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Antibibiotic resistance by nosocomial infections’ causal agents

How to cite this article: Salazar-Holguín HD, Cisneros-Robledo ME. [Antibibiotic resistance by nosocomial infections’ causal agents]. Rev Med Inst Mex Seg Soc 2016 Jul-Aug;54(4):462-71.



Received: May 27th 2015

Accepted: December 10th 2015

Antibibiotic resistance by nosocomial infections’ causal agents

Héctor Daniel Salazar-Holguín,a María Elena Cisneros-Robledob

aServicio de Medicina Preventiva y Epidemiología

bLaboratorio Clínico

Hospital General Regional 1, Instituto Mexicano del Seguro Social, Chihuahua, Chihuahua, México

Communication with: Héctor Daniel Salazar-Holguín

Telephone: (614) 230 5667


Background: The antibibiotic resistance by nosocomial infections (NI) causal agents constitutes a seriously global problematic that involves the Mexican Institute of Social Security’s Regional General Hospital 1 in Chihuahua, Mexico; although with special features that required to be specified and evaluated, in order to concrete an effective therapy.

Methods: Observational, descriptive and prospective study; by means of active vigilance all along 2014 in order to detect the nosocomial infections, for epidemiologic study, culture and antibiogram to identify its causal agents and antibiotics resistance and sensitivity.

Results: Among 13527 hospital discharges, 1079 displayed NI (8 %), standed out: the related on vascular lines, of surgical site, pneumonia and urinal track; they added up two thirds of the total. We carried out culture and antibiogram about 300 of them (27.8 %); identifying 31 bacterian species, mainly seven of those (77.9 %): Escherichia coli, Staphylo-coccus aureus and epidermidis, Pseudomonas aeruginosa, Acinetobacter baumannii, Klebsiella pneumoniae and Enterobacter cloacae; showing multiresistance to 34 tested antibiotics, except in seven with low or without resistance at all: vancomycin, teicoplanin, linezolid, quinupristin-dalfopristin, piperacilin–tazobactam, amikacin and carbapenems.

Conclusion: When we contrasted those results with the recommendations in the clinical practice guides, it aroused several contradictions; so they must be taken with reserves and has to be tested in each hospital, by means of cultures and antibiograms in practically every case of nosocomial infection.

Keywords: Cross infection; Bacterial infections; Microbial drug resistance

In April 2014 the World Health Organization issued its first global report (based on data from 114 countries) about antimicrobial and especially antibiotic resistance; according to the agency, this has come to constitute a major public health threat in all regions of the world. In the case of the Americas, the main findings said: "high resistance by Escherichia coli to third-generation cephalosporins and fluoroquinolones"; and Klebsiella pneumoniae resistance to these cephalosporins, "is also high and widespread"; while "up to 90% of Staphylococcus aureus infections are resistant to methicillin, meaning that treatment with standard antibiotics does not work".1

Europe, especially in critically ill patients, has seen increased morbidity and mortality from pneumonia associated with mechanical ventilation, urinary infection associated with urethral catheterization, and bacteremia from vascular lines, whose etiology prominently features: Pseudomonas aeruginosa, E. coli, and Staphylococcus aureus and epidermidis. Multi-antibiotic-resistance was also detected in all them.2

In the United States it is estimated that at least 2 million people acquire serious infections from bacteria that are resistant to one or more of the antibiotics designed to combat them, causing at least 23,000 deaths. Resistance in hospitalized patients stands out, in particular: beta-lactams, including carbapenems with E. coli; methicillin and vancomycin with S. aureus; and multiple antimicrobials with P. aeruginosa and Acinetobacter. Therefore, these four bacteria were included among the top ten risks of serious infection in hospitals.3

In the case of Mexico, the four most common causes of nosocomial infection are considered to be: urinary tract, surgical wound, pneumonia, and bacteriemia.4

According to a clinical practice guideline (CPG), with Gram-negative (E. coli, Klebsiella, etc.) as the most prevalent flora in nosocomial urinary tract infections associated with urinary catheters, the recommended antibiotics are: fosfomycin, gentamicin, and, in more severe or recurrent cases, third-generation cephalosporins or fluoroquinolones.5

