|Year : 2021 | Volume
| Issue : 1 | Page : 80-87
Prevalence and antibiotic susceptibility pattern of uropathogenic Escherichia Coli strains in sonipat region of Haryana in India
Shikha Malik, Jogender Singh Rana, Kiran Nehra
Department of Biotechnology, Deenbandhu Chhotu Ram University of Science and Technology, Sonipat, Haryana, India
|Date of Submission||16-Jan-2021|
|Date of Acceptance||20-Feb-2021|
|Date of Web Publication||13-Mar-2021|
Dr. Kiran Nehra
Department of Biotechnology, Deenbandhu Chhotu Ram University of Science and Technology, Murthal, Sonipat - 131 039, Haryana
Source of Support: None, Conflict of Interest: None
Background: To study the prevalence and antibiotic susceptibility pattern of uropathogenic Escherichia coli strains in Sonipat region of Haryana in India. Urinary tract infections (UTIs) are among the most widespread infections, caused most frequently by Escherichia coli. The past few years have witnessed a rapid rise in the spread of high antibiotic-resistant forms of these uropathogenic E. coli (UPECs). Methods: In the current study, a total of 53 UPEC isolates from patients of all age groups were collected from Sonipat and its adjoining areas from September 2017 to April 2018. All the uropathogens were subjected to antibiotic susceptibility profiling using a set of 23 antibiotics and confirmed using standard microbiological procedures. The isolates which exhibited high degree of multidrug resistance (MDR) were characterized at molecular level using 16S rRNA sequencing. Results: The evaluation of age- and gender-wise prevalence of UTI revealed that women (77.3%) were more susceptible to infection as compared to men (22.6%). It was observed that 83% of the collected UPEC isolates exhibited MDR pattern. The isolates exhibited maximum resistance to cephalosporins and fluoroquinolones; and the highest susceptibility (100%) was shown toward tigecycline, followed by 96.2% to colistin, 90.5% to amikacin, 86.7% to fosfomycin, and 84.9% to nitrofurantoin. Conclusion: The study concludes that the prevalence of MDR pathogens is high in studied region. For empirical antibiotic therapy, amikacin, fosfomycin, and nitrofurantoin should be preferred; and for MDR uropathogens, colistin, and tigecycline should be recommended.
Keywords: Escherichia coli, multi-drug resistance, predominance, urinary tract infections, uropathogenic Escherichia coli
|How to cite this article:|
Malik S, Rana JS, Nehra K. Prevalence and antibiotic susceptibility pattern of uropathogenic Escherichia Coli strains in sonipat region of Haryana in India. Biomed Biotechnol Res J 2021;5:80-7
|How to cite this URL:|
Malik S, Rana JS, Nehra K. Prevalence and antibiotic susceptibility pattern of uropathogenic Escherichia Coli strains in sonipat region of Haryana in India. Biomed Biotechnol Res J [serial online] 2021 [cited 2021 Aug 5];5:80-7. Available from: https://www.bmbtrj.org/text.asp?2021/5/1/80/311096
| Introduction|| |
Urinary tract infections (UTIs) are one of the most frequently occurring bacterial infections, wherein an abnormal bacterial growth causes inflammation of the urinary tract. In a healthy person, the urinary tract generally lacks any bacterial growth; however, in conditions when the bacteria arise from the rectal reservoir, they may give rise to UTI. The human urinary system comprises of kidneys, urinary bladder, ureters, and urethra; and bacterial multiplication and colonization in any of these parts can result into UTI. In humans, the urinary tract remains the most common site for Gram-negative bacterial infections. Approximately 150 million cases related to UTIs are reported annually. Women, as compared to men, are more susceptible to UTI and close to 50% of them encounter UTI once in their lifespan.
