. bovis-specific purified antigen as the test rea- end of the dry season (period of drought), and the
gent is imperative for improved test performances return of animals from transhumance. Stress due
(Pollock et al. 2003; de la Rua-Domenech et al. 2006a). to starvation, long trekking, other environmental
The SIT-BT detection rates were not affected by herd stressors and clinical symptoms of ill-health due
size and animals in intensive (and diary) and semi- to trypanosomosis, tick-borne diseases, heavy ec-
71
Original Paper Veterinarni Medicina, 57, 2012 (2): 59–76
toparasitoses and gastro-intestinal parasitoses were Ameni G, Medhin G (2000): Effect of gastrointestinal
common in the herds in this study. These conditions parasitosis on tuberculin test for the diagnosis of bo-
could have contributed at varying degrees to the vine tuberculosis. Journal of Applied Animal Research
observed higher rates of doubtful SICCT-BT reac- 18, 221–224.
tors and the widespread SICCT-AT and SIT-AT re- Ameni G, Wudie A (2003): Preliminary study on bovine
actors. Alternatively, a lack of a positive SICCT-BT tuberculosis in Nazareth municipality abattoir of Cen-
response and doubtful SICCT-BT reactions in old tral Ethiopia. Bulletin of Animal Health and Produc-
animals could have been due to age related anergy tion in Africa 51, 125–132.
and other conditions that compromised their im- Ameni G, Miorner H, Roger F, Tibbo M (2000): Comparison
mune function (Thoen et al. 2009). The animal’s between comparative tuberculin and gamma-interferon
immune system would not have been stimulated tests for the diagnosis of bovine tuberculosis in Ethiopia.
enough for a positive response to be measured Tropical Animal Health and Production 32, 267–276.
(Ameni and Medhin 2000; Inangolet et al. 2008). Ameni G, Amenu K, Tibbo M (2003): Bovine tubercu-
However, the variation in bovine TB detection rates losis: Prevalence and risk factor assessment in cattle
observed in this study between geographic regions and cattle owners in Wuchale-Jida district, Central
and herds could have been due to the consequences Ethiopia. International Journal of Applied Research in
of environmental and management factors and the Veterinary Medicine 1, 1–13. http://www.jarvm.com/
risks these pose for the transmission and develop- articles/Vol1Iss1/AMENIJVM.htm
ment of tubercle bacilli infections (Morris et al. Ameni G, Aseffa A, Engers H, Young D, Hewinson G,
1994; Edwards et al. 1997). Vordermeier M (2006): Cattle husbandry in ethiopia
This study reports the first comparative TST in is a predominant factor affecting the pathology of bo-
cattle in the highlands of Cameroon and confirms vine tuberculosis and gamma interferon responses to
that bovine TB is an current livestock health and mycobacterial antigens. Clinical and Vaccine Immu-
production problem in Cameroon which needs to nology 13, 1030–1036.
be further investigated. Analyses of the relative Ameni G, Aseffa A ,Engers H, Young D, Gordon S,
susceptibility and genetic resistance of indigenous Hewinson G, Vordermeier M (2007): High prevalence
zebus to bovine TB are needed to clarify the situa- and increased severity of pathology of bovine tuber-
tion. However, the habits and level of awareness of culosis in holsteins compared to zebu breeds under
cattle professionals and handlers of cattle products field cattle husbandry in Central Ethiopia. Clinical and
of the significance of zoonotic bovine TB, and the Vaccine Immunology 14, 1356–1361.
hygienic status of cattle farms and abattoir environ- Ameni G, Aseffa A, Engers H, Young DB, Gordon SV,
ments as potential risk factors for zoonotic TB dis- Hewinson GR, Vordermeier HM (2008): A compara-
ease are not known. The need for comprehensive tive study on the epidemiology and immunopathology
research into the molecular epidemiology, risk fac- of bovine tuberculosis in Bos taurus and Bos indicus
tors, reservoir and maintenance host status and the cattle in Ethiopia. Ethiopian Journal of Health Develo-
public implications of zoonotic bovine TB in cattle ment 22, 221–224.
in Cameroon cannot be overemphasised. Ameni G, Desta F, Firdessa R (2010): Molecular typing
of Mycobacterium bovis isolated from tuberculosis
lesions of cattle in North Eastern Ethiopia. Veterinary
Acknowledgements Record 167, 138–141.
Ane-Anyangwe IN, Akenji TN, Mbacham WF, Penlap
The authors thank the MINEPIA Staff and cat- VN, Titanji VPK (2006): Seasonal variation and prev-
tle professionals of the Northwest and Adamawa alence of tuberculosis among health seekers in the
regions, Cameroon for their generous cooperation. South Western Cameroon. East African Medical Jour-
nal 83, 588–595.
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Received: 2011–06–01
Accepted after corrections: 2012–01–31
Corresponding Author:
Julius Awah Ndukum, University of Ngaoundere, School of Veterinary Medicine and Sciences,
BP 454 Ngaoundere, Cameroon
E-mail: [email protected]
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