In a review of the scientific literature it was observed that early surgical wound infections (24 to 48 hours) are typically due to beta-hemolytic streptococci of groups A or B, while the later are often due to S. epidermidis, S. aureus, and E. coli.6 Surgeries with implants have a particular risk, such as orthopedic surgeries, whose main causative agents of nosocomial infection are: coagulase-negative Staphylococcus (36%) and S. aureus (25%), and other common pathogens are E. coli and P. aeruginosa (4% each). Prolonged oral treatment with linezolid-rifampin or trimethoprim-sulfamethoxazole is recommended for Gram-positive bacteria. If Gram-negative, there is no recommendation for a specific antibiotic, with cephalosporins usually used. Carbapenems are generally indicated for resistant pathogens. Methicillin-resistant S. aureus is presented with 4% frequency, against which glycopeptides and/or cephalosporins are recommended and vancomycin is contraindicated because beta-lactams are more effective.7

In cases of nosocomial pneumonia, and specifically that associated with mechanical ventilation, one CPG indicates that they be considered hospital-based microorganisms (methicillin-resistant Gram-negative bacteria or S. aureus), and therefore empirical treatment should be commensurate with the risk of infection by multidrug-resistant microorganisms. When this is low, third-generation cephalosporin (ceftriaxone) is recommended. Against multidrug-resistant Gram-negative agents such as Pseudomonas spp., combined therapy is recommended.8

Overall, the most frequent microorganisms in venous catheter-related infection are coagulase-negative Staphylococci, S. aureus, Enterobacteriaceae, and Candida spp. In the insertion site, Gram-positive (55-80%) and -negative bacteria (7-45%) outnumber yeast (0-12%). And coagulase-negative staphylococci, generally methicillin-resistant, is more frequent in cases of catheter-related bacteremia. For treatment, the empirical use of vancomycin should be considered with the possibility of this causal agent, as well as the combined use of antimicrobials against multidrug-resistant Gram-negative bacteria such as P. aeruginosa, especially in neutropenic or septic patients, until antimicrobial sensitivity is obtained in cultures and tests.9

However, such antibiotic therapy recommendations may be faulty due to resistance developed by the causative agents of nosocomial infection.

Antimicrobials, particularly antibiotics, are substances that attack certain bacterial life processes, especially those using enzymes or other structures that are absent or rare in eukaryotic cells. There are four main targets of attack: the synthesis of the cell wall, proteins and nucleic acids, metabolic pathways, and the integrity of the cytoplasmic membrane. Such processes and targets characterize and differentiate antibiotics and, simultaneously, define resistance to them.10,11

Bacteria resist antimicrobials thanks to various innate or acquired mechanisms, with four general types: changes in the target molecule, decreased uptake, inactivating enzymes, and increased elimination of drugs.12-14

Thus, against beta-lactams (penicillins, cephalosporins, carbapenems, etc.), for example, bacteria have developed lactamase, catalytic function enzymes that, by hydrolyzing the beta-lactam ring’s chemical bond, inhibit the antibiotic action: preventing the synthesis of the cell wall, causing lysis. The case of E. coli is paradigmatic in this regard, given its ability to produce the four groups of this enzyme, including extended-spectrum beta-lactamases (ESBLs),15 specifically in nosocomial infections, of which it can cause outbreaks;16 it has even been seen that this bacterial resistance continues to grow.17,18 Similar phenomena have also been observed in nosocomial infections caused by P. aeruginosa, K. pneumoniae, and E. cloacae.19

In the Hospital General Regional No. 1 of IMSS in Chihuahua, Mexico in 2013, a total of 1042 nosocomial infections were detected, mainly related to: vascular lines (25%), surgical site (24%), pneumonia (14%), and urinary tract (12%). Out of 405 cultures performed, a majority identified: E. coli (19.7%), S. aureus (12.8%), P. aeruginosa (10.3%), E. cloacae (7.9%), Acinetobacter baumannii (6.4%), K. pneumoniae (5.1%), and Enterococcus faecalis (3.7%). This time, only the resistance of E. coli, the main causative agent of nosocomial infections in the HGR No.1, was investigated, which was identified in 80 of infections (surgical, urinary, lung, vascular); it was found resistant to 19 out of 24 antimicrobials sampled: significantly to fluoroquinolones, carbapenems, monobactams, and sulfonamides; and exceptional within their group (high sensitivity): amoxicillin, cefepime, and amikacin.20

With this background and the possibility of being part of a global issue, we decided to investigate the antimicrobial resistance of the causative agents of the main nosocomial infections in this hospital during 2014, in order to define prevention and control strategies, particularly pharmacologically.


