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Piperacillin–Tazobactam Plus Vancomycin-Associated Acute Kidney Injury: Comparison
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Please note this is a comparison between Version 2 by Dean Liu and Version 1 by Abdullah Tarik Aslan.

Numerous observational studies and meta-analyses have suggested that combination therapy consisting of piperacillin–tazobactam (TZP) and vancomycin (VAN) augments acute kidney injury (AKI) risk when compared to viable alternatives, such as cefepime–vancomycin (FEP–VAN) and meropenem–VAN.

  • piperacillin–tazobactam
  • vancomycin
  • teicoplanin

1. Introduction

Acute kidney injury (AKI) has been observed in up to a quarter of hospitalized patients and is associated with excess mortality and morbidity [1]. As a risk factor for the development of AKI in these patients, antibiotics undoubtedly play a critical role with the main offending agents, such as acyclovir, amphotericin B, aminoglycosides, colistin, and vancomycin (VAN) [2,3][2][3]. The relationship between AKI and VAN exposure has been known for a long time and was initially the result of impurities in early formulations. Owing to the technical developments in drug manufacturing, the increased nephrotoxicity risk related to early VAN formulations was eventually eliminated [4]. Nevertheless, nephrotoxicity may be augmented with several drug combinations, including piperacillin–tazobactam (TZP) plus VAN for which the incidence of AKI has been reported within a range of 5.5% to 46.0% [5]. Besides a TZP–VAN combination regimen, high VAN trough levels, concurrent exposures to other nephrotoxic medications, long duration of VAN therapy (>7 days), the severity of illness, underlying kidney dysfunction, obesity, and ICU admission are other relevant risk factors for VAN-related AKI [6]. From a pathophysiological point of view, VAN-associated AKI can be mediated by proximal tubular injury, interstitial nephritis, and cast nephropathy [7,8][7][8]. However, the mechanisms underlying the synergistic nephrotoxic interaction between TZP and VAN are still unclear.
Many retrospective cohort studies and meta-analyses have demonstrated that TZP plus VAN is associated with a higher risk of AKI than those of other VAN plus β-lactam combinations [9,10,11,12][9][10][11][12]. In a meta-analysis that included 14 observational studies, concomitant use of VAN and TZP was reported as a risk factor for increased AKI (p = 0.001). Intriguingly, a higher risk of AKI was detected only in those studies in which the ratio of patients receiving antibiotic therapy in ICUs was <50% (in adjusted analysis OR, 3.04; 95% CI, 1.49–6.22; p = 0.002) [13]. Similarly, another recent systematic review and network meta-analysis reported that the TZP–VAN combination was significantly more nephrotoxic than VAN alone or VAN in combination with meropenem (MER) or cefepime (FEP) [12].
As another parenteral glycopeptide antibiotic, teicoplanin (TEI) can well be used in place of VAN in many indications and it is widely available worldwide, including in Europe, the Middle East, and Asia-Pacific, but not in the US [14]. Previous studies comparing TEI and VAN usually indicated a safer nephrotoxicity profile with the former antibiotic [15]. In a Cochrane systematic review and meta-analysis, 24 randomized controlled trials that included 2610 patients with proven or suspected Gram-positive infections, TEI had a lower risk of nephrotoxicity than VAN (RR, 0.66; 95% CI, 0.48–0.90; I2 = 10%) and no patient required dialysis in either TEI or VAN group. Furthermore, clinical cure and microbiological eradication rates were similar to TEI and VAN (RR, 1.03; 95% CI, 0.98–1.08; I2 = 0%). However, the randomized controlled trials included in this meta-analysis were small and most of the studies had methodological problems. Therefore, the quality of the evidence regarding the risk of AKI of TEI compared to that of VAN was assessed as moderate according to the GRADE system [16].

