Community-acquired pneumonia (CAP) is a common pulmonary infection in women of childbearing age [1]. Especially in pregnant women, CAP not only affects the body of pregnant women, but also affects the fetus [2, 3]. According to the diagnosis guidelines for CAP by the American Thoracic Society, patients can be diagnosed with CAP through clinical manifestations, pulmonary signs, and laboratory examinations. Among them, imaging examination is indispensable in the diagnosis of CAP. However, there is certain radiation whether it is chest CT or chest radio-graph. It has been reported that it is not recommended for pregnant women to have a larger chest radiograph and chest CT examination [4, 5, 6].

Therefore, in the diagnosis of pregnant women with CAP, whether there is a convenient, non-radiative, sensitive and specific imaging examination is particularly important. Color Doppler ultrasound is a convenient and non-radiative influential examination method. Some studies have shown that lung ultrasound is particularly sensitive to pathological changes, including gas, water, consolidation, etc. The ultrasound imaging changes of CAP are mainly pleural rupture and local pleural effusion [4, 7, 8, 9]. Community-acquired pneumonia has acoustic characteristics without echo or uneven echo [5, 6, 10, 11, 12, 13]. The most typical sign is the bronchial aeration sign. Whether the application of pulmonary ultrasound to CAP diagnosis of pregnant women is better than or consistent with chest X-ray and chest CT examination, can it be used as an alternative to chest X-ray and chest CT diagnosis of CAP in pregnant women? So we designed the following study to explore the accuracy of pulmonary ultrasound in the diagnosis of CAP in women of childbearing age, especially in pregnant women.

This study is an observational study of prospective cross-sectional design with women with suspected CAP in the childbearing age (20–45 years) who were treated in Jiangyou people’s Hospital. The study was approved by the Ethic Committee of Jiangyou People’s Hospital (No. RM097646). Patients signed a paper-based informed consent before participating in the study. This study strictly enforces the Standards for the Reporting of Diagnostic Accuracy Studies statement [12].

Patients aged 20–45 years who were clinically suspected of CAP were included in the study. The diagnosis of patients with suspected CAP includes clinical symptoms and typical signs (auscultation may be wet rales or bronchial breath sounds). The five suspected clinical symptoms of pneumonia included fever, cough, expectoration, chest pain, and dyspnea.

Suspected CAP women of childbearing age were grouped according to pregnancy or not, and they were divided into pregnant women group and non-pregnant women group. On the day of the visit (Day 0), a medical history of all suspected CAP patients, including concomitant diseases and risk factors, was recorded. The clinical symptoms of pneumonia in the suspected patients were evaluated on day 0 and day 7–10 after treatment, and the results of the examinations obtained at that time (mainly auscultation of the lungs) were recorded. All patients with suspected CAP in childbearing age underwent pulmonary ultrasonography on day 0. Non-pregnant women with suspected CAP should also underwent chest X-ray and chest CT examination on the same day. Non-pregnant women with suspected CAP of CT positive test and pregnant women with LUS positive test were given anti-infective treatment for 7–10 days. And then the non-pregnant women diagnosed with CAP, chest X-ray, LUS and chest CT examination and pregnant women with CAP suspected patients were reviewed their LUS. The pregnant patients were diagnosed by ultrasonic examination and sputum culture, and the discharge diagnosis in the discharge medical record was taken as the gold standard.

Exclusion criteria: hospital-acquired pneumonia; confirmed CAP or other disease; interval between lung ultrasound and chest radio-graph or low-dose lung CT over 24 h; sonographers learned chest and chest CT in advance results.

Lung ultrasound is performed by a sonographer who has been trained in lung ultrasound for more than two years, and it is done immediately after the patient is admitted to the hospital. At the time of ultrasonography, chest X-ray and chest CT findings were not returned or the sonographer was not informed of chest X-ray and chest CT findings. The ultrasonic instrument used a 3.5–5 MHz convex array probe and a 7.5 MHz linear probe. When the patient took the sitting position to collect the image of the back, the supine position was taken to collect the image of the chest. All lung ultrasound examinations were performed by an experienced sonographer for a systematic examination of all intercostal spaces.

Pulmonary ultrasound assessed the number, location, volume, and presence and absence of pleural fluid. The incidence of necrosis, the incidence of bronchial aeration, and the incidence of pleural effusion were recorded on the day of the visit and on day 7–10.

All patients underwent a posterior anterior or lateral chest radio-graph on the day of the visit, and the test was performed as much as possible on day 7–10. Radiologists were invited to read the film and the ultrasound results of the lungs are blinded.