As per the findings reported by several workers, UTIs most frequently stem from uropathogenic Escherichia coli, which alone is responsible for 80% of the cases. Other less common UTI pathogens include Klebsiella, Pseudomonas aeruginosa, Staphylococcus saprophyticus, Proteus, Enterobacter, and Enterococci species. Various virulence factors such as adhesins, siderophores, toxins, capsular polysaccharides, and fimbrial adhesins of uropathogenic E. coli (UPECs) encourage bacterial colonization and infection of the urinary tract. UPECs, which are a type of extra-intestinal pathogenic E. coli, are among the most widespread class of extra-intestinal infections subsequent to meningitis and neonatal sepsis. The other common types of pathogenic E. coli comprise intestinal pathogenic E. coli (InPEC), which include entero-toxigenic E. coli, entero-pathogenic E. coli, enterohaemorrhagic E. coli, enteroaggregative E. coli, enteroinvasive E. coli, enteric syndromes, Crohn's disease, and hemorrhage.,
The currently available treatment measures for UTI involve the use of antibiotics as antibacterial agents; however, unrestricted and overuse of these antibiotics by clinical practitioners and patients has led to the inception and advancement of multi-drug-resistant strains in uropathogens, especially in UPEC isolates. To avoid the likelihood of any kind of kidney-related complications, timely diagnosis followed by an early initiation of antibiotic treatment is required. Hence to circumvent the onset of complicated symptoms, the physicians normally tend to recommend an antibiotic course without waiting for the antibiotic susceptibility results which generally come in 3-4 days. These prior treatments with antibiotics encourage the onset of antibiotic resistance since different people tend to be susceptible to different antibiotics. This rise in antibiotic resistance has become a major hurdle in the treatment measures and has also been found to account for an increase in cases of morbidity and mortality in case of humans. Furthermore, a rise in extended spectrum beta lactamase strains (ESBL) and biofilm formation by uropathogens has made the existing treatment measures even more complicated.
This emergence and rapid spread of multi-drug resistance among UPECs has now become a global phenomenon. According to the findings from Japan, China, US, India, Brazil, Nepal, and Saudi Arabia; the predominance of multidrug resistance (MDR) in UPEC isolates is rising at a very fast pace. Therefore, to start a proper empirical antibiotic therapy, a prior knowledge of the causal organism and its antibiotic susceptibility pattern is necessary to prevent a further rise of antibiotic resistance in uropathogens. Considering the fact that the data related to causal organism and its antibiotic susceptibility pattern changes continuously from one hospital to other and from one region to another; careful monitoring, assembly, and updating of such data is highly recommended., As an attempt in this direction, the current study focuses on determining the prevalence and phenotypes of UPEC isolates showing MDR in Sonipat and adjoining regions of Haryana state in India.
| Materials and Methods|| |
Collection of clinical bacterial isolates
A total number of 53 clinical bacterial uropathogenic isolates were collected from diagnostic laboratory of FIMS hospital, Sonipat, and Balaji Clinical Laboratory, Panipat, after a preliminary microscopic examination which indicated the isolates to be E. coli. The isolates were obtained from urine samples collected from September 2017 to April 2018. The isolates were streaked on nutrient agar, and the isolated colonies were further streaked on differential medium, namely, MacConkey agar and Eosin methylene blue agar (Himedia laboratories, India), and incubated at 37°C for 24 h to get pure isolates in the form of single colonies. After culturing the single colonies in nutrient broth, glycerol (30%) stocks were prepared and stored at −80°C.
Antibiotic susceptibility analysis
Susceptibility of the isolated uropathogens for a total of 23 antibiotics commonly used in the treatment of UTIs was determined with the help of Kirby-Bauer agar disc diffusion method. These 23 antibiotics belonged to four major antibiotic classes, namely, (i) β-lactams which included penicillins like ampicillin; cephalosporins like cefotaxime, ceftazidime, ceftriaxone, cefuroxime, cefepime and cefoperazone/sulbactam; and carbapenems like imipenem and meropenem; (ii) β-lactamase inhibitors like amoxicillin/clavulanate, ampicillin/sulbactam and piperacillin/tazobactam; (iii) Fluoroquinolones which included ciprofloxacin, levofloxacin, and ofloxacin; (iv) Aminoglycosides which consisted of amikacin, gentamycin, and netilmicin. Besides these four major classes, a few other antibiotics (nitrofurantoin, tigecycline, colistin, cotrimoxazole, and fosfomycin) which are also used for the treatment of UTI, were also included for antibiotic susceptibility analysis in the present study. The culture of each bacterial isolate was spread evenly on Mueller Hinton agar plates followed by the placement of antibiotic discs on them. After overnight incubation at 37°C, the inhibition zone was examined as per the recommendations of Clinical and Laboratory Standards Institute 2019 (CLSI). [Table 1] lists the various antibiotics along with the concentrations in which they were used in the present study.
|Table 1: Percent resistance and sensitivity profile of clinical bacterial isolates to antibiotics belonging to five major classes of antibiotics|
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After the susceptibility testing, the isolates were studied for their MDR pattern. The isolates which exhibited resistance to antibiotics belonging to three or more than three different classes were considered as multi-drug-resistant strains.
