Risk Factors of Bovine Tuberculosis in Cattle in Rural Area in Kaloubia Province

Benha Vet. Med. J., Vol. 20, No.1, Jun. 2010

Risk Factors of Bovine Tuberculosis in Cattle in Rural Area in Egypt

* El-Newishy,A,A. ** Sylvia, O. Ahmed Zoonoses Department, Faculty of Veterinary Medicine, Benha University * Dept. of Animal Hyg. and Zoonoses, Faculty of Veterinary Medicine, Assiut University **

Abstract This study shows a representative stratified cluster samples survey of the prevalence of comparative intradermal tuberculin test in cattle from two rural regions in Kalyobia province in project which held by Benha University from 1 to 26 March 2009 (National Project for Tuberculosis Protection) to assess possible risk factors for tuberculin-positive reaction in cattle. Two villages located in North Benha city the capital of Kalyobia province , (Kafr saad- Meet rady) in where 200 cattle were randomly selected, and tested. In addition, 200 of these cattle owners were tested and interviewed for risk factor assessment. Hundred percent of the tested cattle in this study were traditional species (native). The individual overall highest prevalence of cattle bovine tuberculosis (BTB) was 3 cases (1.5 %), in Kafr saad, and the lowest in Meet rady 1 cases (0.5 %). A total of 6 cases tuberculosis complex identified as M.bovis, 4 of them were isolated from cattle and two isolates were obtained from human in the same locality of those cattle. M.bovis were isolated from two (12.5 %) of 16 animals in group A {(Tuberculin +ve with signs of tuberculosis (having clinical signs such as debilitated condition, cough, decreasing milk production, etc)}, two (6 %) of 33 animals in group B (Tuberculin +ve and apparently healthy), (0%) of 87animals in group C (Tuberculin -ve with clinical signs of tuberculosis), (0%) of 64 animals in group D (Tuberculin -ve and apparently healthy animal). There was no positive M.bovis samples isolated from cattle blood, or pharyngeal swabs, (total n =200 each), while positive isolates from milk samples were (1.5 %), (n=200), but from

1 Benha Vet. Med. J., Vol. 20, No.1, Jun. 2010 fecal samples were (0.5 %), (n=200). As well as two positive cases from 200 human samples were obtained only from pharyngeal swabs. The assessed potential risk factors of disease transmission between cattle and human (food consumption, livestock husbandry and presence of positive cattle) were statistically significant. Introduction Mycobacterium bovis has the broadest host range of the members of the Mycobacterium tuberculosis complex and is well established as a zoonotic disease causing disease in a wide range of mammals. Historically, milk-borne transmission has been responsible for most human M. bovis infections [1]. In developed countries, this route of transmission was virtually eliminated following the widespread adoption of milk pasteurization [2]. The wide diversity of infected species suggests several potential new routes of transmission for M. bovis from animals to humans. However, the extent of M. bovis involvement in the global TB burden in Africa is still largely unknown. This can be partly explained by the fact that in humans, TB due to M. bovis is indistinguishable from that due to M. tuberculosis in terms of clinical signs, radiological and pathological features [3]. Although cattle are considered to be the main hosts of M. bovis, the disease has been reported in many other species, including humans, other domesticated animals and wildlife. Infected animals shed M. bovis via milk, saliva, faeces, urine and discharging lesions [4]. It is generally accepted that human beings get infected either by inhalation of bacteria-containing dust-particles and aerosols shed by infected animals or by ingestion of contaminated animal products (e.g., raw milk) [5]. The main route of infection in cattle is through aerosol exposure, facilitated by close contact between animals [6]. In cattle, ingestion of contaminated products (e.g., pasture and water) is generally considered to be a secondary, less important route of transmission [7]. A high prevalence of M. bovis was isolated from faeces and from milking cattle. This indicates that transmission to young animals by milk

2 Benha Vet. Med. J., Vol. 20, No.1, Jun. 2010 should not be neglected. Recent publications from Africa also suggest that ingestion of M. bovis might be an important mode of disease transmission in cattle, since mesenteric lymph nodes were shown to be more affected than mediastinal lymph nodes [8]. In this article, we attempt mainly to assess possible risk factors for bovine TB in cattle and humans in rural areas in Kalyobia province.

