PubMed search resulted in 16 eligible articles followed by an additional 8 articles included from the Googlescholar search. Rigorous reference list review supplemented another 14 eligible publications making a total of 39 (Figure 1).
Data concerning S. aureus prevalence, antimicrobial resistance and genotyping were extracted from studies performed in 5 zones of the 9 administrative zones in Tanzania. Table 1, describes the distribution of the published articles review in their consecutive zones. The majority of the publications reviewed were from regions in the eastern and lake zones (i.e. 43.6% and 30.8% respectively), showing lack of S. aureus researched data in the other parts of the country figure
Table 1: Distribution of the reviewed articles by zone in Tanzania.
Zone
|
Human
|
Animal
|
Human & Animal
|
Eastern Zone
|
14
|
2
|
1
|
Lake Zone
|
12
|
-
|
-
|
Northern Zone
|
5
|
1
|
-
|
Central
|
1
|
-
|
-
|
Zanzibar
|
2
|
1
|
-
|
Total
|
34
|
4
|
1
|
Majority of the publications were reported in the eastern and lake zones. S. aureus data of animal origin have been poorly represented throughout the country
Prevalence, antibiotic resistance and genotyping of S. aureus isolated from humans
S. aureus prevalence was reported in thirty three (33) human related studies, gave an account which ranged from 11 – 60 % as summarized in Table 2. Higher infection rates were typically observed in SSTI’s nevertheless the bacterium was also implicated in other infections. Furthermore it was notably observed that S. aureus colonization ranged between 27% - 60% in the three zones that reported on colonization. Since most colonization studies involved healthy individuals these finding are indicative of the considerable circulation of community associated S. aureus in the country.
The publication under review showed that S. aureus was isolated in a number of infections including SSTI’s, bloodstream, otitis media, respiratory tract and urinary tract infections (Figure 3) staying true to characteristically causing a wide range of infections. It was also evident how various vulnerable populations such as children, elderly and immune compromised individual were at risk of S. aureus infections/colonization. This observation emphasises the necessity to establish a reliable and sustainable surveillance system to monitor the S. aureus bacterium countrywide.
Table 2: Human related studies investigating S. aureus in different conditions and populations across Tanzania
S.No
|
Prevalence
S. aureus % (n)
|
Prevalence MRSA % (n)
|
Population
|
Source of
S aureus isolates
|
Location
|
Reference
|
1
|
41.4% (157)
|
37.6% (59)
|
Health care workers adults male and female from
June 2016 -October 2016.
|
Nasal carriage
|
Dar es Salaam
(Eastern zone)
|
Joachim A et al 2018 (
11)
|
2
|
NR
|
11.8% in ICU patients and 2.1% in ICU HCW.
|
ICU patients (male and female of all age groups) and ICU HCW from October 2012 - March 2013
|
Nasal carriage
|
Dar es Salaam
(Eastern zone)
|
Geofrey A et al 2015 (
12)
|
3
|
34.5% (89) in swabs collected on admission.
20% (4) in swabs collected 48hrs after admission
|
24.7% (22) from samples on admission, and 50% (2) in samples collected after 48hrs.
|
Patients admitted to emergency or medical ward aged 5 and above.
|
Nasal carriage
|
Dar es Salaam
(Eastern zone)
|
Joachim A et al 2017 (
13)
|
4
|
40% (114)
|
8.3% (12)
|
Healthy children <5yrs
From April 2010 -June 2010
|
Nasal carriage
|
Dar es Salaam
(Eastern zone)
|
Moyo S et al 2014 (
14)
|
5
|
Overall 23.2%(223), where by 26.2%(95),detected in children with acute respiratory infection and 21.4% (128) were detected in children without acute respiratory infection
|
NR
|
ages 2 to 10, with axillary temperature of ≤ 380C Dar es Salaam from April to August 2008(DSM) and June to December 2008 (Ifakara)
|
Nasal carriage
|
Dar es Salaam and Morogoro
(Eastern zone)
|
Chochua et al 2016 (
15)
|
6
|
13.2% (138)
|
NR
|
Healthy children <5yrs born after mass distribution of Azithromycin for tranchoma control. Study was conducted in 2014
|
Nasal carriage
|
Kilosa, Morogoro
(Eastern zone)
|
Bloch EM et al 2017 (
16)
|
7
|
22% (22)
|
0%
|
100 nasal swabs from healthy individuals with no epidemiological connection were collected within urban and peri urban Morogoro Municipalities
|
Nasal carriage
|
Morogoro
(Eastern zone)
|
Katakweba et al 2016 (
17)
|
8
|
13.2% (245)
|
23.3% (57)
|
Male and female of all age groups who were subjected to microbiology testing between January 2005 and December 2009 (Retrospective study).
