Co esponding au ho : Ayoub Aame
Copy igh © 2025 Au ho (s) e ain he copy igh o his a icle. This a icle is published unde he e ms o he C ea i e Commons A ibu ion License 4.0.
Mic obiological P o ile and An ibio ic Resis ance in Diabe ic Foo In ec ions: A
Re ospec i e S udy om Ma akech
Ayoub Aame *, Yous a Boughalem, Yousse El Kamouni, Lamiae A salane and Said Zouhai
Depa men o Mic obiology, A icenne Milli a y Hospi al, Ma akech, MAR.
GSC Biological and Pha maceu ical Sciences, 2025, 33(01), 246-251
Publica ion his o y: Recei ed on 15 Sep embe 2025; e ised on 22 Oc obe 2025; accep ed on 25 Oc obe 2025
A icle DOI: h ps://doi.o g/10.30574/gscbps.2025.33.1.0411
Abs ac
In oduc ion: Diabe ic oo in ec ion (DFI) is a se e e complica ion o diabe es, o en leading o hospi aliza ion and
ampu a ion. This s udy aimed o desc ibe he causa i e pa hogens and hei an imic obial esis ance pa e ns.
Me hods: We conduc ed a e ospec i e s udy o 146 pa ien s hospi alized o DFI a A icenne Mili a y Hospi al,
Ma akech, be ween 2018 and 2023. Clinical da a, mic obiological esul s, and an ibio ic suscep ibili y p o iles we e
collec ed and analyzed acco ding o CASFM/EUCAST (Comi é De l'An ibiog amme de la Socié é F ançaise de
Mic obiologie/Eu opean Commi ee on An imic obial Suscep ibili y Tes ing) 2025 guidelines.
Resul s: The mean age was 63.27 yea s, wi h a male p edominance (125, 86%) and ype 2 diabe es in 90% (131) o
cases. A o al o 146 bac e ial isola es we e iden i ied, mainly G am-nega i e bacilli (104, 71.2%), wi h En e obac e ales
being he mos equen (87, 60%). The mos equen species we e Esche ichia coli (26, 17.8%), Klebsiella pneumoniae
(21, 14.3%), Pseudomonas ae uginosa (16, 11%), and S aphylococcus au eus (15, 10.3%). En e obac e ales showed
high esis ance o ampicillin (84%), amoxicillin-cla ulanic acid (81%), and cip o loxacin (57%), while suscep ibili y o
imipenem and amikacin emained high. Pseudomonas ae uginosa was also suscep ible o hese agen s, and
S aphylococcus au eus isola es we e uni o mly suscep ible o ancomycin and cip o loxacin.
Conclusion: DFIs in Ma akech a e cha ac e ized by a p edominance o mul id ug- esis an G am-nega i e bacilli. These
indings emphasize he impo ance o a ional an ibio ic use, in ec ion con ol, and con inuous mic obiological
su eillance.
Keywo ds: An ibio ic Resis ance; Diabe ic Foo ; In ec ion; Ma akech; Mic obiology
1. In oduc ion
Diabe ic oo e e s o all in ec ious, ulce a i e, o nec o ic lesions o he oo occu ing in pa ien s wi h diabe es,
ypically associa ed wi h pe iphe al neu opa hy and/o pe iphe al a e ial disease [1]. This complica ion a ec s
app oxima ely 15% o 25% o diabe ic pa ien s [2] and is equen ly complica ed by seconda y in ec ion, epo ed in
25% o 80% o cases [2].
Diabe ic oo in ec ion ep esen s a leading cause o hospi aliza ion, mo bidi y, and non- auma ic ampu a ion, wi h
subs an ial socio-economic and psychological consequences [3]. The isk o ampu a ion can be up o 155 imes highe
in pa ien s wi h DFI [4]. The condi ion o en p og esses insidiously, beginning wi h supe icial issue in ol emen and
po en ially ex ending o deep issues o bone. Ea ly, mul idisciplina y managemen is he e o e c ucial, including
GSC Biological and Pha maceu ical Sciences, 2025, 33(01), 246-251
247
ascula and neu ological assessmen , su gical deb idemen , a ge ed mic obiological sampling, app op ia e an ibio ic
he apy, and op imal glycemic con ol.
In Mo occo, epidemiological da a on ampu a ions ela ed o DFI a e limi ed, unlike in coun ies such as F ance, whe e
diabe ic oo ep esen s he leading cause o lowe limb ampu a ion, a ec ing app oxima ely 8,000 pa ien s annually
[2].