2. Epidemiology of TZP Plus VAN-Associated AKI

For the first time in the literature, the risk of AKI related with the TZP–VAN combination regimen was reported in 2011 [17]. Since then, contemporary literature has been inundated with a deluge of observational studies comparing the AKI risk of TZP–VAN with either those of VAN alone or VAN plus other antipseudomonal β-lactam agents. The TZP plus VAN combination provides a wide spectrum of activity against methicillin-resistant Staphylococcus aureus (MRSA), Enterobacterales, Enterococcus spp., Pseudomonas aeruginosa, and anaerobes; thus, the combination is typically used as empirical therapy in patients who are at risk of infections caused by these pathogens. TZP can be substituted with other antipseudomonal β-lactams, including meropenem for the same indications. In this regard, a large number of observational studies have been published comparing the rates of AKI seen in patients receiving TZP–VAN and those treated with FEP–VAN or MER–VAN. It should be noted that these studies minimize the confounding by indication that is typical when the comparator group comprises patients receiving VAN monotherapy. The results of the studies are summarized in Table 1 [9,10,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41][9][10][18][19][20][21][22][23][24][25][26][27][28][29][30][31][32][33][34][35][36][37][38][39][40][41]. According to these studies, patients treated to the TZP–VAN combination regimen are 1.2–9.5 times more likely to develop AKI compared to those receiving FEP–VAN or MER–VAN combinations. However, these results should be cautiously evaluated due to following reasons: (I) the presence of significant heterogeneity between the comparison groups in terms of baseline characteristics of recruited patients, (II) differences in criteria used to define AKI, (III) different comparison groups (e.g., TZP–VAN vs. FEP–VAN), (IV) variations in the level of VAN exposure, (V) percentage of critically ill patients in the whole cohort, (VI) number of other nephrotoxic agents received, (VII) sample size of the studies, (VIII) statistical methodologies being used, (IX) percentage of patients with baseline kidney dysfunction within the entire cohort. In addition, although some studies performed multivariate analyses and propensity score–matched analyses, the impacts of other confounding factors not taken into account and selection bias could not be eliminated completely. Moreover, in the vast majority of the studies, since the data collections were done retrospectively and extracted in a nonblinded manner from the electronic patient records in single institutions, no causal relationships can be established. In some studies, the details of the patients’ records do not allow for evaluation of each potential risk factor for AKI, such as the Acute Physiology and Chronic Health Evaluation II (APACHE II) score, hypovolemia, hypoalbuminemia, VAN serum level, and hypotension. Moreover, the impacts of multiple generic products of antibiotics on the AKI risk should not be underestimated. Because of the retrospective nature of the studies, urine output could not be assessed for the AKI definition, which may affect the rates of AKI. Finally, in some studies, the nephrotoxic potentials of the agents were thought to be the same, but this is not true. Furthermore, the dual representation of nephrotoxic exposure does not explain the duration and dose of agents taken over the course of treatment. Therefore, this approach cannot reflect the actual exposure to other nephrotoxic agents.
Table 1. Studies comparing the rate of AKI with piperacillin–tazobactam plus vancomycin and meropenem or cefepime plus vancomycin.
Authors and Type Year Country Population Definition of AKI * ICU Residence and/or Critically Ill, % Sample Size, n Exposure to Other Nephrotoxins, % Mean or Initial VAN Trough Level (mg/dl) Treatment Duration, Days Comparison Groups Rate of AKI
Moenster RP, et al. R, SC, [18] 2014 USA Adult patients with or without renal dysfunction RIFLE Not provided 139 Yes, percentage unknown 15.8 vs. 14.5 14.7 vs. 11.3 TZP–VAN vs. FEP–VAN 29.3% vs. 13.3%;

