AGING AND INFECTIOUS DISEASES

INVITED ARTICLE

Thomas T. Yoshikawa, Section Editor

Intra-abdominal Sepsis in Elderly Persons

Yale D. Podnos, Juan Carlos Jimenez, and Samuel E. Wilson
Department of Surgery, University of California, Irvine Medical Center, Orange

Individuals aged 165 years constituted 6.2% of the worlds

population in 1992 and are expected to constitute 120% by
2050 [1]. In the US 2000 census, persons aged 165 years
accounted for 12.4% of the US population, a number that
is similarly expected to increase [2]. Elderly persons use
125% of all prescription drugs and are the major recipients
of medical interventions. Intraperitoneal infections that affect persons aged 165 years are challenging to manage, because the etiology, presentation, severity, and outcome differ
from those of younger populations.
Intra-abdominal sepsis, although it affects all age groups,
takes a greater toll on the elderly population than it does on
younger populations. As individuals age, a variety of physiologic
alterations become manifest, many of which affect such vital
functions as wound healing, oxygen delivery to tissues, immunosurveillance, and eradication of infection. A loss of physiologic reserve, together with concomitant systemic illness, results in worse outcomes for intra-abdominal sepsis. Less ability
to tolerate illness and a relative immunoincompetence affects
how and when elderly patients present to health care providers
with infections. Nutritional status can be deficient in aged persons because of poor dentition, which renders chewing difficult.
Appetite may be decreased as a result of a reduction in the
number of taste buds. Thinning of the stomach mucosa, acReceived 18 December 2001; revised 8 March 2002; electronically published 7 June 2002.
Reprints or correspondence: Dr. Samuel E. Wilson, Dept. of Surgery, University of California, Irvine Medical Center, 101 The City Dr., Bldg. 53, Rte. 81, Orange, CA 92868
(sewilson@uci.edu).
Clinical Infectious Diseases 2002; 35:628
 2002 by the Infectious Diseases Society of America. All rights reserved.
1058-4838/2002/3501-0009$15.00

62 CID 2002:35 (1 July) AGING AND INFECTIOUS DISEASES

companied by a decrease in the amount of enzyme and acid

secretion, makes digestion and absorption less efficient.
Aging causes the skin to lose elasticity and blood supply,
rendering it fragile and more susceptible to injury and infection.
Similarly, the lungs lose their elasticity, resulting in less compliance and recoil. Shallow breathing and hypoventilation of
the bases of the lungs are the consequences. A lifetime of inhaling environmental pollutants also causes parenchymal fibrosis, inhibited ciliary action, and greater mucus production.
These factors result in diminished oxygenation of the arterial
blood and a concomitant reduction in oxygen delivery to peripheral tissues. Peritonitis or postoperative abdominal pain
further restricts pulmonary excursion. Chronic lung disease
foreshadows nosocomial or ventilator-associated pneumonia in
elderly patients who have undergone abdominal operations.
Atherosclerotic changes in the arterial system and increased
cross-linking of collagen and connective tissue cause elevated
peripheral vascular resistance in older patients. Because of this
and other cardiovascular comorbidities, elderly individuals are
less able to withstand and have resolution of intra-abdominal
sepsis. In addition to affecting coronary circulationand,
hence, systemic blood flowatherosclerotic processes and either endogenous or vasopressor-induced vasoconstriction impair blood supply uniformly throughout the body, including
the cerebral, renal, and splanchnic systems. Among other manifestations, this results in a loss of nephrons, which results in
diminished ability to filter blood and concentrate urine. Also,
there is a loss of lean body mass as a result of the breakdown
of muscle and deposition of fatty tissues throughout the body.
The changes occurring in each organ system in elderly patients deplete physiologic reserves and, consequently, the re-

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Elderly patients represent a greater percentage of the population now than ever before, with 12.4% of North Americans being
165 years of age. Intra-abdominal illnesses in this population often have different etiologies than those seen in younger
populations. Because of a variety of physiologic changes that occur as people age, elderly persons have different sites of
infection, may present with vague symptoms and longer histories, are more gravely ill, and, overall, have worse prognoses.
The major causes of intra-abdominal sepsis in elderly persons are reviewed, explanations for the differences in presentation
and prognosis are offered, and the treatments of each cause are reviewed.

Table 1.

Etiologies of intra-abdominal sepsis.

Percentage of
patients, by age

Etiology

165 years

65 years

Appendicitis

28

Diverticulitis

28

Cholecystitis

12

Cholangitis

12

14

11

Intra-abdominal abscess
Colon cancer, sigmoid volvulus,
and mesenteric ischemia
NOTE.

