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Technical Report No: Clin/Epid/ICAR-IVRI/02/2021
Antimicrobial Susceptibility of Rare Enterobacteriaceae Causing Clinical
Infections
Funding: ICAR-Indian Veterinary Research Institute under different projects from 2011-2020.
Team Leader: Dr. Bhoj R Singh, Head, Division of Epidemiology, Indian Veterinary Research Institute,
Izatnagar, Bareilly-243122, India. Email: br.singh@icar.gov.in
Collaborators: Dr. DK Sinha (Principal scientist, Epidemiology), Dr. Vinodhkumar OR (Senior
Scientist, Epidemiology), Dr. AM Pawde (Principal Scientist Surgery and i/c Wild Life section), Dr. AK
Sharma (Rtd. Principal Scientist, Wild Life Section) and PG and Ph.D. Students of Epidemiology, Indian
Veterinary Research Institute, Izatnagar, Bareilly-243122, India.
Abstract:
Among Enterobacteriaceae members Escherichia coli, Salmonella enterica, Edwardsiella tarda,
Klebsiella spp., Raoltella spp., Proteus spp., Citrobacter spp. and Enterobacter spp. strains are well
known opportunistic and the major cause of infections in birds and animals but strains of Arsenophonus
spp., Buvicia spp., Cedecea spp., non-coli Escherichia spp., Kluyvera spp., Leclercia spp., Leminorella
spp., Moelerella spp., Morganella spp., Obesumbacterium spp., Pragia spp., Providecia spp., Shimwellia
spp., and Xenorhabdus spp. are rarely reported to cause illness in animals, birds and humans. This report
summarises the 121 (20 in birds, 7 in humans, 29 in wild and zoo animals and 65 in domestic animals)
cases of infections associated with rare Enterobacteriaceae strains of the 2186 cases referred in the last 10
years to our laboratory. Almost 5.5% of cases were found associated with rare Enterobacteriaceae strains.
The most important infections and illness associated with rare Enterobacteriaceae strains included
abortions (23), abscesses (3), septicemic deaths (49), death-in-shell of chick embryos (2), diarrhoea and
enteritis (11) endometritis and metritis (3), mastitis (3), upper respiratory tract infections (3), otorrhoea
(1), prostatitis (1), repeat breeding (2), multiple skin and mandibular abscesses (4), wound infections (5)
and urinary tract infections (UTI, 4). The seven human clinical cases associated with rare
Enterobacteriaceae referred to our lab included two cases of diarrhoea (one each by Moelerella
wisconsensis and Xenorhabdus bovienii) and five cases of UTI (one each caused by Budvicia aquatica,
Escherichia ulneris, Morganella morganii and two by E. fergusonii). Bacterial isolates were tested for 13
herbal antimicrobials (ajowan oil, agarwood oil, betel leaf oil, carvacrol, Citral, cinnamaldehyde,
cinnamon oil, guggul oil, holy basil oil, lemongrass oil, patchouli essential oil, sandalwood oil, thyme
oil) and 27 conventional antimicrobials (ampicillin, amoxicillin+clavulanic acid, amoxicillin, aztreonam,
azithromycin, chloramphenicol, ceftazidime, ceftazidime+Clavulanic acid, colistin, cotrimoxazole,
cefepime, ceftriaxone, cefotaxime, cefotaxime+clavulanic acid, cefoxitin, erythromycin, enrofloxacin,
gentamicin, imipenem, meropenem, moxalactam, nalidixic acid, nitrofurantoin, piperacillin,
piperacillin+tazobactam, tetracycline and tigecycline). The multiple herbal drug resistance indices ranged
from zero (sensitive to all tested herbs) to one (resistant to all tested herbs) and 78.51% strains were
resistant to three or more herbs. The most effective herbal antimicrobial against rare Enterobacteriaceae
strains was carvacrol (93.81%) followed by ajowan oil (91.75%), cinnamaldehyde (88.66%), cinnamon
oil (86.11%), thyme oil (85.42%), holy basil oil (70.75%), betel leaf oil (55.26%), citral (38.14%),
lemongrass oil (36.28%), sandalwood oil (22.83%), guggul oil (15.63%), patchouli essential oil (14.75%)
and agarwood oil (9.62%). Multiple herbal drug indices (MRI) varied from zero to 0.92 and 85.95% of
strains were resistant to three or more antibiotics and 46 strains produced extended -spectrum lactamases
and six stains produced New Delhi metallo--lactamases (Budvicia aquatic a1, Moellerella wisconsensis
1, Escherichia vulneris 1, Escherichia fergusonii 2). The most effective antibiotic was tigecycline
(92.39%) followed by imipenem (87.91%), chloramphenicol (86.87%), meropenem (84.78%) and
cefotaxime + clavulanic acid (83.33%). The least effective antibiotic was erythromycin (2.27%) followed
by tetracycline (33.67%), nalidixic acid (35.29%), ampicillin (37.89%) and amoxicillin (40.40%).
2
Introduction
The report is based on an analysis of data on antimicrobial sensitivity patterns of rare
Enterobacteriaceae strains isolated from clinical samples received (Table 1) at Clinical epidemiology
Laboratory, Division of Epidemiology, Indian Veterinary Research Institute, Izatnagar, Bareilly-243122,
India during last decade (2011-2020). The data has been analyzed using, Chi-square test, Odds ratio and
correlation using Microsoft Excel worksheet.
