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Saudi Journal of Kidney Diseases and Transplantation
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Year : 2011  |  Volume : 22  |  Issue : 1  |  Page : 83-89
High mortality in critically ill patients infected with 2009 pandemic influenza A (H1N1) with pneumonia and acute kidney injury

1 Department of Nephrology and Clinical Transplantation, Smt Gulabben Rasiklal Doshi and Smt Kamlaben Mafatlal Mehta Institute of Kidney Diseases & Research Centre, Dr. H. L. Trivedi Institute of Transplantation Sciences (IKDRC-ITS), Civil Hospital Campus, Asarwa, Ahmedabad, Gujarat, India
2 Department of Pathology, Laboratory Medicine, Transfusion Services and Immunohematology, Smt Gulabben Rasiklal Doshi and Smt Kamlaben Mafatlal Mehta Institute of Kidney Diseases & Research Centre, Dr. H. L. Trivedi Institute of Transplantation Sciences (IKDRC-ITS), Civil Hospital Campus, Asarwa, Ahmedabad, Gujarat, India
3 Department of Anasthesia and Critical Care Medicine, Smt Gulabben Rasiklal Doshi and Smt Kamlaben Mafatlal Mehta Institute of Kidney Diseases & Research Centre, Dr. H. L. Trivedi Institute of Transplantation Sciences (IKDRC-ITS), Civil Hospital Campus, Asarwa, Ahmedabad, Gujarat, India

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Date of Web Publication30-Dec-2010


Patients infected with H1N1 virus may develop pneumonia and acute kidney injury (AKI). To determine the epidemiological characteristics, clinical features, management and out­comes of patients with confirmed H1N1 complicated by pneumonia and AKI and treatment with oseltamivir and to identify the prognostic indicators, we studied all the patients with a confirmed diagnosis of H1N1 infection with pneumonia and AKI, using real-time reverse transcriptase­polymerase chain reaction (RT-PCR) assay, between October 2009 and March 2010. H1N1 infection was confirmed in 20 patients with pneumonia and AKI; the mean age was 42.8 ± 18.2 years and 12 (60%) of the patients were males. Eleven patients were between 15 and 50 years of age, and 15 had preexisting medical conditions. All patients had fever, cough, dyspnea or respiratory distress, increased serum lactate dehydrogenase levels, pneumonia and AKI. Fifteen (75%) patients required mechanical ventilation and 14 (70%) died. None of the health care workers developed influenza-like illness, when they received oseltamivir prophylaxis. Mortality was associated with higher Acute Physiology and Chronic Health Evaluation (APACHE) II, Sequential Organ Failure Assessment score (SOFA), Multiple Organ Dysfunction Score (MODS), XRChest score, in addition to requirement of inotrope, ventilator support, renal replacement therapy (RRT), and presence of underlying risk factor for severe disease.

How to cite this article:
Kute V B, Godara S M, Goplani K R, Gumber M R, Shah P R, Vanikar A V, Shah V R, Trivedi H L. High mortality in critically ill patients infected with 2009 pandemic influenza A (H1N1) with pneumonia and acute kidney injury. Saudi J Kidney Dis Transpl 2011;22:83-9

How to cite this URL:
Kute V B, Godara S M, Goplani K R, Gumber M R, Shah P R, Vanikar A V, Shah V R, Trivedi H L. High mortality in critically ill patients infected with 2009 pandemic influenza A (H1N1) with pneumonia and acute kidney injury. Saudi J Kidney Dis Transpl [serial online] 2011 [cited 2021 May 9];22:83-9. Available from: https://www.sjkdt.org/text.asp?2011/22/1/83/74362

   Introduction Top

As of 21 March 2010, worldwide, more than 213 countries and overseas territories had re­ported laboratory confirmed cases of pandemic influenza H1N1 2009, including over 16,931 deaths. [1] World Health Organization (WHO) declared pandemic of H1N1 on 11 June 2009. [1] Originating in Mexico in April 2009, influenza A/H1N1 2009 virus has since then spread to many countries worldwide. [2] In India, the first case was reported on 16 May 2009 in Hyde­rabad. As of 31 March 2010, samples from 132,019 persons had been tested for influenza A H1N1 in government laboratories and a few private laboratories across the country in India, and 30,197 (22.87%) of them were found po­sitive. [2] Death of lab confirmed cases cumulative were 1453 (4.9%). [2]