A descriptive, observational, and prospective study was chosen, based on detection of all cases of nosocomial infection in the HGR No. 1 in 2014, through active surveillance; performing the corresponding epidemiological study and, where relevant, culture and sensitivity testing. In such cases, there was a double selection: predominant infections and their main causative agents, in order to determine their resistance to the antibiotics available in this hospital (Table I).

Table I Antibacterials tested10,11
Target Family Type Drug
  1. Cell wall synthesis
Beta-Lactams A. Penicillins: Ampicillin
Broad spectrum Amoxicillin/clavulanate
Extended spectrum Piperacillin
B. Cephalosporins: Cephalexin
1st generation Cephalothin
2nd generation Cefuroxime
3rd generation Cefotaxime
4th generation Cefepime
C. Carbapenem Imipenem
D. Monobactams Aztreonam
E Glycopeptide Vancomycin
II. Protein synthesis 1. Aminoglycosides Amikacin
2. Tetracyclines Tetracycline
3. Macrolides Erythromycin
4. chloramphenicol Chloramphenicol
5. clinical Clindamycin
6. Linezolids Linezolid
7. Streptogramins Quinupristin
III. Nucleic acid synthesis Fluoroquinolones 2nd generation Ciprofloxacin
3rd generation Levofloxacin
4th generation Moxifloxacin
IV. Folic acid biosynthesis Sulfonamides Trimethoprim Trimethoprim/sulfamethoxazole

The recommendations of the Sociedad Española de Enfermedades Infecciosas y Microbiología Clínica, exposed in its in Clinical Microbiology Procedures, were adopted for the cultures and sensitivity testing of the nosocomial infections detected, in order to standardize criteria and procedures for higher sensitivity and specificity for each step in this process: sample collection, transport and storage, receiving in the laboratory, processing, appropriate culture media, inoculation, incubation, reading and interpretation of results, with special care for antimicrobial resistance and susceptibility and the reporting of results.21


A total of 1079 nosocomial infections were detected in Hospital General Regional No. 1 during 2014. Among them, four stood out for their frequency: those related to vascular lines (21%), surgical site (20.2%), pneumonia (17.3%), and urinary tract (7.5%); contributing two thirds of the total, with the remaining 34% from the rest.

In 300 cases of all the nosocomial infections (27.8%), culture and sensitivity testing was performed, identifying mostly bacteria (94.8%) and a fraction of fungi (Candida albicans and sp, 5.2%). In turn, most bacteria were Gram-negative (60.9%), among which facultative anaerobic bacilli were salient (60.5%), like E. coli, Enterobacter, and Klebsiella genera. The aerobic Gram-negative bacilli (39.5%) were from the genera Pseudomonas (68%) and Acinetobacter (32%). With respect to Gram-positive bacteria (39.1%), a large portion were cocci (98.4%), especially from the genus Staphylococcus (72.1%) and a very small portion bacillus (Corynebacterium sp, 1.6%).

A total of 31 species were identified from these bacterial genii, among which seven stood out as more common: Staphylococcus aureus (20%), Escherichia coli (19.3%), Pseudomonas aeruginosa (15.3%), Acinetobacter baumannii (7.3%), Staphylococcus epidermidis (7%), Klebsiella pneumoniae (5.3%), and Enterobacter cloacae (3.7%). These seven bacteria accounted for 77.9%, compared to all the rest (22.1%). But their importance was different depending on the site of nosocomial infection.

NI related to vascular lines

In the 227 infections related to vascular lines, a total of 194 microorganisms were isolated belonging to 28 bacterial species, with four main species standing out (42.8% of total): S. aureus (22.5%), P. aeruginosa (7.2%), S. epidermidis (7.2%), and E. coli (6.2%).

As shown in Table II, all these bacteria have developed a great overall multidrug resistance: from 55.5% (P. aeruginosa) to 67.6% (S. aureus), with significant variations in the inhibitory actions of antimicrobials. Therefore, in the case of NI of vascular lines, these bacteria are more efficient against nucleic acid synthesis inhibitors (fluoroquinolones) and cell wall inhibitors (beta-lactam), and less so against those that inhibit protein synthesis and folate.