Purpose
To update the knowledge about antimicrobial susceptibility of clinical and para-clinical isolates
of bacteria so that clinicians may use the ready-reckoner for prescribing the best antimicrobial with the
choice.
Methodology
The isolation was made in Clinical Epidemiology Laboratory, Division of Epidemiology, ICAR-
Indian Veterinary Research Institute, Izatnagar from samples (clinical samples submitted by veterinary
and human clinicians of the Institute) for pathogen identification and antimicrobial sensitivity assays.
Samples were processed as per standard protocols for isolation and identification of bacteria using
conventional culture, phenotypic and biochemical characterization techniques (Holt et al., 1994, Singh,
2009). All isolates were tested for antimicrobial sensitivity using disc diffusion assay on Mueller Hinton
agar and classified as either sensitive or resistant following guidelines of CLSI (2014). All media and
antimicrobial discs were purchased from BBL Difco, USA.
The bacterial isolates were also tested using disc diffusion assay for susceptibility to 13 herbal
antimicrobials using discs containing 1 mg of >99% pure active herbal contents in each discs namely,
Ajowan (Tachyspermum ammi) oil (Subh Flavor and Fragrance Pvt. Ltd., New Delhi), Holy basil
(Ocimum sanctum) oil (Subh Flavor and Fragrance Pvt. Ltd., New Delhi), Cinnamledehyde (Sigma
Aldrich, USA), Carvacrol (Sigma Aldrich, USA) , Lemongrass (Cymbopogon citratus) oil (Sigma
Aldrich, USA), Thyme (Thymus vulgaris) oil (Sigma Aldrich, USA), Citral (Sigma Aldrich, USA),
Cinnamon (Cinnamomum verum) oil (Sigma Aldrich, USA), Agarwood (Aquilaria malaccensis) oil
(Naga Fragrance Ltd., Dimapur, India), Patchouli (Pogostemon cablin) essential oil ((Subh Flavor and
Fragrance Pvt. Ltd., New Delhi), Betel (Piper betle) leaf essential oil (Subh Flavor and Fragrance Pvt.
Ltd., New Delhi), Guggul (Commiphora wightii) oil and Sandal (Santalum album) wood oil (Government
Sandalwood Oil factory, Mysore, India). Testing was done in the similar way for different antibiotics and
any measurable zone of inhibition around disc of the test strain was classified as sensitive else resistant as
described earlier (Singh, 2013).
New Delhi metallo-β-lactamase (NDM): Phenotypically determined using E-test and for all carbapenem
resistant strains (CLSI, 2014) and then custom sequenced to identify the gene.
Extended spectrum β-lactamase (ESBL): All cephalosporin resistant strains were tested using E-test for
determining ESBL activity.
Herbal preparations tested for their antimicrobial activity: AO, ajowan oil; AWO, agarwood oil;
BLO, betel leaf oil; Cav, carvacrol; Citral; CNH, cinnamaldehyde; CO, cinnamon oil; GO, guggul oil;
HBO, holy basil oil; LGO, lemongrass oil; PEO, patchouli essential oil; SWO, sandalwood oil; TO,
thyme oil.
Conventional antimicrobials used for their antimicrobial activity: A, ampicillin; AC,
amoxicillin+clavulanic acid; AMX, amoxicillin; AT, aztreonam; AZM, azithromycin; C,
chloramphenicol; CA, ceftazidime; CAC, ceftazidime+Clavulanic acid; Cl, colistin; Co, cotrimoxazole;
CPM, cefepime; CTR, ceftriaxone; CTX, cefotaxime; CTX/CLA, cefotaxime+clavulanic acid; Cx,
cefoxitin; E, erythromycin; Ef, enrofloxacin; G, gentamicin; I, imipenem; MR, meropenem; Mox,
moxalactam; Na, nalidixic acid; Nf, nitrofurantoin; Pi, piperacillin; PTT, piperacillin+tazobactam; T,
tetracycline; TGC, tigecycline.
3
Table 1. Year-wise referred clinical samples analyzed in Clinical Epidemiology Laboratory
Year
2011
2012
2013
2014
2015
2016
2017
2018
2019
2020
Total
Samples
239
184
153
128
224
212
292
305
194
255
2186
Arsenophonus nasoniae
A total of four isolates of A. nasoniae were isolated from four clinical samples (Tab. 2.) viz., aborted
foetal tissue of cow, urine of a urinary tract infection (UTI) in a dog, and heart blood of lion and hyena
died of septicemia.
Table 2. Antimicrobial susceptibility pattern of Arsenophonus nasoniae identified from
different clinical sources.
Arsenophonus
nasoniae sources
Sensitive to herbal
antimicrobials
Sensitive to conventional antimicrobials
Cattle
AO, AWO, BLO, Cav,
Citral, CNH, CO, GO,
HBO, LGO, PEO, TO
A, AC, AMX, AT, AZM, CA, CAC, CPM, CTR, CTX,
CTX/CLA, Cx, I, MR, Mox, Nf, Pi, PTT, TGC
Lion
AO, BLO, Cav, Citral,
CNH, CO, GO, HBO,
LGO, PEO, TO
A, AC, AMX, AT, AZM, C, CA, CAC, Cl, CPM, CTR, CTX,
CTX/CLA, Cx, Ef, G, I, MR, Mox, Na, Nf, Pi, PTT, T, TGC
Hyena
AO, AWO, Cav, Citral,
CNH, CO, GO, HBO,
LGO, PEO, SWO
A, AC, AMX, C, CAC, Cl, Co, CPM, CTR, CTX, CTX/CLA,
Cx, Ef, G, I, MR, Mox, Na, Nf, Pi, PTT, T, TGC
Dog
AWO, Cav, Citral, CO,
PEO, SWO, TO
A, AC, AMX, AT, CA, Co, CPM, CTR, CTX, CTX/CLA, I,
MR, Mox, Na, Nf, Pi, PTT, TGC
Arsenophonus strains are shown to have a wide host range and is one of the most widespread
symbiotic bacteria which primarily infect insects and known as the cause of Killer-Son trait of the wasps
due to its vertical transmissibility (Darby et al., 2010). It is rarely been reported to cause infection in
human beings of animals except a few cases of co-infection.