Microscopic and biochemical characterization of uropathogenic isolates
The identification of the collected UPEC isolates was preliminarily confirmed by subjecting them to microscopic and biochemical characterization studies. All the isolates were studied microscopically by Gram staining, and biochemical characterization was done using standard tests including indole test, methyl red, Voges-Proskauer, and Simmons citrate agar test.
Molecular characterization of selected multidrug-resistant uropathogenic isolates
To confirm the identity of the collected uropathogens at molecular level, a few selected bacterial isolates which exhibited high multi-drug-resistance were subjected to molecular characterization studies using 16S rRNA gene amplification and sequencing. To isolate genomic DNA, each isolate was grown overnight at 37°C in nutrient broth medium and next day, the DNA isolation was performed using genomic DNA extraction kit (Wizard® Genomic DNA Purification Kit, Promega India). To amplify the conserved region of 16S rRNA gene, universal primers 27F (forward primer) and 1492R were used, with the primer sequence and the polymerase chain reaction (PCR) working conditions as shown in [Table 2]. Using gel documentation system (BioRad, India), the gel was visualized, and the image laboratory software was used to analyze the gel image. The 16S rRNA gene product of 1500 bp was sequenced from Redcliffe Life Sciences Pvt. Ltd. Noida.
|Table 2: Details of universal primers and polymerase chain reaction working conditions used for 16SrDNA gene amplification|
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Ethical clearance was not required as the patients were neither involved directly nor their urine samples were collected directly by the authors and only the bacterial isolates were collected from the labs of both the hospitals. However, permission was sought from the university as well as from the hospital authorities prior to collection of the isolates.
| Results|| |
Prevalence pattern of uropathogenic Escherichia coli
In this retrospective study, a total number of 53 samples of probable E. coli isolates from both in-patients and out-patients suffering from UTI were collected and further processed in the laboratory. Out of the total isolates, 41 samples (77.36%) belonged to females, and 12 samples (22.64%) could be obtained from males, indicating that females were more prone to infection as compared to men [Figure 1].
|Figure 1: Age- and gender-wise distribution of urinary tract infection patients in Sonipat region|
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In case of females, the UTIs were reported highest (31.7%) in the age group of 33–42 y, which was followed by the age group of 43–52 y, wherein the infection rate was 26.8% [Figure 1]. However, in case of males, infections were more prevalent (58.3%) in the age group of 53 and above as compared to other ages [Figure 1].
Analysis of antibiotic susceptibility pattern of uropathogenic Escherichia coli
The antibiotic susceptibility tests were carried out using a set of 23 antibiotics; wherein resistance was observed to be exhibited by the collected UPECs against all the antibiotics except tigecycline [Table 1]. For 13 antibiotics, more than 50% of the UPECs were found to be resistant; whereas, sensitivity by more than 80% of the isolates could be observed only for five antibiotics [Figure 2]a and [Figure 2]b. The majority of UPECs were observed to exhibit least sensitivity toward ampicillin, ofloxacin and amoxicillin/clavulanate, showing a high resistance rate of 88.7%, 83.1%, and 81.1%, respectively, against these antibiotics.
|Figure 2: (a) Antibiotic resistant profile of isolated uropathogenic Escherichia coli. (b) Antibiotic sensitivity profile of isolated uropathogenic Escherichia coli|
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Among β-lactam group of antibiotics, a very high number of bacterial isolates (88.7%) were observed to exhibit resistance to penicillins. More than 50% of the isolates were also found to be resistant to all cephalosporins, except cefoperazone/sulbactam where the resistance rate was slightly less than 50%. However, in case of carbapenems, both imipenem and meropenem exhibited a fair amount of antimicrobial activity (with 75.4% and 62.3% sensitivity, respectively) against UPECs.
