key: cord-257099-8k28vkgf
authors: Fan, Jingchun; Liu, Xiaodong; Shao, Guojun; Qi, Junpin; Li, Yi; Pan, Weimin; Hambly, Brett D.; Bao, Shisan
title: The epidemiology of reverse transmission of COVID-19 in Gansu Province, China
date: 2020-05-12
journal: Travel Med Infect Dis
DOI: 10.1016/j.tmaid.2020.101741
sha: 
doc_id: 257099
cord_uid: 8k28vkgf

BACKGROUND: The transmission of COVID-19 is about to come under control within China, however, an emerging challenge to the Chinese authorities is reverse transmission due to COVID-19 patients/carriers evacuating from overseas to China. METHODS: We analysed the epidemiological characteristics of 311 Chinese citizens evacuated from Iran. All confirmed COVID-19 cases amongst the returnees were displayed by the spatial distribution pattern of the extent of COVID-19 infection. RESULTS: Characteristics that differed significantly amongst these returnees compared to the original infected cohorts in Gansu were mean age, occupation and sex. Differences observed between infected patients and non-patients amongst returnees were age, sex, race, occupation, the use of facemasks, and residential situation in Iran. The clinical features that were significantly related to infection were chill, shortness of breath, chest pain and nausea. Spatial distribution pattern analysis indicated that infected returnees had resided within Iranian provinces that had experienced high levels of COVID-19. The spatial distribution of the original homes of these returnees before departure for Iran demonstrated that returnees will largely return to northwest China, to regions that have only experienced low levels of infection within China. CONCLUSION: Blocking the reverse transmission of COVID-19 is critical in preventing a secondary outbreak of COVID-19.

Quarantine of the People's Republic of China, now requires that a mandatory 14 days quarantine is 92 to be applied to anyone entering China from abroad from countries that have had COVID-19 93 patients till further notice [12] . 94

On 2 nd March 2020, there were 978 confirmed COVID-19 cases and 385 new cases in Iran with the 95 mortality rate of 5.5% [13] . To provide support to Chinese citizens who are currently overseas in 96 significant COVID-19 outbreak regions, to minimize their risk of COVID-19 infection, the Chinese 97 government has sent charter planes to evacuate Chinese citizens from a number of 98 COVID-19-affected countries, particularly Italy [14] and Iran [15] to designated provinces. A total 99 of 311 overseas Chinese citizens were returned from Iran, arriving at Lanzhou, the capital of Gansu 100

Province on 3 and 4 March 2020, to escape this international epicenter of COVID-19, and also to 101 provide COVID-19-affected patients with better medical care [15] . 102

Thus, the most urgent task/challenge for the Chinese quarantine authority (CDC equivalent) has 103 been to identify possible/actual COVID-19 infected patients and/or people highly suspected of 104 developing a COVID-19 infection, to enable quarantine of these high risk individuals, to minimise 105 possible reverse transmission of COVID-19 from overseas to the Chinese population. We report 106

here the epidemiological characteristics and the clinical features of 311 Chinese people evacuated 107 from Iran to the quarantine centre of Gansu Province. We aim to provide critical and objective 108 information to help control the spread of COVID-19 to other provinces and countries. 109 110 5

There were a total of 311 Chinese overseas citizens evacuated from Iran. All of these returnees had 113 resided in provinces within Iran that had experienced high levels of local COVID-19 disease. None 114

of the returnees had been tested or clinically screened for COVID-19 prior to their return to China. 115

These returnees were quarantined in Lanzhou, Gansu Province upon arrival. On arrival at Lanzhou 116 airport in Gansu Province, the returnees were isolated in a designated hotel and screened using 117 clinical tools i.e. thermometer, and questions concerning any symptoms, any history of close 118 contact with any known infected people or any persons with symptoms suggestive of COVID-19. 119

All of the returnees were tested using a swab of the oral/nasopharynx for PCR testing for the 120 