Budvicia aquatica
In a total of 8 cases B. aquatica strains were detected from heart blood of dead fish, pig, poultry and tiger,
faeces of diarrhoeic pigs, bacteriuria cases of human and pus swab of a dog. Most of the strains were
resistant to multiple drugs and one strain produced NDM-5 and two strains were positive for ESBL
(Table. 3).
Table 3. Antimicrobial susceptibility pattern of Budvicia aquatica from different clinical
sources.
Budvicia
aquatica
sources
Sensitive to herbal
antimicrobials
Sensitive to conventional antimicrobials
Comments
Dog (abscess)
AO, AWO, Cav, Citral, CNH,
CO, GO, HBO, PEO, TO
Cl
NDM-5
Positive
Fish
(septicemia)
AO, AWO, Cav, Citral, CNH,
CO, TO
A, CTX/CLA, I, MR, Pi
No
Human (UTI)
AO, Cav, CNH, CO, TO
CPM, CTR, C, CTX/CLA, G, I, MR, Mox, T
ESBL
positive
Pig
(Septicemia)
Cav
AC, C, Cl, Co, CPM, CTR, CTX, EF, G, I, T
ESBL
positive
Pig
(Diarrhoea)
AO, BLO, Cav, Citral, CNH,
CO, GO, HBO, LGO, PEO,
SWO, TO
A, AC, AMX, AT, AZM, C, CA, CAC, Cl, Co,
CPM, CTR, CTX, CTX/CLA, Cx, EF, G, I, MR,
Mox, Na, Nf, Pi, PTT, TGC
No
Pig
AO, AWO, BLO, Cav, Citral,
A, AC, AMX, AT, AZM, C, CA, CAC, Cl, Co,
No
4
(Diarrhoea)
CNH, CO, GO, HBO, LGO,
PEO, SWO, TO
CPM, CTR, CTX, CTX/CLA, Cx, EF, I, MR,
Mox, Na, Nf, Pi, PTT, TGC
Poultry
(septicemic
death)
AO, Cav, Citral, CNH, CO,
GO, HBO, LGO, PEO, SWO,
TO
C, Cx, E, G, I, MR, Nf, Pi, PTT
No
Tiger
(septicemic
death)
AO, Cav, Citral, TO
Cl, I, MR, TGC
No
Budvicia aquatica, a rarely cultured Enterobacteriaceae member, was first isolated in the Czech Republic
in 1983. It inhabits waters of streams, rivers, wells and swimming pools (Schubert and Groeger-Sohn,
1998) and an opportunistic pathogen especially in immunocompromised patients (Tomczak,
Smuszkiewicz, 2014). Though it is known as a fish pathogen (Walczak et al., 2017), has also been
reported from a few cases of septicemia (Cobin et al., 2007) and urinary tract infections (UTI) in humans
(Cobin et al., 2007; Singh, 2019).
Cedecea lapagei
In a mastititc cow milk C. lapagei was identified, which was sensitive to most of the herbal
antimicrobials except ajowan oil, thyme oil and lemongrass oil but resistant to most of the antibiotics
tested except chloramphenicol, gentamicin, imipenem, meropenem, nitrofurantoin, tetracycline and
tigecycline. It also produced ESBL.
Cedecea lapagei, a member of Enterobacteriaceae, was first identified in 1977 from
environmental samples but proved an opportunistic pathogen in 2006 to cause soft tissue infection with
multiple hemorrhagic bullae. Cedecea strains rarely cause pneumonia, urinary tract infections (Mohamed
and Mohamud, 2018) wound infection (Salazar et al., 2013), peritonitis (Arishi et al., 2017),
osteomyelitis, bacteremia, sepsis (Thompsom and Sharkady, 2020; Chavez-Herrera et al., 2018; Hong et
al., 2015) and enterocolitis (Neu, 2014).
Kluyvera spp.
A total of five isolates, two of K. ascorbata and three of K. cryocrescens were identified from clinical
samples (Tab. 4). Most of the isolates were resistant to common herbal antimicrobials but sensitive to
most of the antibiotics. One isolate from metritis case in a bitch produced ESBL but none was
carbapenem resistant.
Table. 4. Antimicrobial susceptibility pattern of Kluyvera spp. from different clinical
sources.