Among the β-lactamase inhibitors, UPECs showed highest resistance toward amoxicillin/clavulanate (81.1%), followed by ampicillin/sulbactam (67.9%) and piperacillin/tazobactam (26.5%). In case of fluoroquinolones as well, all the three tested antibiotics exhibited very low efficacy; with ofloxacin remaining the least effective with a resistance rate of 83.1%, followed by levofloxacin (79.3%) and ciprofloxacin (73.6%). Among aminoglycosides, isolates were most sensitive to amikacin, exhibiting resistance rate of only 9.4%, followed by netilmicin (resistance rate of 41.6%), and gentamycin (56.6% resistance).
Upon further susceptibility analysis of UPECs to five additional antibiotics not belonging to any of the above stated antibiotic class (nitrofurantoin, tigecycline, colistin, cotrimoxazole, and fosfomycin), a comparatively higher sensitivity was observed towards nitrofurantoin and fosfomycin with resistance rate of only 15.1% and 13.2%, respectively. Colistin (a type of polymyxin) and tigecycline (a type of glycylcycline) showed the maximum antibacterial activity against UPECs with a sensitivity rate of 96.2% and 100%, respectively. However, cotrimoxazole, a class of sulphonamides, exhibited 69.8% resistance rate for UPECs.
A further analysis of the results of antibiotic susceptibility assessment for the presence of MDR among the collected isolates revealed that eighty three percent of the isolates exhibited resistance to three or more than three different classes of antibiotics, thus exhibiting a higher prevalence of multi-drug-resistance in the UPEC isolates. Among the MDR UPEC isolates obtained in Sonipat region in the present study, 84% belonged to women and only 16% of the isolates belonged to men [Figure 3].
|Figure 3: Prevalence of multidrug resistance in uropathogenic Escherichia coli isolated from male and female urinary tract infection patients|
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Characterization of selected multidrug-resistant clinical bacterial isolates
All the clinical bacterial isolates were characterized microscopically and biochemically using standard biochemical tests like IMViC. The microscopic analysis using Gram-staining confirmed the presence of pink color rod shaped cells, a characteristic of Gram-negative E. coli bacterium. Similarly, biochemical results also confirmed the clinical isolates as E. coli [Table 3].
|Table 3: Microscopic and biochemical characteristics of clinical bacterial isolates collected from urinary tract infection patients in Sonipat region|
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Upon antibiotic susceptibility analysis, a few isolates which exhibited high degree of multidrug-resistance (isolates resistant to more than 10 antibiotics belonging to three or more than three classes of antibiotics) were selected for confirmatory studies using molecular characterization by 16S rRNA sequencing. The amplification of the 16SrRNA gene resulted into a PCR product of approximately 1500 bp [Figure 4], which was subjected to further sequencing. The consensus sequences generated using Bioedit software when used for studying their homology with the existing sequences in the NCBI database using BLASTn tool, confirmed the MDR clinical isolates as E. coli. The confirmed sequences were submitted in GenBank database to obtain their accession numbers [Table 4].
|Figure 4: Representative gel image of polymerase chain reaction amplified 16S rRNA sequence|
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|Table 4: Molecular identification of the collected uropathogenic Escherichia coli isolates based upon 16S rRNA sequencing|
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| Discussion|| |
The present study was focused on studying the prevalence of UTIs caused mainly by E. coli isolates, since these are the most frequent pathogens responsible for causing UTIs. Several previous studies have reported a higher occurrence of UPECs in the urinary tract as compared to other pathogens namely Klebsiella sp. Pseudomonas, Enterococci, and Proteus.,,, This may be because in Enterobacteriaceae family (especially E. coli), several factors play a key role in the attachment of bacteria to the uroepithelium; pili, fimbriae, P1-blood group phenotype receptor, and adhesins help bacteria in colonizing the urogenital mucosa of the urinary tract.
