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\begin{document}


\def\RunningAuthor{Nandakumar U~P et al.}
\firstPage{160}
\articleType{Original Article}
\receivedDate{10 Aug 2020}
\acceptedDate{12 Sep 2020}
\revisedDate{01 Sep 2020}
\journalVolume{2021, 12}
\journalIssue{1}
\journalDoi{ijrps.v12i1.3972}
\copyrightYear{2021}
\def\authorCount{8}
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\def\journalTitle{International Journal of Research in Pharmaceutical Sciences}

\title{Bacterial Profile and Antibiotic Susceptibility Pattern among Diabetic Foot Ulcer Patients}
\author{Steffy~Ligi~Binu\textsuperscript{1},  
            Abhishek~Chandran\textsuperscript{1},  
            Chaitrashree\textsuperscript{1},  
            Abhijith~Shetty\textsuperscript{2},  
            Sharad~Chand\textsuperscript{1},  
            Juno~J.~Joel\textsuperscript{1},  
            Bharath~Raj~K~C\textsuperscript{1}, 
            Nandakumar~U~P\textsuperscript{*}\textsuperscript{1}~\\[5pt]{\textsuperscript{1}Department of Pharmacy Practice, NGSMIPS, Nitte (Deemed to be University), Mangaluru, Karnataka, India- 575018}~\\{\textsuperscript{2}Department of General Surgery, Justice K.S. Hegde Charitable Hospital, Nitte (Deemed to be University), Deralakatte, Mangaluru- 575018, India}}

\begin{abstract}
The current study was undertaken to analyze the bacteriological profile among diabetic foot ulcer patients and to determine the antibiotic susceptibility and resistance pattern of the organisms isolated. This was a prospective observational study conducted among 102 patients for six months. All patients, aged above 18 years diagnosed with diabetic foot ulcers and performed with culture and sensitivity tests in the department of general surgery, were enrolled in the study. All the relevant details of the study were collected and analyzed. Out of 102 patients enrolled, 72 were males and 30 were females. The majority of the bacteria that were isolated from the culture samples were found to be gram-negative, 119 (79.33\%) and 31 (20.97\%) were found to be gram-positive. Methicillin-resistant coagulase-negative Staphylococcus was the most frequently isolated gram-positive micro-organism. It was found to have more sensitivity to both vancomycin and teicoplanin (100\%) whereas it showed high resistance to benzylpenicillin (84.6\%). Among various gram-negative organisms, Pseudomonas aeruginosa was the most commonly isolated. It showed high sensitivity to doripenem (70.9\%) and was found to be more resistant to levofloxacin (51.6\%). Our study concluded on the predominance of gram-negative bacteria among the enrolled patients. Among the 22 different types of bacteria identified, Pseudomonas aeruginosa was the most frequently isolated species.
\end{abstract}\def\keywordstitle{Keywords}

\begin{keywords}Diabetes,\newline diabetic complication,\newline antibiotics,\newline bacterial resistance,\newline ulcer,\newline antibiotic susceptibility
\end{keywords}
\twocolumn[ \maketitle {\printKwdAbsBox}]
\makeatletter{\raggedright\textsuperscript{*}Corresponding Author\par Name:\ Nandakumar~U~P~\\ Phone:\ ~\\  Email:\ nandakumarvtkv@gmail.com 
        \par}\vspace*{-11pt}\hrulefill\par{\fontsize{12}{14}\selectfont ISSN: 0975-7538}\par% 
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\section{Introduction}
Diabetes mellitus is one of the most prevalent chronic diseases. It is defined as a ``group of metabolic disorders of an endocrine system characterized by increased blood glucose level due to the defects in the insulin secretion, functions of insulin or both'' \unskip~\citep{882223:20294944,882223:20294943}. It can also be caused due to abnormalities in protein, carbohydrate and fat metabolism \unskip~\citep{882223:20294941}. 

World Health Organization has stated that diabetes mellitus is one of the most predominant endocrine disorders of the twenty-first century, holding about 10\% of the global adult population, who would be at risk of being affected \unskip~\citep{882223:20294942,882223:20294947}. Uncontrolled diabetes will lead to several macro and microvascular complications. One of the significant complications of uncontrolled diabetes is diabetic foot ulcers (DFU) \unskip~\citep{882223:20294948}. 

A diabetic foot ulcer is a leading concern that is seen in Type 1 as well as Type 2 diabetes mellitus \unskip~\citep{882223:20294946}. It is estimated that approximately 15-25\% of diabetic patients develop diabetic foot ulcers during the disease, causing severe disability and hospitalization. In diabetic patients, if adequate care is not given, the foot ulcer may develop and progress to severe infection/necrosis which may lead to amputation of the infected foot \unskip~\citep{882223:20294945}. 

The most catastrophic condition in patients with DFU is chronic wounds which may be caused due to compromised immune response with the association of microbial burden \unskip~\citep{882223:20294948}. Timely and proper treatment of ulcers and infections can lower the chances of amputations. The selection of an appropriate antibiotic regimen has become the need for the proper management of diabetic foot ulcers. The services by a clinical pharmacist can help in optimizing the therapy \unskip~\citep{882223:20294949}. 

Adequate knowledge about the microbes that cause infection helps to analyze and determine appropriate antibiotic therapy. Hence, the present study was carried out to assess the microbiological characteristics of diabetic foot ulcers and their susceptibility pattern to various antibiotics.
    