Materials and methods A-Materials: 1. Study sites: This study was carried out in two regions in Kalyobia province during project which held by Benha University (National Project for Tuberculosis Protection from 1 to 26 March 2009). Although belonging to different ethnic groups with different culture and religion, all farmers were sedentary small holders with similar mixed livestock-crop farming system. 2. collection of the samples:- 2.1. Sampling of cattle: Cattle herds were selected by a stratified cluster sampling proportional to the size of the cattle population, in which the unit village was considered as a cluster. Sample size was calculated using the formula described by [9]. A total of 200 specimens each from two regions in Kalyobia province, the cattle were grouped to: group A (Tuberculin +ve and showing signs of tuberculosis), (mastitis, enteritis, and pyrexia of unknown origin, group B (Tuberculin +ve and apparently healthy animals), group C (Tuberculin -ve and showing clinical signs of tuberculosis), D (Tuberculin -ve and apparently healthy animals). Sample analyzed were heparinized as well as EDTA containing blood (n=200), milk (n=200), pharyngeal swab (n=200) and faecal sample (n=200) [10]. 2.1. Sampling of human: A total of 200 pharyngeal swabs were obtained from human in the same locality of tested cattle.

3 Benha Vet. Med. J., Vol. 20, No.1, Jun. 2010

3. Tuberculin testing of cattle: The same person conducted the entire process of tuberculin testing and reading of the result to avoid bias related to injection and reading technique. The comparative intradermal tuberculin test was conducted in all cattle using bovine purified protein derivatives (PPDs) supplied by the Public Veterinary Service Agency in Egypt. Intradermal injections of 0.1 ml (2500 IU) bovine (PPD) were administered in shaved site in the middle neck region, after having recorded skin thickness with a caliper. Skin thickness was measured again at injection site after 72 h. The reaction at the site of injection was derived by measuring the skin thickness before and 72 h after the injection. An animal was considered positive if the thickness of the skin in the reaction site was greater than 10 mm [11]. 4. Interview of cattle owners Cattle owners were interviewed conducted on the two random selected sites by a trained interviewer. Questionnaires included closed and open questions on livestock husbandry/management and household characteristics, such as herd size and structure, presence of other livestock, vaccination/de-worming of cattle, mixing of cattle and other livestock at night, cattle housing at night, watering and grazing system and reproduction. Furthermore, questions related to human consumption habits, contact between humans and cattle, knowledge of TB and known TB status in the household were also asked. B- Methods: The cattle samples obtained from (blood, pharyngeal swab, milk and feces) were processed for isolation of mycobacteria. As well as human samples were obtained only from pharyngeal swab, were mixed with equal volume of 4 % sodium hydroxide and processed by modified Petroff’s method of washing with water rather than neutralization recommended in the original method. A few drops (about 5 ml) of processed sample were inoculated on Lowenstein-Jensen (L-J)

4 Benha Vet. Med. J., Vol. 20, No.1, Jun. 2010 media then incubated at 37ºC in incubator for culture for a maximum period up to 8 wk [12]. C- Identification: Species level identification of growth of acid fast bacilli (AFB) positive mycobacterial isolates was done by standard biochemical tests [niacin production, nitrate reduction, catalase activity at 68°C and at room temperature, tween hydrolysis, arylsulphatase and thiophen-2 carboxylic acid hydrazide (TCH) sensitivity, etc.]. A combination of positive activity for niacin, nitrate reduction, TCH and negative activity for catalase at 68°C and arylsulphatase were considered as characteristics of M. tuberculosis while negative activity for niacin, nitrate reduction, catalase at 68°C, tween hydrolysis, arylsulphatase and TCH were considered as characteristics of M. bovis as per CDC Manual [13]. D- Statistical analysis: Data were analyzed by using statistical package STATA-7 State Corporation. Chi square at 5 per cent level of significance was used to assess statistical significance.

