Radiological & clinical findings in sporadic cases hospitalized for H1N1 pneumonia

The Egyptian Journal of Radiology and Nuclear Medicine xxx (2017) xxx–xxx

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Original Article

Radiological & clinical findings in sporadic cases hospitalized for H1N1 pneumonia Osama Lamie Nakhla a,⇑, Salah Ahmed Ali b, Eman Farouk Dola c, Amr Mohammad Al Sharawy d a

Department of Radiology, Faculty of Medicine, Beni Sueif University, Egypt Mouwasat Hospital, Jubail Industrial City, Saudi Arabia c Radiology Department, Faculty of Medicine, Ain Shams University, Egypt d Ain Shams University, Mouwasat Hospital, Jubail Industrial City, Saudi Arabia b

a r t i c l e

i n f o

Article history: Received 7 October 2016 Accepted 15 January 2017 Available online xxxx Keywords: CT scan of the chest GGO Consolidation H1N1 pneumonia

a b s t r a c t Purpose: To evaluate the CT and clinical findings in patients with H1N1 pneumonia and to discuss any differences between our results and previously reported articles. Patients and methods: Screening for cases was started in April 2015. First case was diagnosed in October 2015. The number of cases increased with Peak in December. We reviewed and analyzed the primary CT patterns and the clinical presentation. Results: Our patients were more prevalence in the age ranges from 30 to 60 years, equally distributed in both sex. Cough & fever (94%) were the most frequent clinical presentation .The commonest CT finding was the patchy Ground-glass appearance (either alone or associated with other findings) found in 11 cases (69%) followed by Consolidation in 10 patients (63%). The lung affection was bilateral in 14 patients (88%), multifocal in 13 patients (81%), Peripheral location was in 10 patients (62%). Out of the 16 positive cases in CT scan, the X-ray showed positive findings in only 12 cases (75%). Conclusions: The most common lung pattern in H1N1 was GGO and consolidation, with bilateral and multifocal involvement in the majority of cases showing peripheral tendency. X-ray missed about 25% of cases. Ó 2017 The Egyptian Society of Radiology and Nuclear Medicine. Production and hosting by Elsevier. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/ 4.0/).

1. Introduction The first two cases of the 2009 pandemic influenza A (H1N1) virus was diagnosed by the Centers for Disease Control and Prevention (CDC) in the United States, Which was newly discovered swine origin influenza A virus (S-OIV). Then it was identified in Mexico, Canada and elsewhere. This was followed by spread of H1N1 throughout the world [1]. And the World Health Organization (WHO) declared in July 2009 that H1N1 reached pandemic level [2]. However the decrease in number of patients infected by H1N1 after 2009, It was reported by many studies that the virus was circulating with other seasonal viruses [3]. In 2015 there was a resurgence of H1 N1 infection in Saudi Arabia.

Peer review under responsibility of The Egyptian Society of Radiology and Nuclear Medicine. ⇑ Corresponding author. E-mail address: [email protected] (O.L. Nakhla).

The clinical presentations were variable (flu-like symptoms as fever, cough, sore throat, body aches, headache, chills, and fatigue) as well as nausea, vomiting, and/or diarrhea had been frequently reported [4]. Diagnostic imaging based on chest radiography and computed tomography (CT) was very useful in the study of disease because it allowed to assess the extent of lung parenchymal damage [5]. The purpose of this study was To describe and analyze the primary CT findings as well as the clinical presentation of confirmed cases of H1N1 pneumonia. 2. Patients and methods This was retrospective study included 16 hospitalized patients, 8 female and 8 male with their age ranged from 10 months to 86 years. All the patients were confirmed to have H1N1 pneumonia at our hospital in Saudi Arabia from October 2015 to March 2016. Our work had ethical approval from the hospital ethical committee.