|
Bacteremia
|
Dar es Salaam
(Eastern zone)
|
Moyo S et al 2010 (
18)
|
9
|
28% (12)
|
NR
|
Male and female sickle cell anemic patients of all age groups seeking health care at MNH from January 2006-December 2008
|
Bacteremia
|
Dar es Salaam
(Eastern zone)
|
Makani J et al 2015 (
19)
|
10
|
In blood 36.5% (27), and in pus swabs 52.3% (132)
|
NR
|
Neonates aged 3 - 26 days suspected with neonatal sepsis. Study duration October 2009 -January 2010
|
Bacteremia and wound swabs
|
Dar es Salaam
(Eastern zone)
|
Mhada T et al 2012 (
20)
|
11
|
12.2% (18)
|
44.4% (8)
|
100 participants (male and female aged 18-80) with clinical evidence of Surgical site infection. Duration from September 2011 to February 2012
|
Wound infections
|
Dar es Salaam
(Eastern zone)
|
Manyahi Jet al 2014 (
21)
|
12
|
71.4% (132)
|
0.8% (1)
|
Skin and soft tissue infections patients of all age groups
|
Wound infections
|
Bagamoyo
(Eastern zone)
|
Kazimoto T et al 2018 (
22)
|
13
|
48.3% (131)
|
NR
|
Asymptomatic otitis media (OM)-associated bacteria found in patients living with HIV
|
Ear colonization
|
Morogoro
(Eastern zone)
|
Mwabete KD et al 2018 (
23)
|
14
|
The overall carriage rate of S. aureus was 21.0 % (66). 47 % (31) were from preclinical students while 53 % (35) from clinical students
|
1.5% (1)
|
Healthy students (clinical and Pre clinical) aged 18 and above. Study duration February to June 2013
|
Nasal carriage
|
Mwanza
(Lake zone)
|
Okamo B et al 2016 (
24)
|
15
|
21.5%
|
28% (9)
|
300 neonates with clinical neonatal sepsis
|
Bacteremia
|
Mwanza
(Lake zone)
|
Kayange N et al 2010 (
25)
|
16
|
14.8 (8)
|
50% (4)
|
402 malnourished under five children.
Study duration September 2012- January 2013.
|
Bacteremia
|
Mwanza
Lake zone
|
Ahmed M et al 2017 (
26)
|
17
|
13.7% (29)
|
79% (23)
|
Patients of all age groups and gender with lower limb ulcers seen at the surgical ward or outpatient department from November 2010-April 2012
|
Wound infection
|
Mwanza
(Lake zone)
|
Mbunda F et al 2012 (
27)
|
18.
|
8.9%(18)
|
44.4%
(8)
|
Patients of all age groups with chronic lower limb ulcers seen at the surgical ward.300 wound infection were swabbed between November 2011 and February 2012
|
Wound infection
|
Mwanza
(Lake zone)
|
Moremi et al 2014 (
28)
|
19
|
28.6% (18)
|
19% (3)
|
65 patients of all age groups who underwent major surgery at BMC between July 2009 and June 2010
|
Surgical site wound infection
|
Mwanza
(Lake zone)
|
Mawalla et al 2011 (
29)
|
20
|
27.3% (6)
|
16.7% (1)
|
Woman aged 14 to 44 who have developed surgical site infections after having undergone a caesarean section. 345 woman were swabbed between October 2011 and February 2012
|
Surgical site wound infection
|
Mwanza
(Lake zone)
|
Mpogoro et al 2014 (
30)
|
S.No
|
Prevalence
S. aureus % (n)
|
Prevalence MRSA % (n)
|
Population
|
Source of
S aureus isolates
|
Location
|
Reference
|
21
|
29.2% (7)
|
NR
|
162 patients of all age group and gender who underwent major limb amputations at BMC between March 2008 and February 2010. 24 of the participants had surgical site infections out of which different bacteria were recovered as the cause of infection.