\section{Materials and Methods}
\textbf{Ethical approval}

The Institutional Ethical Committee approved this study of the NGSM Institute of Pharmaceutical Sciences (REF: NGSMIPS/IEC/11/2019-20). 


\begin{table*}[!htbp]
\caption{\boldmath {Gender and Age wise distribution} }
\label{tw-1ef9fa43d439}
\def\arraystretch{1.1}
\ignorespaces 
\centering 
\begin{tabulary}{\linewidth}{p{\dimexpr.12\linewidth-2\tabcolsep}p{\dimexpr.12\linewidth-2\tabcolsep}p{\dimexpr.12\linewidth-2\tabcolsep}p{\dimexpr.12\linewidth-2\tabcolsep}p{\dimexpr.12\linewidth-2\tabcolsep}p{\dimexpr.12\linewidth-2\tabcolsep}p{\dimexpr.12\linewidth-2\tabcolsep}p{\dimexpr.16\linewidth-2\tabcolsep}}
\tbltoprule \rowcolor{kwdboxcolor}Age Group (in years) & 30-39 & 40-49 & 50-59 & 60-69 & 70-79 & 80-89 & Total\\
\tblmidrule 
Males  &
  2  &
  13 &
  21 &
  25 &
  10 &
  1  &
  72\\
Females &
  3  &
  3  &
  8  &
  11 &
  4  &
  1  &
  30\\
Total &
  5  &
  16 &
  29 &
  36 &
  14 &
  2  &
  102\\
\tblbottomrule 
\end{tabulary}\par 
\end{table*}

\begin{table*}[!htbp]
\caption{\boldmath {Distribution of patients based on duration of hospital stay} }
\label{tw-1088bec85428}
\def\arraystretch{1.1}
\ignorespaces 
\centering 
\begin{tabulary}{\linewidth}{p{\dimexpr.33\linewidth-2\tabcolsep}p{\dimexpr.3279\linewidth-2\tabcolsep}p{\dimexpr.3421\linewidth-2\tabcolsep}}
\tbltoprule \rowcolor{kwdboxcolor}No of days of hospital stay & Frequency (n) & Percentage (\%)\\
\tblmidrule 
1-7 &
  13 &
  12.7\\
8-14 &
  45 &
  44.1\\
15-21 &
  28 &
  27.5\\
22-28 &
  11 &
  10.8\\
29-35 &
  4  &
  3.9\\
36-42 &
  1  &
  1.0\\
Total &
  102 &
  100\\
\tblbottomrule 
\end{tabulary}\par 
\end{table*}

\begin{table*}[!htbp]
\caption{\boldmath {Bacteria isolated from DFUs of the study patients} }
\label{tw-d5d15ca164f8}
\def\arraystretch{1.1}
\ignorespaces 
\centering 
\begin{tabulary}{\linewidth}{p{\dimexpr.33\linewidth-2\tabcolsep}p{\dimexpr.24700000000000003\linewidth-2\tabcolsep}p{\dimexpr.42300000000000004\linewidth-2\tabcolsep}}
\tbltoprule \rowcolor{kwdboxcolor}Bacteria & Frequency (n) & Percentage (\%)\\
\tblmidrule 
\textbf{Gram-Positive Organisms} &
  \textbf{30} &
  \textbf{20.97}\\
Enterococcus faecalis &
  3  &
  2.1\\
Enterococcus spps. &
  1  &
  0.7\\
Staphylococcus aureus &
  8  &
  5.5\\
Methicillin-resistant Staphylococcus aureus &
  5  &
  3.4\\
Methicillin-resistant coagulase-negative Staphylococcus &
  13 &
  9.0\\
\textbf{Gram-Negative Organisms} &
  \textbf{113} &
  \textbf{79.03}\\
Acinetobacter baumanni &
  6  &
  4.1\\
Citrobacter frundii &
  4  &
  2.7\\
Citrobacter koseri &
  3  &
  2.0\\
Escherichia coli &
  17 &
  11.8\\
Enterobacter aerogenes &
  3  &
  2.0\\
Klebsiella pneumoniae &
  21 &
  14.7\\
Morganella morganii spp &
  6  &
  4.1\\
Proteus hauseri &
  4  &
  2.7\\
Proteus mirabilis &
  11 &
  7.6\\
Proteus penneri &
  2  &
  1.3\\
Proteus vulgaris &
  5  &
  3.4\\
Pseudomonas aeruginosa &
  31 &
  21.7\\
\tblbottomrule 
\end{tabulary}\par 
\end{table*}