http://dx.doi.org/10.1016/j.ejrnm.2017.01.006 0378-603X/Ó 2017 The Egyptian Society of Radiology and Nuclear Medicine. Production and hosting by Elsevier. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Please cite this article in press as: Nakhla OL et al. . Egypt J Radiol Nucl Med (2017), http://dx.doi.org/10.1016/j.ejrnm.2017.01.006

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O.L. Nakhla et al. / The Egyptian Journal of Radiology and Nuclear Medicine xxx (2017) xxx–xxx

10

9

9 8 7 6 5

4

4 3

2

2

Aug-15 Sep-15 Oct-15 Nov-15 Dec-15

Jan-16

2 1 0

0

0

0

Apr-15 May-15 Jun-15

0

Jul-15

0

0

1

1

Feb-16 Mar-16

Fig. 1. Time distribution of the cases.

Table 1 Age distribution of H1N1 pneumonia patients. Age group

Number of cases

Percentage of cases (%)

0–15 16–30 31–45 46–60 61–75 76–90 Total

1 2 4 5 3 1 16

6 12.5 25 31 19 6 100

presentation, risk factors, possible complications and laboratory findings. Chest X-ray and CT were done to all cases to identify new pulmonary infiltrates.

2.1. Radiographic evaluation

The records of patients with confirmed H1N1 who presented with influenza like symptoms such as fever >38C, headache, running nose, cough, sore throat, breathlessness, hemoptysis, myalgia, diarrhea and vomiting were reviewed. Nasal and pharyngeal swabs from suspected cases were tested for H1N1 by RT PCR (Roche, Germany) at the Ministry of health regional laboratory in the eastern province, Saudi Arabia. Nasal swabs were tested for influenza antigen at our hospital using rapid immunofluorescence technique. A confirmed patient with H1N1pneumonia was considered if the patient had influenza-like symptoms and the respiratory sample positive for H1N1 influenza A virus by RT-PCR. During the study period, the clinical profile of our patients were analyzed with reference to sex, age, and time distribution, clinical

100%

94%

All the CT chest were done using 128 multislice CT machine (SOMATOM Perspective, SIEMENS Technology). 14 patients did non-contrast CT chest, only two patients did contrast study for the suspicion of pulmonary embolism. All the CT examinations were done within 2 days of patient admission. Two patients only did follow up CT during their period of admission. All the patients did X-ray examination (PA view) at time of admission with different number of follow up X-rays during the period of admission.

2.2. CT chest protocol 2.2.1. Adult patients CT chest was done with the following parameters kV 130, M.A 80, FOV 395 & slice thickness 5 mm for mediastinum window, followed by reconstruction for lung window with slice thickness 3 mm. Scan time was 4.7 s.

94%

90% 75%

80%

69%

70% 60% 50%

56% 50% 38%

40% 30%

25%

20% 10%

13% 6%

6%

6%

6%

0%

Fig. 2. Clinical presentation of the studied patients.

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O.L. Nakhla et al. / The Egyptian Journal of Radiology and Nuclear Medicine xxx (2017) xxx–xxx Table 2 Risk factors for H1N1 pneumonia patients. Risk factor

Numbers

Percentage of cases (%)

Diabetes Hypertension IHD B asthma Tuberculosis Obesity Total

4 2 2 4 0 4 16

25 12.5 12.5 25 0 25 100

2.2.2. Child CT chest was done with the following parameters kV 80, M.A 70 & slice thickness was 3 mm for mediastinum window, followed by reconstruction for lung window with slice thickness 3 mm. Scan time was 3.5 s. 2.3. CT data analysis All CT chest were transferred to a workstation (syngo.via – 3D reading and advanced visualization, SIEMENS) equipped with a software designed for image reconstruction. CT axial and multiplanar reconstructions (MPR) were analyzed. CT images were evaluated with a mediastinal window (width 350 HU, window 40 HU) and for lung window (width 1500 HU, window –700 HU).Two radiologists (blinded) analyzed the CT findings. The differences between them were resolved by consensus. The CT chest examinations were assessed for: (A) The main pattern of lung affection (ground glass opacity (GGO)), alveolar space consolidation, nodular pattern, peribronchial wall thickening, and interstitial thickening), presence of pleural effusion and lymphadenopathy. (B) The extent of lung affection (uni or bilateral), the distribution of abnormalities was categorized as focal or multifocal. (C) Abnormality was further divided into central, peripheral or mixed (random). (D) The chest X-ray was interpreted as negative or positive. 3. Results Time Wise Distribution of Cases: We started screening case with suspected H1N1 pneumonia in April 2015. The first case of