Currently, little information exists about the impact of kidney injury and resource utiliza­tion in the form of dialysis support in critically ill patients with pandemic H1N1 infections. [3],[4] Patients admitted to the intensive care units (ICUs) with acute kidney injury (AKI) are at increased risk of mortality, prolonged ICU and hospital stay, and the development of chronic kidney disease. [5],[6],[7],[8] During the severe adult res­piratory syndrome corona virus outbreak, kid­ney injury and the need for dialysis were un­common; however, whether this holds true for pandemic H1N1 infection is unknown. [9],[10]

Genomic analysis of this new 2009 virus in­dicated it to be a reassorted virus containing genes from influenza A virus strains endemic in (mainly Eurasian) swine, avian species and humans. [11] The transmissibility of the strain is substantially higher than that seen in seasonal influenza strains. [12] An unknown proportion of patients with 2009 influenza A (H1N1) infec­tion developed acute respiratory failure. [12] A recent epidemiological study from the USA found that 40% of all hospitalized patients on admission had findings consistent with pneu­monia on chest radiography. [13] Pregnancy, obe­sity and diabetes have been identified as potential risk factors for severe disease. [12],[13],[14]

The aim of our study was to determine the epidemiological characteristics, clinical features, management and outcomes of patients with confirmed H1N1 complicated by pneumonia and AKI and treatment with oseltamivir and to identify the prognostic indicators.

   Patients and Methods Top

The study population included 20 patients ad­mitted to hospital and revealed a laboratory?confirmed H1N1 infection, pneumonia and AKI, from 1 October 2009 to 23 March 2010. The patients complained of fever, flu-like symp­toms and had influenza H1N1 virus subtype­specific RNA detected in a nasopharyngeal swab using reverse transcriptase-polymerase chain reaction (RT-PCR). We retrospectively obtained the clinical data of the confirmed cases from the original case files and reviewed the medical charts and radiological and labo­ratory findings.

Severity of illness was assessed using the Acute Physiology and Chronic Health Evalua­tion (APACHE) II, Sequential Organ Failure Assessment (SOFA) score, Multiple Organ Dys?function Score (MODS), [15],[16] and the PaO 2 /FIO 2 (partial pressure of arterial O2 to the fraction of inspired O2 on high flow oxygen mask), which was calculated on admission. We adapted a scoring system described by Opravil et al [17] to grade the severity of pulmonary infiltrates (XRChest score), i.e., each lung was divided into four equal quadrants and each quadrant was scored on a scale of 0-3 (0: normal; 1: subtle increased interstitial markings; 2: pro­minent interstitial opacities; 3: confluent inters­titial and acinar opacities), giving a maximum score of 24 for both lungs.

Co-morbidities were recorded as the presence of one or more of the following chronic me­dical conditions: hypertension (HT), diabetes mellitus (DM), ischemic heart disease (IHD), steroid and immunosuppressive drugs, chronic lung disease [chronic obstructive pulmonary disease (COPD)/asthma], chronic kidney disease (CKD), dyslipidemia, pregnancy, and obesity. [12]?[13],[14]

The measured outcomes included mortality in hospital after the onset of critical illness, AKI or need for dialysis therapy, frequency and duration of mechanical ventilation, and dura­tion of hospital stay.

Nasopharyngeal-swab specimens were col­lected from all the patients on admission. Spe­cimens were placed in transport medium and kept at a temperature from 2 to 4°C and in­fluenza A (H1N1) infection was confirmed by means of RT-PCR in accordance with Centers for Disease Control (CDC) guidelines. [18] In addition, respiratory specimens from all patients were tested for pathogenic bacteria and/viruses on admission.

   Statistical Analysis Top

Data entry and statistical analysis were per­formed using the SPSS 12.0 software. The con­tinuous variables were presented as mean ± standard deviation (SD) or median and assessed by analysis of Mann-Whitney U-test to iden­tify the differences between groups, with sta­tistical significance set at P < 0.05.