The statistical analysis included demographic characteristics, exposure history, clinical symptoms, 137 and pre-existing illness. Median (IQR) was used to describe the ages of the returnees and 138 case-patients due to the data being not normally distributed. For categorical variables, if expected 139 cell sizes were <5, the Fisher exact test was used to compare the frequency between or among 140 groups; otherwise, the χ 2 test was used. A two-sided α of less than 0.05 was considered statistically 141 significant. Statistical analyses were performed using the SAS software, version 9.4, unless 142 otherwise indicated. 143

This study has been approved by the Ethics Committee of the Affiliated Hospital of Gansu 145 University of Chinese Medicine (no. 20200201). 146 7 3. Results 148

There was a total of 311 overseas Chinese evacuated from Iran to Gansu Province, China, arriving 150 on 3-4 March ( Figure 1 ). Most of these returnees were students (82%, 255/311). Their 151 demographics were: male vs female 209 vs 102, age range 3 months to 77 years, median age was 23 152 years (IQR: 20, 26). The ethnicity of the majority of these returnees (78%, 242/311) is from the Hui 153 race whose religious background is Islamic. There were 37 COVID-19 laboratory confirmed cases 154 (12%, 37/311) among the returnees until 14 March 2020 (first 10-11 days after arrival in Gansu) 155 and no more new cases up to date. Most of the cohort were between 20-35 years old, because most 156 are students studying in Iran, with the exception of 18 children, who were 3 months to 3 years old, 157 and 6 people who were > 50 years old. Of the positive 37 cases, there were only 17 or 23 persons 158 who believed that they had no close contact with either COVID-19 symptomatic persons or 159 COVID-19 patients, respectively. Among a total of 311 returnees, there was a significant positive 160 correlation between the incidence of COVID-19 infection and male sex (χ 2 =11.615, p=0.001), 161 younger age (16-30 y) (p=0.014), Hui/other races (p=0.026), or residing in a dormitory (χ 2 =4.088, 162 p=0.043) ( Table 1) . Paradoxically, we also observed that wearing a facemask while in Iran 163 increased the risk for COVID-19 infection (χ 2 =7.902, p=0.005) ( Table 1) . 164

Among the 37 confirmed COVID-19 patients, the age ranged from 18 to 29 years, median 23 years 166 (IQR: 22, 25). There were 2 cases that developed into a critical condition (5%, 2/37 COVID-19 167 cases) in the period till 21 March 2020. 168

We further analysed differences in clinical symptoms and pre-existing illnesses as a function of 169 COVID-19 status between the infected patients and non-infected returnees. The clinical 170 presentations included fever, chill, cough, stuffy nose, running nose, sore throat, headache, fatigue, 171 dizziness, muscle pain, joint pain, shortness of breath, dyspnoea, chest stress, chest pain, 172 conjunctivitis, nausea, vomiting, diarrhoea, and stomach ache. Significant differences were 173 observed for the following symptoms: chill (p=0.038), shortness of breath (p=0.038), chest pain 174 (p=0.038) and nausea (p=0.038), comparing the infected patients and non-infected returnees (Table  175 2). Pre-existing diseases amongst all the returnees included hypertension, diabetes mellitus, 176 cardiovascular diseases, asthma, chronic obstructive pulmonary disease, lung cancer, chronic renal 177 and liver diseases, and immunodeficiency diseases. However, there was no difference in the 178 presence of pre-existing disease between the infected patients and non-infected returnees. 179

The original places of residence of these 311 returnees were from 25 provinces or municipalities in 181

China, mainly within the north west of China, e.g. Ningxia Hui Autonomous Region (87, 28%), 182

Gansu Province (60, 19%) and Henan Province (48, 15%) ( Figure 2 ). Prior to their evacuation from 183

Iran, the majority of these returnees had been living in Qom Province (108, 35%), Tehran Province 184 Our data are consistent with the reports above, demonstrating that most of these returnees from Iran 232 were young adult international students, who would be expected to have strong immune systems 233 and few co-morbidities. However, in the current study, the infection rate was extraordinarily high 234 among the 311 returnees, being 12% (37/311), compared to the rates in the general population in 235