OR, 3.45 (0.96–12.4); p: 0.05
Gomes DM, et al. R, SC, [19] 2014 USA Adult patients without renal dysfunction AKIN 34.8 vs. 53.6 224 Yes, percentage unknown 14.1 vs. 13.06 7.1 vs. 6.7 TZP–VAN vs. FEP–VAN 34.8% vs. 12.5%; OR, 3.74 (1.89–7.39); p: <0.001
Hammond DA, et al. R, SC, [20] 2016 USA Adult patients without renal dysfunction AKIN 100 122 Yes, percentage unknown 17.9 vs. 15.1 Not provided TZP–VAN vs. FEP–VAN 32.7% vs. 28.8%; p: 0.76
Al Yami MS, et al. R, MC, [21] 2017 Saudi Arabia and USA Adult patients without renal dysfunction KDIGO 17.6 vs. 17.3 183 62.9 vs. 46.6 15.7 vs. 16.9 4.3 vs. 5.4 TZP–VAN vs. MER–VAN 7.4% vs. 5.3%; p: 0.4
Rutter WC, et al. R, SC, [9] 2017 USA Adult patients with or without renal dysfunction RIFLE Not provided 4193 60.7 vs. 59.4 Percentage of >20 mg/L

30.4% vs. 27.4%		 3.0 vs. 4.0 TZP–VAN vs. FEP–VAN 21.4% vs. 12.5%; OR, 2.18 (1.64–2.94); p: < 0.001
Jeon N, et al. R, SC, [22] 2017 USA Adult patients with or without renal dysfunction KDIGO 14.09 vs. 18.75 5335 Yes, percentage unknown Percentage of >20 mg/L

2.5% vs. 1.9%		 5.0 vs. 5.0 TZP–VAN vs. FEP–VAN 19.6% vs. 16.2%; aHR, 1.25 (1.11–1.42); p: < 0.05
Navalkele B, et al. R, SC, [23] 2017 USA Adult patients without renal dysfunction RIFLE and AKIN 21 vs. 23 558 Yes, percentage unknown 17.3 vs. 17.7 Not provided TZP–VAN vs. FEP–VAN 29% vs. 11%; HR, 4.27 (2.73–6.68); p: <0.001
Peyko V, et al. P, SC, [24] 2017 USA Adult patients with or without renal dysfunction KDIGO Not provided 85 33.9 vs. 38.5 16.6 vs. 18.3 Not provided TZP–VAN vs. MER–VAN or FEP–VAN 37.3% vs. 7.7%; p: 0.005
Cannon JM, et al. R, SC, [25] 2017 USA Adult patients without renal dysfunction RIFLE 15.8 vs. 31.1 366 Yes, percentage unknown Percentage of >20 mg/L

21.9% vs. 28.4%		 Not provided TZP–VAN vs. MER–VAN 25.3% vs. 9.5%; p: 0.008
Clemmons AB, et al. R, SC, [26] 2018 Georgia Adult patients with or without renal dysfunction KDIGO Not provided 170 Not provided Percentage of >20 mg/L

42.9% vs. 31.6%		 4.0 vs. 4.0 TZP–VAN vs. FEP–VAN 68% vs. 27%; OR, 5.1 (2.5–10.5); p: < 0.001
Mullins BP, et al. P, MC, [27] 2018 USA Adult patients without renal dysfunction RIFLE 34 vs. 41 242 Yes, percentage unknown 16.3 vs. 15.2 5.4 vs. 6.4 TZP–VAN vs. MER–VAN or FEP–VAN 29.8% vs. 8.8%; OR, 6.6 (2.8–15.8), p: <0.001
Robertson AD, et al. R, SC, [28] 2018 USA Adult patients without renal dysfunction RIFLE 0 169 81.2 vs. 83.3 Percentage of >20 mg/L