   Results Top

Characteristics of the study patients are shown in [Table 1]. Comparison of patients who survived and died is shown in [Table 2]. The mean age of the 20 patients was 42.8 ± 18.2 years (range 4- 75 years); 12 (60%) were males, 11 out of 20 patients were between 15 and 50 years of age, and only 8 patients were 50 years old or older. Fifteen (75%) patients had preexisting medical conditions, most common of which were car­diac disease and diabetes. All the patients had PaO2/FIO2 ratios below 300 at the time of their admission (mean 177.7 ± 61) and in 13 cases this value was ≤ 200. The time between onset of symptoms and admission to the hos­pital ranged from 2 to 7 days (median 6 days).
Table 1: Characteristics of the 20 study patients with confirmed H1N1 pneumonia and acute kidney injury (AKI).

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Table 2: Comparison of patients who survived and died.

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All the patients had fever, with temperature higher than 38°C, cough and dyspnea or res­piratory distress. Fourteen patients (70%) had muscle and joint pain. The mean APACHE II score was 25.4 ± 10 (range 6-41), and the mean SOFA score was 9.55 ± 4 (range 4-15); the mean MODS was 9 ± 4 (range 3-14).

At the time of admission, 11 tested patients had elevated lactate dehydrogenase levels; five pa­tients exceeded the level of 1000 IU/L (range 205-1980 IU/L). Four of all 20 patients had in­creased creatine kinase levels (range 19-378). Five of all 20 patients (25%) had lymphopenia (<1000 lymphocytes/mm 3 ). The mean leuko­cyte count was normal at admission but six patients had more than 10,000 leukocytes/mm 3 and six patients had mild thrombocytopenia (platelet count 1.2 to 1.5 × 10 3 /μL) at admission. The mean leukocyte count at 5-7 days was 16,274 ± 6946 (median 16,500). All the pa­tients had elevated creatinine levels (1.6-10 mg/dL) with a mean of 4.4 ± 2.3 mg%. Six patients had elevated serum bilirubin (range 1.5-3.5 mg/dL), aspartate aminotransferase (60- 95 U/L), and alanine aminotransferase (48- 158 U/L).

The bacterial cultures of blood/sputum spe­cimens obtained within 24 hours after admi­ssion were negative in all the patients. No pa­tient had evidence of a secondary pathogen on admission, but nosocomial infections (>48 hours after admission) were diagnosed in 6 (30%) patients. The most common secondary isolates were Staphylococcus aureus, Streptococcus pneumonia (n = 1), Kleibsella pneumoniae (n = 1),  Acinetobacter baumannii Scientific Name Search 1), Pseu­domonas aeruginosa (n = 1),  Escherichia More Details coli (n = 1) and Candida albicans (n = 2).

All the patients had radiologically confirmed pneumonia with unilateral/bilateral opacities. In 15 out of 20 patients, the findings on chest radiographs were consistent with an acute res­piratory distress syndrome that required me­chanical ventilation.

None of the patients had history either of vac­cination with seasonal influenza, H1N1 or pneu­mococcal vaccine within the last year or use of antivirals (oseltamivir, zanamivir, amantadine or rimantadine) as prophylaxis, 14 days before the onset of illness. None of the patients had received oseltamivir treatment before admi­ssion. Initially, eight patients received a single­dose (SD) of oseltamivir (75 mg twice daily for 5-10 days) therapy, but the rest received a double-dose (DD) (150 mg twice daily for 5- 10 days). The patients experienced transient nausea and vomiting. Then, all the patients received amantidine 100 mg, two to three times daily for 5-10 days. Five (25%) patients received corticosteroids (intravenous hydrocortisone 50 mg six hourly or methylprednisolone at a dose of 125-500 mg/day), the indications included septic shock, COPD, post-renal transplant, and phemphigus vulgaris. Broad-spectrum antibac­terial agents (dose adjusted according to renal function and clinical course) were initiated in almost all patients because of the initial sus­picion of community-acquired bacterial pneu­monias. However, super-imposed bacterial lung infection was documented later in the course of illness. The commonly used antibiotics were ceftriaxone (n = 4), piperacilin-tazobactum (n = 12) and imipenem-cilastatin (n = 4).