Species and sources
of isolation
Herbal
antimicrobial
sensitivity
Conventional antimicrobial sensitivity
Comments
Kluyvera ascorbata sources
Mithun (repeat
breeder, deep vaginal
swab)
Cav, LGO
A, AC, AMX, AT, AZM, C, CA, CAC, Cl, Co, CPM,
CTR, CTX, CTX/CLA, Cx, E, EF, G, I, MR, Mox, Na, Nf,
Pi, PTT, T, TGC
No
Bitch (metritis,
vaginal discharge)
AO, BLO,
CNH, CO, TO
AC, AMX, EF, I, MR, Nf, TGC
ESBL
Kluyvera cryocrescens sources
Mithun (repeat
breeder, deep vaginal
swab)
AO, Cav, TO
A, AC, AMX, AT, AZM, C, CA, CAC, Cl, Co, CPM,
CTR, CTX, CTX/CLA, Cx, E, EF, G, I, MR, Mox, Na, Nf,
Pi, PTT, T, TGC
No
Black buck deer
(enteritis, intestinal
AO, BLO,
Cav, CNH,
A, AC, AMX, AT, C, CA, CAC, Cl, Co, CPM, CTR,
CTX, CTX/CLA, Cx, EF, G, I, MR, Mox, Na, Nf, Pi,
No
5
contents)
CO, HBO, TO
PTT, T, TGC
Spotted deer
(septicemic death,
heart blood)
AO, Cav,
CNH, CO,
HBO, TO
A, AC, AMX, AT, C, CA, CAC, Cl, Co, CPM, CTR,
CTX, CTX/CLA, Cx, EF, G, I, MR, Mox, Na, Nf, Pi,
PTT, TGC
No
Kluyvera an inhabitant of water, soil and sewage may cause opportunistic infections (Farmer et
al., 1981). It may colonize in the respiratory, gastrointestinal, or urinary tract causing gastrointestinal or
urinary tract and the soft tissues infections (Juan et al., 2011). Though Kluyvera strain rarely cause
serious infections (Esper et al., 2011), are potentially dangerous pathogens due to their ability to cause
persistent and chronic infections (Zou et al., 2019) and their ability to transfer the gene encoding for
ESBLs and other drug resistant traits (Lartigue et al., 2006; Moonah et al., 2010). In recent years it is
reported to cause urinary tract infections in humans (Oncel et al., 2015; Kirvalidze et al., 2019).
Laclercia adecarboxylata
The only strain of Leclercia adecarboxylata identified in last 10 years was from heart blood of
goat died of septicemia/ pneumonia. The Isolate was resistant to AO, AWO, BLO, citral, GO, LGO and
SWO but sensitive to Cav, CO, HBO and TO. It was sensitive to all antibiotics except aztreonam,
erythromycin and tetracycline.
Laclercia adecarboxylata is an emerging opportunistic pathogen sometimes associated with
bacteremia (Forrester et al., 2012), genital tract (Anuradha, 2014) and wound (Col Michael et al., 2013)
infections, endocarditis (Lee et al., 2009) and death due to sepsis (Nelson et al., 2013).
Leminorella ghrimontii
The only strain of Leminorella ghrimontii was isolated from gill swabs of a dead fish, might be a
secondary invador or commensal. It was sensitive to most of the herbal preparations except guggul oil,
parchouli essential oil and sandalwood oil but was resistant to many of the antibiotics including
ampicillin, amoxicillin, amoxicillin+clavulanic acid, azithromycin, colistin and erthromycin. The strain
produced ESBL.
Leminorella genus of the family Enterobacteriaceae, strains are isolated from faeces and urine
specimen but rarely been associated with pathology. However, retrospectively analysis revealed their
definitive role in pathogenesis (Blekher et al., 2000) including peritonitis, sepsis (Dalamaga et al., 2006)
and neonatal mortality (Sharma et al., 2017).
Moellerella wisconsensis
A total of five strains of Moellerella wisconsensis isolated from clinical samples (Tab. 5) were
invariably sensitive to azithromycin, tetracycline and tigecycline but varied in their resistance. One isolate
from uterus of a buffalo aborted preterm was NDM-14 positive.
Moellerella wisconsensis often associated with human enteritis (Stock et al., 2003) is rarely
reported to cause infections in animals has been reported to cause lung infection (Casalinuovo and
Musarella, 2009) and even abortion in bovines (Wolf-Jackel et al., 2021).
Table 5. Antimicrobial resistance pattern of Moellerella wisconsensis strains from different
clinical sources.
Moellerella
wisconsensis
sources
Resistant to herbal
antimicrobial
Resistant to conventional antimicrobials
Comments
Buffalo (abortion,
deep vaginal swab)
BLO, Cav, GO, SWO
A, AC, AMX, CA, CAC, Cl, Co, CPM, CTR,
CTX, CTX/CLA, Cx, E, EF, I, MR, Mox, Na,
Nf, Pi, PTT
NDM-14
Positive
Cattle (Pneumonia/
septicemia, heart
blood)
AO, AWO, BLO, Citral,
CO, GO, HBO, LGO,
PEO, SWO
AT, C, CL, CPM, CTR, CTX, E, G, Mox
NO
6
Human (diarrhoea,
faecal swab)
AWO, PEO, SWO
AC, AMX, E
NO
Poultry (Inshell
embronic death,
yolk)
AWO, LGO
Cl, E
NO
Tigress (metritis,
uterine swab)
AWO
Nil
No
Morgenella morganii
A total of three samples one each from cattle (abortion), dog (UTI) and human (UTI) were positive
for ESBL producer Morganella morganii (Tab. 6).
Morganella morganii, commonly found in the environment and gastro-intestinal tracts of humans,
mammals, and reptiles as normal flora, is an uncommon cause of community-acquired infection but a
nosocomial pathogen (Liu et al., 2016; Singla et al., 2010) often associated with urinary tract infections
(Leyla, 2019), sepsis (Kim et al., 2007), abortions (Dessie et al., 2020) and postpartum infections
(Petruzziello et al., 2020).