|
Surgical wound infection
|
Mwanza
(Lake zone)
|
Chalya et al 2012 (
31)
|
22
|
59.3%
|
NR
|
All patients of all age groups and gender presenting with animal related injuries at the BMC between September 2007 and August 2011. Postoperative wound infection was the most commonest complication reported lead by S aureus infections
|
Surgical site wound infections
|
Mwanza
(Lake zone)
|
Gilyoma et al 2013 (
32)
|
23
|
Overall prevalence 16.1 (25) out of which 28% (7) were isolated in HIV positive patients and 72%(18) in HIV negative patients
|
NR
|
The study was done to compare magnitude of bacterial resistance to cotrimoxazole/other antimicrobials among isolates from HIV infected patients on cotrimoxazole prophylaxis and those not on prophylaxis and non-HIV patients attending BMC between January and October 2012
|
Urine and wound swabs
|
Mwanza
(Lake zone)
|
Marwa et al 2015 (
33)
|
24
|
18.2% (34)
|
41.2% (14)
|
301 patients aged more than one year who presented with ear discharge for more than 6 weeks and tympanic
membrane perforation at the ENT department between October 2013 and March 2014 were recruited into the study
|
Ear infection
|
Mwanza
(Lake zone)
|
Mushi et al 2016 (
34)
|
25
|
Overall 22.8% (100)
Blood 80% (80)
Pus swabs 18% (18)
Other infections 2% (2)
|
Only 78 were subjected to AST.34.6% (27) were MRSA
|
A total of 3330 microbiological culture results scripts representing non-repetitive specimens reported between June 2013 and May 2015 were retrieved and analyzed for pathogens and their susceptibility patterns using STATA-11 software.
|
Bacteremia, wound infection, urinary tract infection and pulmonary infection
|
Mwanza (Lake zone)
|
Moremi et al 2016 (
35)
|
26
|
55.3% (68)
|
NR
|
Primary school children (aged 6-15) from 4 schools in Moshi municipality assessed/self-reported respiratory tract infection symptoms. The community based study was conducted between January and March 2014.
|
Nasal and Trought swabs
|
Moshi
Northen zone
|
Ngocho et al 2015 (
36)
|
27
|
66% (103) at 6 weeks, 36% (47) at 3 months and 24% (33) at 6 months. 38% (17) mothers were colonized by S aureus parallel to their children.
|
NR
|
Children born to HIV positive mothers attending RCH clinics to establish prevalence and influence of nasal pharyngeal bacterial colonization on children. Nasal swabs from children were taken at 6 weeks (n=156), 3 (n=136) and 6 (n= 130) months consecutively. Mothers (45)of the infants were also swabbed at 3 and 6 month visits( Study duration 2005-2009
|
Nasal carriage
|
Moshi
Northen zone
|
Kinabo et al 2013 (
37)
|
28
|
16% (23)
|
NR
|
Patients presenting with SSI, infected diabetic wounds, infected wounds due to trauma, and
patients with other infected wounds admitted in surgical
ward (study duration July 2013 to June 2014)
|
Wound infections
|
Moshi
(Northen zone)
|
Kassam et al 2017 (
38)
|
29
|
9.3% (35) of which 82.9 (29) were from wound infections, 11% (4) from blood samples and 6% (2) from sputum samples
|
Only 22 isolates were subjected to AST. 27.3% (6) were MRSA
|
People admitted to the medical or surgical wards at KCMC between 2013 and 2015. The study collected stool, sputum, blood and wound/pus samples from patients of all age groups to describe causative agents of different infections.