21.2% vs. 19.0%		 4.6 vs. 4.7 TZP–VAN vs. MER–VAN 16.5% vs. 3.6%; OR, 6.8 (1.5–0.9); p: 0.009
Balcı C, et al. R, SC, [29] 2018 Turkey Adult patients with or without renal dysfunction AKIN Not provided 132 52.8 vs. 65.2 Not provided Not provided TZP–VAN vs. MER–VAN 41.3% vs. 10.1%; OR, 0.33 (0.21–0.77); p: <0.001
Buckley MS, et al. R, SC, [30] 2018 USA Adult patients with or without renal dysfunction RIFLE 100 333 Yes, percentage unknown 13.5 vs. 13.1 5.1 vs. 5.8 TZP–VAN vs. FEP–VAN 19.5% vs. 17.3%; OR, 0.86 (0.49–1.53); p: 0.6
Rutter WC, et al. R, SC, [10] 2018 USA Adult patients with or without renal dysfunction RIFLE Not provided 10,236 Yes, percentage unknown Not provided 5.0 vs. 5.0 TZP–VAN vs. MER–VAN 27.4% vs. 15.4 %; OR, 2.53 (1.82–3.52); p: < 0.001
Ide N, et al. R, SC, [31] 2019 Japan Adult patients with or without renal dysfunction KDIGO 0 82 Yes, percentage unknown Percentage of >15 mg/L

52.0% vs. 50.0%		 Not provided TZP–VAN vs. MER–VAN 33.3% vs. 9.1%; p: 0.015
Schreier DJ, et al. R, SC, [32] 2019 USA Adult patients with or without renal dysfunction AKIN 100 3299 Yes, percentage unknown Not provided All patients received 24-72 h combination therapy TZP–VAN vs. MER–VAN vs. FEP–VAN 1.04 (0.71–1.42); p: 0.84