Table 6. Antimicrobial resistance pattern of Morganella morganii strains from different
clinical sources.
Morganella morganii sources
Resistant to
herbal
antimicrobial
Resistant to conventional
antimicrobials
Comments
Cattle (abortion, deep vaginal swab)
AWO, GO, PEO
A, AMX, AZM, Co, E,Nf
ESBL +ve
DOG (UTI, urine)
AWO, GO, PEO,
SWO
A, AC, AMX, CO, Cx, E, EF, G,
MR, Na, Pi, T
ESBL +ve
Human (UTI, urine)
Not tested
Cl, Nf, Pi, T
ESBL +ve
Non-coli Escherichia
Escherichia fergusonii
Clinical samples of a total of 41 cases including abortions (8), septicemic death (16), diarrhoea (4),
endometritis (2), enteritis (1), mandibular abscesses (5), prostatitis (1), and urinary tract infections (4)
were carrying E. fergusonii strains. Of the 41 strains in the study two were positive for NDM-5 and MIC
of imipenem for both the strains was >32µg/mL, and both were isolated from cases of UTI in lionesses.
Besides 17 strains also detected producing ESBL and were distributed among different animals (Tab. 7).
Though herbal antimicrobials like ajovan oil, carvacrol, cinnamaldehyde and thyme oil inhibited majority
of the strains but a few strains were highly drug resistant (Tab. 8).
Escherichia fergusonii is often considered a commensally occurring bacterium and considered along
with faecal coliforms, a few strains may infect open wounds, cause bacteraemia, urinary tract infections,
haemorrhagic uremic syndrome (Baek et al., 2019; Savini et al., 2008).The pathogenic strains of E.
fergusonni are usually multiple drug-resistant (MDR), usually resistant to ampicillin, gentamicin and
chloramphenicol (Mahapatra et al., 2015). It may cause infections in animals like enteritis in goats
(Hariharan et al., 2007), pneumonia in cow (Rimoldi and Moeller, 2013), enteritis and septicemia in horse
(Weiss et al., 2011) and fibrino-necrotic typhlitis in ostriches (Herráez et al., 2005).
Escherichia hermannii
A single isolate of Escherichia hermannii from bone marrow of poultry bird died of septicemia was
susceptible to all herbal antimicrobial but resistant to ampicillin, amoxicillin, amoxicillin + clavulanic
acid, azithromycin, chloramphenicol, colistin, erythromycin, nitrofurantoin, piperacilllin and tigecycline.
Though a close relative of Escherichia coli, it is rarely a cause infection in animal and humans but
often isolated as co-infection. It can easily be distinguished from E. coli by its yellow pigment (Dahl et
al., 2002). Now evidences suggest that it may be pathogenic even to apparently healthy people (Tong et
7
al., 2014). Commonly E. hermannii is reported to cause bacteremia, urinary tract, and central nervous
system infections and sometimes sepsis. Cephalosporins and aminoglycosides are reported to be effective
in its treatment (Ioannou, 2019).
Escherichia vulneris
A total of 20 isolates of E. vulneris associated with abortions in cows in 3rd trimester (4),
septicemic deaths in birds (9 poultry birds, 1 owl), Himalayan black bear (2) and an Gaur ungulate (1),
diarrhoea (poultry 1), enteritis (tiger 1) and one from urinary tract infections with bacteriuria in an adult
lady. All the 20 isolates were susceptible to ajovan oil and carvacrol (Tab. 9). Though antimicrobial
susceptibility varied among strains tested (Tab. 10), all were susceptible to chloramphenicol, imipenem,
cefotaxime+clavulanic acid and piperacillin+ tazobactam. Six strains produced ESBL but none was
metallo--lactamase positive.
Escherichia vulneris, an opportunistic pathogen mostly affecting immune-suppressed individuals,
in healthy people may cause diarrhoea (Jain et al., 2016) wound infections (Brenner et al., 1982),
peritonitis, bacteraemia (Kilani et al., 2008), sepsis (Horii et al, 2001), osteomyelitis (Levine and
Goldberg , 1994), meningitis (Mohanty et al., 2005), peritonitis (Senanayake et al., 2006) and urinary
tract infections (Awsare and Lillo, 1991). Though animals and birds are rarely reported to be affected by
E. vulneris, carriage of MDR strains is reported by wild birds (Shobrak and Abo-Amer, 2014).
Obesumbacterium proteus
From a case of liver damage the Obesumbacterium proteus isolation was made from liver tissue in
pure culture. The isolate was resistant to agarwood oil, guggul oil, holy basil oil, lemongrass oil, patchouli
essential oil, sandalwood oil, ampicillin, amoxicillin, amoxicillin clavulanic acid, cotrimoxazole,
enrofloxacin, piperacillin, piperacillin tazobactam and tetracycline. It is a bear spoilage bacterium but has
rarely been reported from infections in animals or humans (Praadh, 2015; Priest and Baker, 2010).
Pragia fontium
Of the five strains of Pragia fontium detected from clinical samples (Tab. 11) four were from
cattle only (2 aborted foetus stomach contents, 1 peritoneal fluid of dad cow and faecal sample from a
diarrhoeic calf) and one from liver and spleen of a dead wild crow. One isolate was phenotypically ESBL
producer.