Table II Percentages of antimicrobial resistance by mechanism of action of nosocomial infection agents
Cell wall synthesis
A. baumannii - - 88.9 -
E coli 56.2 74.3 58.1 45.3
E. cloacae - - - 74.5
K. pneumoniae - 66.8 - 60.7
P. aeruginosa 52.8 56.4 59 -
S. epidermidis 73 - - -
S. aureus 57.6 78.5 63.7
Protein synthesis
A. baumannii - - 63.4 -
E coli 50 34.6 60 42.6
E. cloacae - - - 40
K. pneumoniae - 45.3 - 38.1
P. aeruginosa 72.4 65.6 76 -
S. epidermidis 50 - - -
S. aureus 47.7 36.8 43.1 -
Nucleic acid synthesis
A. baumannii - - 100 -
E coli 75 89 50 54.3
E. cloacae - - - 82.5
K. pneumoniae - 57.9 - 71.4
P. aeruginosa 58.3 75 56.5 -
S. epidermidis 64.3 - - -
S. aureus 90.9 83.3 86.7 -
Folate synthesis
A. baumannii - - 88.9 -
E coli 75 78.3 50 56.1
E. cloacae - - - 100
K pneumoniae - 89.5 - 57.1
P aeruginosa - - - -
S. epidermidis 71.4 - - -
S. aureus 11.4 0 6.7 -
R.L.V. = related to vascular lines; S Site = surgical site; NP = nosocomial pneumonia;
UT = urinary tract

S. aureus showed the greatest overall antimicrobial resistance (67.6%); especially fluoroquinolones, which inhibit nucleic acid synthesis (90.9%), followed by beta-lactam (cell wall synthesis inhibitors), with 57.6%, and protein synthesis blockers (47.7%), with folate biosynthesis inhibitors to a lesser extent (11.4%).

Maximum resistance was observed to the following in particular: macrolides and lincosamides (erythromycin and clindamycin: 97.7%), penicillins (95.5%; 100% for ampicillin), cephalosporins (94.9%, 100% for cefoxitin), carbapenems (93.2%), and third-generation fluoroquinolones (levofloxacin: 90.9%). This was low in the case of tetracycline (25%) and minimal for linezolid and glycopeptides (4.5%), trimethoprim-sulfamethoxazole (11.4%), and quinupristin-dalfopristin (13.6%), the latter therefore being more effective in treating NI related to vascular lines.

The overall resistance of P. aeruginosa was 55.5%; especially against protein synthesis inhibitors (72.4%; chloramphenicol, 95.8%), fluoroquinolones (58.3%), and beta-lactams (52.8%). And except in two cultures with zero percent carbenicillin resistance, no low resistance was observed, because the minimum was 45.8% (amikacin) and 47.8% (aztreonam).

In cases of S. epidermidis, the overall resistance was observed in more than two thirds (65.2%); especially: beta-lactams (73%), folate biosynthesis inhibitors (71.4%), and fluoroquinolones (64.3%); and intermediate (50%) for protein synthesis inhibitors. The maximum values ​​obtained by: lincosamides (100%), penicillins, cephalosporins, and carbapenems (92.9%), and macrolides (85.7%). By contrast, the resistance was minimal against: glycopeptides (3.5%, with zero for vancomycin), linezolids, and quinupristin-dalfopristin (7.1%).

In the NI related to vascular lines, E. coli showed an overall antimicrobial resistance of 56.9%, especially against nucleic acid synthesis inhibitors (fluoroquinolones: 75%) and folate inhibitors (sulfonamides: 75%). Resistance was intermediate against protein synthesis blockers (50%) and cell wall inhibitors (56.2%). The maximum values ​​were for ampicillin (100%), cefotaxime (87.5%), piperacillin, aztreonam and cefuroxime (83.3%). Minimal resistance was shown to carbapenems (11.1%), cefepime and amikacin (16.7%).

Overall, considering the four main causative agents of NI related to vascular lines, only four antibiotics showed minimal resistance: glycopeptides (vancomycin and teicoplanin), linezolid, and quinupristin-dalfopristin.

Surgical site NI

24 causative bacterial species were isolated in the 218 surgical site NI. Of these, four caused the majority (55.3%): E. coli (26.7%), S. aureus (14.3%), P. aeruginosa (8.3%), and K. pneumoniae (6%).

As noted in Table II, the overall multidrug-resistance of all of them was considerable: 60 to 73.8%, varying according to the antimicrobials’ mechanism of action. In general, unlike the vascular line NI, in the surgical site, these bacteria were more effective in counteracting the folate synthesis inhibitors (sulfonamides), than the protein synthesis inhibitors.

