Sociodemographic characteristics of farmers
A total of 147 farming households were randomly selected for the study. The farmers were predominantly male (74.1%). There was, however, no significant (p=0.375) differences in gender distribution of farmers in the two districts. Most (67.3%) of the respondents were 20-50 years of age, with Isingiro having a significantly (p=0.023) higher percentage in the category (74.6%) compared to Kamuli (60.5%).
The majority (85.7%) of the cattle in the study were female, with Isingiro having a significantly (p<0.001) higher percentage (98.6%) compared to Kamuli (73.7%). The cattle were mostly cross breeds (76.2%), and Isingiro had a significantly (p=0.022) higher percentage (84.5%) than Kamuli (31.6%). Most (77.4%) of the farmers in Isingiro had >5 head of cattle while up to 82.9% of the farmers in Kamuli were smallholders, keeping 1-5 head of cattle (Table 1) with the percentages in the different categories varying significantly (p<0.001).
Table 1: Socio-demographic characteristics of farmers and their cattle in Kamuli and Isingiro districts, Uganda.
Characteristic
|
Both districts (n=147)
|
Isingiro (n=71)
|
Kamuli (n=76)
|
|
|
%(95% CI1)
|
%(95% CI1)
|
%(95%CI1)
|
P-Values
|
Gender of farmers
|
|
|
|
|
0.375
|
Male
|
74.1(66.3, 81.0)
|
77.5(66.0, 86.5)
|
71.5(59.5,80.9)
|
|
Female
|
25.9(19.0, 33.7)
|
22.5(13.5, 34.0)
|
29.0(19.1, 40.5)
|
|
Age of farmers
|
|
|
|
|
0.023
|
<20 years
|
13.6(8.5, 20.2)
|
5.6(1.6, 13.8)
|
21.1(12.5, 31.9)
|
|
20-50 years
|
67.3(59.1, 74.8)
|
74.6(62.9, 84.2)
|
60.5(48.6, 71.6)
|
|
>50 years
|
19.1(13.0, 26.3)
|
19.7(11.2, 30.9)
|
18.4(10.4, 29.0)
|
|
Sex of cattle
|
|
|
|
|
<0.001
|
Female
|
85.7(79.0, 90.9)
|
98.6(92.4, 100)
|
73.7(62.3, 83.1)
|
|
Male
|
14.3(9.1, 21.0)
|
1.4(0.0, 7.6)
|
26.3(16.9,37.7
|
|
Cattle breed
|
|
|
|
|
0.022
|
Cross breed
|
76.2(68.5, 82.8)
|
84.5(74.0, 92.0)
|
31.6(21.2, 43.2)
|
|
Local breed
|
23.8(17.2, 31.5)
|
15.5(8.0, 26.0)
|
68.4(56.7, 78.6)
|
|
Age of cattle
|
|
|
|
|
<0.001
|
1-5 years
|
42.2(34.1, 50.6)
|
22.5(13.5, 34.0)
|
61.8(50.0, 72.7)
|
|
6-10 years
|
44.9(36.7, 53.3)
|
56.3(44.0, 68.1)
|
32.9(22.5, 44.6)
|
|
>10 years
|
12.9(8.0, 19.4)
|
21.1(12.3, 32.4)
|
5.3 (1.4, 12.9)
|
|
Herd size of cattle kept
|
|
|
|
|
<0.001
|
1-5
|
43.5(35.4, 51.9)
|
1.4(0.0, 7.6)
|
82.9(72.5, 90.6)
|
|
6-15
|
10.9(6.3, 17.1)
|
8.4(3.2, 17.5)
|
13.2(6.5, 22.9)
|
|
>15
|
45.6(37.3, 54.0)
|
90.1(80.7, 95.9)
|
3.9(0.8, 11.1)
|
|
195% Confidence interval
Prevalence of S. aureus and AMR
Of the 147 nasal swab samples collected from cattle, only 14 (9.5%) tested positive for S. aureus and were assessed for AMR. All (100%) the S. aureus isolates assessed for antibiotic resistance were resistant to Nitroimidazoles while 92.9% were resistant to Penicillins. None of the isolates were resistant to Fluoroquinolones (0.0%) and Aminoglycosides (0.0%) (Table 2). All the 14 isolates exhibited antimicrobial resistance (AMR) to at least one of the assessed antibiotics and 92.9% (13/14) showed evidence of multidrug resistance (MDR).