Results Table1: Identification profile of M. bovis isolates from different clinical groups of cattle: Number of Tested No. & category of cattle Cattle Group A Group B Group C Group D No.16 No.33 No.87 No.64 2cases (12½ %) 2cases (6 %) Zero case (0 %) (% Zero case (0 M. bovis isolated Tuberculin +ve Tuberculin +ve Tuberculin Tuberculin -ve from -ve with clinical and apparently with signs of and apparently 200 each tested healthy animals signs of tuberculosis healthy cattle samples tuberculosis (having clinical signs)

Table2: Identification profile of M. bovis isolated samples from cattle:

Number of Tested Cattle Type of sample

M. bovis isolated Milk Fecal Blood Pharyngeal from (n=200) (n=200) (n=200) (n=200) 200 each tested (3) 1.5 % (1) 0.5 % (0) 0 % (0) 0 % cattle samples

Table 3: PPD prevalence in cattle in 2 different rural areas in Kalyobia province :

Percentage of reactor Location Tested animal PPD-positive reactors animals (prevalence) Kafr saad 100 3 % ½1 Meet rady 100 1 % ½ Total 200 4 2%

Table 4: Identification profile of M. bovis isolated samples from cattle:

Number of Tested human No. of individuals positive to % of individuals positive M. bovis to M. bovis isolate

M. bovis isolated from 200 tested human samples 2 1%

Table 5: Analysis of risk factors for positive TB cases in humans as random :effect

Proportion% Risk factor (Nb/Total) OR 95% CI for OR p-value Cattle housing Outside shed (24/200) 1 1.7 3.9 ;0.7 0.4 Indoor with people (176/200) 3 1 2.6 ;0.4 0.2 Raw milk - consumption (57/100) 3 0.3 1.8 ;0.5 0.7 Meat - consumption (83/100) 4 1.1 2 ;0.6 0.6 Keeping other - livestock (183/100) 70 1 1.8 ;0.6 0.8 Cattle herd Base: <5 size animals (164/200) 54 - - 0.2 <10 animals (25/200) 33 1.4 2.5 ;0.8 - <20 animals (11/200) 13 1.5 3.3 ;0.7 - Shepherding Youth (144/200) 36 0.7 1.7 ;0.3 0.4 Adult (56/200) 64 1.7 4.4 ;0.6 0.3

Discussion

From (table1) a total of 4 cases tuberculosis complex identified as M.bovis, M.bovis were isolated from two of 16 (12½ %) animals in group A {(Tuberculin +ve with signs of tuberculosis (having clinical signs such as debilitated condition, cough, decreasing milk production, etc)}, two of 33(6 %) animals in group B (Tuberculin +ve and apparently healthy), zero, (0%) of 87animals in group C (Tuberculin -ve with clinical signs of tuberculosis), zero, (0%) of 64 animals in group D ( Tuberculin -ve and apparently healthy animals). Our study reports a representative estimate of BTB prevalence in rural areas. The overall prevalence

7 Benha Vet. Med. J., Vol. 20, No.1, Jun. 2010 found in our study is consistent with the results found in some African countries [14, 15]. This suggests that BTB epidemiology in rural extensive systems very likely differs from peri-urban livestock-production systems in our country. This could be explained by different husbandry practices and a higher number of cross-breeds and exotic breeds (considered to be more susceptible to BTB) found in peri-urban settings. Bovine TB seems to be endemic and widespread in rural areas, with 2% of the tested randomly selected village herds [16, 17]. Although the situation in the sampled villages is favorable for BTB transmission among animals (very close contact throughout the year in poor ventilated houses, communal grazing/ploughing/threshing/watering, overcrowded pastures), only a few animals per herd were found positive, with an overall individual prevalence of 2%. This indicates a low transmission in the investigated livestock systems which are characterized by small herd size; mostly communal grazing with some crop residue supplementation [18]. From (Table2) the positive M.bovis samples isolated from cattle were (0 %) (n=200) from blood, and pharyngeal swabs, while positive isolates from milk samples were (1.5%) (n=200), but from fecal samples (0.5%), (n=200) were positive. Maximum numbers of M.bovis were isolated from milk [(1.5%) (n=200)], followed by feces [(0.5%), (n=200)] and as well as there was no M.bovis (0 %) (n=200 of each samples) isolated from blood, or pharyngeal swabs of cattle. There was significant difference in percentage of M. bovis isolates among the different groups (faecal samples, pharyngeal swabs, milk and blood). Thus milk samples and pharyngeal swabs were the most reliable sample which was significantly different than others in terms of isolation rates and can thus be considered as appropriate types of samples for diagnosis of tuberculosis from cattle. Our study showed that milk samples were the most appropriate specimens for isolation of M.bovis from infected cattle. Swollen udder lymph node and