61

Adapted from [3].

iaceae; anaerobes from the Bacteroides fragilis group and streptococci are also common [13, 14]. Extensive data from clinical
trials have been accumulated in an attempt to determine the
optimal antimicrobials and doses for the management of intra-abdominal sepsis. Although each practitioner prefers his
or her own antibiotic regimens, a consensus for intra-abdominal infections was proposed by a committee from the Surgical
Infection Society [15]. Listed in its Summary of Proposed
Guidelines are many well-studied single and combination
therapies useful in the treatment of intra-abdominal infections. Modified guidelines derived from these recommendations are listed in table 2 [15]. These guidelines recommend
that, after minimal intra-abdominal contamination (including
nonperforated cholecystitis; early, simple appendicitis; or
bowel obstruction without perforation), antibiotics should be
given for 24 h. In patients with documented infection, clinical evidence of persistent infection should be the determining
factor when deciding the duration of the antimicrobial course,
rather than use of an arbitrary 10-day or 2-week regimen.
When the source of the infectious process has been controlled
and there is clinical response (as determined by maintenance
of an afebrile state for 48 h, normal WBC count, absence of
abdominal tenderness, and return of peristalsis), the antibiotic
regimen may be discontinued as soon as 5 days after initiation.
In the high-risk patient (including the elderly patient), recommendations include extending the antimicrobial regimen
to cover Enterococcus species, and, in carefully selected highrisk patients, to provide empiric antifungal coverage [15].
Tertiary peritonitis has emerged as a significant problem
even among elderly patients who have received seemingly appropriate treatment (both medical and operative) of sepsis.
Tertiary peritonitis is defined as the recurrence or persistence
of intra-abdominal infection after the receipt of appropriate
care. Nathens et al. [16] found that this occurred most often
after postoperative peritonitis, pancreatitis, and necrotic
bowel. However, it could occur after appendicitis, diverticulitis, and perforated ulcers. In that study, the mortality rate
was 63.6%. In comparison with the organisms associated with
AGING AND INFECTIOUS DISEASES CID 2002:35 (1 July) 63

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sponse to peritonitis while they inhibit the ability to localize,

combat, and eradicate infections [3, 4]. This is compounded
by the fact that elderly patients are more likely to seek care at
the hospital later in the course of infection than are younger
patients because of difficulty walking and leaving home, fear
of hospitalization, altered symptoms, and decreased ability to
appreciate and express symptoms [59]. Consequently, overall,
the outcome of intra-abdominal sepsis is poorer in older patients than it is in younger patients [10]. The additional morbidity and mortality seen in older patients with intra-abdominal
sepsis is calculated using Acute Physiology and Chronic Health
Evaluation II scores [11].
All of the aforementioned physiologic changes affect pharmacokinetics (particularly antimicrobial pharmacokinetics) in
elderly persons [12]. These consequences present a therapeutic
dilemma when elderly patients are treated. Because there is less
blood flow to organs, higher concentrations of antimicrobials
need to be administered, but the mechanisms for detoxifying
the drugs and their metabolites are diminished. Not unexpectedly, the toxicity of antimicrobial agents is greater in elderly
patients than it is in younger patients [1].
Elderly patients with intra-abdominal sepsis present to physicians with less acute and delayed symptoms, compared with
younger patients. Cooper et al. [3] found that elderly patients
present with nausea, vomiting, and fever approximately onehalf as often as do younger patients. In addition, the duration
of symptoms was more than twice as long. In that study, 14%
of patients aged 165 years presented with temperatures of
!36C, compared with only 3% of younger patients, and the
mean temperature of elderly patients was significantly lower.
Older patients were also more likely than young patients to
present with polymorphonuclear lymphocyte counts of !2000
lymphocytes/mm3. With regard to the resolution of infection,
the elderly population had an increase of 50% in the number
of days to euthermia and in the length of hospital stay [3].
The spectrum of diseases that cause intra-abdominal sepsis
in elderly individuals is different from the spectrum in younger
populations (table 1). Also, because of the variety of physiologic
and anatomic changes that occur with age, the frequency of
each disease changes. In a study of elderly patients by Cooper
et al. [3], acute appendicitis and diverticulitis each caused intraabdominal sepsis in 28% of patients, and cholecystitis and cholangitis each caused 12% of cases; intra-abdominal abscesses
were present in 9% of subjects [3]. Other causes of intraabdominal sepsis in elderly persons, such as volvulus, mesenteric vascular ischemia, and perforation of the colon as a result
of obstructing adenocarcinoma, are unusual in the young.
Selected endogenous organisms of the gastrointestinal tract
become the predominant pathogens in intra-abdominal sepsis. Escherichia coli and Klebsiella, Enterococcus, Enterobacter,
and Pseudomonas species are the predominant Enterobacter-

