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Geriatr Gerontol Int 2017; 17: 1076–1080

O R I G I N A L A R T I C L E : E P I D E M I O L O G Y,
C L I N I C A L P R A C T I C E A N D H E A LT H

Prevalence and prognostic influence of bacterial pyuria in


elderly patients with pneumonia: A retrospective study
Hiroaki Oka,1,2,5 Kosaku Komiya,1,2,5 Minoru Ohama,1,5 Yoshiyuki Kawano,1 Masahiro Uchida,1
Hajime Miyajima,1 Tomohiko Iwashita,1 Eiji Okabe,1 Tadao Kawamura,3 Kazuhiro Yasuda,4
Taisuke Matsumoto1 and Jun-ichi Kadota5
1
Department of Internal Medicine, 2Clinical Research Center of Respiratory Medicine, 3Neurosurgery, 4Gastroenterological Surgery, Tenshindo
Hetsugi Hospital and 5Respiratory Medicine, and Infectious Diseases, Oita University Faculty of Medicine, Oita, Japan

Aim: The number of elderly patients with pneumonia is significantly increasing as the populations in many countries
age. Although elderly patients with pneumonia are at risk of developing urinary tract infections, no studies have examined
the prevalence or the prognostic impact of this complication. The aim of the present study was to investigate the preva-
lence of comorbid bacterial pyuria and the impact on the prognosis of elderly patients with pneumonia.
Methods: We retrospectively evaluated 132 patients aged >65 years who were hospitalized for pneumonia and who
underwent a urinary sediment test on admission. The background characteristics, laboratory results and treatment regi-
mens were documented, and the risk factors for the complication of bacterial pyuria and its association with 90-day mor-
tality in pneumonia patients were elucidated.
Results: A total of 37 (28%) of 132 patients were complicated by bacterial pyuria. The patients with bacterial pyuria were
more often women, showed a poorer performance status, were more frequently fed by percutaneous endoscopic
gastrostomy, and more frequently used diapers and/or a bladder catheter. Regarding first-line drugs, 82.6% of the patients
received beta-lactamase inhibitors and extended-spectrum penicillins. The use of a bladder catheter and a poor perfor-
mance status were associated with bacterial pyuria. A multivariate analysis showed that a poor performance status was
the only factor associated with 90-day mortality.
Conclusions: Bacterial pyuria did not affect the prognosis of patients who were treated with penicillin-based regimens.
Thus, broad-spectrum antibiotics are not necessarily required for elderly patients with pneumonia complicated by urinary
tract infection. Geriatr Gerontol Int 2017; 17: 1076–1080.

Keywords: bacterial pyuria, bacteriuria, elderly patient, pneumonia, urinary tract infection.

Introduction high as 7.5–30%.2 UTI can therefore be life-threatening


if physicians do not diagnose them promptly and provide
The incidence of pneumonia is increasing as the popula- appropriate treatment to elderly patients with pneumonia.
tion ages. The decreased immune function of older adults However, there have been no studies regarding the clinical
allows them to be complicated with other infections. impact of UTI as a complication in pneumonia patients.
Urinary tract infections (UTI) are the second most com- The present study aimed to investigate the prevalence of
mon form of infectious disease (after pneumonia) in the bacterial pyuria and its relationship with the prognosis of
elderly population.1 Although the overall mortality rate pneumonia in elderly patients.
of pyelonephritis, a typical UTI, is approximately 0.3%,
elderly patients with pyelonephritis are susceptible to bac-
teremia, the mortality rate of which is reported to be as Methods

Study design and participants


Accepted for publication 13 April 2016. This was a retrospective observational study that was car-
ried out in a single facility. The study population included
Correspondence: Dr Hiroaki Oka MD PhD, Department of Internal
Medicine and Clinical Research Center of Respiratory Medicine, patients who were aged >65 years who required hospital-
Tenshindo Hetsugi Hospital, 5956 Nakahetsugi, Oita 879–7761, Japan. ization for pneumonia, and who underwent a urinary test
Email: ch9a4g63@oita-u.ac.jp between January 2012 and April 2014 at Tenshindo