\begin{table*}[!htbp]
\caption{\boldmath {Antibiotic susceptibility pattern of gram-positive organisms} }
\label{tw-5b910549c9ab}
\def\arraystretch{1.1}
\ignorespaces 
\centering 
\begin{tabulary}{\linewidth}{p{\dimexpr.1849\linewidth-2\tabcolsep}p{\dimexpr.1531\linewidth-2\tabcolsep}p{\dimexpr.14059999999999999\linewidth-2\tabcolsep}p{\dimexpr.1628\linewidth-2\tabcolsep}p{\dimexpr.1586\linewidth-2\tabcolsep}p{\dimexpr.20\linewidth-2\tabcolsep}}
\tbltoprule \rowcolor{kwdboxcolor}{\multirow{2}{*}{Antibiotics}} & Enterococcus faecalis & Enterococcus spps. & Staphylococcus aureus & Methicillin-resistant Staphylococcus aureus & Methicillin-resistant coagulase-negative Staphylococci\\
\rowcolor{kwdboxcolor} & n=3 (\%) & n=1(\%) & n=8 (\%) & n=5 (\%) & n=13 (\%)\\
\tblmidrule 
Benzylpenicillin &
  3 (100) &
  1 (100) &
  1 (12.5) &
  1 (20) &
  2 (15.3)\\
Gentamicin &
  2 (66.6) &
  1 (100) &
  7 (87.5) &
  3 (60) &
  8 (61.5)\\
Levofloxacin &
  1 (33.3) &
  1 (100) &
  1 (12.5) &
  2 (40) &
  5 (38.4)\\
Linezolid &
  3 (100) &
  1 (100) &
  8 (100) &
  4 (80) &
  12 (92.3)\\
Daptomycin &
  3 (100) &
  \_  &
  4 (50) &
  4 (80) &
  8 (61.5)\\
Teicoplanin &
  3 (100) &
  1 (100) &
  8 (100) &
  5 (100) &
  13 (100)\\
Vancomycin &
  3 (100) &
  \_  &
  8 (100) &
  4 (80) &
  13 (100)\\
Tetracycline &
  1 (33.3) &
  \_  &
  7 (87.5) &
  5 (100) &
  9 (69.2)\\
Tigecycline &
  3 (100) &
  1 (100) &
  8 (100) &
  5 (100) &
  12 (92.3)\\
Ciprofloxacin &
  \_  &
  1 (100) &
  1 (12.5) &
  2 (40) &
  5 (38.4)\\
Oxacillin &
  \_  &
  \_  &
  6 (75) &
  2 (40) &
  4 (30.7)\\
Erythromycin &
  \_  &
  \_  &
  5 (62.5) &
  3 (60) &
  5 (38.4)\\
Clindamycin &
  \_  &
  \_  &
  5 (62.5) &
  3 (60) &
  7 (53.8)\\
Rifampicin &
  \_  &
  \_  &
  2 (25) &
  1 (20) &
  1 (7.6)\\
Trimethoprim+ \mbox{}\protect\newline sulfamethoxazole &
  \_  &
  \_  &
  7 (87.5) &
  5 (100) &
  9 (69.2)\\
\tblbottomrule 
\end{tabulary}\par 
\end{table*}

\begin{table*}[!htbp]
\caption{\boldmath {Antibiotic susceptibility pattern of gram-negative organisms} }
\label{tw-5b983dc69481}
\def\arraystretch{1.1}
\ignorespaces 
\centering 
\begin{tabulary}{\linewidth}{p{\dimexpr.18990000000000002\linewidth-2\tabcolsep}p{\dimexpr.1138\linewidth-2\tabcolsep}p{\dimexpr.13409999999999998\linewidth-2\tabcolsep}p{\dimexpr.1222\linewidth-2\tabcolsep}p{\dimexpr.14\linewidth-2\tabcolsep}p{\dimexpr.14\linewidth-2\tabcolsep}p{\dimexpr.16\linewidth-2\tabcolsep}}
\tbltoprule \rowcolor{kwdboxcolor}{\multirow{2}{*}{Antibiotics}} & Acineto-bacter baumanni & Citro- \mbox{}\protect\newline bacter frundii & Citro- \mbox{}\protect\newline bacter koseri & Escherichia coli & Entero-bacter aerogenes & Klebsiella pneumoniae\\
\rowcolor{kwdboxcolor} & n=6 (\%) & n=4(\%) & n=3(\%) & n=17(\%) & n=3(\%) & n=21(\%)\\
\tblmidrule 
Amoxicillin+clavulanic acid &
  - &
  - &
  3 (100) &
  3 (17.64) &
  - &
  7 (33.3)\\
Amikacin &
  3 (50) &
  4 (100) &
  3 (100) &
  16 (94.1) &
  3 (100) &
  18 (85.7)\\
Minocycline &
  2 (33.3) &
  - &
  - &
  - &
  1 (33.3) &
  -\\
Tigecycline &
  4 (66.6) &
  3 (75) &
  3 (100) &
  17 (100) &
  2 (66.6) &
  13 (61.9)\\
Trimethoprim+sul famethoxazole &
  1 (16.6) &
  3 (75) &
  3 (100) &
  3 (17.64) &
  2(66.6) &
  9 (42.8)\\
Cefoperazone+s ulbactum &
  1 (16.6) &
  2 (50) &
  3 (100) &
  6 (35.2) &
  1 (33.3) &
  16 (76.1)\\
Piperacillin+tazobactum &
  - &
  3 (75) &
  3 (100) &
  5 (29.41) &
  1 (33.3) &
  14 (66.6)\\
Cefuroxime &
  - &
  - &
  3 (100) &
  3 (17.64) &
  - &
  8 (38)\\
Cefepime &
  - &
  2 (50) &
  2 (66.6) &
  3 (17.64) &
  1 (33.3) &
  11(52.3)\\
Imipenem &
  - &
  - &
  3 (100) &
  10 (58.8) &
  1(33.3) &
  16 (76.1)\\
Meropenem &
  - &
  3 (75) &
  3 (100) &
  11(64.7) &
  2 (66.6) &
  18 (85.7)\\
Gentamicin &
  - &
  4 (100) &
  3 (100) &
  11(64.7) &
  2(66.6) &
  15(71.4)\\
Ciprofloxacin &
  - &
  2(50) &
  3 (100) &
  - &
  1 (33.3) &
  9 (42.8)\\
Ceftriaxone &
  - &
  2 (50) &
  3 (100) &
  3 (17.64) &
  1 (33.3) &
  9 (42.8)\\
Ertapenem &
  - &
  2 (50) &
  3 (100) &
  9 (52.9) &
  1 (33.3) &
  16 (76.1)\\
\tblbottomrule 
\end{tabulary}\par 
\end{table*}