1.11 (0.85–1.45); p: 0.44
Blevins AM, et al. R, SC, [33] 2019 USA Adult patients with or without renal dysfunction KDIGO 100 2492 76.0 vs. 82.7 vs. 78.0 12.0 vs. 12.0 vs. 11.6 4.0 vs. 3.0 vs. 3.0 TZP–VAN vs. MER–VAN vs. FEP–VAN 39.3% vs. 23.5% vs. 24.2%; OR, 2.16 (1.62–2.88); p: < 0.001
Kang S, et al. R, SC, [34] 2019 South Korea Adult patients with or without renal dysfunction KDIGO 100 340 Yes, percentage unknown Not provided 6.5 vs. 8.0 vs. 8.0 TZP–VAN vs. MER–VAN vs. VAN 52.7% vs. 27.7% vs. 25.7%; p: <0.001
Molina KC, et al. R, SC, [35] 2019 USA Adult patients without renal dysfunction AKIN 100 394 Yes, percentage unknown 11.2 vs. 11.0 3.3 vs. 3.7 TZP–VAN vs. FEP–VAN 28.7% vs. 21.3%; OR, 1.50 (0.88–2.57); p: 0.13
Haruki Y, et al. R, SC, [36] 2020 Japan Adult patients without renal dysfunction RIFLE 25.0 vs. 28.3 272 68.5 vs. 67.8 13.3 vs. 13.4 6.0 vs. 7.0 TZP–VAN vs. VAN-Other β-lactams 25.0% vs. 12.2%; OR, 2.40 (1.20–4.78); p: 0.01
O’ Callaghan K et al. R, SC, [37] 2020 Australia Adult patients with or without renal dysfunction AKIN 100 260 Yes, percentage unknown Not provided 4.0 vs. 5.0 TZP–VAN vs. MER–VAN or FEP–VAN RRR, 2.2 (1.0–4.9); p: 0.05
Yabes JM, et al. R, SC, [38] 2021 USA Adult patients without renal dysfunction RIFLE and AKIN 88.5 vs. 93.7 268 Yes, percentage unknown 9.4 vs. 10.9 Not provided TZP–VAN vs. VAN-Other β-lactams 13.1% vs. 9.7%; OR, 1.72 (1.02–2.76); p: 0.04
Aslan AT, et al. R, SC, [39] 2021 Turkey Adult patients with or without renal dysfunction RIFLE 32.0 vs. 34.6 154 Yes, percentage unknown Not provided 5.0 vs. 9.0 TZP–VAN vs. MER–VAN 40.0% vs. 24.0%; aOR, 2.28 (1.01–5.18); p: 0.048
Tookhi RF, et al. R, SC, [40] 2021 Saudi Arabia Adult patients without renal dysfunction KDIGO 18.2 vs. 30.9 158 49.4 vs. 51.9 Not provided Not provided TZP–VAN vs. MER–VAN 10.4% vs. 21.0%; p: 0.07
Elliott BP, et al. R, SC, [41] 2022 USA Adult patients with sepsis KDIGO 100 418 Yes, percentage unknown Not provided Not provided TZP–VAN vs. FEP–VAN 15.2% vs. 11.0%; p: 0.44
Abbreviations: R, retrospective; SC, single-center; P, prospective; MC, multi-center; AKI, acute kidney injury; n, number; ICU, intensive care unit; VAN, vancomycin; TZP, piperacillin–tazobactam; FEP, cefepime; MER, meropenem; OR, odds ratio; aOR, adjusted odds ratio; HR, hazard ration; aHR, adjusted hazard ratio; RRR, relative risk reduction. * For definitions of AKI, please see text.
Considering the absence of randomized controlled trials comparing the risk of AKI with TZP–VAN and FEP–VAN or MER–VAN, meta-analyses evaluating the same pool of observational studies may only serve to amplify bias. Nevertheless, seven meta-analyses have been reported to address the relationship between TZP–VAN and AKI [5,12,13,42,43,44,45][5][12][13][42][43][44][45]. Hammond et al. conducted a meta-analysis that included 14 observational studies and showed that TZP–VAN was significantly associated with a higher rate of AKI compared to FEP–VAN or MER–VAN in adults (the adjusted odds ratio (OR, 3.15; 95% CI, 1.72–5.76) [13]. However, it is noteworthy that substantial statistical heterogeneity was found among the studies (I2 = 78.1%). In another meta-analysis, Giuliano et al. evaluated 15 observational studies, 7 of which overlapped with the studies included in the meta-analysis by Hammond et al. [5]. The authors demonstrated considerable risk for AKI with TZP–VAN compared to vancomycin with or without another β-lactam (OR, 3.649; 95% CI, 2.157–6.174; I2 = 83.5%; p < 0.001) [5]. Furthermore, this association remained significant when the TZP–VAN combination was compared to VAN alone (OR, 3.980; 95% CI, 2.749–5.763; I2 = 31.4%; p < 0.001). In a recent meta-analysis (47 cohort studies with a total of 56,984 adult and pediatric patients), TZP–VAN was significantly associated with higher odds of AKI than vancomycin monotherapy (OR, 2.05; 95% CI, 1.17–3.46) and its concomitant use with meropenem (OR, 1.84; 95% CI, 1.02–3.10) or cefepime (OR, 1.80; 95% CI, 1.13–2.77) [12]. On the other hand, all secondary outcomes, including the severity of AKI, time to AKI, duration of kidney injury, the need for renal replacement therapy, length of hospitalization, and mortality were similar between the comparison groups. In this meta-analysis, the level of evidence was interpreted to be moderate, mainly because of the presence of inter-study heterogeneity as a consequence of the methodological differences of the included studies. The power of the outcomes was strengthened by performing a sensitivity analysis, which indicated that TZP–VAN was the most nephrotoxic combination regimen when only studies at low risk of bias were analyzed. The definition used to define AKI varies significantly between the studies. Some studies use acute kidney injury network (AKIN) and kidney disease improving global outcomes (KDIGO) criteria, which include more AKI cases with smaller serum creatinine elevations (>0.3 mg/dl) than the RIFLE (risk, injury, failure, loss of kidney function, and end-stage kidney disease) criteria, which require at least ≥50% increment in the serum creatinine level to quantify the presence of AKI. Therefore, selected AKI definition criteria seem to impact the incidence of stage 1 AKI without affecting the frequency of stage II or III AKI [46]. It is important to underline that TZP–VAN-associated AKI is generally mild in severity (stage I AKI or risk class of the RIFLE criteria). The incidence of severe AKI requiring renal replacement therapy is not significantly higher in the TZP–VAN group compared to other groups [27,39][27][39]. Similarly, studies that included ICU patients indicated that there was no incremental risk of either persistent kidney dysfunction or requirement of renal replacement therapy for patients receiving TZP–VAN over those receiving FEP–VAN or MER–VAN [12,21][12][21]. Although the TZP–VAN combination does not seem to increase the risk of severe AKI (stage II or stage III AKI or requirement of RRT) over other comparators, even stage I AKI can dramatically reduce long-term survival rates, increase morbidity, prolong hospitalizations, and ramp up healthcare-related costs [47,48][47][48]. Taken together, the TZP–VAN combination appears to be frequently associated with mild (stage 1) AKI in critically and non-critically ill patients. The clinical importance of stage I AKI should not be underestimated as it is significantly associated with adverse clinical and economic consequences.