|
Wound infection
Blood infection
Bronchial infection
|
Moshi
(Northen zone)
|
Kumburu et al 2017 (
39)
|
30
|
9.1% (6)
|
NR
|
A total of 867 patients aged between 2 and 5 with fever above 370C were enrolled between January and October 2013. 373 urine samples were collected and 66 tested positive for UTI. All S aureus isolates were recovered from UTI patients
|
Urinary tract infection
|
Tanga (Korogwe)
(Northen zone)
|
Mahende et al 2014 (
40)
|
31
|
17% (17)
|
NR
|
Children aged 0-12yrs dismissed from the hospital with pneumonia diagnosis.100 children were enrolled in the attempt to characterize etiology of community acquired pneumonia. (study duration August 2014- April 2015)
|
Blood infection
|
Itigi
(Central zone)
|
Caggiano et al 2017(
41)
|
32
|
11.3% (9)
|
0%
|
Febrile adults and children seeking care at the Mnazi mmoja hospital between March 2012- April 2013
|
Blood infection
|
Zanzibar
|
Onken et al 2015 (
42)
|
33
|
6.3% (5)
|
0%
|
Febrile patients seeking outpatient health care at 3 different district hospitals (Wete, Chake chake, and Mkoani) on Pemba island between March 2009 to December 2010
|
Blood infection
|
Zanzibar
|
Thriemer et al 2012 (
43)
|
Antibiotic resistance in human originated isolates.
The primary method for establishing S. aureus antibiogram in the reviewed work was done phenotypically by the use of the Kirby-Bauer disk diffusion test along with Clinical Laboratory Standard Institute (CLSI) guidelines. Kirby-Bauer is a test for antimicrobial susceptibility of bacteria, based on the size of inhibition zones of bacterial growth in a lawn culture around disks impregnated with the antimicrobial drug (44). This method has been reported to have inherent shortcomings such as being highly dependent on experimental conditions that may affect end results (45). With this fact in mind the Kirby Bauer antibiogram results would have to be confirmed by another test of a different principle such as genomic based method to prevent over reporting of resistance, particularly in the confirmation of MRSA and VRSA strains. In this review, four studies had MRSA confirmed genotypically which showed 100% agreement with the phenotypic Kirby-Bauer disk diffusion test. This agreement between the methods should encourage the use of the Kirby-Bauer disk diffusion test as an antibiotic sensitivity monitoring strategy in the country, since it is the most available and affordable method in our settings.
Twenty two (22) studies contributed information on antibiotic susceptibility of S. aureus bacteria. MRSA in most cases was identified by resistance against cefoxitin, however one study used methicillin as their identification drug. As summarized in Table 3, extremely high resistance rates against β-lactams i.e. penicillin (87 - 99%) and ampicillin (67 - 91%) were observed.
S. aureus colonization is considered being a risk factor for eventual infection as well as a potential source of spread of resistant strains. Examination of colonization strains is therefore key in understanding the epidemiology of S. aureus infection/diseases. This review discovered that the antibiotic resistance patterns in colonization strains showed uncharacteristically high resistance to commonly used antibiotics compared to studies reported in Europe and Asia. In den Heijer et al 2013’s report about antibiotic resistance of commensal S. aureus across Europe described resistance rates lower than 20% against erythromycin, gentamicin, tetracycline and co-trimoxazole (46). Similar low resistance rates were reported in some parts of Asia with an exception of tetracycline which was slightly higher than 30% (47). This review on the other hand recorded higher mean resistance rates of 49%, 38% and 28% against erythromycin, co-trimoxazole and tetracycline respectively. Further resistance against gentamicin was significantly higher than recorded in other parts outside Africa (46, 47).
Resistance pattern in clinical S. aureus observed in this review were in accordance with other reports around Africa (48, 49). As in many parts recorded resistance against β lactams was high, further markedly resistance rates ranging from 44-50% against erythromycin, gentamicin, co-trimoxazole and clindamycin were also described in this review. The affected antibiotics are readily available in the community and also commonly used for empirically treatment of different cases of bacterial suspected infections. A notable presence of resistance against these antibiotics is an indication of their failure in treatment and a need for broader class antibiotics which are expensive and not accessible for most Tanzanians.