With an overall antimicrobial resistance of 70.2%, E. coli was mainly able to resist nucleic acid synthesis inhibitors (89.1% to fluoroquinolones), cell wall inhibitors (81.4% to beta-lactam), and folate inhibitors (78.3 % to trimethoprim-sulfamethoxazole). Even the lowest resistance, to protein synthesis inhibitors, was almost two-thirds (60.6%). Thus, the maximal resistance was to monobactams (aztreonam 100%) and penicillin (ampicillin 97.6% and piperacillin 90.2%). And conversely the minimum resistance found was to carbapenems (9.5%) and amikacin (16.9%) and piperacillin-tazobactam (28.9%), with moderate resistance against cefepime (54.2%) and gentamicin (60.5%).

S. aureus presented a general resistance of 66.9%, especially against nucleic acid synthesis inhibitors (83.3%) and cell wall inhibitors (78.5%). It was moderate in the case of protein synthesis inhibitors (36.8%) and zero (0%) in folate inhibitors (trimethoprim-sulfamethoxazole). In particular, it absolutely resisted (100%) ampicillin, carbenicillin, cephalothin, cefoxitin, cefotaxime, ceftazidime, imipenem, and chloramphenicol. It was very high against clindamycin (95.4%), erythromycin (90%), oxacillin (89.5%), amoxicillin-clavulanate, cefuroxime, and ceftriaxone (86.4% in all three). In contrast, there was very low resistance against teicoplanin, quinupristin-dalfopristin (2.6% both), and tetracycline (10.8%). No resistance was observed against vancomycin, aminoglycosides, ciprofloxacin, and linezolid. Thus, in the case of cell wall synthesis inhibitors, beta-lactams, with resistance up to 100% or close (penicillin, cephalosporins, and carbapenems), presented extreme exceptions against glycopeptides: 0 (vancomycin) and 2.6% (teicoplanin).

P. aeruginosa had the most resistance to virtually all antimicrobials tested: 73.8% in general. 90 to 100% against: ticarcillin-clavulanate and aztreonam (91.7%) and chloramphenicol (100%). The lowest was for amikacin (41.7%), medium for piperacillin-tazobactam (58.3%), piperacillin alone and gentamicin (66.7%); and 75% against cephalosporins, carbapenems, and fluoroquinolones.

By contrast, of the four main bacteria causing surgical wound infection, K. pneumoniae showed relatively lower antimicrobial resistance: 59.6% in general. It was absolute (100%) for: ampicillin, cefotaxime, ceftazidime, and aztreonam. Very high for: sulfonamides (trimethoprim-sulfamethoxazole: 89.5%), piperacillin and tetracycline (84.2%), ticarcillin-clavulanate (78.9%), cefuroxime and ciprofloxacin (73.7%). Medium for gentamicin (57.9%) and levofloxacin (42.1%). And the lowest resistance was observed for amikacin (7.7%), piperacillin-tazobactam (10.55%), cefepime (21%), and chloramphenicol (31.6%). Only imipenem achieved zero resistance.

In short, considering the four main causative agents of surgical site NI, only six showed the lowest antimicrobial resistance: linezolid, quinupristin-dalfopristin, glycopeptides (vancomycin and teicoplanin), piperacillin-tazobactam, and amikacin.

Nosocomial pneumonia

During 2014, in the 187 cases of nosocomial pneumonia, 24 causative bacterial species were identified; four of them had the majority (50.9%): P. aeruginosa (20.9%), S. aureus (12.7%), E. coli (9.1%), and A. baumannii (8.2%).

As seen in Table II, the overall multidrug-resistance capacity of these bacteria in nosocomial pneumonia was a minimum of 54.5% (E. coli), to a maximum of 85.3% (A. baumannii); it was mainly against nucleic acid synthesis inhibitors (fluoroquinolones) and less so against folate biosynthesis inhibitors (sulfonamides).

Overall, 60.7% of antimicrobials were resisted by P. aeruginosa, primarily protein synthesis inhibitors (76%), especially chloramphenicol (95.6%) and gentamicin (69.6%). Secondly beta-lactams (59%), especially aztreonam (65.2%), carbapenems (58.7%), and amoxicillin-clavulanate (56.5%), and also fluoroquinolones (56.5%). Thus, the minimum relative resistance was observed only for: amikacin (43.5%) and piperacillin-tazobactam (47.8%).