The objec i e o his s udy was o desc ibe he mic obiological p o ile o DFIs and o e alua e he an ibio ic suscep ibili y
pa e ns o he isola ed pa hogens.
2. Ma e ials and me hods
We conduc ed a e ospec i e desc ip i e s udy o 146 pa ien s hospi alized o diabe ic oo in ec ions a A icenne
Mili a y Hospi al, Ma akech, be ween Feb ua y 2018 and May 2023. Pa ien s wi h oo ulce s o in ec ions in a diabe ic
con ex we e included, while non-diabe ic pa ien s, admissions ou side he s udy pe iod, o incomple e eco ds we e
excluded.
Clinical and mic obiological da a we e collec ed om medical eco ds using a s anda dized elec onic da a shee and
analyzed wi h Mic oso Excel.
Mic obiological samples we e collec ed om clinically in ec ed wounds a e p ope wound cleaning and deb idemen .
Depending on he wound, sampling me hods included supe icial swabs, deep cu e age, issue biopsy, o ine needle
aspi a ion. Samples we e anspo ed p omp ly o he labo a o y in app op ia e media. Labo a o y analysis included
mac oscopic and mic oscopic examina ion, cul u e on selec i e and en iched media, and bac e ial iden i ica ion using
G am s aining, colony mo phology, biochemical es s, API s ips, o au oma ed sys ems.
An ibio ic suscep ibili y es ing was pe o med o all bac e ial isola es using disk di usion, b o h mic odilu ion, o
au oma ed me hods, and in e p e ed acco ding o CASFM/EUCAST 2025 guidelines [5].
3. Resul s
A o al o 146 pa ien s we e included, wi h a mean age o 63.27 yea s ( ange 37-86), p edominan ly males (86%). Type
2 diabe es was he mos common (90%), wi h a mean du a ion o 13.44 yea s. Mos pa ien s we e ea ed wi h insulin
(72%) (Figu e 1).
GSC Biological and Pha maceu ical Sciences, 2025, 33(01), 246-251
248
Figu e 1 T ea men egimens among pa ien s (n=146)
Mic obiological analysis yielded 146 bac e ial isola es om clinically in ec ed wounds. G am-nega i e bacilli (71.2%)
we e mo e equen han G am-posi i e cocci (28.7%). En e obac e ales we e he mos equen (60%), ollowed by
s aphylococci (14%), non- e men ing G am-nega i e bacilli (11%), and s ep ococci (10%) (Figu e 2). The mos
common species we e Esche ichia coli (17.8%), Klebsiella pneumoniae (14.3%), Pseudomonas ae uginosa (11%), and
S aphylococcus au eus (10.3%).
Figu e 2 Dis ibu ion o majo bac e ial g oups (n=146)
In ou s udy, we analyzed he esis ance pa e ns o he mos equen ly isola ed bac e ia. The de ailed an ibio ic
esis ance a es o he main bac e ial species a e summa ized in Table 1.
Table 1 An ibio ic esis ance a es o main bac e ial isola es
Bac e ial species
Main an ibio ic esis ances
Mos e ec i e an ibio ics
En e obac e ales (n=87)
AMP 84%, AMC 81%, TIC 67%, SXT
58%, CIP 57%
IMI, AMK
Esche ichia coli (n=26)
AMP 76%, TIC 71%, AMC 69%, CIP
58%, SXT 58%, TZP 42%, CRO 29%,
FOS 19%
IMI 8%, GEN 4%, AMK 8%
Klebsiella pneumoniae (n=21)
AMC 75%, CIP 76%, SXT 71%, TZP
48%, GEN 43%, CRO 33%, FOS 40%,
IMI 31%
AMK 0% (all suscep ible)
Pseudomonas ae uginosa (n=16)
TIC 69%, CIP 44%, FOS 28%, ATM
22%, GEN 13%, CAZ 13%, TZP 13%
IMI 6%, AMK 6%
S aphylococcus au eus (n=15)
PEN 92%, MRSA 25%, GEN 20%, FUS
20%, TOB 13%, SXT 10%, RIF 7%
VAN 0%, CIP 0% (all suscep ible)
AMP = ampicillin; AMC = amoxicillin-cla ulanic acid; TIC = ica cillin; SXT = ime hop im-sul ame hoxazole; CIP = cip o loxacin; IMI = imipenem;
AMK = amikacin; TZP = pipe acillin- azobac am; CRO = ce iaxone; FOS = os omycin; GEN = gen amicin; CAZ = ce azidime; ATM = az eonam; FUS
= usidic acid; TOB = ob amycin; RIF = i ampicin; VAN = ancomycin; MRSA = me hicillin- esis an S. au eus.