3. Epidemiology of TZP Plus VAN-Associated AKI in ICU Patients

Although many observational studies have included ICU patients as part of the entire cohort, eight studies have investigated the risk of AKI only in ICU patients receiving TZP–VAN compared to patients receiving FEP–VAN or those receiving FEP–VAN or MER–VAN. All these studies have retrospective single-center designs with sample sizes ranging from 122 to 3299. Except for two studies (one from South Korea and the other from Australia), all were published in the USA. Among them, Blevins et al. reported that the AKI rates were 39.3% for TZP–VAN patients, 24.2% for FEP–VAN patients, and 23.5% for MER–VAN patients (p < 0.0001 for both comparisons). Similarly, the frequencies of stage II and stage III AKI were also significantly higher for TZP–VAN patients than for other patients receiving MER–VAN or FEP–VAN (15% and 6.6% for TZP–VAN patients, 5.8% and 1.8% for FEP–VAN patients, and 6.6% and 1.3% for MER–VAN patients, p < 0.0001 for both comparisons). In a multivariate analysis, utilization of TZP–VAN was found to be an independent risk factor of AKI (OR, 2.161; 95% CI, 1.62–2.88) [33]. In line with these results, Kang et al. revealed an increased risk of AKI in the TZP–VAN group in comparison with the FEP–VAN group (52.7% vs. 27.7%, p < 0.001) in 340 ICU patients [34]. In other studies (n = 6), although the incidences of AKI were higher in the TZP–VAN patients than in the comparison groups numerically, these differences were not able to attain statistical significance [20,30,32,35,37,41][20][30][32][35][37][41]. Similarly, in a meta-analysis, Hammond et al. showed that a higher risk of AKI was not observed in the TZP–VAN group when the studies with ≥50% of patients receiving antibiotic therapy in ICUs were included in the analysis alone (in adjusted analysis OR, 2.83; 95% CI, 0.74–10.85) [13]. In another meta-analysis, Luther et al. conducted a subanalysis of critically ill patients (n = 968) and the odds of AKI in the TZP–VAN group were not significantly different from those of the FEP–VAN or MER–VAN groups (odds ratio, 1.43; 95% CI, 0.83–2.47) [43]. Consistently, Bellos et al. indicated that concomitant administration of TZP and VAN had the highest probability of AKI as compared to other groups in a separate analysis of ICU patients (i.e., VAN monotherapy, FEP–VAN, and MER–VAN). However, the results did not reach statistical significance when compared with other combinations [12]. It is unclear why a statistically significant difference in AKI risk could not be obtained in ICU patients in those receiving TZP–VAN compared to other comparison groups. Nevertheless, some specific risk factors prevailingly seen in ICU patients, such as critical illness, hypotension, and exposure to vasopressors, may have precluded uresearchers to uncover the real impact of TZP–VAN exposure on the risk of AKI. More data are needed to clarify the precise pathophysiological mechanism(s) for the reasons of the non-significant association between TZP–VAN exposure and AKI compared to VAN plus FEP or MER in ICU patients.

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