H1N1 pneumonia was diagnosed in October 2015 and the number of cases increased steadily with Peak in December which correlated with the seasonal influenza epidemic during winter (Fig 1). Total of 19 patients test positive for H1N1 by RT PCR, from them only 16 patients proved to have H1N1 pneumonia (included in the study). The other three patients were excluded (one patient showed normal CT chest, another patient did only X-ray and was normal, the third one escaped without doing either CT or X-ray). Most of our patients were in the age groups 30–60 years (Table 1). They were distributed equally in both sex (8 male and 8 female). The most common clinical manifestations were cough & fever (94%) followed by malaise (75%), myalgia (69%), breathlessness (56%), headache (50%) and sore throat (38%) (Fig. 2). Obesity, diabetes and bronchial asthma (25%) were the most common risk factors for H1N1 pneumonia. None of the females affected was pregnant (Table 2). Only 25% of our cases were positive by immunofluorescence influenza test at time of hospitalization (false negative). There was no history of definite exposure to H1N1 case in our patients. One patient developed ARDS and respiratory failure needed mechanical ventilation. His condition deteriorated further and required extracorporeal oxygenation. He was transferred to Ministry of health center with facilities to provide ECMO. He died after two weeks of treatment. The most common CT pattern was GGO (alone or in combination with other findings) were seen in 11 patients (69%). It is seen associated with consolidation in 5/11 patients (45%), with alveolar space nodules in 4/11patients (36.4%), with interstitial thickening in 3/11patients (27.3%), with bronchial thickening in 3/11patients (27.3%), and with pleural effusion in 2/11patients (18.2%) (Table 3). The second most common finding was alveolar space Consolidation were found in 10/16 patients (63%). Air space nodules were found in 6/16 patients (37.5%). Bronchial wall thickening was also seen in 6 patients (37.5%), Interstitial thickening (reticular pattern) was seen in 4/16 patients (25%), Pleural effusion was found in 2/16 patients (12%). No pathologically enlarged lymph nodes (Fig. 3). The lung affection was bilateral in 14/16 patients (88%), The lesions were multifocal in 13/16 patients (81%), Peripheral location was found in 10/16 patients (62%). Out of the 16 positive cases in CT scan, the X-ray showed positive findings in only 12/16 cases (75%). (Figs. 4 and 5) (see Fig. 6–8).

Table 3 Summarize the CT pattern, extend and distribution of primary lung lesion in our 16 patients. Patient Number

Ground glass

Consolidation

Nodular pattern

Bronchial thickening

Interstitial thickening

Pleural effusion

Axial distribution

Bilateralism

Focality

X-ray finding

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16

Positive Negative Negative Positive Positive Positive Negative Positive Positive Positive Positive Positive Positive Negative Positive Negative 11

Negative Positive Positive Positive Positive Positive Positive Positive Negative Negative Negative Negative Positive Positive Negative Positive 10

Positive Negative Negative Negative Negative Positive Positive Positive Positive Negative Negative Negative Negative Positive Negative Negative 6

Negative Positive Negative Negative Positive Negative Positive Negative Negative Positive Positive Negative Negative Positive Negative Negative 6

Negative Negative Negative Negative Negative Negative Negative Negative Positive Negative Positive Negative Negative Positive Positive Negative 4

Negative Negative Negative Negative Negative Negative Negative Negative Positive Negative Positive Negative Negative Negative Negative Negative 2