All the patients developed AKI after a mean time of 3.3 days of admission (median 2 days). Only four patients had history of renal disease (CKD) before admission to the hospital and developed AKI due to H1N1, leading to re­quirement of renal replacement therapy (RRT). The 6 patients who survived recovered from AKI and 3 (50%) of them required RRT. AKI worsened in all patients who died and 9 (65%) of them required RRT. Thus, 12 out of 20 (60%) patients required RRT for AKI. Relative risk of requirement of RRT for mortality was 1.2 (confidence interval- 0.5- 3). HT (n=8), DM (n-5), IHD (n-4), steroid and immunosuppre­ssive drugs (n-4), chronic lung disease (COPD/ asthma) (n-3), CKD (n-4), obesity (n-3), tuber­culosis (n-2) and pregnancy (n-1), were the co­morbid conditions associated with AKI.

Respiratory distress requiring intubation and mechanical ventilation developed in 9 (45%) patients within the first 48 hours after admi­ssion. These patients had a median oxygen sa­turation of 77% (range 74-81%) in the ab­sence of supplementary oxygen and PaO2 63 ± 19 on high flow oxygen mask; six additional patients required mechanical ventilation during their stay in the hospital. Therefore, a total of 15 (75%) patients required mechanical ventila­tion. Only one patient survived out of these 15 patients. Duration of mechanical ventilation was 5 days in patients who survived and from 2-16 (mean 5 ± 4.6) days in patients who died. Dopamine and nor-epinephrine infusion was begun in 16 of 20 patients (80%) during the period of hospitalization.

Of the 20 patients, 14 (70%) died; death oc­curred within 12-26 days (median 17) after the onset of illness, 5-19 days (median 11) after admission. The most common primary cause of death was acute respiratory distress syn­drome (ARDS)\multi-organ dysfunction syn­drome. The age of the non-survivors was 20- 75 years and all the clinical scores were higher in the group of patients who died, indicating more severe abnormalities in them than among those who survived.

   Discussion Top

Our analysis of critically ill patients with H1N1 reveals that this disease affected middle­aged patients, most of them with underlying chronic medical conditions. The patients ful­filled the criteria of acute lung injury or the acute respiratory distress syndrome. [19] The death was due to ARDS/multi-organ system failure, and the most common risk factors were car­diac disease and diabetes mellitus.

There is significant variation in the reported mortality rates of H1N1, ranging from 11 to 69% and higher in older patents and those who required RRT. [14],[20],[21],[22],[23],[24],[25],[26]

We observed 70% mortality rate, even excee­ding 68.7% reported from South Africa out­break. [27] A potential explanation for the varia­bility in mortality rates may be a pure selection bias with regard to the population reported, as our hospital offers a referral service to many secondary and districts hospitals and our study population, therefore, represented the more se­rious end of the spectrum of affected indivi­duals.

The probable contributing factors for death in our patients included late presentation to hos­pital, delayed initiation of oseltamivir, multi­organ dysfunction, higher SOFA, APACHE II, MODS, XRC scores and possible oseltamivir resistance. Whether obesity is an independent risk factor or a reflection of commonly asso­ciated underlying diseases such as diabetes is unclear. [28] We do not currently know whether our patients, especially those who died, had viremia, as was reported in association with H5N1 infection, a very aggressive variety of influenza. [29],[30] Coinfection with other respiratory pathogenic viruses could also explain the increased pathogenicity among our patients; [31],[32] however, no other common respiratory patho­gen was found in our patients on admission. Viral shedding in seasonal influenza is maxi­mal, close to the onset of the disease, and then decreases rapidly. [33] Our patients got admitted to the hospital with a median of 6 days after disease onset, which may in part explain the apparent lack of nosocomial transmission a­mong critically ill patients.

