Chapter 8: PPI-Associated Kidney Injury

Urine Nephrology Now: A Primer for Students in Nephrology

Andrew Bland, MD

Introduction

The relationship between proton pump inhibitor (PPI) use and kidney disease represents one of the most controversial topics in contemporary nephrology and gastroenterology. PPIs have become among the most widely prescribed medications globally since their introduction in 1989, with widespread use often for inappropriate indications or excessive duration.

Clinical Controversy

While large observational studies have consistently demonstrated associations between PPI use and both acute kidney injury (AKI) and chronic kidney disease (CKD), establishing definitive causation remains challenging due to inherent limitations in observational study design. This chapter examines the current evidence base, addresses methodological limitations, and provides evidence-based guidance for clinical practice.

Mechanism of Action and Clinical Use

By irreversibly inhibiting the H+/K+-ATPase enzyme in gastric parietal cells, PPIs effectively reduce gastric acid secretion and are highly effective in treating peptic ulcer disease, gastroesophageal reflux disease, and preventing NSAID-induced gastropathy. However, concerns regarding long-term safety have emerged, particularly regarding potential nephrotoxicity.

Acute Interstitial Nephritis: The Established Connection

Epidemiology and Clinical Significance

Acute interstitial nephritis represents an important cause of acute renal failure, accounting for approximately 5 to 15 percent of patients hospitalized for acute renal failure. In a large single-center case series of 133 patients with biopsy-proven AIN from 1993 through 2011, proton pump inhibitors accounted for 14% of drug-induced cases, representing the second most common cause after antibiotics (49%).

Drug-Induced AIN Statistics

  • Antibiotics: 49% of drug-induced cases
  • Proton Pump Inhibitors: 14% of drug-induced cases
  • NSAIDs: 11% of drug-induced cases
  • Top individual agents: Omeprazole (12%), Amoxicillin (8%), Ciprofloxacin (8%)

Pathophysiology of PPI-Induced AIN

PPI-induced acute interstitial nephritis represents an immune-mediated reaction involving the interstitium and renal tubules. Initially, tubule epithelial cells are injured, followed by a lymphocytic inflammatory infiltrate containing predominantly T cells. Renal scarring may initiate as a consequence of the spread of the infiltrate, followed by decrease in renal function.

Immunologic Mechanisms

There is strong evidence that AIN is immunologically mediated. The precise disease mechanism is unclear, but antigen-driven immunopathology is the key mechanism. The presence of helper-inducer and suppressor-cytotoxic T lymphocytes in the inflammatory infiltrate suggests that T-cell mediated hypersensitivity reactions and cytotoxic T-cell injury are involved in pathogenesis of AIN.

Clinical Presentation and Diagnostic Challenges

The clinical diagnosis of acute interstitial nephritis presents significant challenges for practicing physicians. Classic findings of fever, rash, and arthralgias may be absent in up to two thirds of patients, making clinical recognition difficult.

PPI-Induced AIN Characteristics

Patients with PPI-induced AIN were older, were less symptomatic, and had longer durations of drug exposure and longer delays in getting kidney biopsy and steroids than for antibiotic-induced or NSAID-induced AIN. This delayed recognition can negatively impact outcomes.

Clinical Evaluation and Diagnosis

Laboratory Findings and Limitations

Typical Urinalysis Findings in AIN

  • Proteinuria: Usually mild (1+ proteinuria), typically less than 1-2 grams per day
  • Leukocyte esterase: Positivity (2+)
  • White blood cell count: Elevated (>5 cells/high power field, often 13+ cells/hpf)
  • Urinary eosinophils: >6% (when present, but low sensitivity)
  • White blood cell casts: When present, highly suggestive of AIN

Diagnostic Limitations

Despite historical emphasis on urine eosinophilia as a diagnostic marker, diagnostic studies such as urine eosinophils provide suggestive evidence, but they are unable to reliably confirm or exclude the diagnosis of acute interstitial nephritis. The sensitivity and specificity of urine eosinophilia are insufficient for definitive diagnosis, with many cases of confirmed AIN lacking this finding.

Novel Diagnostic Approaches

Emerging Biomarkers

Novel biomarkers such as urine TNF-α and interleukin-9 may be able to differentiate AIN from acute tubular injury. For example, if the prebiopsy probability of AIN is 0.25:

  • Urine IL-9 below 0.41: Can rule out AIN diagnosis (posttest probability 0.07)
  • Urine IL-9 above 2.53: Can rule in AIN diagnosis (posttest probability 0.84)

Renal Biopsy Findings

Renal biopsy remains the gold standard for diagnosis, but it may not be required in mild cases or when clinical improvement is rapid after removal of an offending agent or medication.

