Keywords
COVID-19 - pandemics - sonography - ultrasound
Background
The coronavirus disease 2019 (COVID-19) caused an ongoing pandemic and has raised
a global public health concern. More than 220 million cases have been confirmed worldwide
up to September 2021 [1]
[2]. In the first period of the pandemic in Germany, the peak incidence of more than
7 cases per 100 000 inhabitants per day was reached in March 31 to April 3, 2020,
while the first confirmed COVID-19 case in Germany occurred on January 27, 2020 [3]
[4]. In this initial period, the treatment of critical cases of the disease required
a significant number of medical resources [5]. Intensive care units had to use a substantial percentage of their ventilation capacity
for the treatment of COVID-19 patients, whereas a certain additional portion of this
capacity always had to be kept free for possible further severely ill patients due
to the indeterminacy of the pandemic development [6]. Thus, on the one hand to ensure that the number of available beds particularly
at intensive care units were kept to a sufficient level, Germany implemented a strategy
of postponing elective medical procedures that are not time-critical [7]
[8]. On the other hand, due to hygiene and isolation procedures, common workflows were
adapted to minimize face-to-face exposure to patients and to minimize the risk of
infection for patients and healthcare professionals [9]
[10]. The radiology department, as a discipline interacting with almost every other discipline,
played a special role during this period. On the one hand, acute COVID-19-associated
clinical pathologies had to be diagnosed, while on the other hand, other patients
with an increased risk for infection had to be diagnosed [9]
[11]
[12].
The subdiscipline of sonography played a special role in this consideration. Due to
the physically close and prolonged contact between the patient and examiner, it was
attempted to shift as much of the urgent examinations as possible to other modalities
(computed tomography and magnetic resonance imaging) to minimize the risk of infection
in this way as well [13]. Furthermore, elective non-urgent ultrasound examinations were canceled or postponed
in advance, resulting in a drastic reduction in sonographic examinations starting
March 2020 [14].
Subsequently, a partial return to the pre-epidemic situation was achieved with a successive
attempt to increase the number of emergency examinations and to finally resume regular
elective sonographic procedures to fully restore standard patient care in Germany
[15].
The aim of this study is to determine the decrease in the number of sonographic examinations
due to the above-mentioned reasons and to determine if the number of sonographic examinations
in the post-pandemic (from May 2023) era is similar to the number of sonographic examinations
before February 2020 (first COVID-19 case on January 27, 2020) [2]. Possible explanations will be discussed.
Materials and Methods
In accordance with the guidelines of the institutional review boards, this retrospective,
non-patient-centered, entirely epidemiologic multicenter analysis did not require
an ethics vote. No patient-related private information was collected at any time during
the investigation.
Participating institutions
Four university hospitals in Germany agreed to participate in the present study, including:
-
Institute of Diagnostic and Interventional Radiology, University of Cologne, Faculty
of Medicine and University Hospital Cologne
-
Institut für Diagnostische und Interventionelle Radiologie, Universitätsklinikum Würzburg,
Würzburg
-
Department of Radiology and Nuclear Medicine, Mannheim, Germany, University of Heidelberg,
University Medical Center Mannheim
-
Institute of Diagnostic and Interventional Radiology, University of Frankfurt, Faculty
of Medicine and University Hospital Frankfurt
Included examinations and data collection
The participating institutions were provided with an online questionnaire (Google forms; Alphabet Inc., Mountain View) for a detailed assessment of the ultrasound examinations
performed during the included examination periods [16]. Due to data privacy regulations, only the number of conducted examinations was
collected, and any information about the patient and clinical constellation was not
included. The number of examinations per year from January 2015 to June 2018 was collected
to generate an overview of the average number of ultrasound examinations. In the period
from June 2018 to September 2023, the examinations were assessed on a monthly basis
to obtain a more detailed overview of the impact of the pandemic on the number of
ultrasound examinations performed.
To better illustrate the pandemic event and the sonographic examination numbers, three
periods were defined:
-
Pre-pandemic period before the initial outbreak of COVID-19 in Germany in January
2020 (January 2015 – January 2020)
-
Pandemic period:
-
initial pandemic period from the outbreak of the COVID-19 pandemic in Germany, including
first six months (January 2020 – June 2020)
-
post-initial pandemic period (June 2020 – April 2022)
-
late pandemic period (May 2022 – April 2023)
-
Post-pandemic period (May 2023 – September 2023), according to WHO criteria, the official
end of the COVID-19 pandemic.
Inclusion criteria:
-
Completed ultrasound examination at one of the participating radiology departments
(derived from the radiological information system based on the accounting department
or based on DICOM tag in the picture archiving system).