S. aureus showed a general antimicrobial resistance of 61.3%, especially against fluoroquinolones (86.7%) and beta-lactams (63.7%); ranging from absolute (ampicillin and cefoxitin: 100%), high for cephalosporins (88.3%) and penicillins (86.7%), and zero for glycopeptides (vancomycin and teicoplanin: 0%). It was moderate for protein synthesis inhibitors (43.1%), high for clindamycin (85.7%), very low for quinupristin (6.7%), and zero for linezolid (0%). It was also very low against trimethoprim-sulfamethoxazole (6.7%).

The lowest overall antimicrobial resistance in nosocomial pneumonia corresponded to E. coli (54.5%); higher in protein synthesis inhibitors (60%) and beta-lactams (58.1%), and medium for fluoroquinolones and sulfonamides (50%). The range varied from 100% (cefotaxime, ceftazidime, and aztreonam) and 90% (tetracycline) to 0% (carbapenems and amikacin); with intermediate values ​​against piperacillin-tazobactam (10%), cefepime (30%), chloramphenicol (40%), gentamicin (50%), and ticarcillin-clavulanate (60%).

By contrast, the greatest overall antimicrobial resistance in this disease was developed by A. baumannii (85.3%), resisting fluoroquinolones, penicillins, cephalosporins, and gentamicin (100% all); very high for aztreonam, sulfonamides (88.9%), and amikacin (77.8%); less so against carbapenems (66.7%), and the lowest only to tetracycline (12.5%).

Thus, in the case of nosocomial pneumonia, considering its four main causative agents in general, only four achieved the lowest antimicrobial resistance: linezolid, quinupristin-dalfopristin, vancomycin, and teicoplanin.

Nosocomial urinary tract infections

The 80 urinary tract infections acquired in the hospital were caused by 24 bacterial species, with three having the majority (56.3%): E. coli (39.8%), E. cloacae (9.7%), and K. pneumoniae (6.8%).

As shown in Table II, the effectiveness of the overall multidrug resistance of these bacteria was 48.2% (E. coli) to 80.3% (E. cloacae); it is greater against folate synthesis inhibitors, and less against protein synthesis inhibitors.

In cases of nosocomial urinary tract infections, E. coli resistance ranged from 100% (cefotaxime, ceftazidime, and aztreonam) to 0% to carbapenems and amikacin. It was very high for tetracycline (82.9%); medium for penicillins (54.1%), fluoroquinolones (54.3%), and sulfonamides (56.1%); slightly higher for cephalothin (65.8%); low only for piperacillin-tazobactam (2.4%) and cefepime (12.2%).

Meanwhile, E. cloacae showed an overall resistance of 80.3%, which was absolute (100%) against cephalosporins, aztreonam, sulfonamides, and almost all penicillins. It was high for fluoroquinolones (82.5%) and moderate (60%) for aminoglycosides. By contrast, it did not show any resistance (0%) to carbapenems and tetracycline.

The overall resistance of K. pneumoniae was 59.5%, ranging from absolute to ampicillin, carbenicillin, cefotaxime, ceftazidime, and aztreonam, to zero against carbapenems. It was high for fluoroquinolones (71.4%), moderate for other penicillins, sulfonamides (57.1% for both), and aminoglycosides (50%), and low only to tetracycline (14.3%).

In general and considering the three main causative agents of nosocomial urinary tract infections, its resistance to carbapenems proved zero (0%); these are the only effective antibiotics against them.

Variations of antimicrobial resistance

In the analysis, it can be seen that the resistance of the selected bacteria varies, first, by the inhibition target of the antimicrobials and, secondly, by the site of nosocomial infection.

Thus, although A. baumannii has great capacity for resistance (85.35%), it is not the same in all cases. It has absolute resistance to nucleic acid synthesis inhibitors, lower against beta-lactam and folate synthesis inhibitors (both 88.9%), and relatively lower (63.45%) for protein synthesis inhibitors. Meanwhile, E. cloacae is quite effective against antimicrobials that inhibit folate synthesis; less so those that inhibit nucleic acid synthesis (82.5%) and cell walls (74.5%), and lower for protein synthesis (40%). In turn, the most moderate resistance expressed by S. epidermidis also varies: it is high faced with cell wall synthesis inhibitors (73%) and folate inhibitors (71.4%), and moderate to protein synthesis inhibitors (50%) and nucleic acid inhibitors (64.3%).