1076 | doi: 10.1111/ggi.12830 © 2016 Japan Geriatrics Society


Influence of bacterial pyuria

Hetsugi Hospital, Japan, an acute care hospital with 173 Cox proportional hazards model was used to analyze
beds, in Oita, Japan. Patients who were aged <65 years, the factors in the cases that were complicated by bacte-
or who had interstitial pneumonia, pneumomycosis, ma- rial pyuria after adjusting for other variables.
lignant tumors or other coexisting diseases, which could
be obvious sources of fever (other than respiratory tract Results
or urinary tract infections), were excluded from the pres-
ent study. The primary outcome was 90-day mortality Patient characteristics
after hospitalization for pneumonia; the secondary out-
come was the risk factors for the complication of pyuria During the observation period, 316 patients were admit-
in patients with pneumonia. The study protocol was ted for pneumonia, 132 of the patients met the inclusion
approved by the ethics committee of the hospital (approval criteria. A total of 37 cases were complicated by bacterial
number 13010; approval date 23 July 2014). pyuria; 95 were not. Although there was no significant
difference in age, the bacterial pyuria complicated group
Definitions included a significantly higher proportion of women and
patients with a longer hospital stay (Table 1). No statistical
Pneumonia was defined by radiological evidence with differences were observed in the C-reactive protein and
fever or hypothermia at the time of examination (tempera- albumin levels, whereas the sequential organ failure
ture >38 °C or <35 °C, or cases in which fever or hypo- assessment score was higher in the cases that were compli-
thermia could be confirmed to have occurred within 48 h cated with bacterial pyuria. The use of bladder catheters,
before hospitalization through the records of the intro- percutaneous endoscopic gastrostomy or diapers, a diag-
ducing hospital or previous physician), in addition to the nosis of nursing and healthcare-associated pneumonia
confirmation of two or more of the following symptoms: (as defined by the Japanese Respiratory Society) or a poor
coughing, dyspnea, respiratory failure and purulent spu- performance status (PS) were associated with a higher
tum.3 Pyuria was defined as a leukocyte count of ≧ 10/ prevalence of bacterial pyuria. There were no significant
mm3 in a urine specimen that had not been centrifuged, differences in the selection of antibiotics in the bacterial
or a leukocyte count of ≧ 5/high power field in a urine spec- pyuria compound and non-compound groups (Table 2).
imen that had been centrifuged. Bacteriuria was defined A majority of the patients (62.9 %) were treated with
by the observation of one or more bacteria in each field ampicillin/sulbactam alone or as combined therapy at the
of a high-power field.4,5 Broad-spectrum antibiotics were time of admission, followed by piperacillin/tazobactam
defined by the characteristics of their antipseudomonal alone or as combined therapy in 19.7% of the cases.
and/or anti-methicillin-resistant Staphylococcus aureus
activity. Bacteriological findings
Statistical analysis Microbiological examinations of the sputum were car-
ried out in 56% of 316 patients with pneumonia. The
The PASW statistics 22.0 software package (IBM SPSS, leading six causative organisms were as follows: Klebsi-
Tokyo, Japan) was used for the statistical analyses in ella pneumoniae (9.1%), Pseudomonas aeruginosa (9.1%),
the present study. For “bacteria pyuria compound” and methicillin-sensitive Streptococcus aureus (9.1%),
“rate of death after 90 days” the α value was set at methicillin-resistant Streptococcus aureus (9.1%) Hae-
0.05, and the β value was set at 0.2. With an effect size mophilus influenzae (8.5%) and Streptococcus pneumoniae
of 0.3 (χ 2-test), the required target sample size was 88 (7.9%). Just 2% of the admitted patients underwent bi-
patients. The patients who met the inclusion criteria ological examinations of urine, which showed no
were separated into a bacterial pyuria compound group specific tendency. The leading six UTI causative
and a non-compound group. We compared the back- organisms isolated from 401 urine specimens in our
ground factors, carried out a blood analysis and investi- hospital during the surveillance period were as follows:
gated the imaging findings. Student’s t-test and the Enterococcus faecalis (22.9%), Escherichia coli (10.5%),
Mann–Whitney U-test were carried out for interval Pseudomonas aeruginosa (10.5%), methicillin-resistant
scales, while the χ 2-test or Fisher’s exact test were car- Streptococcus aureus (8.5%), Klebsiella pneumoniae (3.0%)
ried out for nominal and ordinal scales. The confidence and methicillin-sensitive Staphylococcus aureus (2.0%).
interval of the two-sided analyses was set at 95%. Mul-
tivariate analyses were carried out with selected items,
Ninety-day mortality in the patients with pneumonia
mainly those in which a significant difference was
with or without bacterial pyuria and the risk factors for
observed between the two groups using the forced entry
bacterial pyuria
method. These stratified parameters were used to draft a
Kaplan–Meier curve and carry out a log–rank test to The survival curve showed that the coexistence of
compare the rate of 90-day mortality in the bacterial bacterial pyuria had no significant effect on survival
pyuria compound and non-compound groups. The (Figure 1). A multivariate logistic regression analysis