-
Examination between January 1, 2015, and September 30, 2023.
Exclusion criteria:
Statistical Analysis
Statistical data analysis was performed using R version 3.6.2 on R studio version
1.2.5033.35 (https://cran.r-project.org/). Figures were plotted using MS Excel. Continuous variables were reported as the
mean. The number of examinations performed was compared using Student’s T-test. Linear
regression models were used to predict the respective periods.
Results
a) Analysis of the annual examination numbers
In total, n = 288,562 sonographic examinations were included in the study from January
1, 2015 until September 30, 2023. Analyzing the total number of examinations performed
in the pre-pandemic time from January 2015, the average number of sonographic examinations
per month and center was n = 1051.6. In the pandemic time (initial and post-initial
period) from January 2020 to April 2022, a significantly lower number of examinations
(742.7) (p = 0.01) per month and included center was performed ([Fig. 1])[
1
].
Fig. 1 Summary of examination numbers. Bar chart of the number of sonographic examinations
performed at three of the four included centers from 2015 to 2023 (color-coded). Line
graph of the average number of examinations performed. Center 3 was excluded from
the annual analysis due to missing pre-pandemic values before 2018 as well as the
comparison to post-pandemic time due to a potential bias.
b) Detailed analysis of the annual examination numbers in the individual periods of
the pandemic:
The detailed monthly analysis of the number of examinations from June 2018 to September
2023 shows a sharp decline from an average of just over 700 examinations per month
and center to an all-time low of 383 examinations in April 2020. From this point on,
more examinations were conducted and for the first time in June 2020, more than 700
examinations were performed on average ([Fig. 2]).
Fig. 2 Center-specific monthly examination averages. Average number of examinations per
month and center (color-coded bar charts) as well as the average number of examinations
of all centers (black line).
It should be noted that the monthly average numbers cannot be directly transferred
to the annual average numbers presented above, as another center that performed relatively
fewer sonographic examinations compared to the other centers was included from June
2018 onwards.
The average number of examinations per center and month before the COVID-19 pandemic
was n = 698, at the time of the initial pandemic outbreak from the end of December
2019 to July 2020 it was n = 591, and in the period after the initial pandemic-related
decline in examination numbers it was n = 648 (post-initial pandemic period; significantly
less than in the pre-pandemic period; p < 0.05; [Table 1]). Looking at the individual centers, there is a similar effect for Center 1 and
Center 3 (p < 0.05), whereas the number of examinations in the post-initial pandemic
period in Center 2 and Center 4 has returned to the pre-pandemic level (p > 0.05;
[Table 1]).
Table 1
Report of the number of cases per month in the defined periods as well as the percentage
in relation to the pre-pandemic period. Pre-pandemic period: January 2015 – January
2020. Initial pandemic period: January 2020 – June 2020. Post-initial pandemic period:
June 2020 – April 2022. Late pandemic period: Mai 2022 – April 2023, Post-pandemic
period: Mai 2023 – September 2023.
|
Pre-pandemic period
|
Initial pandemic period
|
% pre
|
Post-initial pandemic period
|
% pre
|
Late pandemic period
|
% pre
|
Post-pandemic period
|
% pre
|
|
Cologne
|
984.47
|
775.67
|
78.79
|
833.82*
|
84.70
|
967.67
|
98.29
|
1106.23
|
112.364
|
|
Würzburg
|
882.84
|
774.67
|
87.75
|
879.27
|
99.60
|
798.75
|
90.47
|
845.45
|
95.76
|
|
Mannheim
|
685.68
|
490.17
|
71.49
|
632.59*
|
92.26
|
669.42
|
97.62
|
692.66
|
101.01
|
|
Frankfurt
|
240.74
|
324.33
|
134.73
|
242.00
|
100.52
|
292.00
|
121.29
|
315.61
|
131.02
|
|
Mean of all centers
|
698.43
|
591.21
|
84.65
|
648.06*
|
92.79
|
681.96
|
97.64
|
739.95
|
105.94
|
In a linear univariate regression analysis for the three different time intervals,
the number of examinations in the pre-pandemic period is prognostically constant,
the number of examinations in the initial pandemic period is markedly decreased, and
the number of examinations in the post-initial period is prognostically slightly decreased
(for the corresponding equations and coefficients, [Fig. 3]).
Fig. 3 Regression analysis of monthly exam averages by time periods of the pandemic. Linear
univariate regression analysis for the pandemic periods based on the average number
of examinations per month and the included center.