Free-Living enterobacterium Pragia fontium is not a specific host associated bacteria and often
isolated from water sources (Snopková et al., 2017), foods and other environmental sources (Singh,
2013). It has been reported as part of healthy vaginal microobiome of Bos frontalis (Singh et al., 2014)
and sows (Singh and Ebibeni, 2016) and samples of rodents and birds (Jemilehin et al., 2016) but rarely
reported to be associated with diarrhoea in animals (Singh et al., 2017).
Providencia
Of the seven strains of Providenicia isolated from clinical cases of animals and birds, three belonged
to P. alkalifaciens, one each to P. rettgerii and P. rustigianii and two strains were of P. stuartii species
(Tab. 12).
Providencia genus has five species, except P. heimbachae strains all produce indole (P. stuartii, P.
rettgeri, P. alcalifaciens, P. rustigianii). Most of the isolates are of faecal origin and also been reported
from amphibians, insects and lizards (Singh et al., 2014). Among all Providencia species P. rettgeri and
P. stuartii are the most common opportunistic pathogen often associated with nosocomial infections in
severe burn patients or with long-term indwelling urinary catheters causing bacteriuria (Armbuster et al.,
2014; Wei, 2015). Providencia stuartii strains are mostly resistant to tetracyclines, penicillins,
cephalosporins, but susceptible to late-generation cephalosporins, aztreonam, and carbapenems (Charbek,
2019).
8
Table 7. Antimicrobial drug resistance among Escherichia fergusonii species strains from different clinical sources.
Antimicrobials
Number of isolates showing resistance to different antimicrobial according to source (total number of isolates)
Cattle
(9)
Dogs (4)
Goat (1)
Horses
(5)
Humans
(2)
Lions
(2)
Peacocks
(2)
Pig (1)
Poultry
birds (7)
Tigers (8)
Total
(41)
ESBL Producers
6
3
1
1
2
0
2
0
1
1
17
Amoxicillin +
clavulanic acid
3
1
0
2
0
2
2
0
3
6
19
Amoxicillin
6
0
1
2
1
2
2
0
4
7
25
Ampicillin
8
1
1
2
2
2
0
0
5
7
28
Azithromycin
3
2
1
0
0
0
0
0
2
6
14
Aztreaonam
2
0
0
1
0
0
0
0
0
3
6
Cefepime
4
1
0
0
0
2
0
0
0
5
12
Cefotaxime
3
0
0
2
1
2
0
0
0
0
8
Cefotaxime +
clavulanic acid
0
0
0
0
0
2
0
0
0
0
2
Cefoxitin
2
0
0
1
0
0
0
0
2
0
5
Ceftazidime
2
1
0
0
0
2
0
0
0
0
5
Ceftazidime +
clavulanic acid
0
1
0
0
0
0
0
0
0
0
1
Ceftriaxone
3
0
0
2
0
2
0
0
1
0
8
Chloramphenicol
0
0
0
0
0
0
0
0
2
0
2
Colistin
3
3
0
0
0
0
2
0
3
0
11
Co-trimoxazole
1
2
1
1
0
2
0
0
4
6
17
Erythromycin
9
3
1
5
2
2
2
1
4
1
30
Enrofloxacin
3
0
1
2
1
2
0
0
3
6
18
Gentamicin
2
0
0
1
0
2
0
0
2
5
12
Imipenem
0
0
0
0
0
2
0
0
0
5
7
Meropenem
0
0
0
0
0
2
0
0
0
5
7
Moxalactam
2
0
0
1
0
0
0
0
1
0
4
Nalidixic acid
3
2
1
1
2
2
0
0
4
0
15
Nitrofurantoin
2
2
0
2
0
2
0
0
5
7
20
Piperacillin
6
0
1
1
1
2
2
0
2
6
21
Piperacillin +
tazobactam
3
0
0
0
0
2
1
0
0
0
6
Tetracycline
6
2
1
2
1
2
2
0
4
7
27
Tigecycline
0
0
0
0
0
0
0
0
0
0
0
9
Table 8. Herbal antimicrobial drug resistance among Escherichia fergusonii species strains from different clinical sources.
Herbal
antimicrobials
Herbal antimicrobial resistant strains and source of isolates of Escherichia fergusonii in association with different clinical
disorders (total number of isolates)
Tota
l
Cattle
Dogs
Goat
Horses
Human
s
Lion
s
Peacocks
Pig
Poultry
birds
Tiger
abortions
(8) ,
septicemi
c death
(1)
diarrhoea
(1),
prostatitis
(1) ,
endometriti
s (2)
diarrhoea
(1),
prostatitis
(1),
endometritis
(2)
mandibular
abscess (5)
UTI
cases
(2)
UTI
cases
(2)
septicemi
c deaths
(2)
diarrhoe
a (1)
septicemi
c deaths
(7)
septicemi
c deaths
(7),
diarrhoea
(1)
41
Agarwood oil
7
0
1
4
1
2
2
1
1
NT
19
Ajowan oil
0
0
0
0
0
0
0
0
1
1
2
Betel leaf oil
4
0
0
1
0
0
2
0
3
NT
10
Carvacrol
1
0
0
0
0
0
0
0
2
0
3
Cinnamledehyde
2
0
0
0
0
0
0
0
0
1
3
Cinnamon oil
2
0
0
0
0
0
0
0
1
2
5
Citral
8
3
1
2
0
0
2
1
4
7
28
Guggul oil
7
1
1
5
2
2
2
1
5
NT
26
Holy basil oil
1
2
0
0
0
1
0
0
3
5
12
Lemongrass oil
3
3
1
4
1
1
1
1
4
7
26
Patchouli essential
oil
8
0
1
4
1
2
2
1
1
0
20
Sandalwood oil
4
2
1
4
2
2
1
1
4
0
21
Thyme oil
1
0
0
0
0
0
0
0
2
1
4
10
Table. 9. Herbal antimicrobial drug resistance among Escherichia vulneris species strains from different clinical sources.