8 Benha Vet. Med. J., Vol. 20, No.1, Jun. 2010 discharging lymph node abscesses were important clinical signs of tuberculosis infection in animals. Thus swollen of the udder lymph glands could be recommended as a preferred specimen for confirmation of diagnosis of bovine tuberculosis [19, 23, 24, 25]. Faeces and milk are considered as important media for transmission of bovine tuberculosis [20, 22]. As is also evident from the data published by others blood could be used as specimen for detection of tuberculosis in cattle [26, 28]. From (table 3) representative survey of the prevalence of comparative intradermal tuberculin test in cattle from two regions in Kalyobia province which randomly selected to assess possible risk factors for tuberculin-positive reaction in cattle. The two villages (Kafr saad- Meet rady) (altitude range are same) in North Benha city the capital of Kalyobia province was randomly selected, from which 200 cattle were tested. In addition hundred percent of the tested cattle in this rural livestock were traditional species (native), varied significantly between the overall prevalence of cattle bovine tuberculosis (BTB) was highest (1½ %), in Kafr saad, (3 cases) and low in Meet rady (½ %) (1cases), of the two village herds had tested at least one positive tuberculin reactor, giving an overall herd prevalence of 2% in all. In general, not all animals per owner were tested since as many owners as possible per village were included in the study, either randomly from a list of all owners. From (Table 4) out of 200 swabs isolated from human in the same locality of tested cattle, 2 cases tuberculosis complex identified as positive M.bovis. Similar approaches have been also reported to be useful for diagnosis of mycobacterial infection from pharyngeal swabs in humans [21, 29, 30]. Isolation of M. bovis from pharyngeal swabs of human in the same locality would be important to watch animal handlers, who would be the most probable category of suspects to have transmitted these infections to animals. Transmission could have been by aerosols or contamination of fodder due to indiscriminate spitting [31, 32, 33].

Suggested that the possible route of human to cattle transmission is by inhalation of bacilli from grass contaminated with infected human urine, faeces, or sputum [34]. There may be a small risk for transmission of tuberculosis carried by M. bovis from cattle to human, making continued vigilance particularly necessary [35]. Approximately 1 per cent of human tuberculosis cases could be attributed to M. bovis. Milk and meat are one of the most important links between bovine tuberculosis and human beings especially children [7, 24, 36]. Zoonotic tuberculosis due to M. bovis in developing countries and estimated that the proportion of human cases due to M. bovis accounted for 3.1 per cent of all forms of tuberculosis. Accurate information about tuberculosis in animals particularly its transmission to humans is speculative and studies using classical epidemiological as well as molecular typing should be conducted to determine the exact magnitude and also mode as well as chain of transmission. The isolation of M. bovis from apparently healthy animals shows active transmission in the infected herds and such findings have also been reported earlier [7, 24, 37]. Conventionally, tuberculin reactivity has been used to identify animal infected with tuberculosis. Our data and also an earlier report show that tuberculin reactivity is not a reliable indicator of active disease and/or tuberculosis infection in cattle. Half of isolates of M. bovis and M. tuberculosis were obtained from animals that were tuberculin positive. Thus our study showed wider circulation of M. bovis in this herd, which did not correlate with clinical findings and/or tuberculin activity. It would thus not be realistic to rely on this marker for control of tuberculosis in animals [27, 28]. From Table (5) show the Analysis of risk factors for positive TB cases in humans as random effect, although the situation in the sampled villages is favorable for BTB transmission among animals (very close contact throughout the year in poor ventilated houses, communal grazing/threshing/watering, overcrowded pastures), only a few animals per herd were found positive, with an

10 Benha Vet. Med. J., Vol. 20, No.1, Jun. 2010 overall individual prevalence of 2%. This indicates a low transmission in the investigated livestock systems which are characterized by small herd size; mostly communal grazing with some crop residue supplementation; if housing, then only at night but not during the day and cattle that are often kept together with small ruminants [1,2, 8]. The reported human TB in our study comprised all forms of the disease and no differentiation was made between M. tuberculosis and M. bovis. It is plausible that M. bovis might play a role. Farmer consumption habits (raw milk, raw meat) did not show any statistical significance, as against previous findings in Kalyobia province. However, statements on the zoonotic potential of BTB require confirmed M. bovis cases to address their risk factors specifically. Vice versa, having confirmed TB cases in a household was not associated with cattle reactors. However, considering the very low prevalence of the disease in the country, the power of the study should be further increased in future research. Because of the clustered distribution of livestock, random effects models are more appropriate and risk factor assessments more conservative. Further studies on risk factors of BTB in humans require case–control studies with confirmed M. bovis infection. ‘Classical’ risk factors have been investigated to a certain extent in small studies in the Kalyobia province Highlands, sometimes showing divergent results [37]. It appears that the epidemiology of BTB varies not only between different African countries but also between different regions in Egypt depending on livestock systems (extensive, intensive), breeds (local, exotic, and cross-breed) but also ecological and geographic factors. Further research is needed to better understand BTB transmission in extensive livestock systems of Kalyobia province as well as the true potential of zoonotic risk of transmission and finally to address the potential of control options [38].