Gansu of 0.35 per 100,000 or < 0.001% (92/26,257,100). The 12% infection rate amongst the 236 returnees was also much higher than that of a symptomatic secondary attack rate of 0.45% (95% 237 acknowledge that the explanation for the higher infection rate among these 311 returnees may be 240 mainly due to two possible reasons: firstly, the relative lack of self-protection or, secondly, lack of 241 sanitisation during the early stages of spread during their stay in Iran. 243

Additionally, it is likely that the Iran government has experienced difficulties scaling up its 244 response to combating the epidemic due to the economic loss and supply issues caused by the after an apparently asymptomatic infection [31] . Thus, a substantial threat could occur in the 275 community if such COVID-19 case(s) are misdiagnosed and these returnees are allowed to 276 eventually proceed to their final destination(s) after 14 days quarantine. Although the infection rate 277 was high (12%), there was a relatively low severe/critical attack rate among these returnees from 278

Iran with only 2 (5%), which was far below the results from Jiangxi Province (18%) [32] and Gansu 279 Province (17.1%) within China [7] . However, this rate is close to the age-based rate published 280 recently by Imperial College London of approximately 1.2% of patients requiring hospitalisation in 281 the age range 20-29 years [33] . Our explanation for such a difference might be due to most of the 282 returnees were male students, which may be mainly due to the Universities preference for religious 284 study in Iran [34] . Interestingly, the attack rate of COVID-19 amongst females was rather less than 285 male (1:4.5) in our current study, which is very different from the reports in the general population 286 There was 15% rate of COVID-19 cases amongst international students, which is substantially Paradoxically, our data show that the COVID-19 infection rate was greater amongst those who 306 wore masks while in Iran (24% infection rate) compared to those who did not wear masks (10% 307 infection rate). We speculate that this observation may be related to several factors: firstly, returnees 308 who chose to wear masks may have been involved in activities that placed them at greater risk of 309 exposure, for example, living in dormitories, attending university classes and mosques. All three of 310 these activities were identified in this study as increasing the risk of infection. By comparison, those 311 returnees who chose not to wear masks may have been largely involved in low risk activities, for 312 example, house-bound spouses engaged in domestic duties and childcare. Secondly, those who 313 wore masks may have over-estimated the effectiveness of the masks in preventing infection, and 314 thus may have neglected other measures to avoid infection, such as social distancing and scrupulous 315 hygiene. Thirdly, the masks may not have met P2/N95 standards for use against viral infections 316 and/or the technique for using the masks may have been inadequate, for example, touching the 317 outside of the mask after use or multiple uses of the same mask. We note that recommendations 318 concerning the mass wearing of masks remains controversial [39], and we urge caution in the 319 application of our data in relation to this issue. 320

Apparently, prior to and during the evacuation, many of these returnees were not fully aware who 321 was/were COVID-19 patients, particularly since a number of them (27, 9%) were asymptomatic 322 prior to their return, with their clinical presentations occurring during the current study. Therefore, 12 considerable caution should be exercised in screening for COVID-19 infection based only on 324 clinical presentation. 325

Our data further confirm that among the reverse transmission COVID-19 returnees, the clinical 326 presentations, including chill, shortness of breath, chest pain and nausea were still the typical 327 manifestations for COVID-19, in comparison with presentations of COVID-19 within the local 328

Chinese population. Furthermore, the transmission routes is/are likely to still be similar to the local 329 routes, i.e. the droplet inhalation and faecal-oral routes [40] . Currently, the quarantine approach 330 used at the airport and/or on the airplane is primarily based on the measurement of body 331 temperature only, which is unlikely to be sufficient; alternative more sensitive and specific 332 screening approaches are urgently needed. However, we acknowledge that there does not seem to 333 be another more appropriate screening measurement that is more sensitive and similar in cost 334 available at this stage. 

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Address for correspondence: Shisan Bao, Discipline of Pathology