O e all, En e obac e ales we e highly esis an o β-lac ams and luo oquinolones bu emained suscep ible o
imipenem and amikacin. Pseudomonas ae uginosa showed simila suscep ibili y pa e ns. S aphylococcus au eus
isola es we e ully suscep ible o ancomycin and cip o loxacin.
GSC Biological and Pha maceu ical Sciences, 2025, 33(01), 246-251
249
4. Discussion
In ou se ies o 146 pa ien s, he mean age was 63.27 yea s, simila o p e ious epo s [6]. Male p edominance (86%)
was also obse ed in o he s udies [6,7]. Type 2 diabe es was he mos common o m (90%), consis en wi h he
li e a u e [8,9], wi h a mean du a ion o 13.44 yea s, compa able o 12.5 and 11.7 yea s epo ed in hese s udies. Mos
pa ien s we e ea ed wi h insulin (72%), in line wi h p e ious indings [10].
Bac e iological sampling is a co ne s one in DFI managemen . Deep echniques such as cu e age, aspi a ion, and biopsy
a e p e e ed o hei diagnos ic accu acy. Al hough hese me hods we e used in ou s udy, hei indi idual equencies
could no be de e mined due o he e ospec i e design.
Unlike classical epo s showing G am-posi i e cocci p edominance, ou esul s e ealed a majo i y o G am-nega i e
bacilli (71.2%), mainly En e obac e ales (60%), consis en wi h da a om A ica and Asia [11,12]. E.coli was he mos
equen isola e (17.8%), compa able o o he se ies [13,14]. S ep ococcus spp. Accoun ed o 9.6%, sligh ly highe han
in p e ious s udies [13,15,16], whe eas S. au eus ep esen ed 10.3%, lowe han epo ed elsewhe e [7,16].
Pseudomonas ae uginosa was isola ed in 11% o cases, a a e simila o o he indings [13,17].
Rega ding an imic obial esis ance, all S. au eus s ains we e suscep ible o ancomycin, while i ampicin was e ec i e
in 93% o isola es, in acco dance wi h ea lie s udies [18,19]. Me hicillin esis ance was de ec ed in 25% o S. au eus,
simila o p e iously epo ed a es [20,21]. En e obac e ales showed high esis ance o be a-lac ams, pa icula ly
amoxicillin and ica cillin, while main aining suscep ibili y o aminoglycosides and imipenem. Ce iaxone esis ance
was 30%, close o he 28% epo ed elsewhe e [22]; ampicillin esis ance eached 76% compa ed o 48% in ano he
se ies [18].
Pseudomonas ae uginosa exhibi ed 13% esis ance o pipe acillin, lowe han in o he epo s [15,18], while esis ance
o o he be a-lac ams, aminoglycosides, and luo oquinolones was in e media e compa ed o he li e a u e [15,19].
O e all, ou indings emphasize he p edominance o mul id ug- esis an G am-nega i e bacilli in DFI and highligh he
impo ance o a ge ed an ibio ic he apy based on local mic obiological su eillance.
This s udy is limi ed by i s e ospec i e design, which led o incomple e medical eco ds and loss o ollow up o some
pa ien s. Impo an de ails we e o en missing, including he ype o mic obiological sample collec ed, cul u e ou comes
(s e ile, monomic obial, o polymic obial), de ec ion o mul id ug- esis an bac e ia, classi ica ion o diabe ic oo
in ec ions acco ding o he In e na ional Consensus, an ibio ic egimen and du a ion, and pa ien clinical e olu ion.
These ac o s may ha e in luenced he comple eness and in e p e a ion o ou indings.
5. Conclusion
Diabe ic oo in ec ions a e a common cause o hospi aliza ion, associa ed wi h high mo bidi y, long an ibio ic cou ses,
and inc eased isk o ampu a ion. Ou s udy demons a es a p edominance o G am-nega i e bacilli, pa icula ly
Esche ichia coli, wi h high esis ance o se e al commonly used an ibio ics.