In the late pandemic period (from May 2022 to April 2023), the average number was
n = 681.9, which shows no significant difference (p = 0.25) from the pre-pandemic
phase, and in the post-pandemic phase (from May 2023 to September 2023), the average
was n = 739.9, which is numerically more yet not significantly higher than the pre-pandemic
phase (p = 0.056; [Fig. 2] and [Table 1]). In all centers, the average number of monthly examinations in the late pandemic
phase was not different from the pre-pandemic phase, with the exception of one center
(Center 2), which still showed significantly fewer examinations compared to the pre-pandemic
period ([Table 1]). In the post-pandemic phase (from May 2023 to September 2023), all included centers
did not perform significantly fewer examinations than in the pre-pandemic period.
Center 1 was able to conduct significantly more examinations with an average of n = 1106.2
compared to n = 984 in the pre-pandemic period (approximately 112 %; p = 0.001). Similarly,
Center 4 performed significantly more examinations with n = 315.6 compared to n = 240.7
(approximately 130 %; p = 0.001; [Table 1]).
Discussion
On the one hand, the COVID-19 pandemic brought a decrease in ultrasound examinations
due to the need to keep emergency and intensive care capacities available and, on
the other hand, to keep the probability of infection as low as possible. To the best
of our knowledge, this is the first study to show this quantitatively, based on the
example of four large radiology departments at German university hospitals focusing
on ultrasound examinations. Recent research demonstrated a substantial decrease in
overall radiological examinations during the initial period of the pandemic, with
trauma and orthopedics emerging as the most affected specialties [14]. In subsequent periods an increase in the total number of examinations was shown
[17]. This change in trend was particularly evident in CT imaging, which saw a significant
rise, likely due to its pivotal role in COVID-19 diagnostics [18].
In line with this, our data show that the COVID-19 pandemic led to a significant reduction
in ultrasound examinations in Germany. Furthermore, it was demonstrated that the number
of ultrasound examinations in the post-initial pandemic period was slightly decreased.
However, it is noteworthy that in Center 3, there was initially a brief increase in
the number of examinations from the pre-pandemic period to the initial pandemic period.
In this particular case, this might have been due to the relatively low utilization
of sonographic examinations in the center, so that there was no immediate need to
broadly cancel these examinations. The possible reasons for the initial decline in
the number of examinations are evident and described in the introduction of this paper.
Nevertheless, after the initial phase of the pandemic, the sustained decrease in the
number of examinations indicates that there has been a lasting change in the utilization
of ultrasound within the participating radiology departments throughout the pandemic.
A possible explanation for this might be that delays in ultrasound-related diagnostics
during the COVID-19 pandemic may have led to more patients being referred to alternative
imaging methods for both urgent and routine assessments. Moreover, the pandemicʼs
impact on elective ultrasound examinations prompted a shift in how medical departments
managed admissions, with primary care physicians possibly taking on examinations typically
conducted by the radiology department (for example, the examination of lymph nodes
in oncological patients). Additionally, the postponement or cancellation of examinations
might have contributed to a decline in patient compliance [13]
[14]
[15].
In the analysis of the late pandemic and post-pandemic phases, it has been observed
that the prolonged decline in ultrasound examinations had normalized to pre-pandemic
levels by September 2023 across all participating centers. Notably, some centers have
even recorded an increase in examination numbers. Further analyses should determine
whether this trend will continue.
In this context, the current study is limited by only recording the number of examinations
conducted; future studies should document the specific reasons for omitted examinations
as well as any potential alternative options. Moreover, the extent to which logistical
changes in the various participating centers might have additionally influenced the
number of examinations is not recorded. For the purpose of “pandemic preparedness”,
it is crucial to understand the reasons for the cancellation of examinations. This
knowledge would enable effective adaptation of examination protocols in the event
of another pandemic, incorporating other departments for ultrasound examinations,
and maintaining the best possible healthcare provision for other groups, such as oncological
patients, even under pandemic conditions.
Conclusion
In summary, the prolonged decline in sonographic examinations during the pandemic
does not represent a lasting trend, as evidenced by the return to pre-pandemic levels.
Further investigation is essential to understand in detail the factors behind this
temporary reduction.
Clinical relevance of the study
-
Due to the increasing number of COVID-19 infections since spring 2022, the patient
care workflow underwent changes in Germany.
-
To minimize face-to-face exposure and reduce infection risk, non-time-critical elective
medical procedures were postponed.
-
Therefore, the number of ultrasound examinations performed declined significantly
during the pandemic in all included centers.
-
The prolonged decline in sonographic examinations during the pandemic does not represent
a lasting trend, as evidenced by the return to pre-pandemic levels.
Funding
Bundesministerium für Bildung und Forschung
Project RACOON, NUM 2.0, FKZ: 01KX2121