Random Random Peripheral Random Random Random Peripheral Peripheral Peripheral Peripheral Peripheral Peripheral Random Peripheral Peripheral peripheral 10

Unilateral Bilateral Unilateral Bilateral Bilateral Bilateral Bilateral Bilateral Bilateral Bilateral Bilateral Bilateral Bilateral Bilateral Bilateral Bilateral 14

Bi-focal Multi-focal Uni -focal Multi-focal Multi-focal Multi-focal Multi-focal Bi-focal Multi-focal Multi-focal Multi-focal Multi-focal Multi-focal Multi-focal Multi-focal Multi-focal 13

Negative Positive Negative Positive POSITIVE Positive Positive Positive Positive Negative Positive Negative Positive Positive Positive Positive 12

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O.L. Nakhla et al. / The Egyptian Journal of Radiology and Nuclear Medicine xxx (2017) xxx–xxx

68%

62% 43%

37%

25%

12%

Fig. 3. Incidence of different pattern of primary lung affection as seen in CT scan of the chest.

14 12 10 8 6 4 2 0 Mul-focal

Bi-focal

Uni-focal

Fig. 4. Distribution of lung insolvent as seen in CT.

70% 60% 50% 40% 30% 20% 10% 0% peripheral

central

Mixed paern

Fig. 5. CT axial distribution of primary lung lesions.

4. Discussion Influenza A (H1N1) virus symptoms had a lot of variation starting from mild influenza-like symptoms which is not different from seasonal influenza to community acquired rapidly progressive pneumonia which could progress to respiratory failure or even death [1]. Some observational studies had reported the radiological, clinical and laboratory features of H1N1pandemic in 2009. With most of the patients reported presented with severe form and in need for intensive care unit (ICU) admission [6].

The first 642 reported cases of influenza A (H1N1) were in the United States. The age ranged from 3 months to 81 years with 60% of them were 18 years of age or Younger [1]. Our patient’s age ranged from 10 months to 86 years, and most of our patients (56%) were in the age group 30–60 years, which was unusual in the seasonal flu. In our study, the main risk factors were obesity (25%), diabetes (25%) and asthma (25%).The prevalence of certain underlying conditions requiring hospitalization was similar to the pandemic 2009 H1N1 influenza A with obesity, bronchial asthma and diabetes being the most common risk factors [7].

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Fig. 6. Male patients 28 years old complaining of cough, fever, chest pain, head ache and myalgia. (a) Plain X-ray chest (PA) showed several patchy inhomogeneous opacities bilateral, more extensive on the right side. (b–e) axial CT scan of the chest lung window at different levels showing multiple confluent nodular areas of alveolar space consolidation, much more evident at the right upper lobe as well as several patchy areas of consolidation showing patent air bronchogram, more evident at the apical segment of the right lower lobe. (F and g) coronal reconstruction lung window showing extensive involvement of the right lung.

Fever and cough (94.7%) were the most common clinical manifestations followed by myalgia, malaise (73.6%), breathlessness (57.8%) headache and sore throat (47.3%), which was similar to U.S studies [8]. Regarding the clinical course of our patients in the hospital only one patient (6%) deteriorated and developed

respiratory failure. The only risk factor was multi-lobe involvement of radiology. In our study we noticed that patients with H1N1 virus who required hospitalization. The rapid influenza A test could identify only 25% of infected patients. With one patient giving history of

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Fig. 7. Female patient 28 years old complaining of fever, cough, headache, myalgia and malaise. (a) plain X-ray chest (PA) showing clear both lung field and CP angles. (b and c) axial CT chest mediastinal window showing mild left side pleural effusion. (d–g) axial, (h and i) coronal reconstruction CT scan of the chest in lunge window showing nodular and patchy areas of GGO with mild interstitial thickening involving the anterior and posterior segments of the right upper lobe and the medial segment of the right middle lobe.

