Abstract
Influenza D virus (IDV), a new member of the influenza virus family, was first reported in 2011 in swine in Oklahoma, USA, and then soon found in cattle across North America and Eurasia. Earlier studies suggested cattle serve as natural reservoir for IDV. The goal of this study is to perform a retrospective study looking at sera collected from Nebraska beef herds in 2003–2004 and 2014 for evidence of IDV antibodies. Results showed that all 40 randomly selected farms (2003–2004) we tested contained IDV seropositive adult animals and that approximately 98% of newborn calves (2014) had high levels of maternal antibodies against IDV. This study suggested that IDV exposures were present in Nebraska beef cattle since at least 2003.
Keywords: Influenza D virus, Serological surveillance, seroprevalence, Nebraska, cattle, influenza virus
1. Introduction
Since its identification in 2011, influenza D virus (IDV) has been isolated from cattle and/or swine in the United States, China, France, Italy, and Japan, and serologic evidence suggests it may also be affecting small ruminants such as goats and sheep (Chiapponi et al., 2016; Collin et al., 2015; Ducatez et al., 2015; Ferguson et al., 2015; Hause et al., 2014; Hause et al., 2013; Jiang et al., 2014; Murakami et al., 2016; Quast et al., 2015). Laboratory studies demonstrated cattle, swine, ferrets, and guinea pigs are susceptible to IDV infection (Collin et al., 2015; Ferguson et al., 2016; Hause et al., 2014; Hause et al., 2013; Sreenivasan et al., 2015). Serologic assays in two independent studies showed that IDV could potentially infect humans, although seropositivity rates in the studies differed. One of the studies reported 91% seropositivity among 35 persons working with cattle (White et al., 2016), and the other reported only 1% seropositivity among 741 persons with suspected high exposure to IDV (Eckard, 2016). Nevertheless, epidemiologic, serologic, and pathologic studies have suggested cattle are the primary natural reservoir for IDV (Collin et al., 2015; Ducatez et al., 2015; Ferguson et al., 2015; Ferguson et al., 2016; Hause et al., 2014; Jiang et al., 2014).
A previous study in young calves reported that 94% of newborn calves had high levels of maternal antibodies against IDV, which decreased in the next six months, leading to the increasing susceptibility to IDV (Ferguson et al., 2015). Laboratory studies suggested that IDV can be efficiently transmitted in cattle, with viral replications in the upper and lower respiratory tracts (Ferguson et al., 2016). An earlier study suggested that IDV was detected at higher frequency in cattle with bovine respiratory disease (BRD) than healthy cattle (Ferguson et al., 2015), which was consistent with the findings in two metagenomic studies (Mitra et al., 2016; Ng et al., 2015).
Although cattle are proposed as the natural reservoir for IDV, the natural history of IDV and the extent of IDV prevalence in bovine population is not yet clear. Evolutionary analyses of five gene segments suggested that IDV could have diverged from those in influenza C virus, another member in the Orthomyxoviridae family, from approximately 300 to over 1,200 years ago (Sheng et al., 2014). A serological study reported that IDV was circulating in Mississippi beef cattle as early as 2004. In this study, we aim to investigate the seroprevalence of IDV among randomly selected beef cattle farms in Nebraska between 2003 and 2004.
2. Materials and Methods
2.1. Viruses
D/bovine/Mississippi/C00013N/2014 (D/13N) and D/bovine/Mississippi/C00046N/2014 (D/46N) used in serological assays were genetically separated into two reported clusters of IDVs, which were also antigenically different (Collin et al., 2015; Ferguson et al., 2015).
2.2. Bovine serum samples
From September 2003 to May 2004, a total of 15,402 bovine serum samples were collected from 73 beef cattle farms, in which the total number of cattle were 20,865, across 42 counties in Nebraska [(Smith et al., 2005), Figure 1]. All cattle were 2 years or older. Using these convenient samples, to evaluate the prevalence of IDV, we randomly selected 40 farms representing the 73 farms sampled (Figure 1). From each farm, we selected 4 to 10 samples for serological testing. A total of 293 serum samples were analyzed for the presence of IDV antibody. If at least one serum sample is positive for each farm, by assuming these herds to be representative of beef cattle farms in Nebraska at the time, we would have 95% confidence that the prevalence of seropositive herds was 91% to 100%.
Figure 1.
Geographic distribution of the 40 Nebraska farms where the testing samples were collected (2003–2004).
To evaluate the contemporary situation of IDV in cattle of Nebraska, we collected sera from 242 calves from one farm in the spring of 2014. These sera were collected from the same animals at 1 week post-birth, and again at approximately 3 months later. Measurement of the presence of IDV antibody in these paired sera can help evaluate the status of maternal antibodies against IDV in these sera thus the status of IDV exposure in the bovine herds.