Herbal antimicrobials
Herbal antimicrobial resistant strains and source of isolates of Escherichia vulneris in association with different
clinical sources (total number of isolates)
Total
(20)
Cattle (4)
Gaur antelope (10
Himalayan black
bear (2)
Human (1)
Owl (1)
Tiger (1)
Abortions
Septicemic death
Septicemic death
UTI
Septicemic death
Enteritis
Agarwood oil
3
0
0
0
0
0
3
Ajowan oil
0
0
0
0
0
0
0
Betel leaf oil
0
0
0
0
0
0
0
Carvacrol
0
0
0
0
0
0
0
Cinnamledehyde
0
0
0
0
0
0
0
Cinnamon oil
0
0
0
0
1
1
2
Citral
1
1
1
0
1
1
5
Guggul oil
4
1
1
0
0
0
6
Holy basil oil
0
0
0
1
0
1
2
Lemongrass oil
0
1
1
1
1
1
5
Patchouli essential oil
4
1
1
0
0
0
6
Sandalwood oil
2
1
1
0
0
0
4
Thyme oil
0
0
0
1
0
0
1
Table 10. Antimicrobial drug resistance among Escherichia vulneris species strains from different clinical sources (total
number of isolates).
Antimicrobials
Cattle (4)
Gaur antelope (10
Himalayan black
bear (2)
Human (1)
Owl (1)
Tiger (1)
Total (20)
Abortions
Septicemic death
Septicemic death
UTI
Septicemic death
Enteritis
ESBL Producers
3
0
1
0
1
1
6
Amoxicillin +
clavulanic acid
1
0
0
0
0
0
1
Amoxicillin
1
0
1
0
1
0
3
Ampicillin
0
0
1
0
0
0
1
Azithromycin
0
0
0
0
1
0
1
11
Aztreaonam
1
1
1
1
0
1
5
Cefepime
1
0
0
0
0
1
2
Cefotaxime
1
0
1
0
0
1
3
Cefotaxime +
clavulanic acid
0
0
0
0
0
0
0
Cefoxitin
1
0
0
0
0
0
1
Ceftazidime
1
0
0
0
0
1
2
Ceftazidime +
clavulanic acid
0
0
0
0
0
1
1
Ceftriaxone
1
0
1
0
0
0
2
Chloramphenicol
0
0
0
0
0
0
0
Colistin
1
0
0
1
0
1
3
Co-trimoxazole
1
0
0
0
1
0
2
Erythromycin
3
1
1
1
1
1
8
Enrofloxacin
0
0
0
1
1
0
2
Gentamicin
0
0
0
0
1
0
1
Imipenem
0
0
0
0
0
0
0
Meropenem
0
0
0
0
0
0
0
Moxalactam
0
0
0
0
0
0
0
Nalidixic acid
0
0
0
0
1
0
1
Nitrofurantoin
1
0
0
1
1
0
3
Piperacillin
1
0
0
0
1
0
2
Piperacillin +
tazobactam
0
0
0
0
0
0
0
Tetracycline
1
0
0
0
1
0
2
Tigecycline
0
0
0
0
0
0
0
12
Table. 11. Antimicrobial resistance pattern of Pragia fontium strains from different clinical sources.
Pragia fontium sources
Resistance to herbal
antimicrobials
Resistance to conventional
antimicrobials
Comment
s
Cattle, aborted fetal contents
AWO, LGO, SWO
A, AMX, Cx, E, EF, G, I, MR, Mox,
Na, Nf, Pi, PTT, T, TGC
Produced
ESBL
Cattle, abortion, deep vaginal
swab
AWO, GO, LGO,
PEO, SWO
Nf, T
No
Cattle, faeces of diarrhoeic calf
AWO, GO,PEO,
SWO
AZM, Cx, E
No
Cattle, death due to peritonitis,
peritoneal fluid)
AWO, citral, GO,
LGO, PEO, SWO
E, Na, Nf, T
No
Wild crow, liver and spleen of
the dead crow
AWO, GO,LGO,
PEO, SWO
A, Co, Na, T
No
Table 12. Antimicrobial resistance pattern of Providencia species strains from different
clinical sources.
Species and sources of isolation
Resistance to herbal
antimicrobials
Resistance to conventional
antimicrobials
Providencia alkalifaciens sources
Goat, diarrhoea in kid, rectal swab
AWO, Citral, GO, LGO, PEO,
SWO
A, AC, AMX, AZM, C, Cl, Co, E,
EF, Na, Nf, Pi, T
Goat, nasal catarrh, nasal swab
AWO, BLO, Citral, GO, HBO,
LGO, PEO, SWO
A, AC, AMX, Cl, E, I, Nf, Pi, PiT,
T, TIG
Cattle, abortion, stomach contents of
aborted foetus
BLO, Citral, GO, LGO, PEO,
SWO
AZM, E, Pi, PTT
Providencia rettgeri sources
Cattle, mastitis, milk
AWO, PEO
A, AC, AMX, Cl, Co, CTX, Cx, E,
G,Nf, Pi, T
Providencia rustigianii sources
Pig, wound infection, pus swab
BLO, Citral, GO, HBO, LGO,
SWO
AC, Cl, Co, E, Nf, T
Providencia stuartii sources
Horse, otorrhoea, middle ear swab
AWO, GO, LGO, SWO
A, AC, AMX, CA, Cl, E, MR,
Mox, Nf, T
Poultry, enteritis, cloacal swab
Citral, HBO, LGO
AC, Cl, Co, E, EF, Na, Nf, Pi, T
Shimwellia blattae
Shimwellia blattae was identified in two samples associated with pyogenic infections in animals (a
surgical wound infection in a cattle and an abscess of an adult dog). The isolate from infected surgical
wound was resistant to amoxicillin, amoxicillin + clavulanic acid, aztreonam, cefoxitin and piperacillin
but was sensitive to 2nd-4th generation cephalosporins. The isolate from the abscess of a dog was
resistant to amoxicillin, aztreonam, ceftriaxone and piperacillin.