In the cases of the most important bacteria, S. aureus, E. coli, P. aeruginosa, and K. pneumoniae, resistance also varied depending on the site of NI.

S. aureus ranged in resistance according to a correlation between the site of the NI and each type of inhibition of synthesis: cell wall (beta-lactam), 57.6% (in those related to vascular lines) to 78.5% (surgical site), with intermediate values ​​in the other two inhibitory effects.

E.coli presented the following variations in resistance for each of the mechanisms of inhibition of synthesis: cell wall (beta-lactam), from 45.3% (urinary tract infections) to 74.3% (surgical site); protein, between 34.6% (surgical site) and 60% (pneumonia); nucleic acid, from 50% (pneumonia) to 89% (surgical site), and folate in a range from 50% (pneumonia) to 78.3% (surgical).

P. aeruginosa showed less variation of its resistance to inhibitors of synthesis: cell wall, from 52.8% (in NI related to vascular lines) to 59% (pneumonia); proteins, ranging from 65.6% (surgical site) to 76% (pneumonia); and nucleic acid, between 56.5% (pneumonia) and 75% (surgical site).

Finally, K. pneumoniae also had varied resistance with respect to inhibition of synthesis: cell wall, from 60.7% (urinary tract) to 66.8% (surgical site); protein, from 38.1% (urinary tract) to 45.3% (surgical site); nucleic acid, between 57.9% (surgical site) and 71.4% (urinary tract); and folates, with a range from 57.1% (urinary tract) to 89.5% (surgical).

Antimicrobial susceptibility

Consequently, the antimicrobials with high or absolute sensitivity were few; that is, with little or no resistance. And it also varied according to the site of NI. There were three bacteria with extreme multidrug resistance results: P. aeruginosa, as only one of the antibiotics achieved 0%: carbenicillin, and only in two cases of infections related to vascular lines. With that exception, the lowest resistances were for amikacin, with over 41.7% (surgical site NI) and aztreonam (47.8% in NI related to vascular lines). A. baumannii, which had low resistance only to tetracycline: 12.5%, with all other antimicrobials being above 66.7% (carbapenems). And E. cloacae that, except for 0% resistance to carbapenems and tetracycline (urinary tract NI), all others exceeded 60% (amikacin).

K. pneumoniae showed low resistance only to five antibiotics: from 0% to carbapenems (in surgical site and urinary tract IN), 7.7% for amikacin at the surgical site (and up to 42.9% in the urinary tract), 10.5% to piperacillin-tazobactam (in surgical sites, as it was 57.1% in urinary), 10.8% to tetracycline, and 21% to cefepime (surgical site NI for both).

S. aureus showed no resistance against aminoglycoside (amikacin and gentamicin: 0%) and linezolid, except in the case of vascular line NI (linezolid: 4.5%). For glycopeptides it ranged from 0% (nosocomial pneumonia) to 4.5% (vascular line); and surgical site NI: 0% to 2.6% for vancomycin and teicoplanin. Facing streptogramins (quinupristin), resistance also varied between NI sites; being minimal at the surgical site (2.6%), average for pneumonia (6.7%), and higher in vascular lines (13.6%).

E. coli had no resistance to carbapenems in nosocomial pneumonia and urinary tract NI, but not at the surgical site (9.5%), or those related to vascular lines (11.1% for imipenem and meropenem). For aminoglycosides, kanamycin-resistance varied from 0% (pneumonia and urinary tract) to 16.8% (surgical site and vascular lines). And faced with beta-lactams, only two cases showed low resistance: piperacillin-tazobactam (2.4% in urinary tract NI, 10% in pneumonia, 25% in vascular lines, and 28.9% in surgical site) and cefepime only in urinary NI (12.2%) and vascular lines (16.7%), as it was high in pneumonia (30%) and especially in surgical sites (54.2%).

Finally, S. epidermidis showed low resistance only to four antibiotics: 0% against vancomycin, 7.1% for teicoplanin, linezolid, and quinupristin. The rest exceeded 64%.

In short, only seven showed low antimicrobial resistance (and therefore high susceptibility) in the four most frequent NI in HGR No. 1, considering their seven main causative agents: glycopeptides (vancomycin and teicoplanin), linezolid and quinupristin-dalfopristin, piperacillin-tazobactam, amikacin, and carbapenems.