Table 2. Antimicrobial resistance profiles of S. aureus isolated from cattle in Isingiro and Kamuli of Uganda
Antimicrobial
|
Number
|
Percentage
|
95% CI1
|
Fluoroquinolones
|
0
|
0
|
-
|
Ciprofloxacin
|
0
|
|
|
Aminoglycosides
|
0
|
0
|
-
|
Gentamicin
|
0
|
0
|
-
|
Tetracyclines
|
7
|
50
|
23.0, 77.0
|
Tetracycline
|
7
|
50
|
23.0, 77.0
|
Penicillins
|
13
|
92.9
|
66.1, 99.8
|
Amoxicillin
|
3
|
21.4
|
4.7, 50.8
|
Ampicillin
|
13
|
92.9
|
66.1, 99.8
|
Penicillin G
|
12
|
85.7
|
57.2, 98.2
|
Glycopeptides
|
1
|
7.1
|
0.2, 33.9
|
Vancomycin
|
1
|
7.1
|
0.2, 33.9
|
Macrolides
|
3
|
21.5
|
4.7, 50.8
|
Erythromycin
|
3
|
21.5
|
4.7, 50.8
|
Nitroimidazoles
|
14
|
100
|
76.8, 100
|
Metronidazole
|
14
|
100
|
76.8, 100
|
195% Confidence interval
For the human samples, 30.6% (45/147) of nasal swab samples were positive for S. aureus and were assessed for AMR. Similar to the cattle isolates, S. aureus human isolates showed high levels of resistance to Nitroimidazoles (100%) and Penicillins (93.3%). However, none of the isolates were resistant to Aminoglycosides (0.0%), and only 1 exhibited resistance to Fluoroquinolones (2.2%) (Table 3). As was the case for cattle isolates, all the 45 human isolates exhibited AMR to at least a one antibiotic while 93% (42/45) showed evidence of MDR.
Table 3. Antimicrobial resistance profiles of S. aureus isolated from humans in Isingiro and Kamuli of Uganda
Antimicrobial classes
|
Number
|
Percentage
|
95%CI1
|
Fluoroquinolone
|
1
|
2.2
|
0.1, 11.8
|
Ciprofloxacin
|
1
|
2.2
|
0.1, 11.8
|
Aminoglycosides
|
0
|
0.0
|
-
|
Gentamycin
|
0
|
0.0
|
-
|
Tetracyclines
|
23
|
51.1
|
35.8, 66.3
|
Tetracycline
|
23
|
51.1
|
35.8, 66.3
|
Penicillins
|
42
|
93.3
|
81.7, 98.6
|
Amoxicillin
|
19
|
42.2
|
27.7, 57.8
|
Ampicillin
|
41
|
91.1
|
78.8, 97.5
|
Penicillin G
|
42
|
93.3
|
81.7, 98.6
|
Glycopeptides
|
6
|
13.3
|
5.1, 26.8
|
Vancomycin
|
6
|
13.3
|
5.1, 26.8
|
Macrolides
|
10
|
22.2
|
11.2, 37.1
|
Erythromycin
|
10
|
22.2
|
11.2, 37.1
|
Nitroimidazoles
|
45
|
100
|
92.1, 100
|
Metronidazole
|
45
|
100
|
92.1, 100
|
195% Confidence interval
Perceptions and practices of farmers regarding AMR
Perceptions of farmers regarding AMR
Up to 69.7% (15.6% strongly agreed and 53.1% agreed) of the respondents believed that AMR occurs when bacteria in the body become resistant to antibiotics (Table 4). The percentage of respondents reporting this perception were significantly (p<0.001) higher in Isingiro (15.5% strongly agreed, 73.2% agreed) than Kamuli (15.8% strongly agreed, 34.2% agreed). Slightly more than a half of the respondents (59.2%) either strongly agreed (11.6%), or agreed (47.6%) that infections are becoming increasingly unresponsive to antibiotic treatment. The percentages reporting this were also significantly (p<0.001) higher in Isingiro (15.5% strongly agreed, 67.6% agreed) than Kamuli (7.9% strongly agreed, 28.9% agreed). A total of 62.5% of the farmers (15.6% strongly agreed and 46.9% agreed) believed that if bacteria are resistant to antibiotics, it can be very difficult or impossible to treat the infections they cause. The proportion of farmers with this perception were also significantly higher in Isingiro than Kamuli (Table 4). Seventy percent of the farmers either strongly agreed (26.5%) or agreed (43.5%) that bacteria that are resistant to antibiotics can be spread from humans to humans as well as from animals to humans. Again, this belief was more common among farmers in Isingiro (14.1% strongly agreed, 66.2% agreed) than those in Kamuli (38.2% strongly agreed, 22.4% agreed). A total of 55.7% of the respondents (8.8% strongly agreed and 46.9% agreed) believed that antibiotic-resistant infections could make medical procedures like surgery, organ transplant, and cancer treatment much more dangerous. As for the other knowledge related questions, a higher percentage of the farmers from Isingiro tended to strongly agree (11.3%) or agreed (69.0%) than those in Kamuli (26.3% strongly agreed, 5.3% agreed). Suffice it to say that a higher proportion of the respondents in Isingiro tended to show understanding of AMR compared to those from Kamuli (Table 4).