All suspected patients required low-dose CT: chest CT plain scan, 20–40 mA, 120 kV, layer thickness 4 mm (multi-slice spiral CT, effective dose control at 0.4 mSv); or 50 mA, 120 kV, layer thickness 5 mm (linear CT; effective emission control at 1.2 mSv). Radiologists read the film and blinded the lungs and chest radio-graphs. Pulmonary ultrasound diagnosis of pneumonia based on: lung consolidation sign, dynamic bronchial inflation signs and pleural rupture sign. Pneumonia is diagnosed by more than one item.

The diagnostic value of pulmonary ultrasound and chest radio-graphs were evaluated by calculating sensitivity, specificity, positive predictive value, negative predictive value and likelihood ratio. If the ultrasound and chest radio-graphs were significantly different in sensitivity and specificity, the expansion was evaluated by the McNemar test. The characteristics of the lungs in pregnant and non-maternal lungs were compared and the K values were calculated to evaluate the consistency of pulmonary ultrasound, chest X-ray and chest CT findings. All of the above calculations were done using SPSS statistical software (version 17.0).

Between June 2014 and July 2018, a total of 331 patients were enrolled. A total of 36 patients were excluded, 8 of which were due to refusal to enroll, and 28 were due to incomplete data, loss of blindness, and loss of follow-up. The remaining 275 patients were examined and treated according to doctor’s advice. There were 188 non-pregnant women with suspected CAP who underwent chest X-ray, pulmonary ultrasound and chest CT on the day of admission. Among them, 165 were chest radio-graphs, 23 were chest radio-graphs, 74 were color ultrasound positive, 114 were color ultrasound negative and 140 were chest CT negative. 48 cases of chest CT positive, chest CT positive patients after treatment for 7–10 days, chest X-ray, color Doppler ultrasound and CT, including 44 cases of chest radio-graphs, 4 cases of positive. There were 33 cases of lung ultrasound negative, 15 cases of positive line, 12 cases of chest CT, and 36 cases of positive. 87 pregnant women with CAP suspected patients underwent lung color Doppler ultrasound examination on the day of admission, including 32 cases were positive and 55 cases were negative. Those who were positive were treated with color Doppler ultrasound after 7–10 days of anti-infective treatment, and 7 cases were positive and 25 cases were negative (Fig. 1).

Fig. 1.

Treated with color Doppler ultrasound after 7–10 days of anti-infective treatment.

The age of the patients was 20–45 years. The general characteristics of patients are shown in Table 1.

Chest CT was used as the standard for the diagnosis of CAP. At the time of initial diagnosis, 188 cases of suspected CAP were found in non-pregnant women, 74 cases were positive in lung ultrasound, and 114 cases were negative. The accuracy of pulmonary ultrasound in the diagnosis of community-acquired pneumonia was 87.9%. The sensitivity of pulmonary ultrasound to community-acquired pneumonia was 100%, the specificity was 84.34%, the positive likelihood ratio was 6.39, and the positive predictive value was 0.65. The predicted value is 1. Patients diagnosed with CAP were examined for lung color Doppler ultrasound and chest CT after 7–10 days of anti-infective treatment. The patient’s lung ultrasound was positive in 15 cases and negative in 33 cases. The accuracy of pulmonary ultrasound in the diagnosis of community-acquired pneumonia was 94.12%, and the sensitivity of pulmonary ultrasound to community-acquired pneumonia was 100% and the specificity was 92.31%. The positive likelihood ratio was 13, and the positive predictive value was 0.8 and the negative predictive value was 1.

Compared with pulmonary ultrasound, 23 cases of pneumonia were diagnosed by chest radiography at the time of initial diagnosis, and no abnormalities were found in 165 suspected patients. The accuracy of chest radiography in the diagnosis of community-acquired pneumonia was 88.26%. The sensitivity of chest radiography for community-acquired pneumonia was 65.75%, specificity was 100%, negative likelihood ratio was 2.92, positive predictive value was 1, and negative predictive value was 0.85. Patients diagnosed with CAP were treated with chest X-ray and chest CT after 7–10 days of anti-infective treatment. The patient’s chest radio-graph was positive in 4 cases and negative in 44 cases. The accuracy of chest radiography for community-acquired pneumonia was 85.71%, and the sensitivity of chest radiography for community-acquired pneumonia was 60% and specificity was 100%. The negative likelihood ratio was 2.5, the positive predictive value was 1, and the negative predictive value was 0.82 (Table 2).