positive exposure and no influenza vaccine received. These finding were reported in other studies [9]. In 2009 pandemic the Centers for Disease Control and Prevention (CDC) evaluation found that 40–60% of the virus was missed

by the rapid influenza test [10]. And it proved that rapid influenza test had increased sensitivity with specimens that had high levels of virus. However sensitivity decreased as the load of virus decrease in specimens. Data from patients infected with H5N1

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Fig. 8. Male patient 43 years old complaining of cough and fever, malise, chest pain and dysponea, the patients showed rapid deterioration needing for follow up CT. (a–d) axial CT chest lung window showing patchy areas of alveolar space consolidation, surrounded by GGO mainly involving the apical and basal segments of the right lower lobe, small area of GGO at the right middle lobe. Bronchial wall thickening with few tiny nodules are noted involving the left lung. e,f(lung window) (g and h) (mediastinal window) follow up axial CT 4 days later showing marked progression with newly devolved large areas of consolidation showing patent air bronchogram involving the right middle lobe as well as newly developed pleural effusion.

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influenza virus demonstrated a correlation of viral load with clinical outcome [11]. Our study also indicated the low sensitivity of the rapid influenza test .We found that negative rapid influenza test didn’t exclude H1N1 virus infection in patients with severe influenzalike illness. So starting antiviral therapy shouldn’t be affected by negative rapid test. The most common CT findings in our study were ground-glass opacities and alveolar space consolidations, which could be alone or associated with other findings in the same patient. Amoriam et al., (in their retrospective study of HRCT scan of 71 patients with H1N1 pneumonia, also found that, the most common pattern of lung affection were ground glassing, alveolar space consolidation and a combination of both [12]. Similar findings also were reported by Marchiori et al. in their study of 20 patients with H1N1 pneumonia, they found that, the most common HRCT findings were bilateral ground-glassing, bilateral alveolar patches of consolidation, or a mixture of both [13]. Many other researchers showed similar findings with different incidence [14,15] showing that GGO and consolidation are the predominant CT findings in H1N1 pneumonia patients. The reported incidence of GGO in patients with H1N1 pneumonia was constant finding yet it showed wide range of variation ranging from 12% to 85% [16–22,5,13,12]. In our study GGO was the most frequent pattern found in 11 patients (68%), our result was near to the incidence (65%) reported by Elicker et al. [19]. Our result were lower than the results reported by Lacalamita et al. [5], Marchiori et al. [13] and Amorim et al. [12], they reported higher incidence values, than ours, as they found Ground glass opacities in 79.2%, 80% and 85% of their cases respectively .Yet our results were much higher than the incidence value12% reported by Busi et al. [16] and 24% by Kosar et al. [23]. Although, the presence of GGO is not specific for influenza pneumonia and showed wide range of incidences, However, the recognition of ground opacity of peripheral distribution in symptomatic patients could be an early sign of H1N1 infection [5,24]. In our study consolidation was detected in 10/16 patients (63%). In literature, its incidence showed wide range of variation, Busi et al. [16] detected consolidation in only 5% of their patients, Lacalamita et al. [5] in 33.3%, Kosar et al. [23] in 53% and Elicker et al. [19] in 85% of their patients. Air space nodules were found in 6/16 (37.5%) of our patients, our incidence were higher than the incidence reported by Lacalamita et al. [5] and Amorim et al. [12] they found alveolar space nodules in 12.5% and 25% of their patients respectively. Our higher value could be due to different interpretation of airspace nodules, which could be interpreted as area of consolidation by some authors, or even could be missed by other pathologies especially in cases with extensive parenchymal involvement [12]. Bronchial wall thickening was found in 37.5% of our patients, which was higher than Amorim et al. [12] who had Bronchial wall thickening in 25% of their patients. Al Badrawy et al. [25] and Elicker et al. [19] found bronchial wall thickening in all of their patients, those two studies were involving the immune compromised patients who received prompt medical care and this support the suggestion of Tanaka et al. [26], who suggested that bronchial wall thickening happened in early disease course, When patient didn’t yet seek medical advice, So it was missed. So their high incidence (68%) was attributed to early seeking medical advice. In the present study Interstitial thickening (reticular pattern) was seen in 4 patients (25%), which is lower than the result of Busi et al. [16] and Lacalamita et al. [5] who found reticular interstitial thickening in 37% and 54% of their patients respectively. One the other hand our results were higher than the incidence (3%) reported by Agarwal et al. [17]. Lacalamita et al. [5] explained