Table 2. Guidelines for antimicrobial regimens for treatment of intra-abdominal

infection.
Level of recommendation

Antimicrobial agent

Level 1 (no therapy listed has been shown

to be superior to another)

Cefoxitin
Cefotetan
Ticarcillin-clavulanate
Piperacillin-tazobactam
Ertapenem
Meropenem
Imipenem-cilastatin
Aminoglycoside with antianaerobe
(clindamycin or metronidazole)a
Cefuroxime with antianaerobe
Third- or fourth-generation cephalosporin
with antianaerobic agent
Aztreonam with clindamycin

Piperacillin-tazobactam
Imipenem-cilastatin
Meropenem
Aminoglycoside with antianaerobic agenta

This agent should be used judiciously and cautiously in elderly patients.

secondary peritonitis, the most common offending organisms

were Enterococcus species, Candida species, and Staphylococcus
epidermidis, followed by E. coli, Enterobacter species, B. fragilis,
and Pseudomonas species [16].

ACUTE APPENDICITIS
Acute appendicitis, as another cause of intra-abdominal sepsis,
may have an atypical presentation in elderly patients. These
variations render the diagnosis of appendicitis difficult in this
population, negatively affecting morbidity and mortality. Delays
in diagnosis are more common in the elderly population and
probably account for the higher incidences of perforation, generalized peritonitis, and death in this population [1719].
It has been postulated that changes occur in the appendix
as we age, including atrophy of intraluminal lymphoid tissue
and thinning of the appendiceal wall, which render the appendix more susceptible to inflammation. Atherosclerosis diminishes the blood supply, the lumen becomes narrowed, and the
muscularis becomes fibrotic and laden with fat [20]. Thus, small
changes in intraluminal pressure can produce rapid ischemia,
gangrene, and perforation at rates that are much quicker in
older persons than they are in younger persons. A perforated
appendix may present in the older patient as a distal small
bowel or right colonic obstruction, and, during surgery, it may
have to be distinguished from carcinoma of the cecum.
64 CID 2002:35 (1 July) AGING AND INFECTIOUS DISEASES

Plain films of the abdomen show an appendicolith in 20%

of cases of acute appendicitis. When the diagnosis is in question,
ultrasonography and CT can be useful. Ultrasonography has
been shown to have a sensitivity of 80% and a specificity of
95% [21]. CT is particularly useful for elderly patients who are
mentally confused, obese, or immunosuppressed or who lack
localized symptoms. The mortality rate for appendicitis in the
elderly population is 2%14%, and morbidity is 40% [5, 10,
22, 23].

DIVERTICULITIS
Diverticula are routinely found in elderly persons. In North
America, nearly 25% of patients in their 60s and 40% in their
70s have diverticula [24]. Diagnosis is readily made via CT scan
with a water-soluble contrast enema. Older patients are more
likely than younger patients to have diverticular perforations
that result in generalized, rather than localized, peritonitis [18].
These patients also tend to have a shorter and more rapidly
progressive course of disease. Watters et al. [18] found that the
mortality rate for persons aged 165 years who had perforation
was 17%, compared with 6% for younger patients; the groups
were statistically similar with regard to frequency of treatment
(with the Hartmann procedure).
The trend toward decreasing length of hospitalization has
led to a greater acceptance of primary resection and anas-

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Ciprofloxacin with metronidazole

Level 2 (for patients with moreserious infections)

CHOLECYSTITIS AND CHOLANGITIS

More than one-half of all people aged 170 years have gallstones
[27]. Although most cases are asymptomatic, 20% of older
patients have serious complications of their disease, a much
higher rate than that seen in the 4050-year-old age group [28].
E. coli, Klebsiella species, and B. fragilis commonly colonize the
gallbladder and biliary tree in elderly patients and are the organisms recovered in secondary complications. Biliary operations have become the most commonly performed abdominal
procedure in the elderly population.
Similar to appendicitis and diverticulitis, elderly patients with
cholecystitis have delays in presentation to the hospital, diagnosis, and treatment. Morrow et al. [29] estimated a 33% increase in time from onset of symptoms to diagnosis and treatment. They reported that elderly patients presented with a
seemingly benign course that was not representative of the
severity of illness. In fact, despite a perceived decrease in the
severity of illness, 40% of the patients in their study had empyema of the gallbladder, gangrenous cholecystitis, or free perforation, and 15% had subphrenic abscesses or liver involvement. Glenn and McSherry [30] corroborated this finding by
showing that severe disease and gangrene can be present with
only mild leukocytosis and a lack of peritoneal signs.
As with younger populations, the need for an emergency
operation for cholecystitis is associated with a significantly