Chest CT in 188 patients were analyzed. In the 188 suspected patients, the sensitivity of lung ultrasound (100%) was higher than that of chest radio-graphs (65.75%), and the specificity of chest radio-graph was better than that of lung ultrasound (ultrasound: 84.33%; Chest X-ray: 100%).

Compared with chest X-ray results, 25 patients who were diagnosed by pulmonary ultrasound were missed by chest radiography at the time of initial diagnosis, and 26 patients who were excluded by chest X-ray were misdiagnosed by lung ultrasound. Calculate the k value as 0.691, 0.578. Ultrasound, chest radio-graph, and chest CT were reviewed in 48 patients diagnosed with CAP by chest CT. A total of 37 patients with consistent results were found in 33 patients: none of the 33 patients had abnormalities detected; 4 patients had abnormal signs. At the time of the follow-up, 8 patients diagnosed by pulmonary ultrasound were missed by the chest radio-graph, and 3 patients who were excluded by chest X-ray were misdiagnosed by lung ultrasound. Calculate the k value as 0.895, 0.425.

At the time of initial diagnosis, 87 patients with suspected CAP in pregnant women had 32 cases of pulmonary ultrasound positive and 55 cases of negative (Fig. 2). Suspected patients with ultrasound-positive CAP were examined for lung color Doppler ultrasound after 7–10 days of anti-infective treatment. The patient’s lung ultrasound was positive in 7 cases and negative in 25 cases. In the case of non-pregnant women (87 pregnant women), at least 1 positive consolidation was found in the lung ultrasound. There are positive findings on the chest radio-graph, and there are also positive findings on chest CT. Pulmonary ultrasound in patients (3.1%) showed false positive results. The patient’s lung ultrasound showed a false negative result. The median area of lesion surface area in non-pregnant patients was 5.88 cm [2], and the median depth was 2 cm. There is a bronchial aeration sign in only 20.21% patients (Fig. 3). There is a bronchial filling sign. What is the median area of lesion surface area in pregnant women 5.76 cm [2]. There is a bronchial aeration sign in only 20.21% patients (Fig. 2). There is a bronchial filling sign. After anti-infective treatment in CAP or LUS+ pregnant woman, the median number of symptoms and signswere diagnosed at the time of initial diagnosis. It can also be confirmed by pulmonary ultrasonography (Table 3). On the 7th–10th day after anti-infection, the proportion of non-patients with bronchial aeration sign from the time of initial diagnosis 20.21% reduced to 14.58%, pregnant women from the time of initial diagnosis 24.14% reduced to 6.25%, non-pregnant lung lesion area from 5.88 cm [2] reduced to 0.52 cm [2]; the area of lung lesions in pregnant women from 5.76 cm [2] reduced to 0.55 cm [2]. All of the above lung ultrasound test data are recorded (Table 4).

Fig. 2.

Images before and after treatment. (A) Before treatment. (B) After treatment.

Fig. 3.

Images of lung consolidation and bronchial aeration.

In pregnant women and non-pregnant women, a total of lung areas in pregnant women showed positive lung consolidation results in the lungs. On average, each patient had a lung area, and non-pregnant women had a total of lung areas. Ultrasound in the lungs showed positive lung consolidation results, with an average of one lung area per patient. The diagnostic accuracy and diagnostic value of pulmonary ultrasound in different lung regions were shown in Fig. 4 and Table 5. The characteristics of pregnant women and non-pregnant women in different lung areas were shown in Table 6.

Fig. 4.

Image reviewed after half a month.