These indings unde sco e he impo ance o a ional an ibio ic use guided by local suscep ibili y pa e ns, s ic
hygiene, and p e en i e measu es. To comba he g owing h ea o bac e ial esis ance, con inuous mic obiological
su eillance, a ge ed heal hca e s a aining, and public awa eness a e essen ial o educe ea men ailu es and
p ese e an ibio ic e icacy.
Compliance wi h e hical s anda ds
Disclosu e o con lic o in e es
The e is no con lic o in e es ega ding his pape .
S a emen o in o med consen
The s udy was ca ied ou wi hou any in e ac ion wi h indi iduals, making in o med consen unnecessa y.
A ailabili y o da a and ma e ials
GSC Biological and Pha maceu ical Sciences, 2025, 33(01), 246-251
250
The da a and ma e ials used o suppo he indings o his s udy a e publicly a ailable.
Re e ences
[1] Chidiac, C. (2006). Managemen o in ec ed diabe ic oo . F ench-Language In ec ious Diseases Socie y (SPILF).
[2] Magnan, C., Pan el, A., Dubois, A., e al. (2022). Pa hophysiology, ecology and mic obiological diagnosis o os ei is
o he oo in pa ien s li ing wi h diabe es melli us. Re ue F ancophone des Labo a oi es, 2022(545), 36–44.
h ps://doi.o g/10.1016/S1773-035X(22)00311-2
[3] Bou oille, D., Fé aille, A., Maulaz, D., and K emp , M. (2008). Quali y o li e wi h diabe es-associa ed oo
complica ions: Compa ison be ween lowe limb ampu a ion and ch onic oo ulce a ion. Foo and Ankle
In e na ional, 29(11), 1074–1078. h ps://doi.o g/10.3113/FAI.2008.1074
[4] La e y, L. A., A ms ong, D. G., Wunde lich, R. P., Mohle , M. J., Wendel, C. S., and Lipsky, B. A. (2006). Risk ac o s
o oo in ec ions in indi iduals wi h diabe es. Diabe es Ca e, 29(6), 1288–1293. h ps://doi.o g/10.2337/dc05-
2425
[5] CASFM/EUCAST. (2025). Recommenda ions o he An ibiog am Commi ee o he F ench Socie y o Mic obiology
/ Eu opean Commi ee on An imic obial Suscep ibili y Tes ing ( e sion 2025). h ps://www.s m-
mic obiologie.o g/wp-con en /uploads/2025/07/CASFM2025_V1.1-JUILLET-2025.pd
[6] Zemmou i, A., Ta chouli, M., Benbouha, A., e al. (2015). Bac e iological p o ile o diabe ic oo and i s impac on
he choice o an ibio ics. Pan A ican Medical Jou nal, 20, 1–7. h ps://doi.o g/10.11604/pamj.2015.20.148.5853
[7] Sel a ajan, S., Dhandapani, S., R. A., T. L., and Lakshmanan, A. (2021). Bac e iological p o ile o diabe ic oo ulce s
and de ec ion o me hicillin- esis an S aphylococcus au eus and ex ended-spec um β-lac amase p oduce s in a
e ia y ca e hospi al. Cu eus. h ps://doi.o g/10.7759/cu eus.20596
[8] Laidi, S., El Aziz, S., & Chadli, A. (2016). Managemen o in ec ed diabe ic oo a Ibn Rochd Uni e si y Hospi al in
Casablanca: abou 244 cases. Annales d’Endoc inologie, 77(4), 498–528.
h ps://doi.o g/10.1016/j.ando.2016.07.805
[9] Djib il, A. M., Mossi, E. K., Djagadou, A. K., Balaka, A., Tchamdja, T., & Moukaila, R. (2018). Diabe ic oo :
epidemiological, diagnos ic, he apeu ic, and e olu iona y aspec s a he medico-su gical clinic o Syl anus
Olympio Uni e si y Hospi al in Lomé. Pan A ican Medical Jou nal, 30, A icle 4.
h ps://doi.o g/10.11604/pamj.2018.30.4.14765
[10] Oua adi, A. E. L. (2019). Diabe ic oo : epidemiological, he apeu ic, and p ognos ic p o ile (Doc o al hesis,
Facul y o Medicine and Pha macy, Ma akech).
[11] Sen, P., Demi dal, T., and Emi , B. (2019). Me a-analysis o isk ac o s o ampu a ion in diabe ic oo in ec ions.