\begin{table*}[!htbp]
\caption{\boldmath {Antibiotic susceptibility pattern of gram-negative organisms} }
\label{tw-52ecfa327d05}
\def\arraystretch{1.1}
\ignorespaces 
\centering 
\begin{tabulary}{\linewidth}{p{\dimexpr.19349999999999998\linewidth-2\tabcolsep}p{\dimexpr.14350000000000001\linewidth-2\tabcolsep}p{\dimexpr.1162\linewidth-2\tabcolsep}p{\dimexpr.12459999999999999\linewidth-2\tabcolsep}p{\dimexpr.1471\linewidth-2\tabcolsep}p{\dimexpr.13880000000000003\linewidth-2\tabcolsep}p{\dimexpr.13629999999999999\linewidth-2\tabcolsep}}
\tbltoprule \rowcolor{kwdboxcolor}{\multirow{2}{*}{Antibiotics}} & Morganella morganii spps. & Proteus hauseri & Proteus mirabilis & Proteus penneri & Proteus vulgaris & Pseudomonas aeruginosa\\
\rowcolor{kwdboxcolor} & n=6 (\%) & n=4 (\%) & n=11 (\%) & n=2 (\%) & n=5 (\%) & n=31 (\%)\\
\tblmidrule 
Amoxicillin+ \mbox{}\protect\newline clavulanic acid &
  - &
  1 (25) &
  6 (54.5) &
  2 (100) &
  1 (20) &
  -\\
Amikacin &
  6 (100) &
  4 (100) &
  1 (90.9) &
  2 (100) &
  5 (100) &
  21 (66.7)\\
Trimethoprim+ \mbox{}\protect\newline sulfamethoxazole &
  3 (50) &
  4 (100) &
  8 (72.7) &
  2 (100) &
  5 (100) &
  -\\
Cefoperazone+ \mbox{}\protect\newline sulbactum &
  4(66.6) &
  4 (100) &
  7 (63.6) &
  2 (100) &
  5 (100) &
  19 (61.2)\\
Piperacillin+ \mbox{}\protect\newline tazobactum &
  4(66.6) &
  4(100) &
  7 (63.6) &
  2 (100) &
  5(100) &
  17 (54.8)\\
Cefuroxime &
  -  &
  -  &
  6 (54.5) &
  -  &
  -  &
  - \\
Cefepime &
  4 (66.6) &
  4 (100) &
  8 (72.7) &
  2 (100) &
  5 (100) &
  17 (54.8)\\
Imipenem &
  1 (16.6) &
  -  &
  1 (9) &
  - &
  1 (20) &
  18 (58)\\
Meropenem &
  6 (100) &
  4 (100) &
  7 (63.6) &
  2 (100) &
  5 (100) &
  18 (58)\\
Gentamicin &
  4 (66.6) &
  4 (100) &
  7 (63.6) &
  2 (100) &
  5 (100) &
  19 (61.2)\\
Ciprofloxacin &
  2 (33.3) &
  4 (100) &
  2 (18.1) &
  2 (100) &
  5 (100) &
  17 (54.8)\\
Ceftriaxone &
  3 (50) &
  4 (100) &
  9 (81.8) &
  2 (100) &
  5 (100) &
  - \\
Ertapenem &
  4 (66.6) &
  4 (100) &
  3 (27.2) &
  1 (50) &
  5 (100) &
  - \\
\tblbottomrule 
\end{tabulary}\par 
\end{table*}

\begin{table*}[!htbp]
\caption{\boldmath {Antibiotic resistance pattern of gram-positive organisms} }
\label{tw-83ab84141e4c}
\def\arraystretch{1.1}
\ignorespaces 
\centering 
\begin{tabulary}{\linewidth}{p{\dimexpr.1794\linewidth-2\tabcolsep}p{\dimexpr.1406\linewidth-2\tabcolsep}p{\dimexpr.16\linewidth-2\tabcolsep}p{\dimexpr.16\linewidth-2\tabcolsep}p{\dimexpr.16\linewidth-2\tabcolsep}p{\dimexpr.20\linewidth-2\tabcolsep}}
\tbltoprule \rowcolor{kwdboxcolor}{\multirow{2}{*}{Antibiotics}} & Enterococcus faecalis & Enterococcus spp & Staphylococcus aureus & Methicillin-resistant Staphylococcus aureus & Methicillin-resistant coagulase-negative \mbox{}\protect\newline Staphylococcus\\
\rowcolor{kwdboxcolor} & n=3 (\%) & n=1 (\%) & n=8 (\%) & n=5 (\%) & n=13 (\%)\\
\tblmidrule 
Ciprofloxacin &
  2 (66.6) &
  -  &
  7 (87.5) &
  3 (60) &
  8 (61.5)\\
Levofloxacin &
  2 (66.6) &
  -  &
  7 (87.5) &
  3 (60) &
  8 (61.5)\\
Erythromycin &
  2 (66.6) &
  -  &
  2 (25) &
  2 (40) &
  6 (46.1)\\
Tetracycline &
  2 (66.6) &
  1 (100) &
  1 (12.5) &
  -  &
  4 (30.7)\\
Gentamicin &
  1 (33.3) &
  -  &
  1 (12.5) &
  2 (40) &
  4 (30.7)\\
Benzylpenicillin &
  -  &
  -  &
  7 (87.5) &
  4 (80) &
  11 (84.6)\\
Oxacillin &
  -  &
  -  &
  2 (25) &
  3 (60) &
  8 (61.5)\\
Clindamycin &
  -  &
  -  &
  3 (37.5) &
  2 (40) &
  6 (46.1)\\
\tblbottomrule 
\end{tabulary}\par 
\end{table*}