Shimwellia blattae, earlier known as Escherichia blattae, an aerobic enteric bacterium first isolated
from the hindgut of cockroaches, is not considered pathogenic to humans and animals (Priest and Baker,
2010).
Xenorhabdus
Xenorhabdus strains were isolated from samples of 15 cases in association with abortion in
bovines (4 X. bovienii, 1 X. poinarii), abscess (1 X. bovienii, 1 X. poinarii), septicemic (1 X. bovienii) and
uremic death (1 X. poinarii), death in shell of poultry embryo (1 X. bedingii), diarrhoea (1 X. boviennii),
13
mastitis in cattle (1 X. poinarii) and wound infections (3 X. bovienii). Of the 15 isolates, 7 were
phenotypically positive for ESBL and two isolates of X. bovienii were resistant to carbapenem drugs
(Tab. 13).
It is a genus of in Morganellaceae family known to live in symbiosis with soil entomopathogenic
nematodes from the genus Steinernema. Strains of Xenorhabdus are known to produce a variety of
bioactive agents including antibacterial, antifungal, anti-insects, anti-helminthic, anti-protozoal and
cancer cell-killing compounds (Jönike et al., 2018; Herbert and Goodrich-Blair, 2007; Saux et al., 1999).
More than 26 species of Xenorhabdus are known to be either symbionts or pathogens of nematodes are
rarely reported from human or animals as pathogen. Even Xenorhabdus strains are known to be of
potential use to cure mastitis due to their antibacterial activity against staphylococci.
Table 13. Antimicrobial resistance pattern of Xenorhabdus species strains from different
clinical sources.
Species and sources of
isolation
Resistance to herbal
antimicrobials
Resistance to conventional
antimicrobials
Comments
Xenorhabdus bedingii sources
Poultry, embryonic death in
shell, yolk
GO, SWO
A, AC, AMX, AT, Co, CTR, E,
Nf, Pi
Produced
ESBL
Xenorhabdus bovienii sources
Buffalo, abortion, stomach
contents of the aborted
foetus
GO, PEO
A, AC, AMX, AT, CA, CAC,
Cx, MR, Na
No
Buffalo, abortion, stomach
contents of the aborted
foetus
AWO, citral, GO, LGO, PEO,
SWO
A, AC, AMX, AT, CA, CTX,
Cx, E, Mox, Na, Nf, Pi, PTT
Produced
ESBL
Cattle, abortion, stomach
contents of the aborted
foetus
AWO, GO, LGO, PEO, SWO
A, AC, AMX, Co, E, Pi
Produced
ESBL
Cattle, abortion, stomach
contents of the aborted
foetus
AWO, GO, LGO, PEO, SWO
A, Cl, Cx, E, EF, Na
No
Dog, wound infection, pus
swab
Citral, HBO, LGO
A, AC, AMX, Cl, Co, CTR,
CTX, E, EF, G, I, Na, Nf, Pi, T,
TGC
No
Dog, wound infection, pus
swab
No
A, AC, AMX, AT, Cl, CTR,
CTX, Cx, E, EF, Na, Nf, Pi
Produced
ESBL
Duckling, death, choanal
swab
AWO, citral, GO, LGO, PEO
Co,E, EF, G, Na, Pi, PTT, T
No
Elephant, wound infection,
pus swab
AO, citral, GO, HBO,
LGO,SWO, PO
AC, C, E, T
No
Human, persistent
diarrhoea, faecal swab
AWO, GO, PEO, SWO
A, AC, AMX, AT, CO, CTR,
CTX, E, EF, Na, Nf, Pi, PTT, T
Produced
ESBL
Spotted deer, abscess, pus
swab
AWO, BLO, Citral, CNH, CO,
GO, HBO, LGO, PEO, SWO
Cl, Co, CTX, E, EF, G, Na, T
Produced
ESBL
Xenorhabdus poinarii sources
Buffalo, abortion, stomach
contents of aborted foetus
GO, PEO, SWO
CA, CAC, Cx, E
No
Cattle, mastitis, milk
AO, AWO, BLO, Cav, Citral,
CNH, CO, GO, HBO, LGO,
PEO, SWO, TO
A, AMX, AT, CA, CAC, Cl, Co,
CTR, CTX, CTX/CLA, Cx, E,
EF, Pi, T
Produced
ESBL
Dog, abscess, pus swab
BLO, Cav, Citral, CNH, GO,
SWO, TO
Cl, Mox, Nf, T
No
Rabbit, uremic death, urine
CNH, HBO
AT, Cl, E
No
14
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