MRSA prevalence reported in different studies in this review was between 19-33% which seems to have risen in the last 10 years. Abdulgader et al 2015 in the review of MRSA prevalence on the African continent categorized Tanzania as belonging to countries with low MRSA prevalence ranging from 6-16% between the years 2001-2009 (50). This abrupt increase should be taken seriously by which more research efforts should be directed towards understanding and preventing further spread of these strains in order to safe guard much needed antibiotics
Table 3: Antimicrobial resistance rates of S. aureus in humans
Antibiotic (N*)
|
Resistance rates in S. aureus isolates from humans colonization. References (% range)
|
Mean resistance (n/N*) (%)
|
Penicillin(267)
|
(
11-13) (96 -100)
|
(263/267) (99%)
|
Ampicillin (151)
|
(
17,
24,
36) (84-100)
|
(133/151) (88%)
|
Tetracycline (223)
|
(
12,
14,
17,
24) (9-95)
|
(63/223) (28%)
|
Erythromycin (244)
|
(
11,
12,
24) (19-100)
|
(119/244) (49%)
|
Gentamicin (382)
|
(
11,
13,
14,
17,
36) (9-34)
|
(99/382) (26%)
|
Co-trimoxazole (314)
|
(
11,
12,
14,
17) (14-66)
|
(118/314) (38%)
|
Ciprofloxacin (233)
|
(
13,
14) (4-11)
|
(15/233) (6%)
|
Clindamycin (178)
|
(
11,
12) (9-76)
|
(30/178) (14%)
|
Cefoxitin (388)
|
(
11,
12,
14,
24) (2-100)
|
(93/388) (24%)
|
|
Resistance rates in S. aureus isolates from invasive (blood-born) infections. References (% range)
|
|
Penicillin (46)
|
(
25,
42,
43) (23-80)
|
(40/46) (87%)
|
Ampicillin (27)
|
(
20) (85)
|
(23/27) (85%)
|
Erythromycin (37)
|
(
25,
43) (20-66)
|
(23/37) (62%)
|
Gentamicin (27)
|
(
20) (56)
|
(15/27) (56%)
|
Co-trimoxazole (46)
|
(
25,
42,
43) (22-60)
|
(23/46) (50%)
|
Clindamycin (32)
|
(
25) (44)
|
(14/32) (44%)
|
Methicillin (245)
|
(
18) (23)
|
(57/245) (23%)
|
Cefoxitin (46)
|
(
25,
42,
43) (0-32)
|
(9/46) (20%)
|
|
Resistance rates in S. aureus isolates from non-invasive infections. References (% range)
|
|
Penicillin (202)
|
(
21,
22,
28,
33,
51) (30 -100)
|
(183/202) (91%)
|
Ampicillin (263)
|
(
20,
23) (47-88)
|
(177/263) (67%)
|
Tetracyclin (67)
|
(
33,
34,
51) (6- 45)
|
(14/67) (21%)
|
Erythromycin (221)
|
(
28,
33,
34,
51) (14 – 46)
|
(81/221) (37%)
|
Gentamicin (339)
|
(
20,
23,
28,
34,
51) (11-52)
|
(110/339) (32%)
|
Co-trimoxazole (232)
|
(
23,
28,
33,
34,
51) (43-74)
|
(115/232) (50%)
|
Ciprofloxacin (187)
|
(
23,
33,
34) (4 - 14)
|
(20/187) (17%)
|
Clindamycin (42)
|
(
28,
51) (21-63)
|
(19 /42) (45%)
|
Cefoxitin (226)
|
(
21,
22,
28,
34,
51) (1 – 100)
|
(55/226) (24%)
|
Genotypic characterisation of human originated S. aureus isolates
Four human related studies were reviewed to inform this section (summarized in Table 4). A wide spectrum of MSSA spa types and sequence types (ST) were identified in the review. Nevertheless the limited number of publications on genotypic data could not reveal dominance in any particular strain.