Histologic Features

Renal biopsy revealed AIN with dense lymphocyte and eosinophilic infiltrates in the interstitium. All cases showed almost uniform renal biopsy findings of extensive lymphoplasmacytic infiltrations involving the interstitium with sparing of the glomeruli. Eosinophils were seen in only some cases, highlighting that their absence does not exclude the diagnosis.

Evidence for PPI-Associated Chronic Kidney Disease

Major Observational Studies

ARIC Study Findings

In a prospective community-based cohort of over 10,000 adults, baseline use of PPIs was independently associated with a 20–50% higher risk of incident chronic kidney disease, after adjusting for several potential confounding variables, including demographics, socioeconomic status, clinical measurements, prevalent comorbidities and concomitant use of medications.

Meta-Analysis Evidence

A comprehensive meta-analysis of 6,829,905 participants from 10 observational studies found that compared with non-PPI use, PPI use was significantly associated with an increased risk of CKD (RR 1.72, 95% CI: 1.02–2.87, p = 0.03).

FDA Adverse Event Analysis

Analysis of the US FDA Adverse Event Reporting System from 2004 to 2019 identified:

  • 3,187 PPI-associated AKI cases
  • 3,457 PPI-associated CKD cases
  • Significant signals detected: AKI (ROR = 3.95, 95% CI 3.81–4.10) and CKD (ROR = 8.80, 95% CI 8.49–9.13)
  • Median time to event: 23 days for AKI, 177 days for CKD

Brazilian ELSA Study

The ELSA-Brasil prospective study of 13,909 participants found that after adjustments, PPI users for more than six months had an increased risk of CKD compared to non-users. Compared to non-users, users of PPIs for up to six months and above six months had greater decline in kidney function over time during a mean interval of 3.9 years.

Randomized Controlled Trial Evidence: The COMPASS Study

Study Design and Methodology

The COMPASS trial was a large, international, blinded, placebo-controlled, randomized trial. From March 2013 to May 2016, 17,598 individuals from 580 centers in 33 countries were randomized to pantoprazole or placebo. All participants had chronic coronary artery disease and/or peripheral arterial disease.

Conflicting Results from Different Analyses

The COMPASS trial has produced seemingly contradictory findings depending on the specific analysis conducted:

  • Original safety analysis (2019): Pantoprazole showed a non-significant 17% higher risk of CKD than placebo (OR 1.17; 95% CI 0.94–1.15), leading many to conclude the trial was essentially negative
  • Post hoc kidney-focused analysis: Pantoprazole resulted in statistically significant greater rate of eGFR decline compared with placebo

Key Findings from Post Hoc Analysis

Statistically Significant eGFR Decline

There was a statistically significant 20% faster GFR loss with PPI use:

  • Placebo group: Annual eGFR decline of 1.41 mL/min/1.73m²
  • Pantoprazole group: Annual eGFR decline of 1.64 mL/min/1.73m²
  • Adjusted difference: 0.27 mL/min/1.73m² per year faster eGFR decline

Clinical Significance

If the effect of pantoprazole is relative, an excess loss of 0.8 ml/min per 1.73 m² per year is roughly equivalent to, but in the opposite direction of, the beneficial effect of renin-angiotensin system blockade. This represents the largest and only RCT data which provides unconfounded data on the relationship between PPI use and subsequent CKD and GFR change.

The Causation Versus Correlation Controversy

Limitations of Observational Studies

The pooled evidence from observational studies cannot provide an interpretation regarding causation. The findings are prone to selection bias, confounding bias, and exaggeration of associations.

Inherent Observational Study Biases

  • Selection bias: Participants prescribed PPIs may be at higher risk of CKD for reasons unrelated to their PPI use
  • Confounding bias: PPI users were more likely to be obese, have hypertension, and have greater burden of prescribed medications
  • Residual bias: Difficult to adjust for all confounding factors, some of which may be unknown and unmeasurable
  • Association vs. causation: Observational studies can only provide evidence for associations, not causal links

Contradictory Evidence

Studies Suggesting No Increased Risk

Despite multiple observational studies suggesting associations, several high-quality studies have found no significant increased risk:

  • Propensity score-matched study: CKD incidence was similar between PPI and H2RA groups (5.72/1000 vs. 7.57/1000 person-years; HR = 0.68; 95% CI, 0.35–1.30)
  • Electronic health record meta-analysis: No significant increased CKD risk (HR = 1.03, 95% CI: 0.87–1.23)
  • Bradford Hill criteria analysis: Comprehensive review concluded available literature fails to support association between PPI use and CKD development

Proposed Pathophysiologic Mechanisms

Chronic Interstitial Nephritis Hypothesis

AIN causes acute inflammation and tubulointerstitial damage, which in the long term lead to interstitial fibrosis and chronic interstitial nephritis. Chronic interstitial nephritis may ultimately lead to CKD and, in severe cases, to renal failure.