\begin{table*}[!htbp]
\caption{\boldmath {Antibiotic resistance pattern of gram-negative organisms} }
\label{tw-634efc1d438c}
\def\arraystretch{1.1}
\ignorespaces 
\centering 
\begin{tabulary}{\linewidth}{p{\dimexpr.1922\linewidth-2\tabcolsep}p{\dimexpr.13639999999999999\linewidth-2\tabcolsep}p{\dimexpr.11389999999999999\linewidth-2\tabcolsep}p{\dimexpr.1294\linewidth-2\tabcolsep}p{\dimexpr.1388\linewidth-2\tabcolsep}p{\dimexpr.1412\linewidth-2\tabcolsep}p{\dimexpr.1481\linewidth-2\tabcolsep}}
\tbltoprule \rowcolor{kwdboxcolor}{\multirow{2}{*}{Antibiotics}} & Acineto-bacter baumanni & Citro-bacter frundii & Citro-bacter koseri & Escherichia coli & Entero-bacter aerogenes & Klebsiella pneumoniae\\
\rowcolor{kwdboxcolor} & n=6 (\%) & n=4 (\%) & n=3 (\%) & n=17 (\%) & n=3 (\%) & n=21 (\%)\\
\tblmidrule 
Amoxicillin+ \mbox{}\protect\newline clavulanic acid &
  -  &
  2 (50) &
  -  &
  10 (58.8) &
  -  &
  6 (28.5)\\
Piperacillin+ \mbox{}\protect\newline tazobactum &
  6(100) &
  1(25) &
  - &
  11 (64.7) &
  2 (66.6) &
  5 (23.8)\\
Ampicillin &
  -  &
  -  &
  1 (33.3) &
  15 (88.2) &
  -  &
  3 (14.2)\\
Cefuroxime &
  -  &
  2 (50) &
  -  &
  13 (76.4) &
  2 (66.6) &
  11 (52.3)\\
Cefuroxime axetil &
  -  &
  2 (50) &
  -  &
  13 (76.4) &
  2 (66.6) &
  10 (47.6)\\
Ceftriaxone &
  3 (50) &
  2 (50) &
  -  &
  14 (82.3) &
  -  &
  11 (52.3)\\
Ceftazidime &
  4 (66.6) &
  -  &
  -  &
  -  &
  1 (33.3) &
  1 (4.7)\\
Cefoperazone+ salbactum &
  4 (66.6) &
  1 (25) &
  -  &
  11 (64.7) &
  2 (66.6) &
  3 (14.2)\\
Cefepime &
  6 (100) &
  -  &
  -  &
  11 (64.7) &
  1 (33.3) &
  6 (28.5)\\
Doripenem &
  4(66.6) &
  -  &
  -  &
  1 (5.8) &
  1 (33.3) &
  - \\
Ertapenem &
  -  &
  1 (25) &
  -  &
  6 (35.2) &
  -  &
  4 (19)\\
Imipenem &
  6 (100) &
  2 (50) &
  -  &
  6 (35.2) &
  2 (66.6) &
  3 (14.2)\\
Meropenem &
  6 (100) &
  1 (25) &
  -  &
  6 (35.2) &
  1 (33.3) &
  2 (9.5)\\
Gentamicin &
  5 (83.5) &
  -  &
  -  &
  7 (41.1) &
  1 (33.3) &
  5 (23.8)\\
Ciprofloxacin &
  5 (83.5) &
  -  &
  -  &
  15 (88.2) &
  2 (66.6) &
  12 (57.1)\\
Levofloxacin &
  3 (50) &
  -  &
  -  &
  1 (5.8) &
  1 (33.3) &
  - \\
Cotrimoxazole &
  3 (50) &
  1 (25) &
  -  &
  14 (82.3) &
  1 (33.3) &
  10 (47.6)\\
Amikacin &
  2 (33.3) &
  -  &
  -  &
  1 (5.8) &
  -  &
  2 (9.5)\\
Minocycline &
  2 (33.3) &
  -  &
  -  &
  -  &
  -  &
  - \\
\tblbottomrule 
\end{tabulary}\par 
\end{table*}