In cases of infections related to vascular lines, the CPG recommends the empirical use of vancomycin when the prevalence of methicillin-resistant S. aureus increases; and the use of combined antimicrobial therapy to face multidrug-resistant Gram-negative bacilli such as Pseudomonas aeruginosa, in particular when it comes to neutropenic patients with sepsis or severe illness.9 For the hospital studied, S. aureus effectively presented very low resistance to vancomycin and teicoplanin (4.5%). And against Gram-negative agents like P. aeruginosa, there is only carbenicillin, with low resistance; or for E. coli, carbapenems, amikacin, and cefepime.

Regarding surgical site infections, when facing Gram-positive bacteria, prolonged oral treatment with linezolid-rifampin or trimethoprim-sulfamethoxazole is recommended. And if Gram-negative, there is no recommendation for a specific antibiotic, with cephalosporins usually used. Carbapenems are generally indicated for resistant pathogens. Methicillin-resistant S. aureus is presented with 4% frequency, against which glycopeptides and/or cephalosporins are recommended and vancomycin is contraindicated because beta-lactams are more effective.7 Contrasting such recommendations with what was found at HGR No. 1, effectively, linezolid showed zero resistance (even without combining it with rifampicin) from S. aureus; same for trimethoprim-sulfamethoxazole. As for cephalosporins, the response was primarily of resistance: from 100% (with S. aureus and K. pneumoniae) to cefoxitin, cefotaxime, and ceftazidime; up to 54.2% to cefepime with E. coli; with the only exception of 21% with K. pneumoniae to this antibiotic. Faced with carbapenems, while E. coli showed low resistance (9.5%), S. aureus achieved very high resistance: 100% against imipenem and 85% against meropenem. On the contrary, this bacterium was 0% resistant to vancomycin. 

Suspecting multidrug-resistant microorganisms in the etiology of pneumonia associated with mechanical ventilation, such as P. aeruginosa and Acinetobacter sp, the CPG recommends anti-Pseudomonas cephalosporin (ceftazidime or cefepime), or a carbapenem or a beta-lactam with beta-lactamase inhibitor (piperacillin-tazobactam), plus a fluoroquinolone (ciprofloxacin or levofloxacin) or an aminoglycoside (amikacin, gentamicin, or tobramycin), evaluating better coverage against methicillin-resistant S. aureus.8 But in the case of the hospital studied, P. aeruginosa showed a 56.5% resistance to cefepime and fluoroquinolones, 60% to carbapenem, and 65.2% to ceftazidime; it is only relatively lower against amikacin (43.5%) and piperacillin-tazobactam (47.8%). And in the case of S. aureus, it presented 0% resistance to other antimicrobials (glycopeptides and linezolid). A. baumannii had absolute defense (100%) against piperacillin-tazobactam, cephalosporins, and fluoroquinolones; 77.8% for amikacin and 66.7% carbapenem; observing minimal resistance only to tetracycline (12.5%). Therefore and considering the possibility of infection with E. coli, the relative indication for empirical treatment of VAP would be a carbapenem (meropenem) plus a fluoroquinolone (levofloxacin).

The CPG recommends in cases of uncomplicated lower urinary tract infection, the use of trimethoprim-sulfamethoxazole, ampicillin, and/or second-generation cephalosporins, fluoroquinolones; with mild symptoms: levofloxacin; and when E. coli presents resistance, it only recommends the use of fluoroquinolones. Alternatives for persistent or severe cases are: amoxicillin-clavulanate, amikacin, ceftazidime, ceftriaxone, and carbapenem.5 But in this hospital E. coli showed low resistance only to: carbapenems and amikacin (0%), piperacillin-tazobactam (2.4%), and cefepime (12.2%). And resistance against the other recommended antibiotics ranged from 53.7 to 100%.


As in most of Mexico, in HGR No. 1 IMSS in Chihuahua during 2014 the four most common causes of nosocomial infections were urinary tract, surgical wound, pneumonia, and bacteremia.4 As regards their main causative agents, this hospital has become a case observed globally, as for its corresponding antimicrobial resistance.

And as for its therapy, contrasting the results obtained to the antibiotic therapy recommendations indicated by the clinical practice guidelines, we see great contradictions, so these should be taken with reserve and, above all, must be tested at each hospital, by culture and sensitivity testing in virtually all cases of nosocomial infection.

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Conflict of Interest Statement: The authors declared that there is no personal or institutional conflict of interest of a professional, financial, or commercial nature, during the planning, execution, writing of this article.

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