Table 4: Opinions regarding antimicrobial resistance among farmers in Isingiro and Kamuli districts of Uganda
Question
|
Both districts (n=147)
|
Isingiro (n=71)
|
Kamuli (n=76)
|
|
|
%(95%CI1)
|
%(95%CI1)
|
%(95%CI1)
|
P-value
|
AMR occurs when bacteria in the body become resistant to antibiotics
|
|
|
|
<0.001
|
Strongly agree
|
15.6(10.2, 22.5)
|
15.5(8.0, 26.0)
|
15.8(8.4, 26.0)
|
|
Agree
|
53.1(44.7, 61.3)
|
73.2(61.4, 83.1)
|
34.2(23.7, 46.0)
|
|
Neutral
|
29.2(22.0, 37.3)
|
9.9(4.1, 19.3)
|
47.4(35.8, 59.2)
|
|
Disagree
|
2.0(0.4, 5.8)
|
1.4(0.0, 7.6)
|
2.6(0.3, 9.2)
|
|
Strongly disagree
|
0(0)
|
0(0)
|
0(0)
|
|
Infections are becoming increasingly unresponsive to treatment by antibiotics
|
|
|
|
<0.001
|
Strongly agree
|
11.6(6.9, 17.9)
|
15.5(8.0, 26.0)
|
7.9(2.9, 16.4)
|
|
Agree
|
47.6(39.3, 56.0)
|
67.6(55.4, 78.2)
|
28.9(19.1, 40.5)
|
|
Neutral
|
38.1(30.2, 46.5)
|
12.7(6.0, 22.7)
|
61.8(50.0, 72.7)
|
|
Disagree
|
1.4(0.2, 4.8)
|
2.8(0.3, 9.8)
|
0(0)
|
|
Strongly disagree
|
1.4(0.2, 4.8)
|
1.4(0.0, 7.6)
|
1.3(0.0, 7.1)
|
|
If bacteria are resistant to antibiotics, it can be very difficult or impossible to treat the infections they cause
|
|
|
|
0.001
|
Strongly agree
|
15.6(10.2, 22.5)
|
18.3(10.1, 29.3)
|
13.2(6.5, 22.9)
|
|
Agree
|
46.9(38.7, 55.3)
|
62.0(49.7, 73.2)
|
32.9(22.5, 44.6)
|
|
Neutral
|
35.5(27.7, 43.7)
|
16.9(9.0, 27.7)
|
52.6(40.8, 64.2)
|
|
Disagree
|
2.0(0.4, 5.8)
|
2.8(0.3, 9.8)
|
1.3(0.0, 7.1)
|
|
Strongly disagree
|
0(0)
|
0(0)
|
0(0)
|
|
Bacteria that are resistant to antibiotics can be spread from humans to humans as well as animals to humans
|
|
|
|
<0.001
|
Strongly agree
|
26.5(19.6, 34.4)
|
14.1(7.0, 24.4)
|
38.2(27.2, 50.0)
|
|
Agree
|
43.5(35.4, 51.9)
|
66.2(54.0, 77.0)
|
22.4(13.6, 33.4)
|
|
Neutral
|
25.8(19.0, 33.7)
|
12.7(5.6, 21.3)
|
38.2(27.2, 50)
|
|
Disagree
|
4.1(1.5, 8.7)
|
7.0(2.3, 15.7)
|
1.3(0.0, 7.1)
|
|
Strongly disagree
|
0(0)
|
0(0)
|
0(0)
|
|
Antibiotic-resistant infections could make medical procedures like surgery, organ transplant, and cancer treatment much more dangerous
|
|
|
|
<0.001
|
Strongly agree
|
8.2(4.3, 13.8)
|
11.3(5.0, 21.0)
|
5.3(1.5, 12.9)
|
|
Agree
|
46.9(38.7, 55.3)
|
69.0(56.9, 79.5)
|
26.3(16.9, 37.7)
|
|
Neutral
|
38.1(30.2, 46.5)
|
14.1(7.0, 24.4)
|
60.5(48.6, 71.6)
|
|
Disagree
|
6.8(3.3, 12.1)
|
5.6(1.6, 13.8)
|
7.9(2.9, 16.4)
|
|
Strongly disagree
|
0(0)
|
0(0)
|
0(0)
|
|
195% Confidence interval
Farmers’ practices associated with AMR
The farmers mostly consulted qualified professionals (66%) whenever their animals were sick. Significantly (p<0.001) more farmers did this in Kamuli (98.7%) than in Isingiro (31%) (Table 5). Consulting veterinary drug vendors was also commonly practiced (32.7%) by the farmers, with significantly (p<0.001) more of the farmers in Isingiro (64.8%) undertaking it than those in Kamuli (2.6%). Spraying against ectoparasites was the most (96.6%) practiced routine measure of diseases and parasites control, with no significant differences in the proportion of farmers practicing this in the two districts (Table 5). Vaccination was another commonly practiced (72.8%) routine measure of diseases control, with significantly (p<0.001) more farmers from Isingiro (93.0%) undertaking it than those from Kamuli (53.9%) (p< 0.001). Antibiotic prophylaxis was observed to be the least practiced measure of control of diseases and parasites (17.0%), with significantly (p<0.001) more farmers in Isingiro (33.3%) undertaking it than those in Kamuli (1.3%).