\begin{table*}[!htbp]
\caption{\boldmath {Antibiotic resistance pattern of gram-negative organisms} }
\label{tw-77b0abc57139}
\def\arraystretch{1.1}
\ignorespaces 
\centering 
\begin{tabulary}{\linewidth}{p{\dimexpr.1522\linewidth-2\tabcolsep}p{\dimexpr.119\linewidth-2\tabcolsep}p{\dimexpr.11059999999999999\linewidth-2\tabcolsep}p{\dimexpr.1313\linewidth-2\tabcolsep}p{\dimexpr.0468\linewidth-2\tabcolsep}p{\dimexpr.13719999999999999\linewidth-2\tabcolsep}p{\dimexpr.1429\linewidth-2\tabcolsep}p{\dimexpr.16\linewidth-2\tabcolsep}}
\tbltoprule \rowcolor{kwdboxcolor}{\multirow{2}{*}{Antibiotics}} & Morganella morganii spp & Proteus hauseri & Proteus mirabilis & \multicolumn{2}{p{\dimexpr(.184\linewidth-2\tabcolsep)}}{Proteus penneri} & Proteus vulgaris & Pseudo-monas aeruginosa\\
\rowcolor{kwdboxcolor} & n=6 (\%) & n=4 (\%) & n=11 (\%) & \multicolumn{2}{p{\dimexpr(.184\linewidth-2\tabcolsep)}}{n=2 (\%)} & n=5 (\%) & n=31 (\%)\\
\tblmidrule 
Amoxicillin+ \mbox{}\protect\newline clavulanic acid &
  6 (100) &
  -  &
  4 (36.3) &
  \multicolumn{2}{p{\dimexpr(.184\linewidth-2\tabcolsep)}}{} &
  1 (20) &
  - \\
Ticarcillin+ \mbox{}\protect\newline clavulanic acid &
  -  &
  -  &
  -  &
  \multicolumn{2}{p{\dimexpr(.184\linewidth-2\tabcolsep)}}{- } &
  -  &
  15 (48.3)\\
Piperacillin+ \mbox{}\protect\newline tazobactum &
  2 (33.3) &
  -  &
  3 (27.2) &
  \multicolumn{2}{p{\dimexpr(.184\linewidth-2\tabcolsep)}}{- } &
  -  &
  9 (29)\\
Ampicillin &
  5 (83.3) &
  3 (75) &
  3 (27.2) &
  \multicolumn{2}{p{\dimexpr(.184\linewidth-2\tabcolsep)}}{2 (100)} &
  2 (40) &
  - \\
Cefuroxime &
  5 (83.3) &
  3 (75) &
  1 (9) &
  \multicolumn{2}{p{\dimexpr(.184\linewidth-2\tabcolsep)}}{2 (100)} &
  2 (40) &
  - \\
Cefuroxime axetil &
  6 (100)  &
  3 (75) &
  1 (9) &
  \multicolumn{2}{p{\dimexpr(.184\linewidth-2\tabcolsep)}}{2 (100)} &
  2 (40) &
  - \\
Ceftriaxone &
  3 (50)  &
  -  &
  2 (18.1) &
  \multicolumn{2}{p{\dimexpr(.184\linewidth-2\tabcolsep)}}{- } &
  -  &
  - \\
Ceftazidime &
  -  &
  -  &
  -  &
  \multicolumn{2}{p{\dimexpr(.184\linewidth-2\tabcolsep)}}{- } &
  -  &
  11 (35.4)\\
Cefoperazone+ salbactum &
  2 (33.3) &
  -  &
  3 (27.2) &
  \multicolumn{2}{p{\dimexpr(.184\linewidth-2\tabcolsep)}}{- } &
  -  &
  10 (32.2)\\
Cefepime &
  -  &
  -  &
  3 (27.2) &
  \multicolumn{2}{p{\dimexpr(.184\linewidth-2\tabcolsep)}}{- } &
  -  &
  9(29.0)\\
Doripenem &
  -  &
  -  &
  -  &
  \multicolumn{2}{p{\dimexpr(.184\linewidth-2\tabcolsep)}}{- } &
  -  &
  8(25.8)\\
Ertapenem &
  -  &
  -  &
  4 (36.3) &
  \multicolumn{2}{p{\dimexpr(.184\linewidth-2\tabcolsep)}}{- } &
  -  &
  - \\
Imipenem &
  4 (66.6) &
  3 (75) &
  9 (81.8) &
  \multicolumn{2}{p{\dimexpr(.184\linewidth-2\tabcolsep)}}{1 (50)} &
  1 (20) &
  11 (35.4)\\
Meropenem &
  -  &
  -  &
  4 (36.3) &
  \multicolumn{2}{p{\dimexpr(.184\linewidth-2\tabcolsep)}}{- } &
  -  &
  10 (32.2)\\
Gentamicin &
  1 (16.6) &
  -  &
  -  &
  \multicolumn{2}{p{\dimexpr(.184\linewidth-2\tabcolsep)}}{- } &
  -  &
  10 (32.2)\\
Ciprofloxacin &
  3 (50) &
  -  &
  8 (72.7) &
  \multicolumn{2}{p{\dimexpr(.184\linewidth-2\tabcolsep)}}{= } &
  -  &
  14 (45.1)\\
Levofloxacin &
  -  &
  -  &
  -  &
  \multicolumn{2}{p{\dimexpr(.184\linewidth-2\tabcolsep)}}{- } &
  -  &
  16 (51.6)\\
Trimethoprim+ sulfamethoxazole &
  3 (50) &
  -  &
  3 (27.2) &
  \multicolumn{2}{p{\dimexpr(.184\linewidth-2\tabcolsep)}}{- } &
  -  &
  - \\
Amikacin &
  -  &
  -  &
  1 (9) &
  \multicolumn{2}{p{\dimexpr(.184\linewidth-2\tabcolsep)}}{- } &
  -  &
  10 (32.3)\\
Tigecycline &
  1 (16.6) &
  3 (75) &
  4 (36.3) &
  \multicolumn{2}{p{\dimexpr(.184\linewidth-2\tabcolsep)}}{2 (100)} &
  4 (80) &
  6 (19.3)\\
Nalidixic acid &
  -  &
  -  &
  3 (27.2) &
  \multicolumn{2}{p{\dimexpr(.184\linewidth-2\tabcolsep)}}{- } &
  -  &
  - \\
Ceftazidime &
  -  &
  -  &
  -  &
  \multicolumn{2}{p{\dimexpr(.184\linewidth-2\tabcolsep)}}{- } &
  -  &
  11 (35.4)\\
\tblbottomrule 
\end{tabulary}\par 
\end{table*}
\textbf{Study design, duration, and site}

This was a prospective observational study conducted for six months (Sept 2019-Feb 2020) in the department of general surgery of Justice K.S. Hegde Charitable Hospital.