The present study was therefore conducted on UPECs, and it revealed that the prevalence of UTI is more common in women as compared to men. These findings are supported by similar studies conducted by Maji et al., Lawhale et al., and Kumar et al., wherein they have reported a higher infection rate in females as compared to males.,, Females of a particular age group (33–42y) were found to be more susceptible to this disease as compared to all other groups. This may be due to a greater involvement of this age group in sexual activity. Similar findings were also reported by Dash et al., Nalini et al., and Lawhale et al.,, Unlike females, males in the age group of 53 years and above showed more susceptibility toward this disease. Parallel results have been reported in studies conducted by various other groups.,, This prevalence in men of old age is most likely because of the enlargement of the prostate gland, use of catheters and neurogenic bladder.
The analysis of the results of antibiotic susceptibility tests carried out using a set of 23 different antibiotics revealed ampicillin, ofloxacin and amoxicillin/clavulanate as being the least effective antibiotics for the control of UPECs. A few earlier studies have also reported similar findings in case of these three antibiotics., For β-lactams such as penicillin and cephalosporin, UPECs exhibited a wide degree of resistance; however, unlike carbapenems, which exhibited comparatively higher antimicrobial activity against UPECs. These findings are in accordance with a few earlier reports of susceptibility pattern of these antibiotics.,,, However, the antimicrobial response of the antibiotics as observed in the bacterial isolates obtained from the patients in Sonipat region was less as compared to that reported in previous studies. In a previous study conducted on urban population of Meerut city in India, it was stated that carbapenems emerged as the most sensitive class of antibiotics having sensitivity rate of 84.52 and 92.26% (imipenem and meropenem, respectively); and in another study carried out by Kulkarni et al. and Lawhale et al., also, imipenem showed high sensitivity rate of 96.71% and 99.32% respectively. Hence, based upon a comparison of the results obtained in our study with these earlier findings, it can be concluded that in Sonipat region, UPEC strains are turning more resistant with time to both imipenem and meropenem, which were observed to exhibit higher sensitivity in other regions. Beside E. coli, the new species (Klebsiella oxytoca) of second most common uropathogen Klebseilla, was also found to produce carbapenemase which made the isolates resistant to both imipenem and meropenem.
In the current study, UPECs had also shown high degree of resistance to the β-lactamase inhibitors. Since the past decade, it has been observed that a substantial use of β-lactam antibiotics in healthcare is leading to higher instances of antibiotic resistance against this group of antibiotics. Therefore, more recently to counter these β-lactamases, the treatment measures have been proposed to involve pairing of a β-lactam antibiotic with β-lactamase inhibitors such as clavulanic acid, sulbactam, and tazobactam. However, due to their inappropriate use, resistance rate against these paired antibiotics is also on the rise, with amoxicillin/clavulanate being the least effective, also shown in earlier studies. Sensitivity toward the other two β-lactamase inhibitor pairs (ampicillin/sulbactam and piperacillin/tazobactam) is also decreasing. These results are in accordance with a few earlier studies conducted in the present decade, wherein the sensitivity rate for ampicillin/sulbactam was reported to be 16% and 26.08%; and for piperacillin/tazobactam, it was observed to be 89.3% by Kulkarni et al. and 80.76% by Mehrishi et al.
The effectiveness of antibiotics belonging to another class, namely, fluoroquinolones towards UPECs, was also observed to be on a decline. These observations are in accordance with findings reported in a few previous studies.,, This high rate of resistance to fluoroquinolones may be attributed to several factors such as the ubiquitous recommendations of this group of antibiotics, and their high permeability to the various body compartments.
Amikacin, a type of aminoglycoside, remained one of the most effective antibiotics in killing UPECs, unlike other antibiotics (netilmicin and gentamycin) of this class. Similar results in case of amikacin were observed in earlier studies; however, resistance rate of netilmicin and gentamycin has been found to increase in the present study as compared to previous studies.,, Amikacin, being an injectable antibiotic, remained the most effective in its class, most probably because of its restrictive use in community care settings.
As far as the last class of antibiotics is concerned, colistin and tigecycline remained the most effective antibiotic in controlling UTIs, followed by nitrofurantoin and fosfomycin. These findings are in line with the earlier studies conducted by Kumar et al., Lawhale et al., and Mehrishi et al.,, Unlike these four antibiotics, cotrimoxazole showed least sensitivity towards UPECs, also reported in earlier studies (48.5% as reported by Kulkarni et al., and 59.2% as reported by Mehrishi et al.).