Acknowledgements

We are very grateful to the Welcome Trust to all physicians, veterinarian, and workers which did the work which held by Benha University Kalyobia province from 1 to 26 March 2009 (National Project for Tuberculosis Protection).

References

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عوامل الخطر للدرن البقرى فى الماشية فى المناطق الريفية فى مصر

*د/ سيلفيا أسامة أحمد** د/ عادل محمد عبد العزيز

قسم المراض المشتركة كلية الطب البيطرى جامعة بنها قسم صحة الحيوان والمراض المشتركة كلية الطب البيطرى جامعة أسيوط

الملخص العربى

أجريت دراسة لمسح للعينات العشوائية لمعدل إنتشارمرض الدرن البقرى بأستخدام إختبار التيبركلين الجلدى للمقارنة بين الماشية فى منطقتين ريفيتين في محافظة القليوبية من خلل الم شروع الذي أقامتة جامعة بنها م ن 1 إلى 26 مارس 2009 (المشروع الوطني ل لحماية من الدرن) لتققييم عوامل الخطر المحتملة ل لماشية اليجابية أختبار التيبركلين الجلدى. قريتان واقعة في شمال مدينة بنها وهى عاصمة محافظة القليوبية، (كفر سعد- ميت راضى) و التى إختير قت قت بشكل عشوائي، إختبرت 200 ماشية بالضافة ألى 200 م ن مالكي الماشية و الذى إختبروا وقوبلوا لتقييم عوا مل الخطر . مائة بالمائة م ن الماشية جالم بجر بة في هذه الدراسة قك انت من ال قنوع ال قتقليدي (متوطن). النتشار العلى بالعام لدرن الماشية قك قان 3 قحالت (1,5 %)، في كفر سعد, والقل كان في حالت ميت راضى و حالة واحدة (5, %). من 6 الحالت المعزولة المنصنف درن بقرى ، 4حالت منهم جع ز قل م ن الماشية وإثنتان عزلل م ن النسان و على نفس المنوال جع ز قل و صنف الدرن البقري من الماشية م ن حالتان بنسبة أصابة (12,5%) و م ن 16 حيوان في المجموعة أية {(أيجابية أختبار التيبركلين الجلدى مع أعراض جالس ل (أعراض سريريةج مثل أعراض قضع ف عام، سعال، ن جقص قإنتاج ال حليب، الخ)}، إثنان (6 %) م ن 33 حيوان في المجموعة بي (أيجابية أختبار التيبركلين الجلدى ل يبدو عليها أعراض الدرن)، (0 %) م ن 87 حيوان في المجموعة سي (سلبية أختبار,التيبركلين الجلدى يبدو عليها أعراض الدرن)، (0 %) م ن 64 حيوان في المجموعة دي (سلبية أختبار التيبركلين الجلدى ل يبدو عليها أعراض الدرن). ليوجد هناك عينات إيجابية للدرن المصنف بقري قع زلت م ن دم الماشية، أقومن مسحات بلعومية لها، (المجموع 200 ل جك بل نوع عينة)، بينما عزل جت جت عينات إيجابي ة م ن الحليب بنسبة (1,5 %) (العدد الكلي 200عينة)، بينما كانت أيجابية ال عينات البرازية بنسبة (5,%)، (العدد الكلى 200عينة). بالضافة إلى إثنان م ن 200 عينة إيجابية من اللنسان عزل جت جت فقط م ن المسحات البلعومية. عوامل الخطر

المحتملة جالم قيم مة ل لمرض بين الماشية والنسان (إستهلك الغذاء وف لحة لل ماشية و وجود د ماشية إيجابية) قكانا بهام بشكل إحصائي.