© 2016 Japan Geriatrics Society | 1077


H Oka et al.

Table 1 Baseline characteristics of the pneumonia patients

Bacterial pyuria (n = 37) Non-bacterial pyuria (n = 95) P


Female 22 (60) 37 (39) 0.033
Age (years) 88.0 (81.5–95.0) 86.0 (80.5–91.5) 0.438
Hospital stay (days) 28.0 (3.5–52.5) 21.0 (3.0–39.0) 0.037
Body temperature (°C) 37.5 (37.0–38.0) 37.6 (37.1–38.1) 0.473
PaO2/FiO2 ≦ 300 17(46) 32(34) 0.190
Systolic blood pressure (mmHg) 119 (108–140) 128 (115–141) 0.057
Diastolic blood pressure (mmHg) 66 (54–79) 70 (62–78) 0.068
Heart rate (b.p.m.) 90 (77–103) 88 (75–102) 0.412
WBC (/μL) 9030 (6625–11 435) 10 070 (7020–13 120) 0.477
Hb (g/dL) 11.2 (10.1–12.3) 11.8 (10.2–13.4) 0.370
Plt (×105/μL) 15.8 (11.4–20.2) 19.7(14.7–24.8) 0.004
BUN (mg/dL) 19.2(12.1–26.3) 21.5 (15.8–27.3) 0.984
Creatinine (mg/dL) 0.89 (0.54–1.25) 0.93 (0.61–1.25) 0.887
Albumin (g/dL) 3.20 (2.85–3.55) 3.30 (2.85–3.75) 0.475
C-reactive protein (mg/dL) 9.09 (3.45–14.74) 8.73 (5.27–14.00) 0.757
SOFA score 3 (1.5–4.5) 2 (1–3) 0.008
Body mass index (kg/m2) 18.6 (16.5–20.8) 19.94 (17.1–22.8) 0.180
Bladder catheter 7 (19) 2 (2) 0.001
Percutaneous endoscopic gastrostomy 8 (22) 7 (7.4) 0.020
Continuous use of diapers 17 (46) 22 (23) 0.010
NHCAP 32 (87) 62 (65) 0.016
Dementia 21 (57) 39 (41) 0.104
Performance status 3 (2.5–3.5) 2 (1–3) 0.000
Success rate of first-line antibiotics (%) 34 (92) 84 (88) 0.561
Broad-spectrum antibiotics (%) 15 (41) 31 (33) 0.392
Diabetes mellitus 3 (8) 14 (15) 0.298
Chronic heart failure 18 (46) 60 (65) 0.047
Data expressed as number (%) or median (interquartile range). BUN, blood urea nitrogen; Hb, hemoglobin; LAMA, long-acting mus-
carinic antagonists; NHCAP, nursing and healthcare associated pneumonia; PEG, percutaneous endoscopic gastrostomy; Plt, platelet;
SOFA, sequential organ failure assessment; WBC, white blood cell.