worse outcome. Elderly men are approximately twice as likely

to require emergency treatment than are older women (58.9%
vs. 32.1%). Associated with this is a 5-fold increase in the
incidence of necrotizing, suppurative, or hemorrhagic cholecystitis and a 50% increase in the incidence of complications
for patients requiring emergency treatment. Infectious complications include empyema, gangrenous cholecystitis, perforation, abscess formation, and fistula, and the mortality rate is
15%20% [31, 32] (table 3).
The overall mortality rate for cholecystectomy for all age
groups is 0.5%1.8% [33, 34]. In the elderly population, it
increases to 0.8%4.4%. If the procedure is performed emergently, the mortality rate for cholecystectomy in the elderly
population has a range of 10%19% [3541]. With the widespread acceptance of laparoscopic cholecystectomy as the treatment of choice for gallbladder disease, and with the increasing
skill with which it is performed, morbidity and mortality associated with cholecystectomy are expected to decrease. Indeed,
Massie et al. [42] have shown that significantly fewer complications are associated with laparoscopic cholecystectomy compared with the open approach.
Acute cholangitis is most commonly caused by choledocholithiasis, iatrogenic strictures, neoplasms, or sclerosing cholangitis [14]. The classic findings of jaundice, abdominal pain,
and fever with chills (Charcots triad) are only found in
55%70% of patients [43]. Common in the elderly population
are hypotension and mental confusionwhich, with Charcots triad, make up Reynolds pentad. Treatment regimens
are based on vigorous fluid rehydration, aggressive monitoring, and nasogastric suction to decrease pancreatic stimulation. Three-quarters of patients who undergo these measures

Table 3.
Complications in patients undergoing elective and
emergent operations for gallbladder disease.
Percentage of patients
Complication

Elective
operations

Emergent
operations

Overall

21

37

Cardiovascular

50

34

Pulmonary

10

19

Urinary

13

13

Abscess/sepsis

Wound infection

13

Renal failure

Pancreatitis

Upper gastrointestinal bleeding

Fistula

Ileus

Liver failure

NOTE.

From [13].

AGING AND INFECTIOUS DISEASES CID 2002:35 (1 July) 65

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tomosis for treatment of left-side colon lesions. Umbach and

Dorazio [25] found that the single-stage procedure had an
incidence of complications of 30% (compared with 29%69%
morbidity for the Hartmann procedure) with no perioperative
mortality. In this series, the most common complications were
wound infections (in 9.1% of patients), urinary retention (in
6.1%), and urinary tract infections (in 6.1%). A single patient
had an anastomotic leak that required conversion to the Hartmann procedure. Hemodynamic instability, malnourishment,
severe anemia, immunosuppression, diffuse peritonitis, and
questionable viability of the bowel wall are contraindications
for the single-stage operation. A 2-stage procedure should be
used in these situations. Unprepared bowel, technical complications, presence of a chronic abscess cavity, and mild anemia, immunosuppression, or malnutrition are relative contraindications for the single-stage operation [26].
In the unusual case of complete sigmoid obstruction that
results from severe acute diverticulitis, a first-stage proximal
colostomy may be indicated, but this procedure is otherwise
rarely used as a definitive treatment. An advancement in treatment of diverticular pericolic abscesses has been percutaneous
drainage with staged primary resection and anastomosis after
the abscess has resolved. A single-stage resection can be performed in 70% of patients in stable condition.

will respond within 2448 h. If they do not respond, patients

with extrahepatic ductal dilatation should undergo endoscopic retrograde cholangiopancreatography, and those with
only intrahepatic ductal dilatation should undergo percutaneous transhepatic cholangiography. If these measures fail,
common bile-duct exploration is required to decompress the
biliary system. Overall, the mortality rate for patients with
cholangitis is 10% [14].