The results of the current study were also compared with other similar studies reported in neighboring countries. In a study conducted in Nepal on the susceptibility pattern of uropathogens, amikacin surfaced as the most efficient antibiotic followed by gentamycin. A similar study carried out in Iran on girls below the age of five has also concluded that for E. coli, the most common uropathogen, imipenem remained the most effective antibiotic for treating UPEC infections, and cephalosporins were the least sensitive class of antibiotics. In a recent study conducted in Peshawar area of Pakistan on uropathogenic isolates, UPECs were found to be most sensitive towards carbapenems followed by amikacin.
The existing treatment measures for UTI infections include amikacin (an aminoglycoside), fosfomycin (a phosphonic acid derivative), nitrofurantoin (a nitrofuran), piperacillin/tazobactam (a penicillin and β lactamse inhibitor) and carbapenems (imipenem and meropenem). However, variations in terms of antibiotics are often seen from one region to another, and no common treatment measures are determined for patients.,, Therefore, the selection of antibiotics should be made based on patient's history, drug availability and resistance pattern in a local area. The antibiotic resistance pattern of the isolates collected from the Sonipat region in the present study indicates an increase in the development of resistance towards several antibiotics belonging to all the four major classes, including carbapenems which are commonly used in the present times for the control of UPECs. Hence, from the results of the present study, it can be suggested that only a few antibiotics such as amikacin, nitrofurantoin, fosfomycin, and piperacillin/tazobactam which are still exhibiting a considerable amount of sensitivity can be used for empirical treatment against UPECs; and tigecycline and colistin which showed very high sensitivity when used alone or in combination with other antibiotics such as carbapenems or piperacillin/tazobactam, may be recommended for MDR uropathogens in Sonipat region.
The prevalence of MDR strains in the studied region was also found to be significantly higher as compared to that reported in similar studies from other regions of India as well as from other neighboring countries.,,, The likelihood of simple UPEC isolates transforming into MDR strains over a long period of time depends on several factors namely biofilm formation in the bladder, rise of ESBL producing strains, inappropriate use of antibiotics by physicians or unqualified practitioners, and easy accessibility of antibiotics. The MDR isolates are often correlated with nosocomial infections and their outspread is associated with increased mortality, morbidity, and health-care expenses. Among other pathogens, Enterobacteriaceae family illustrates the biggest threat due to the presence of extended spectrum β lactamases. Hence, a multidisciplinary perspective is required to control the outspread of MDR pathogens at a community level. The isolates collected in the present study are also being studied for their ESBL properties and biofilm forming abilities as a part of further studies in the host lab.
| Conclusion|| |
In view of an extreme dearth of reports regarding a detailed study of UTIs and their causal organisms in Sonipat region (Haryana) India; the present study is an attempt to ascertain the predominance of UPECs-the most frequently occurring pathogen responsible for causing UTI. The study also focused upon analyzing the consequence of gender and age on the prevalence of UPECs, and the antibiotic susceptibility pattern of these pathogens in the community of Sonipat region. As per our knowledge, this is the only such study reported from this region. From the results of the study, it could be concluded that the incidences of MDR strains are comparatively higher in Sonipat and adjoining regions, wherein women were found to be more prone to UTI as compared to men. From a set of 23 antibiotics, only four antibiotics namely amikacin, fosfomycin, nitrofurantoin and piperacillin/tazobactam were found to be efficient in treating E. coli associated UTIs; and two antibiotics-colistin and tigecycline for treating MDR pathogens. Therefore, in these times of constantly increasing antimicrobial resistance; judicious use of antibiotics, in vitro susceptibility profiling, and continuous monitoring of resistance pattern in a particular region are highly recommended to avoid the emergence of MDR pathogens. The authors are currently also working on antibiotic susceptibility pattern, age and gender-wise distribution of other less common uropathogens, namely Klebsiella sp., Pseudomonas, Shigella and Enterobacter sp.
Financial support and sponsorship
The authors wish to acknowledge National Project Implementation Unit, a unit of ministry of Human Resource Development, Government of India, for the financial assistantship awarded to Ms. Shikha Malik through TEQUIP-III project at Deenbandhu Chottu Ram University of Science and Technology, Murthal, Sonipat, Haryana.
Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4]
[Table 1], [Table 2], [Table 3], [Table 4]