showed that bladder catheter use and a poor PS were as- poor PS) were consistent with the commonly accepted
sociated with bacterial pyuria (Table 3). A Cox hazards evidence on the risk factors for UTI, our data showed
analysis showed that a poor PS was the only factor that that the complication of bacterial pyuria in elderly pa-
was significantly associated with 90-day mortality. The tients with pneumonia was not significantly associated
complication of bacterial pyuria did not affect the with 90-day mortality when the patients were treated
mortality rate of the patients in the present study ( with a penicillin-based antibiotic regimen, such as
Table 4). ampicillin/sulbactam or piperacillin/tazobactam (Table 3
, Fig. 1). Similarly, no significant relationship was
Discussion observed with 30-day and in-hospital mortality (data
not shown). This might be because these drug combina-
The present study showed that the prevalence of bacterial tions result in better therapeutic effects, not only in pa-
pyuria (approximately 30%) was not so high in elderly pa- tients with pneumonia, but also in patients with
tients with pneumonia (Table 1). This was lower than the comorbid UTI, as the two drugs have a sensitivity rate
rate of asymptomatic pyuria in long-term care facilities of ≥80% against the causative agents of the UTI that
(approximately 90%).6,7 This discrepancy might be ex- were typically detected in the urine cultures of patients
plained by the fact that although our study population at our hospital from 2012 to 2014 (data not shown). In
was composed of elderly patients, they did not all come line with our previous finding regarding the treatment
from long-term facilities. of elderly patients with pneumonia in which the pa-
Second, although the risk factors for bacterial pyuria tients’ prognoses mainly depended on host factors, such
in patients with pneumonia (bladder catheter use and as the overall body condition and nutritional condition,

1078 | © 2016 Japan Geriatrics Society


Influence of bacterial pyuria

Table 2 Characteristics of the selected antibiotics in the rather than the type of antibacterial drug, a poor PS was
pneumonia patients associated with 90-day mortality in the present study.8 It
is therefore more important to properly prevent illness
Bacterial pyuria Bacterial pyuria and the deterioration of the PS of elderly patients.
compound non-compound To our knowledge, this is the first study to show the
(n = 37) (n = 95) prevalence of comorbid bacterial pyuria and its impact
ABPC/SBT 18 (49) 53 (56) on the prognosis of elderly patients with pneumonia.
ABPC/SBT 3(8) 4 (4) However, the present study is associated with several
+ new quinolone limitations. First, it was a retrospective study based on
ABPC/SBT 0 (0) 4 (4) medical records. The patients who were admitted with
+ macrolide pneumonia did not always undergo a urinary sediment
ABPC/SBT + TEIC 0 (0) 1 (1) test. Thus, the possibility of bias arising from the
PIPC/TAZ 6 (16) 12 (13) clinical findings and physicians’ judgment cannot be
PIPC/TAZ + 1 (3) 1 (1) eliminated. Second, a thorough bacteriological investi-
new quinolone gation could not be carried out. Accordingly, it was dif-
PIPC/TAZ 1 (3) 5 (5) ficult to evaluate the effectiveness of the antibiotics that
+ macrolide were given to the recruited patients. Third, the condi-
PIPC 2 (5) 2 (2) tion of the patients who were diagnosed with bacterial
AZM 1 (3) 0 (0) pyuria based on urinary sediment findings was not
LVFX 0 (0) 4 (4) necessarily identical to the condition of the patients
LVFX + CPZ/SBT 0 (0) 1 (1) who are treated for UTI, as in many cases patients
CTRX 3 (8) 6 (6) without clinical symptoms do not require medical care,
CPZ/SBT 0 (0) 1 (1) even if bacteriuria is detected.9 Woodforth et al.
DRPM 1 (3) 0 (0) reported that in a study population of patients aged
MEPM 1 (3) 1 (1) >75 years, 48.7% of the patients who were diagnosed
with a UTI showed traditional UTI-related symptoms,
Data expressed as number (%). ABPC/SBT, ampicillin/sulbactam;
AZM, azithromycin; CPZ/SBT, cefoperazone/sulbactam; CTRX,
whereas such symptoms were present in 10.4% of the
ceftriaxone; DRPM, doripenem; LVFX, levofloxacin; MEPM, patients who were deemed to not have a UTI.10 This
meropenem; PIPC, piperacillin; TAZ, tazobactam; TEIC, teicoplanin. shows that the existence of typical symptoms alone is
not enough to either diagnose or dismiss a UTI. Fur-
thermore, the McGeer diagnostic standards referenced
by the Society for Healthcare Epidemiology of America
and Centers for Disease Control and Prevention
exclude other fever-producing illnesses and/or subjec-
tive symptoms from the diagnostic standards for
UTI.11 It therefore appears to be difficult for physicians
to differentiate cases of pneumonia in elderly patients
complicated by asymptomatic bacteriuria from those
complicated by UTI. In the clinical setting, the
treatment of elderly patients often requires prompt
treatment decisions. Physicians should therefore at
least be aware that UTI that show pyuria and bacteri-
uria might occur in patients with pneumonia. In this
context, even if UTI were overdiagnosed in the present
study, our results showed that the penicillin-based
regimens should be effective in the cases that were
complicated by UTI.
In conclusion, although a large prospective study is
required to microbiologically evaluate the effectiveness
of antibiotics against coinfection with bacterial pyuria
in pneumonia patients, penicillin-based antibiotic regi-
mens seem to be effective in patients with pneumonia
Figure 1 A Kaplan–Meier analysis of the survival of pneumonia complicated by UTI. The results of the present study
patients with and without bacterial pyuria. The survival of patients
with pneumonia complicated by bacterial pyuria did not differ suggest that such patients might be more effectively
from that of pneumonia patients without bacterial pyuria (log– managed by exchanging ideas with other fields, such as
rank test, P = 0.654). urology.