\textbf{Sample size}

The minimum required sample was 94 patients calculated based on the anticipated proportion of 6.5\%.

\textbf{Study criteria}

Patients of either gender aged above 18 years, diagnosed with diabetic foot ulcers and performed with culture and sensitivity tests in the department of general surgery were enrolled in the study. Patients with other infections were excluded from the study.

\textbf{Data collection}

A suitable data collection form was prepared. Hospitalized patients diagnosed with diabetic foot ulcers and performed with culture and sensitivity tests were enrolled in the study after obtaining the informed consent signed. The case sheets, including the treatment chart of the enrolled patients, were reviewed by the study pharmacists during their hospital stay to obtain the necessary data. The details on age, gender, domiciliary status, co-morbidities, duration of hospital stay, duration of diabetes, duration of ulcer, family history of diabetes, and type of sample withdrawn were collected. Information regarding the current drug therapy, including the prescribing pattern of antibiotics administered to the patients based on culture and sensitivity report of the sample withdrawn from the patients, was also documented. The bacterial culture reports of the sample collected, and the details of antimicrobial sensitivity and resistance patterns of the isolated organisms were obtained from laboratory investigation data of the patients. All the patients were followed up daily and checked for the culture reports and the prescribing pattern of the drug therapy provided.

\textbf{Statistical Analysis}

Frequencies with percentages were used to summarize gender, co-morbidities of the patients, duration of diabetes and ulcer, bacteria isolated from the ulcers and antibiotic susceptibility pattern of the organisms isolated. Mean, and the standard deviation was used to summarize the age and duration of hospital stay in patients. All analysis was performed using Statistical Package for the Social Sciences software (SPSS Version 20.0).
    
\section{Results}
\textbf{Gender and age-wise distribution}

Among 102 patients enrolled in the study, 72 (70.58 \%) were males, and 30 (29.41\%) were females. The mean age of the study population was found to be 58.59 years \ensuremath{\pm}10.60 standard deviation. Out of the total patients, the majority belonged to the age group of 60-69 years 36 (35.29\%), followed by 50-59 years 29 (28.43 \%). The details are summarized in Table~\ref{tw-1ef9fa43d439}.

\textbf{Distribution of patients based on the domiciliary status}

Among 102 diabetic foot ulcer patients enrolled in the study, 70 (68.6\%) were from the rural area, and 32 (31.4\%) belonged to the urban area.

\textbf{Distribution of patients based on their social habits}

Out of the 102 patients, 13 (29.54\%) had the habit of both alcohol consumption and cigarette smoking and were found to be predominant over the remaining categories.

\textbf{Distribution of patients based on co-morbidities presented}

Among 102 patients, 66 were presented with at least one co-morbid condition. Out of all the co-morbidities reported among patients, Hypertension 48 (45.28\%) was found to be the highest, followed by Ischemic heart disease 25 (23.58\%).

\textbf{Distribution of patients based on the duration of hospital stay}

The mean length of stay of patients in the hospital was found to be 14.46 days \ensuremath{\pm}7.09 standard deviation. Majority 45 (44.1\%) were admitted to the hospital for 8-14 days, followed by 28 (27.5\%) patients for 15-21 days and 13 (12.7\%) for 1-7 days. Table~\ref{tw-1088bec85428} gives a detailed description of the duration of the hospital stay of the patients.

\textbf{Distribution of patients based on family history of diabetes mellitus}

Out of 102 patients, 46 (45.1\%) were found to have a family history of diabetes mellitus.

\textbf{Distribution of patients based on the duration of diabetes}

Forty-seven (46.1 \%) were found to have a history of diabetes mellitus of more than ten years. Forty-one were having diabetes for 5-10 years, and only 14 patients had a history of less than five years.

\textbf{Distribution of patients based on the duration of the ulcer}

The majority of the patients 48 (47.1\%) were presented with ulcer of less than one-month duration, followed by patients 46(45.1\%) with a duration of 1-6  months, and only eight patients were presented with a history of ulcer of more than six months.

\textbf{Distribution of patients based on the sample collected}

Out of 102 patients, pus was collected as the sample for culture and sensitivity test among the majority of the patients 86 (84.3\%), followed by a sample of tissue 12 (11.8\%). It was found that both pus and tissue samples were collected from 4 (3.9\%) patients.

\textbf{Distribution of patients based on microbial growth observed in culture samples}

The growth of micro-organisms was observed among samples taken from 99 patients, whereas samples received from 3 patients showed no growth.

\textbf{Bacteria isolated from DFUs of the study patients}

Out of the total micro-organisms isolated, the majority of the micro-organisms were gram-negative 113 (79.03\%). The details are shown in Table~\ref{tw-d5d15ca164f8}.