Repeated AKI Episodes Theory

There is a hypothesis suggesting that chronic usage of PPIs may precipitate the onset of chronic kidney disease, potentially through repeated episodes of acute kidney injury. This persistent impairment in renal function, potentially coupled with ongoing chronic interstitial nephritis, constitutes a precursor for CKD.

Alternative Mechanisms

Indoxyl Sulfate Pathway

A study found that three-week treatment with PPIs in rodents resulted in an increase in serum levels of indoxyl sulfate. The increased amounts of liver CYP2E1 protein, which promotes indoxyl sulfate production, are likely responsible for this effect. This process may help to explain the link between the use of PPIs and a higher risk of developing CKD.

Management of PPI-Induced Kidney Injury

Acute Interstitial Nephritis Management

Step 1: Immediate PPI discontinuation

Step 2: Assess severity of kidney injury and need for renal replacement therapy

Step 3: Consider corticosteroid therapy based on severity and timing

Step 4: Monitor for recovery of kidney function

Step 5: Plan long-term follow-up and alternative gastroprotection if needed

Corticosteroid Therapy

Steroid Treatment Considerations

At 6 months postbiopsy, 49% of patients with drug-induced AIN treated with steroids achieved complete recovery; 39%, partial recovery; and 12%, no recovery. Correlates of poor recovery included:

  • Longer duration of drug exposure
  • Longer delay in starting steroid therapy
  • Advanced age
  • Severity of initial kidney injury

Alternative Gastroprotection

When PPI discontinuation is necessary due to kidney injury, alternative approaches for gastroprotection should be considered based on the original indication for PPI therapy.

H2 Receptor Antagonists as Alternatives

H2 receptor antagonists may be considered as alternatives in specific clinical scenarios:

  • Mild GERD: Infrequent symptoms (two or fewer episodes per week without esophagitis)
  • PPI intolerance: Patients who cannot tolerate PPIs
  • Rapid onset needed: H2 blockers begin working within 1-3 hours vs. up to 4 days for PPIs

Limitation: PPIs are significantly more effective than H2RAs for healing esophagitis and managing severe GERD (RR 1.59, 95% CI 1.44-1.75).

Clinical Practice Recommendations

Risk Assessment and Monitoring

Until the association between PPI use and kidney disease is better clarified, it is reasonable to monitor estimated glomerular filtration rate annually in patients receiving long-term PPI therapy, based on CKD guidelines for monitoring patients taking potentially nephrotoxic medications.

Balanced Clinical Decision-Making

When real-world evidence suggests potential harm, both the precautionary principle and the Hippocratic principle support use of a careful decision-making strategy, involving both patients and providers, that encourages careful weighing and balancing of potential benefit but also the realism of potential risks.

Deprescribing Considerations

PPI Deprescribing Strategy

Once deprescribing eligibility is established, a deprescribing strategy that tapers PPI use is recommended, since abrupt PPI discontinuation could potentially result in rebound symptoms of acid hypersecretion. The majority of tapering strategies support a reduction of the PPI maintenance dose by 50% in 1- to 2-week intervals.

Patient Communication

Evidence-Based Patient Counseling

Until further randomized control trials and biological studies confirm these results, PPI therapy should not stop patients with gastroesophageal reflux disease. However, caution should be used when prescribing to patients with high-risk kidney disease. Patients should be informed about:

  • The potential but unproven association with kidney disease
  • The established benefits of PPI therapy for their condition
  • The importance of regular monitoring
  • Signs and symptoms that warrant immediate medical attention

Future Research Directions

The principal limitation of current evidence is that it predominantly incorporates observational studies, which are inherently prone to confounding bias. Future research should aim to address gaps by focusing on detailed collection and analysis of variables to enhance understanding of the relationship between PPI use and CKD risk.

Need for Additional Evidence

RCTs may not represent the most practical approach to examine serious but infrequent adverse events associated with long-term use of a medication because they require large number of enrollees to be followed up for an extended duration. However, the debate surrounding causation versus correlation will likely continue until larger, longer-term randomized controlled trials are conducted.