Diabe es/Me abolism Resea ch and Re iews, 35(3), e3175. h ps://doi.o g/10.1002/dm .3165
[12] Ci on, D. M., Golds ein, E. J., Me iam, C. V., Lipsky, B. A., and Ab amson, M. A. (2007). Bac e iology o mode a e-
o-se e e diabe ic oo in ec ions and in i o ac i i y o an imic obial agen s. Jou nal o Clinical Mic obiology,
45(9), 2819–2828. h ps://doi.o g/10.1128/JCM.00551-07
[13] Jouha , L., Jaa a , R. F., Nas eddine, R., I ani, O., Haddad, F., Rizk, N., and Hoballah, J. J. (2020). Mic obiological
p o ile and an imic obial esis ance among diabe ic oo in ec ions in Lebanon. In e na ional Wound Jou nal,
17(6), 1764–1773. h ps://doi.o g/10.1111/iwj.13465
[14] Du gad, S., Ko icha, A., Na a aj, G., Deshpande, A., and Meh a, P. (2014). Diabe ic oo ulce s—whe e do we s and
mic obiologically? In e na ional Jou nal o Diabe es in De eloping Coun ies, 34(3), 169–173.
h ps://doi.o g/10.1007/s13410-013-0180-9
[15] Tu han, V., Mu luoglu, M., Aca , A., e al. (2013). Inc easing incidence o G am-nega i e o ganisms in bac e ial
agen s isola ed om diabe ic oo ulce s. Jou nal o In ec ion in De eloping Coun ies, 7(10), 707–712.
h ps://doi.o g/10.3855/jidc.2967
[16] Mendes, J. J., Ma ques-Cos a, A., Vilela, C., e al. (2012). Clinical and bac e iological su ey o diabe ic oo
in ec ions in Lisbon. Diabe es Resea ch and Clinical P ac ice, 95(2), 153–161.
h ps://doi.o g/10.1016/j.diab es.2011.10.001
[17] Hamid, M. H., A bab, A. H., and Youse , B. A. (2020). Bac e iological p o ile and an ibio ic suscep ibili y o diabe ic
oo in ec ions a Riba Uni e si y Hospi al: A e ospec i e s udy om Sudan. Jou nal o Diabe es and Me abolic
Diso de s, 19, 1397–1406. h ps://doi.o g/10.1007/s40200-020-00660-8
GSC Biological and Pha maceu ical Sciences, 2025, 33(01), 246-251
251
[18] Al Benwan, K., Al Mulla, A., and Ro imi, V. O. (2012). A s udy o he mic obiology o diabe ic oo in ec ions in a
eaching hospi al in Kuwai . Jou nal o In ec ion and Public Heal h, 5(1), 1–8.
h ps://doi.o g/10.1016/j.jiph.2011.07.004
[19] Goh, T. C., Baju i, M. Y., Nada ajah, S. C., Abdul Rashid, A. H., Baha uddin, S., and Zam i, K. S. (2020). Clinical and
bac e iological p o ile o diabe ic oo in ec ions in a e ia y ca e cen e. Jou nal o Foo and Ankle Resea ch, 13,
36. h ps://doi.o g/10.1186/s13047-020-00406-y
[20] Rennie, R. P., Jones, R. N., and Mu nick, A. H. (2003). Occu ence and an imic obial suscep ibili y pa e ns o
pa hogens isola ed om skin and so issue in ec ions: Repo om he SENTRY An imic obial Su eillance
P og am (Uni ed S a es and Canada). Diagnos ic Mic obiology and In ec ious Disease, 45(4), 287–293.
h ps://doi.o g/10.1016/S0732-8893(02)00543-6
[21] Be and, X., Cos a, Y., and Pina, P. (2005). Su eillance o an imic obial esis ance o bac e ia isola ed om
bloods eam in ec ions: Da a o he F ench na ional obse a o y o epidemiology o bac e ial esis ance o
an ibio ics (ONERBA), 1998–2003. Médecine e Maladies In ec ieuses, 35(6), 329–334.
h ps://doi.o g/10.1016/j.medmal.2005.05.002
[22] Labani, Y. (2016). Bac e iological p o ile and equency o an ibio ic esis ance in diabe ic oo in ec ion (Thesis No.
22, Facul y o Medicine and Pha macy, Ma akech).