COLON CANCER PERFORATION

MESENTERIC ISCHEMIA
Fortunately, mesenteric ischemia is a relatively uncommon
cause of acute abdomen in elderly patients, because the mortality rates have a range of 45%90% [53]. Reasons contributing
to this may be delayed diagnosis causing intestinal infarction
before initiation of therapy and the irreversibility of bowel ischemia after a few hours. Embolus of the superior mesenteric
artery accounts for approximately one-half of cases and results
66 CID 2002:35 (1 July) AGING AND INFECTIOUS DISEASES

SIGMOID VOLVULUS
Volvulus of the sigmoid colon is 20 times more likely to occur
in elderly patients than it is in younger patients. An acquired
redundancy of the sigmoid colon over time resulting from a
high residual colonic content and dysmotility likely accounts
for the increased incidence [55]. Patients with sigmoid volvulus
present with colicky abdominal pain, distention, and obstipation. After the bowel becomes strangulated, the elderly patients
symptoms may progress to generalized abdominal pain, fever,
leukocytosis, and hypotension. Plain films of the abdomen
show a birds beak sign pointing to the site of obstruction.
If no peritoneal signs are present, decompression using endoscopy should be performed and a rectal tube should be
placed. This therapy is successful in 170% of patients [53].

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Approximately 140,000 Americans, the great majority of whom

are older than 60 years, develop colon cancer each year. Perforation may occur in advanced tumors, causing peritonitis or
abscess, with an incidence range of 2.6%10% [44, 45]. Chen
and Sheen-Chen [46] found that 19% of perforations at the
lesion site and 33% proximal to the cancer occurred in elderly
patients, despite the fact that elderly patients accounted for
15% of the study population. This latter group likely represents proximal perforation from obstructing colon cancers.
These findings were corroborated by Kyllonen [47] and Runkel
et al. [48].
Crowder and Cohn [44] found that the most common presenting signs and symptoms of colon cancer preceding perforation were abdominal pain (45 of 45 patients), weight loss
(32 of 45 patients), anemia (26 of 45 patients), and melena (21
of 45 patients). Approximately 67% of the patients in this study
were aged 169 years. Kelley et al. [49] found perforation to be
the most deadly complication of colon cancer. In this study,
operative mortality was 33%.
After perforation of the sigmoid colon, the postoperative
mortality increases substantially, with a range of 16%38% [47,
5052]. Peritonitis resulting from perforation has a poorer outcome in elderly patients, with regard to both postoperative
recovery and survival from cancer. Possible reasons for the
worsened outcomes in this scenario are poorer nutritional
status resulting from the cancer, peritoneal spread of the cancer
during perforation, more-advanced local disease, and the emergent nature of interventions in less-than-adequately prepared
patients. In addition to higher operative mortality and morbidity, these patients have poor 5-year survival rates [46].

from embolization of a left atrial or ventricular mural thrombus

after a period of cardiac infarction, dysrhythmia, or both. Superior mesenteric artery thrombosis accounts for !25% of
cases, and, when it occurs, it usually results from progressive
atherosclerosis at the superior mesenteric artery origin. Least
commonly, mesenteric ischemia can be due to venous thrombosis. This condition is most commonly associated with hypercoagulable states, abdominal trauma, portal hypertension,
pancreatitis, viscus perforation, intra-abdominal sepsis, and
cancer.
Elderly patients with mesenteric ischemia present with abdominal pain that is out of proportion to the results of the
physical examination, bloody diarrhea, and forceful evacuation of stool. Risk factors for this condition include age of
150 years, coronary artery disease, peripheral vascular disease,
history of intestinal angina, hypertension, critical illness after
an operation, and presence of multiple comorbid conditions.
Laboratory evaluations may reveal leukocytosis, hemoconcentration, an elevated alkaline phosphatase level, metabolic
acidosis with elevated base deficit, an increased serum lactate
level, hyperamylasemia, and hyperphosphatemia. Plain films
of the abdomen generally reveal nothing remarkable until later
in the course of the condition, when dilated loops of bowel
with air-fluid levels, thumbprinting of the bowel wall, intramural or portal venous gas, and free intraperitoneal air can
be seen [54].
Initial treatment consists of therapy with intravenous fluids,
monitoring with a Swan-Ganz catheter, and urgent mesenteric
arteriogram or exploration. Therapy with digitalis or vasopressors should be discontinued, because their use can exacerbate ischemia. Broad-spectrum antibiotics are indicated to
control bacterial translocation across the ischemic intestinal
wall. When peritoneal signs are present, exploratory laparotomy is indicated. Nonviable bowel must be resected and intestinal blood flow restored.

Even when treatment is successful, incidence of recurrent sigmoid volvulus is high (55%90%), mandating that each patient
be evaluated for elective sigmoid colectomy [53]. When peritoneal signs are present, urgent exploratory laparotomy is indicated. The mortality rate approaches 70% when the bowel is
gangrenous [53].

CONCLUSIONS

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Given the increased mortality and morbidity associated with

intra-abdominal sepsis in the elderly population, and given the
varied means of disease presentation, practitioners must have
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