Two publications gave an account on genetic characterization of MRSA(39, 51). The observed MRSA were dominated by ST88, however sequence types ST8, ST1719, ST 1820, and ST239 were also reported. None of the MRSA were pvl positive consistent with the findings by Abdulgader et al 2015 who suggested that Africa is predominated by pvl negative MRSA belonging to ST88 (50).
Even though some important information was apparent in this review data concerning MSSA and MRSA genotyping is still limited, Kumburu et al 2018 for example was the only one who reported on other virulence factors apart from pvl hence still lacking knowledge on other important factors associated to the bacteria circulating in our communities. Furthermore genotypic characterization studies predominantly focused on screening for the mecA gene the β-lactam associated resistance gene, neglecting other resistant markers for other commonly used antibiotic in the country. Nurjadi et al 2014 whilst researching on trimethoprim resistance genes in S. aureus isolated from different countries determined that 100% of the Tanzanian isolated in the study which were phenotypically trimethoprim resistant in fact harboured a trimethoprim conferring resistant gene (52). This emphasises the need for research efforts to be directed towards researching a wider range of resistance causing genes in S. aureus to get comprehensive resistance profile data.
Most pvl positive MSSA clones associate with skin infections identified in this review belonged to ST152 which concurs with the findings from other African based studies (53).
Table 4: S. aureus genetic diversity as described by the reviewed publications
Author
|
Host
|
Sample type
|
Resistant gene
|
Virulence factor
|
spa Type
|
MLST
|
Moremi et al 2012 (
51)
|
Human
|
Wound, pus, nasal swabs (24 MRSA strains from previous studies)
|
mecA (100%)
|
pvl (16.7%)
|
t7231, t690
t064, t104, t1855,t7237 t186,
t667
|
ST88,
ST1719,
ST8,ST1820
|
Kumburu et al 2018 (
39)
|
Human
|
Blood, Sputum, wound/pus
|
mecA (33.3%)
|
pvl (16.7%) ,txt (6.7%) both in non mecA isolates
|
ND
|
ST-8, ST-1, ST-152, ST1719, ST15, ST1847, ST188, ST22, ST239, ST30, ST5, ST580, ST6, ST97
|
Katakweba et al 2016 (
17)
|
Human
|
Nasal swabs
|
mecA and mecC
(None detected)
|
NS
|
t714, t148, t084, t002, t223, t314, t311, t015, t451, t690, t1849, t2030, t10779*
|
ST15, ST18, ST72, ST22, ST5, ST121, ST231, ST45, ST8
|
Katakweba et al 2016 (
17)
|
Pig
|
Nasal swab
|
mecA and mecC
(None detected)
|
NS
|
t131
|
ST80
|
Katakweba et al 2016 (
17)
|
Dog
|
Nasal swabs
|
mecA and mecC
(None detected)
|
NS
|
t084, t127, t223, t314,
t267, t508, t1476
|
ST15,ST18, ST1, ST22, ST121,
|
Nurjadi et al 2014 (
52)
|
Human
|
Nasal, SSTI swabs
|
dfrA, dfrG and dfrK.
dfrG detected by 37% *
|
NS
|
ND
|
ND
|
ND: Not done, NS: Not screened
Prevalence, antibiotic resistance and genotyping of S. aureus isolated from animals.
Studies reporting on prevalence, antimicrobial resistance and genetic characteristics of S aureus in animals published between 2010 and 2018 in Tanzania were few. Only 5 studies were included in this review, scantly representing a small area in the country. Three publications reported on S. aureus prevalence in milk samples, one study described prevalence in milk and cow nasal swabs and the last study reported on S. aureus prevalence in pig and dog nasal swabs.