© 2016 Japan Geriatrics Society | 1079


H Oka et al.

Table 3 Risk factors for urinary tract infection

Crude OR P Adjusted OR† P


Female 2.299 (1.059–4.991) 0.035 2.096 (0.863–5.5090) 0.102.
Bladder catheter 10.850 (2.138–55.071) 0.004 6.703 (1.228–36.576) 0.028
Performance status 1.863 (1.314–2.641) 0.000 1.712 (1.109–2.644) 0.015
Dementia 1.885 (0.874–4.063) 0.106 0.656 (0.238–1.806) 0.414
SOFA score 1.377 (1.078–1.744) 0.008 1.278 (0.983–1.661) 0.067
Data expressed as the hazard ratio (95% confidence interval). †Adjusted for variables using the forced entry method. SOFA, sequential
organ failure assessment.

Table 4 Cox proportional hazards model for the factors associated with a risk of 90-day mortality

Crude HR P Adjusted HR† P


Female 0.915 (0.317–2.636) 0.869 0.634 (0.203–1.974) P = 0.431
Bladder catheter 0.948 (0.124–7.249) 0.959 0.549 (0.064–4.698) P = 0.584
Performance status 1.878 (1.124–3.138) 0.016 1.945 (1.063–3.559) P = 0.031
Dementia 2.317 (0.777–6.915) 0.132 0.906 (0.245–3.352) P = 0.883
Bacterial pyuria 1.345 (0.451–4.013) 0.595 1.073 (0.318–3.622) P = 0.910
Broad-spectrum antibiotics 0.935 (0.313–2.791) 0.904 0.977 (0.292–3.269) P = 0.970
SOFA score 1.198 (0.928–1.547) 0.165 1.095 (0.826–1.452) P = 0.529
Data expressed as the hazard ratio (95% confidence interval). †Adjusted for variables using the forced entry method. SOFA, sequential
organ failure assessment.

Acknowledgments care-associated, and hospital-acquired pneumonia. Ann Intern


Med 2009; 150: 19–26.
4 Wright WT. Cell counts in urine. AMA Arch Intern Med 1959;
We greatly thank Mr Eto (medical technologist, Tenshindo 103: 76–78.
Hetsugi Hospital), and Ms Okubayashi, Ms Torii, Ms 5 Nicolle LE, Bradley S, Colgan R, Rice JC, Schaeffer A, Hooton
Egoshi and Ms Kudoh (health information manager, TM. Infectious Diseases Society of America guidelines for the
Tenshindo Hetsugi Hospital) for valuable assistance with diagnosis and treatment of asymptomatic bacteriuria in
adults. Clin Infect Dis 2005; 40: 643–654.
collecting the data.
6 Stamm WE, Counts GW, Running KR, Fihn S, Turck M,
Holmes KK. Diagnosis of coliform infection in acutely
Disclosure statement dysuric women. N Engl J Med 1982; 307: 463–468.
7 Nicolle LE. Urinary tract infections in long-term-care facili-
The authors declare no conflict of interest. ties. Infect Control Hosp Epidemiol 2001; 22: 167–175.
8 Komiya K, Oka H, Ohama M et al. Evaluation of prognostic
differences in elderly patients with pneumonia treated by be-
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1080 | © 2016 Japan Geriatrics Society

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