Clinical diagnosis of community-acquired pneumonia often requires chest X-ray or chest CT to diagnose, and chest CT is the gold standard for the diagnosis of community-acquired pneumonia. However, both chest X-ray and chest CT have radiation exposure and cannot be used for the diagnosis of community-acquired pneumonia in pregnant women. Ultrasound in the lungs is non-radiative, easy to operate, non-invasive, and many studies have shown that the ultrasound imaging of gas and liquid in lung ultrasound is very accurate. Researchers have also evaluated lung-acquired ultrasound in children and adults with community-acquired pneumonia and found that pulmonary ultrasound is consistent with chest radiography in the diagnosis of community-acquired pneumonia [9]. However, there have been no reports on the use of pulmonary ultrasound in community-acquired pneumonia in pregnant women. When diagnosing a disease, the vast majority use a likelihood ratio greater than 10 or less than 0.01 to confirm or exclude [13]. In our study, we divided suspected CAP women of childbearing age into two groups, the pregnant group and the non-pregnant group. Sensitivity was determined by calculating sensitivity, specificity, positive likelihood ratio, negative release ratio, positive predictive value, and negative predictive value for lung ultrasound in women with non-pregnant women of childbearing age. Studies have shown that the sensitivity of lung ultrasound is significantly higher than that of chest radio-graphs. The specificity of chest radio-graphs is superior to that of lung ultrasound. The positive likelihood ratio at the initial referral is 6.39, 13 respectively. It is suggested that pulmonary ultrasound is superior to the initial diagnosis in the prognosis of CAP in non-pregnant women of childbearing age. At the time of initial diagnosis, 25 patients diagnosed by pulmonary ultrasound were missed by chest radio-graphs, and 26 patients who were excluded by chest X-ray were misdiagnosed by lung ultrasound. Forty-eight patients who were diagnosed with CAP by chest CT were examined with ultrasound. The chest radio-graph and chest CT were consistent with 37 patients, and 33 patients were not detected abnormally; 4 patients were found to have abnormal signs in 8 cases. Patients diagnosed by pulmonary ultrasound were missed by chest radio-graphs, and 3 patients who were excluded by chest X-ray were misdiagnosed by lung ultrasound.

Pulmonary ultrasound can also be used as a means of detecting CAP consolidation in women of childbearing age. Reissig A et al. found that the mean volume of lung consolidation in the lungs after 10 days of follow-up was 41.31 cm${}^2$ and 11.84 cm${}^2$, respectively [13]. Caiulo et al. reviewed the lung consolidation size reduction and even complete remission in 91.6% of patients with pulmonary ultrasound after 3–6 days. It can be speculated that the rate of decline in lung consolidation size (or volume calculation) can be used to assess efficacy. We also explored CAP consolidation in women of childbearing age, non-pregnant group on day 1, 7–10. The median short axis of the long axis is 24.5, 24, 9.5, 5.5. On the first day of the pregnant women group, the median short axis of the 7–10 days long axis was 24, 24, 8.5, 6.5. There was no significant difference between the pregnant women group and the non-pregnant women group. Compared with adult CAP, there was no significant difference in the volumetric variation of the pregnant women group.

Ho found bronchial aeration in 93.7% of children with socially acquired pneumonia. The results of bronchial aeration in adults with CAP in Reissig A. were 70%–97%. We found that only 24.14% of newly diagnosed pregnant women with bronchoacoacia, and Iuri et al. revealed that 10/28 (36.3%) of the children hospitalized for emergency pneumonia were found to have bronchial aeration [14]. These differences may indicate a consolidation of the lung, and the bronchial aeration sign is a multivariate.

In our experiments, we found that a total of 35 lungs in pregnant women showed positive lung consolidation results in the lungs, with an average of 1.09 lungs per patient. A total of 91 lungs in non-pregnant pregnant women showed positive lungs in the lungs. The results of consolidation showed an average of 1.23 lungs per patient. Reissig A, et al. found that adult CAP areas showed positive lung consolidation results in lung ultrasound, on average per patient. In the lung area, pregnant women’s CAP is compared with adult CAP.

Moreover, pleural rupture is one of the criteria for pneumonia. Pleural effusion is only a concomitant manifestation, not a standard. It has been reported that more than three B lines can be used as signs of pneumonia. We found that the error of the results was large, and the B line was not taken as the standard. It is also possible that more than three b-lines are not included, resulting in the decrease of specificity of our results.

This study calculated the sensitivity, specificity, positive predictive value, negative predictive value, negative release ratio, and positive release ratio of CAP in patients with childbearing age, and compared with the value of the chest X-ray. These results indicated that pulmonary ultrasound can be used as the primary means of diagnosing CAP in women of childbearing age. In summary, pulmonary color Doppler ultrasound can be used as an effective and convenient imaging method for diagnosing CAP, and it is an important means of diagnosis and treatment for CAP diagnosis in pregnant women.

CAP, Community-acquired pneumonia; LUS, Lung ultrasound.

JW, XZ and GW: conceptualization, investigation, analysis. WL, HG and JG: investigation, analysis. GF and JR: manuscript preparation.

All subjects gave their informed consent for inclusion before they participated in the study. The study was conducted in accordance with the Declaration of Helsinki, and the protocol was approved by the Ethics Committee of Jiangyou People’s Hospital (approval number No. RM097646).

Thanks to all the peer reviewers for their opinions and suggestions.

This research received no external funding.

The authors declare no conflict of interest.