Prevalence of S aureus in Animals
As indicated in table 5 most examined specimen in animals was milk. Prevalence of S. aureus varied in different geographic area. Kashoma et al 2018 and Mohammed et al 2018 reported the highest prevalence at 49% and 41% in Morogoro respectively (54, 55). Suleiman et al 2018 (56) did not fall far back when observing a prevalence of 37% describing subclinical mastitis in cows on Unguja Island. The lowest prevalence of 33% was recorded in a study aiming at assessing raw milk quality in Arusha and Meru district(57). Generally prevalence of S. aureus seems to be much lower in swabs taken from nasal cavities as shown by Kashoma et al 2018 who swabbed cows observed a prevalence of 28% whereas Katakweba et al 2016(17) observed a prevalence of 4% and 11% in pig and dog nasal swabs respectively.
MRSA detection in milk associated studies varied tremendously ranging from 4- 35% (54, 55), even though both studies reporting on this data were conducted in Morogoro township. Furthermore, Kashoma et al 2018 reported MRSA prevalence of 16% isolates recovered from cow nasal cavities, whereas no MRSA was detected by Katakweba et al 2016 in pigs and dogs nasal swabs.
Table 5: S. aureus prevalence in Animal related samples
S.No
|
Prevalence
S aureus % (n)
|
Prevalence MRSA % (n)
|
Population
|
Source of
S aureus isolates
|
Location
|
Reference
|
1
|
Milk: 49% (49)
Cow nasal swabs : 28% (37)
|
Milk: 35% (17)
Cow nasal swabs: 16% (6)
|
The study was carried out in 3 dairy farms (A, B and C) that belonged to Sokoine University of Agriculture. All farms were located within the same climatic zone. All 3 farms carried out mixed animal farming
|
Milk samples and cow nasal swabs
|
Morogoro
(Eastern zone)
|
Kashoma et al 2018 (
55)
|
2
|
41% (48)
|
4% (3)
|
The study involved 18 of the 29 Wards within Morogoro Municipality. In each of the selected Wards, sales points and local shops where raw milk is sold were randomly selected. A total of 117 milk samples. The study was conducted between January and June 2015
|
Milk samples
|
Morogoro
(Eastern zone)
|
Mohammed et al 2018 (
54)
|
3
|
37% (217)
|
NR
|
Study conducted between January – July 2014 on Unguja Island to establish prevalence of subclinical mastitis in smallholder dairy cows and pattern of antimicrobial susceptibility of major mastitis pathogens.
|
Milk samples
|
Unguja (Zanzibar)
|
Suleiman et al 2018 (
56)
|
4
|
33% (30)
|
NR
|
105 milk samples from smallholder dairy farmers, milk vendors and retailers were taken within Arusha City and Meru District to assess the quality of raw milk and stakeholders' awareness on milk-borne health risks and factors for poor milk hygiene.
|
Milk samples
|
Arusha city and Meru district
(Northern zone)
|
Ngasala et al 2015 (
57)
|
5
|
Pig nasal swabs 4% (4)
Dog nasal swabs 11% (11)
|
Pig swabs: 0%
Dog nasal swabs: 0%
|
100 pigs and 100 dogs dwelling in urban and peri urban Morogoro Municipality
|
Nasal swabs
|
Morogoro
(Eastern zone)
|
Katakweba et al 2016 (
17)
|
NR: Not reported
Table 6: Antibiotic resistance in animals
Antibiotic (N*)
|
Resistance rates in different studies in Animals.
(References) (range%)
|
Mean resistance (n/N*) (%)
|
Penicillin(265)
|
(
54,
56) (72-88)
|
(225/265) (85%)
|
Ampicillin (99)
|
(
17,
55) (62-100)
|
(72/99) (73%)
|
Tetracycline (364)
|
(
17,
54-56) (16-73)
|
(110/364) (30%)
|
Erythromycin (301)
|
(
55,
56) (5-23)
|
(28/301) (9%)
|
Gentamicin (99)
|
(
17,
55) (6-25)
|
(4/99) (4%)
|
Co-trimoxazole (132)
|
(
54,
55) (22-40)
|
(42/132) (32%)
|
Vancomycin (132)
|
(
17,
54,
55) (2-11)
|
(10/132) (8%)
|
Amoxicillin (217)*
|
(
56) (47)
|
(102/217) (47%)
|
Cephalexin (217)*
|
(
56) (30)
|
(64/217) (30%)
|
Oxacillin (147)
|
(
17,
54,
55) (0-34)
|
(25/147) (17%)
|
Cefoxitin (132)
|
(
54,
55) (4-17)
|
(13/132) (10%)
|
*Reported in one study only
Antibiotic resistance in animal originated S aureus isolates
Four studies described resistance in S. aureus using different antibiotic pallets which included cephalexin, gentamicin, kanamycin, neomycin, tetracycline, streptomycin, amoxicillin, cephalexin, clindamycin, vancomycin, ampicillin, co-trimoxazole, oxacillin, and cefotixin. This review however focused on the most reported antibiotics in this area as indicated in Table 6.