More than half (54%) of the farmers reported that they followed drug withdrawal periods by not consuming milk from lactating cows for >7 days after treatment and this practice was significantly (p<0.001) different in the two districts (71.8% in Isingiro, 38.2 in Kamuli) (Table 5).
Table 5. Farmers’ disease management and antimicrobial use practices in Isingiro and Kamuli districts of Uganda
Practices
|
Both districts (n=147)
|
Isingiro (n=71)
|
Kamuli (n=76)
|
|
|
%(95%CI1)
|
% (95%CI1)
|
% (95%CI1)
|
P-value
|
When your animals are sick, what did you do?
|
|
|
|
|
Consult someone with experience
|
11.6(6.9, 17.4)
|
23.9(14.6, 35.5)
|
0(0)
|
<0.001
|
Consult a qualified professional
|
66(57.7, 73.6)
|
31.0(20.5, 43.1)
|
98.7(92.8, 100)
|
<0.001
|
Consult the Vet drug shop vendor
|
32.7(25.1, 40.9)
|
64.8(52.5, 75.8)
|
2.6(0.3, 9.2)
|
<0.001
|
Use personal experience to treat
|
32(24.5, 40.2)
|
59.2(46.8, 70.7)
|
6.6(2.2, 14.7)
|
<0.001
|
Use previous prescription
|
12.2(7.4, 18.7)
|
23.9(14.6, 35.5)
|
1.3(0.0, 7.1)
|
<0.001
|
Use traditional or Herbal remedies
|
2.0(0.4, 5.8)
|
4.2(0.9, 11.8)
|
0(0)
|
0.07
|
Which methods do you use to prevent disease in your cattle?
|
|
|
|
|
Probiotic
|
0(0)
|
0 (0.0)
|
0 (0.0)
|
-
|
Antibiotic Prophylaxis
|
17.0(11.3, 24.1)
|
33.8(23.0, 46.0)
|
1.3(0.3, 7.1)
|
<0.001
|
Vaccination
|
72.8(64.8, 79.8)
|
93.0(84.3, 97.7)
|
53.9(42.1, 65.4)
|
<0.001
|
Deworming
|
51.7(43.3, 60.0)
|
49.3(37.2, 61.4)
|
53.9(42.1, 65.4)
|
0.469
|
Spraying or dip
|
96.6(92.2, 98.9)
|
95.8(88.1, 99.1)
|
97.4(90.8, 99.7)
|
0.590
|
No treatment
|
0(0)
|
0 (0.0)
|
0 (0.0)
|
-
|
What happens when a lactating cow undergoes antibiotic treatment?
|
|
|
|
|
Keep milking it and consuming the milk
|
11.6(6.9, 17.9)
|
15.5(8.0, 26.0)
|
7.9(2.9, 16.4)
|
0.150
|
Only give milk to calves for the next few days
|
25.2(18.4, 33.0)
|
28.2(18.6, 40.0)
|
22.4(13.6, 33.3)
|
0.418
|
Do not consume the milk for >7days after treatment
|
54.4(46.0, 62.6)
|
71.8(59.9, 81.9)
|
38.2(27.2, 50.0)
|
<0.001
|
195% Confidence interval
Antibiotics used in Humans and Animals
The most common antibiotic classes farmers used for treatment of human infections in both Isingiro and Kamuli were Penicillins and Nitroimidazoles while the least used antimicrobials were glycopeptides (Figure 2).
Significantly more farmers used tetracyclines for treatment of human infections in Isingiro (13.7%) than in Kamuli district. While both sulphonamides and tetracyclines were popular in both districts for treating animal infections, penicillins were popular with Isingiro famers but not those in Kamuli district. (Figure 3).