the difference in incidence by disease severity. As they thought that reticular pattern go with more severe parenchymal affection. We found pleural effusion in two cases representing (12.5%), our result was lower than Coppola et al. [20] and Lacalamita et al. [5] as they found pleural effusion in 44.4% and 37.5% of their patients respectively. Yet our result was relatively higher than the result (10%) reported by Busi et al. [16] and Mineo et al. [22] who stated that pleural effusion was a H1N1 primary injury, on the opposite hand Coppola et al. [20] considered pleural effusion as a secondary complication by bacterial infection . Regarding the extent and distribution of lung affection in our study, the CT scans showed bilateral parenchymal affection in most of the cases (88%) and it was multifocal in 81% and Peripheral location in (62%) of our cases. Our results were almost similar to Amoriam et al. [12] they showed bilateral lung involvement in 89% and both lungs were affected similarly in 77% of their cases. Marchiori et al. [13] in their study found the lung affection was bilateral in all patients (100%) with multifocal sub-pleural distribution in (65%) of their patients. Rodrigues et al. [15] and Elicker et al. [19] also found in their studies that the most common lung distribution were bilateral and multifocal. In our study chest X-ray was negative in 4 cases out of the 16 positive cases in CT chest (25%) and under estimated the lung affection in most of the positive cases. Reittner et al. [27] stated that CT chest was very important especially in patients with normal or indeterminate chest X-ray who had high clinical suspicion of pneumonia, and to define complications or presence of mixed infections in patients not responding to treatment yet with known pneumonia. 5. Conclusion H1N1 virus infection couldn’t be ruled out using rapid influenza test. And the most common CT findings were ground glass opacity and alveolar consolidation or both together. Most cases showed bilateral and multifocal parenchymal involvement with tendency to peripheral distribution. Conflict of interest The authors declare that there are no conflict of interests. References [1] Novel Swine-Origin Influenza A (H1N1) Virus Investigation Team. Emergence of a novel swine-origin influenza A (H1N1) virus in humans. N Engl J Med 2009;360:2605–15. [2] World Health Organization. Transcript of statement by Margaret C, Director General of the World Health organization. [Date last accessed: August 3, 2010. Date last updated: June 11, 2009]. [3] Portal da Saúde [homepage on the Internet]. Brasília: Ministério da Saúde [updated 2012 Nov 7; cited 2012 Nov 14]. Boletim Informativo - Secretaria de Vigilância em Saúde - Influenza (gripe) - Semana Epidemiológica (SE) 44. Available from: . [4] Centers for Disease Control and Prevention. NovelH1N1 flu: background on the situation. . [Accessed September 29, 2009]. [5] Lacalamita MC, Salinaro E, Abrusci MR, et al. CT findings in patients affected by H1N1 influenza virus. Open J Radiol 2012;2:25–30. [6] Perez-P R, de la Rosa-Z D, Ponce de Leon S, et al. Pneumonia and respiratory failure from swine-origin influenza A (H1N1) in Mexico. N Engl J Med 2009;361:680–9. [7] McKenna JJ, Bramley AM, Skarbinski J et al. and for the 2009 Pandemic Influenza A (H1N1) Virus Hospitalizations Investigation Team. Asthma in patients hospitalized with pandemic influenza A(H1N1)pdm09 virus infectionUnited States, 2009.BMC Infect Dis. 2013; 13: 57. http://dx.doi.org/10.1186/ 1471-2334-13-57. [8] United States Centers for Disease Control and Prevention. Novel H1N1 flu: facts and figures. [Accessed October 6, 2009].

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