\textbf{Antibiotic susceptibility and resistance pattern of isolated organisms}

Among various gram-positive organisms, Methicillin-resistant coagulase-negative Staphylococcus was isolated the most. It was found to have more sensitivity to teicoplanin (100\%) and vancomycin (100\%), whereas it showed maximum resistance to benzylpenicillin (84.6\%) followed by ciprofloxacin, levofloxacin and oxacillin with 61.5\% each. 

Among various gram-negative organisms isolated, Pseudomonas aeruginosa was observed to have high sensitivity to doripenem (70.9\%), followed by amikacin (66.7\%). 

On analyzing the resistance pattern of the same, it was most commonly found resistant to levofloxacin (51.6\%), followed by ticarcillin+clavulanic acid (48.3\%) and ciprofloxacin (45.1\%). 

Details on the sensitivity and resistance pattern of various organisms isolated are summarized in Table~\ref{tw-5b910549c9ab}, Table~\ref{tw-5b983dc69481},Table~\ref{tw-52ecfa327d05},Table~\ref{tw-83ab84141e4c},Table~\ref{tw-634efc1d438c}, and Table~\ref{tw-77b0abc57139}.
    
\section{\textbf{Discussion}}
\unskip~\citet{882223:20294950,882223:20294951,882223:20294953}  reported a higher incidence of DFU among the males as found in our study. In comparison with the female population, males are more involved in outdoor activities with improper and inadequate foot care. This could be the reason for the predominance of diabetic foot ulcers among them. 

The majority of diabetic patients with DFU enrolled in this study belonged to the age group of 60-69 years. Similar observations were also made by \unskip~\citet{882223:20294952,882223:20294954} whereas the results obtained by \unskip~\citet{882223:20294956}, were found to be contradictory in which the patients with DFU aged between 40 and 60 years were found to be greater in number. Domiciliary results were comparable to the observation made by \unskip~\citet{882223:20294956},\textit{\space } in which 76.86\% of patients were from rural and 23.14\% from urban areas. Social habits, co-morbid disease conditions and length of hospital stay were found similar to the study conducted by \unskip~\citet{882223:20294952}. This study\textit{\space } revealed that 38.2\% of patients with social habits were found to be both alcoholics and smokers, and 46 (45.1\%) patients had a family history of diabetes mellitus. In contradiction, a study conducted by \unskip~\citet{882223:20294956} presented that only 16.3 \% of the patients had a family history of DM. Majority of the patients were having a chronic history of diabetes; this can be justified by the characteristic of DFU being a chronic complication of diabetes mellitus. The duration of DFU was of less than one month among the majority of patients; this might be due to the debilitating nature of DFU in diabetic patients. 

The culture of 102 patients showed that the growth of micro-organisms was found in the samples obtained from 99 patients, while the samples collected from the remaining 3 showed no microbial growth. A comparable result was obtained from the study by \unskip~\citet{882223:20294954},\textit{\space } in which 80 samples had microbial growth out of 95 samples. In the current study, 79.03\% of the isolated micro-organisms were gram-negative bacteria, and 20.97\% were found to be gram-positive. A study conducted by \unskip~\citet{882223:20294955} \textit{\space } reported similar findings in which 61\% were gram-negative bacteria, and 38\% were gram-positive. Various studies by \unskip~\citet{882223:20294951,882223:20294946}, also observed that gram-negative species were more significant in number compared to gram-positive. In this study, it was observed that Methicillin-resistant coagulase-negative Staphylococcus 13 (8.66\%) was found to be the most common gram-positive organism isolated, followed by Staphylococcus aureus 8 (5.33\%). A study conducted by \unskip~\citet{882223:20294957} showed Methicillin-resistant Staphylococcus aureus (36.4\%) as the predominant gram-positive organism isolated, and 15.2\% of the total gram-positive organisms were found to be coagulase-negative Staphylococcus. The reports of the study conducted by \unskip~\citet{882223:20294958}, showed Staphylococcus aureus as the most frequently isolated gram-positive bacteria. Pseudomonas aeruginosa 31 (20.66\%) was found to be the most commonly isolated gram-negative organism in the present study. Similarly, a study performed by \unskip~\citet{882223:20294946}, indicated Pseudomonas aeruginosa 30 (17.69\%) as the most common organism that has been isolated. \unskip~\citet{882223:20294955} did a study that showed Proteus spps (18.27\%) as the most frequently seen gram-negative organism. 
    
\section{Conclusion}
Out of all the bacteria that have been isolated, 79.03\% were gram negative, and 20.97\% were gram-positive. Pseudomonas aeruginosa was the most frequently isolated gram-negative bacteria, whereas Methicillin-resistant coagulase-negative staphylococcus had the highest frequency among the gram-positive strains. The sensitivity and resistance pattern of the various pathogens isolated were evaluated and catalogued in the study. The present study showed the various potential pathogens associated with diabetic foot ulcers, which can cause serious health issues if therapeutic intervention is not done correctly. The findings of the present study are expected to support clinicians in the development of antibiotic treatment guidelines for diabetic foot infections. It is also mandatory that the therapy provided to the patients must be rationalized based on their socioeconomic status for better outcomes. 
\section*{Acknowledgement}We would like to offer sincere thanks to Prof. (Dr.) C.S. Shastry for his administrative support, motivation, and valuable suggestions given throughout the completion of our research work. 

\textbf{Funding Support}

The authors declare that they have no funding support for this study.

\textbf{Conflict Of Interest}

The authors declare that they have no conflict of interest for this study.


    

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