Colonization with resistant microorganisms in patients transferred from abroad: who needs to be screened?


This study focused on MDRO colonization in transfer patients from abroad admitted
to our institution. Our data show that a significant proportion (18 %) of patients
who were exposed to a healthcare system abroad or had been hospitalized in high endemicity
region within Switzerland over the last six month were colonized with an MDRO. This
observation reflects other reports 8], 11], 20], including two Swiss studies that found similar rates of MDROs in transfer patients
8], 20]. The fact that most screenings yielded resistant Gram-negative bacteria is also consistent
with recently published data 8], 11]. The very low rate of MRSA detections, however, is unexpected given the higher rates
of MRSA abroad, as suggested by data from the European Centre for Disease Prevention
and Control 3].

A number of studies show that traveling to certain foreign countries is a risk factor
for acquiring MDRO colonization 24]–27]. In these studies travel to India and the African continent stood out for the elevated
rates of such colonization. India, in particular, is notable for being the country
where the NDM-1 resistance gene first surfaced 13]. Many other Asian countries are affected by this development. Our data confirm that
patients returning from Asia were more likely to be colonized than those returning
from other regions. In contrast to a study from the Netherlands, southern Europe could
not be linked to MDRO colonization in our work, even though there is a gradient of
Gram-negative resistance from the Mediterranean area to Scandinavia 3], 11]. Transfer of a patient from outside Europe remained an independent factor for colonization
in our analysis.

Our findings also show that transfer patients who received antibiotic treatment on
admission were more likely to have a positive screening. This finding is not surprising.
Even without an appropriate travel history, prior antibiotic use is a well-recognized
risk factor for colonization and infection with MDROs 14], 28]–31].

The Dutch study also meant to elucidate the association between patient-related factors
and MDRO carriage in repatriated patients 11]. It is, however, an older study conducted between 1998 and 2001, when the global
prevalence of MDROs, especially of Gram-negative bacteria, was much lower than today.
This may be an explanation for why we identified additional risk factors. Skin lesions
and a history of surgical procedure abroad, for example, were associated with having
a positive screening in our study. To our knowledge this has not been recognized in
returning patients before. However, our findings align with the commonality of risk
factors for resistant pathogens first highlighted by Safdar and Maki in 2002 31]. Patients who had an active infection on admission to our institution were also more
likely to have a positive screening and this association remained in the multivariate
model.

The standard screening set (nasal, inguinal swab, plus either a rectal swab or stool
sample) was supplemented by additional swabs if certain clinical factors were present
(skin lesions, urine in patients with urinary catheter, drainage fluid in a patient
with wound drain in place, and tracheal secretions in intubated or tracheostomy patients).
Based on this a transfer patient had at minimum of three screening samples taken.
Those who turned out to be carriers had more screening samples taken (corresponding
to the wounds or devices they had) than the non-carriers. In the literature, exposure
to all types of invasive devices appears as a risk factor for MDRO acquisition 31].

The definition of transfer patients is not uniform in older studies. We defined transfer
patients as patients who were exposed to a healthcare system abroad or in a high prevalence
region in Switzerland over the past six months. In some studies the authors only captured
patients who underwent direct transfer from a hospital abroad 8], 11], while others screened patients who were exposed over various time frames, e.g.,
the past 4 weeks 20] or 12 months 2], 15]. In our study, the longest interval between last healthcare exposure and presentation
to our hospital was 126 days. We do not know if longer intervals were missed by the
admitting services or if there were in fact none. The ideal time frame to incorporate
distant healthcare exposure abroad remains unclear.

We screened all transfer patients on admission independent of whether they had been
in- or outpatients abroad and found no association between screening positivity and
the type of hospital exposure. We could not identify other studies that made this
comparison. Kaiser and colleagues 11] found no association between duration of stay at a hospital abroad and MDRO colonization,
which supports our findings. Thus, it appears that the length of hospitalization abroad
has limited influence on the colonization status, just like type of exposure has.
While some studies show that contact to a healthcare institution or a transfer from
abroad is a risk factor 14], 20], others demonstrate that healthy travelers who were never hospitalized abroad were
found to carry MDROs when they returned home 24]–27]. It is unclear if a stay in a hospital abroad is a more relevant determinant of MDRO
acquisition than a visit in a high endemic country. More studies are necessary to
answer this question.

The original aim of the study was to elicit factors that could help us improve our
screening strategy. Had we limited the screening to those with risk factors (hospitalization
outside Europe, history of surgical procedure in the hospital abroad and – on admission
to our hospital – active infection, presence of skin lesion and antibiotic treatment),
we would have swabbed only 61.7 % (145 patients) of all transfer patients. With this
“risk factor based screening” we would have found 36 patients with multiresistant
Gram-negative bacteria, representing 86 % of all carriers we identified with the current
strategy.

A standard screening set costs approximately 118 Swiss Francs. For 235 screenings,
assuming standard triple sets, we spent 27`730 Swiss Francs. This is 660 Swiss Francs
per identified carrier. For comparison, the cost of the alternative strategy would
have been 475 Swiss Francs. Modifying our strategy to only screen patients with???1
out of five risk factors would have meant missing six colonized patients. A detailed
cost-benefit analysis, however, would need to take secondary costs such as clinical
infection and transmission to others into account.

Our study has some limitations. We did not conduct admission screening for all patients
and cannot make a statement on baseline MDRO colonization in our patient population.
Moreover, we cannot be sure that every patient who had a contact to a healthcare system
abroad was screened on admission. This depended on the admitting service and their
thoroughness when taking the history. Because of the missing or insufficient documentation
of patient histories from the hospitals abroad we were only able to analyze antibiotic
treatment on admission in our hospital and could not collect sufficient data on previous
antibiotic treatment. Also, it was not possible for us to determine how long their
stay in the hospital abroad was if patients had been inpatients there. As we screened
patients on admission to our hospital we also cannot be sure if patients acquired
the MDRO in the hospital abroad or if they were colonized with these bacteria before
traveling to the foreign country.