Most of the reviewed studies reported low antibiotic resistance levels with exception of penicillin and ampicillin which showed mean resistances rates of 85% and 73% respectively. Suleiman et al 2018 also further observed resistance against amoxicillin and cephalexin at a rate of 47% and 30%, which was unfortunately not reported by any of the other reviewed studies. Oxy-tetracycline has been stated as being the most over used antibiotic in the livestock keeping business in Tanzania (58). The mean resistance rates against oxacillin (17%) and tetracycline (30%) observed in this review are indicative of the effects of previously reported overuse.
MRSA detection in all studies was confirmed by resistance against cefoxitin and/or oxacillin, whereby mean resistance rates of 10% and 17% were observed respectively. An average of 8% resistance against vancomycin was observed, reported in 3/5 studies as described in
Table 6.
Genotypic characterisation of animal originated S. aureus isolates
Genotypic data were retrieved from 2 of the 5 studies reviewed. In both, real time- PCR (qPCR) was used to confirm S. aureus as well as screening for mecA resistance conferring gene. Katakweba et al 2016 additionally screened for mecC a recently discovered mecA homologue said to have the potential to be mis-categorized as Methicillin sensitive S. aureus (MSSA). None of the two resistance conferring genes were detected in Katakweba’s study, however S. aureus was confirmed in 4 pigs and 11 dog samples respectively. Further spa typing of the pig originating MSSA characterized them as spa type t131 associated with ST80. Additionally isolates of dog origin were characterized as spa types t314 (ST121), t084 (ST15 and ST18) and t223 (ST22) all of which were also identified in human nasal isolates reported in the same study.
In the study by Mohammed et al 2018, both coagulase positive (n=46) and coagulase negative (n=2) S aureus were detected in their milk samples. mecA gene was detected in 2 coagulase positive and one coagulase negative S. aureus isolate making this study the first in Tanzania to report on coagulase negative S. aureus hourboring the mecA gene. Of the 3 MRSA isolates detected in the study only the coagulase negative S. aureus isolate was able to be characterized as spa type t2603, whereas the other two MRSA’s were spa un- typable.
S.aureus is one of the leading causes of bovine mastitis which explains the fact that the majority of publications included in this review concerning S. aureus in animals addressed the pathogen in clinical and sub-clinical mastitis or in regards to milk production quality. This has been instrumental in the reviews failure to make a link in describing animals and/or humans as potential S. aureus reservoir for each other, as well as the effect of such in both public and animal health. Very few studies on genomic S. aureus characterisation were available for review and did not suffice in showing such linkage.
Limitations
The data from this review cannot be generalized as true prevalence, antibiotic resistance patterns or genotypic characterization of S. aureus bacterium in Tanzania. High inter-study variations such as type of specimen analysed, objective of studies, time frame as well as methods employed including criteria set for resistance/MRSA confirmation may have influenced the outcome.
Methods used to genetically characterise S. aureus in this review were very divergent from simple PCR to whole genome sequencing. The data collected in these methods had different focuses which made comparing the results between studies difficult. Since the main objective in characterizing S. aureus or any other bacteria for that matter is understanding the genetic similarities and differences in conferring antibiotic resistance, strain type as well as and virulence factors, it would therefore be useful to have a common guideline that allowing inter laboratory comparability to gather more reliable and holistic data meant to guide treatment and infection prevention strategies in the country.