The etiology of AKI is usually a multifac­torial acute tubular necrosis due to hypoxemia of acute lung injury, hypo-perfusion, renal vaso­constriction and rhabdomyolysis in the setting of a severe systemic inflammatory response syndrome with cytokine cascade. [34] Although to date there is no documented direct cyto­pathic injury in kidneys of patients with in­fluenza, some authors have suggested it as a cause of AKI. [25]

Other investigators reported similar oseltamivir treatment like ours. [20],[27] In patients with severe pneumonia, experts recommend a higher osel­tamivir dose (twice the standard dosing or 150 mg twice daily in adults) and longer duration of treatment (10 versus 5 days) because of po­tential for decreased enteral absorption among critically ill patients, and high and prolonged viral replication in lower respiratory tract. [21]

Our study has limitations since it was a retrospective, single-center observational study. Furthermore, in view of the limited number of cases, our results should be cautiously consi­dered. Despite a large number of reported cases globally, most infections were uncom­plicated, except for patients with underlying diseases. Our focus on critically ill patients may not reflect the important presenting fea­tures in less severe cases. This may lead to overrepresentation or under-representation of certain comorbidities and clinical features. Also, suspected and probable cases of H1N1 were not included for comparison.

We conclude that critical illness from 2009 influenza A (H1N1) may be associated with severe acute lung injury, severe hypoxia, multi­organ dysfunction and a high mortality rate in middle- to old-aged individuals with under­lying risk factor for severe disease. Mortality may be associated with higher APACHE II, SOFA score, MODS, XRC score, requirement of inotrope, ventilator support, RRT and under­lying risk factor for severe disease. Early re­cognition of disease with prompt medical attention may provide opportunities to mitigate the progression of illness and mortality ob­served in our report.

Multicenter, prospective, randomized, con­trolled clinical trials are needed to identify the effectiveness of early treatment and protection offered by H1N1 vaccination.

   References Top

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23.Chacko J, Gagan B, Ashok E, Radha M, Hemanth HV. Critically ill patients with 2009 H1N1 infection in an Indian ICU. Indian J Crit Care Med 2010;14:77-82.  Back to cited text no. 23
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27.Koegelenberg CF, Irusen EM, Cooper R, et al High mortality from respiratory failure secon-dary to swine-origin influenza A (H1N1) in South Africa. QJM 2010;103(5):319-25.  Back to cited text no. 27
28.Novel H1N1 Influenza: Frequently Asked Questions: Medical Topics. Available at; www.mdconsult.com/h1n1.html.  Back to cited text no. 28
29.Yu H, Gao Z, Feng Z, et al. Clinical charac-teristics of 26 human cases of highly patho-genic avian influenza A (H5N1) virus infection in China. PLoS One 2008;3(8):e2985.  Back to cited text no. 29
30.de Jong MD, Hien TT. Avian influenza A (H5N1). J Clin Virol 2006;35:2-13.  Back to cited text no. 30
31.Merler S, Poletti P, Ajelli M, Caprile B, Manfredi P. Co-infection can trigger multiple pandemic waves. J Theor Biol 2008;254:499-507.  Back to cited text no. 31
32.Aberle JH, Aberle SW, Pracher E, Hutter HP, Kundi M, Popow-Kraupp T. Single versus dual respiratory virus infections in hospitalized infants: impact on clinical course of disease and interferon-gamma response. Pediatr Infect Dis J 2005;24:605-10.  Back to cited text no. 32
33.Dominguez-Cherit G, Lapinsky SE, Macias AE, et al. Critically ill Patients With 2009 Influenza A(H1N1) in Mexico. JAMA 2009; 302(17):1880-7.  Back to cited text no. 33
34.Sood MM, Rigatto C, Zarychanski R, et al. Acute kidney injury in critically ill patients infected with 2009 pandemic influenza A (H1N1): report from a Canadian Province. Am J Kidney Dis 2010;55(5):848-55.  Back to cited text no. 34

Correspondence Address:
V B Kute
Department of Nephrology and Clinical Transplantation, 224 Kidney Hospital, IKDRC-ITS B.J. Medical College, Civil Hospital Campus, Ahmedabad 380016, Gujarat
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