2.3. Hemagglutination (HA), Hemagglutination inhibition (HI) and neutralization inhibition (NI) assays
The HA and HI assays were performed against D/13N and D/46N using 0.5% turkey RBC as described elsewhere (Ferguson et al., 2015). The NI assays were performed against D/46N in HRT-18G cells. Simply, serial dilutions of a serum were prepared and mixed with an equal volume of 100 TCID50 influenza virus. Virus and diluted serum were incubated for 1 hour at 37°C, and 200μL of mixture were transferred to a 96-well cell culture plate of HRT-18G cells and incubated for 5 days at 37°C with 5% CO2. The viral titers were determined by HA assay as described elsewhere (Ferguson et al., 2015). The highest dilution of serum that prevents HA is called the NI titer of the serum. A serum sample was determined as seropositive when the HI or NI titer ≥ 1:40.
3. Results and Discussion
Results showed that 235 out of 293 (80.2%) bovine serum samples were seropositive against D/13N and that 237 out of 293 (80.9%) against D/46N (Table 1). Overall, there were 240 samples (81.9%) seropositive against D/13N, D/46N, or both. Among the samples we tested from each farm, the HI titers were as high as 1:1280 against at least one of the tested IDVs (Table 2). Interestingly, three samples were seropositive against D/13N but seronegative against D/46N whereas five samples were seropositive against D/46N but negative against D/13N. Among the 232 samples seropositive to both D/13N and D/46N, 80 samples had a higher titer against D/46N and 33 against D/13N, and 119 samples had the same titer. The log2 difference between the HI titers against D/13N and D/46N for those samples, which did not share the same titer (n = 113), was 1.09 (±0.29) (±standard deviation)], suggesting there were likely two antigenic clusters of IDV circulating in these Nebraska cattle herds (Collin et al., 2015).
Table 1.
Cross-reactive antibody responses against D/13N and D/46N in the bovine sera samples from Nebraska (2003–2004).
| Farm | Sampling date | D/13N | D/46N | Overall | ||
|---|---|---|---|---|---|---|
|
|
|
|||||
| GMT(lowest titer-highest titer) b | Seropositive (%)c | GMT (lowest titer-highest titer)b | Seropositive (%)c | |||
| J5(10) | 10/17/03 | 160 (40–640) | 90.0 | 246 (160–640) | 80.0 | 90.0 |
| J6(10) | 10/17/03 | 160 (80–320) | 80.0 | 103 (40–160) | 80.0 | 80.0 |
| J7(6) | 10/17/03 | 226 (160–320) | 66.7 | 160 (160–160) | 66.7 | 66.7 |
| J8(6) | 10/21/03 | 160 (160–160) | 16.7 | 113 (40–320) | 33.3 | 33.3 |
| J9(6) | 10/21/03 | 80 (40–160) | 66.7 | 80 (40–160) | 50.0 | 66.7 |
| J10(8) | 10/22/03 | 160 (80–320) | 50.0 | 121 (40–320) | 62.5 | 62.5 |
| J14(10) | 10/28/03 | 160 (80–320) | 80.0 | 146 (40–320) | 80.0 | 80.0 |
| J17(10) | 10/31/03 | 177 (80–320) | 70.0 | 190 (40–320) | 80.0 | 80.0 |
| J18(10) | 10/31/03 | 243 (160–320) | 100.0 | 211 (160–320) | 100.0 | 100.0 |
| J19(8) | 10/31/03 | 215 (80–640) | 87.5 | 215 (80–640) | 87.5 | 87.5 |
| J20(8) | 10/31/03 | 269 (160–320) | 100.0 | 226 (160–320) | 100.0 | 100.0 |
| J23(7) | 11/4/03 | 177 (40–320) | 100.0 | 160 (40–320) | 100.0 | 100.0 |
| J25(10) | 11/6/03 | 173 (40–1280) | 90.0 | 235 (80–640) | 90.0 | 90.0 |
| J26(10) | 11/7/03 | 147 (80–640) | 80.0 | 320 (160–640) | 80.0 | 80.0 |
| J28(7) | 11/10/03 | 143 (80–320) | 85.7 | 180 (80–320) | 85.7 | 85.7 |
| J31(10) | 12/5/03 | 147 (40–320) | 80.0 | 190 (40–320) | 80.0 | 80.0 |
| J33(5) | 11/19/03 | 95 (80–160) | 80.0 | 190.3 (160–320) | 80.0 | 80.0 |
| J34(10) | 11/19/03 | 195 (80–320) | 70.0 | 238 (160–320) | 70.0 | 70.0 |
| J35(10) | 12/3/03 | 226 (40–640) | 80.0 | 177 (80–320) | 70.0 | 70.0 |
| J36(10) | 11/21/03 | 139 (80–320) | 50.0 | 160 (80–320) | 50.0 | 50.0 |
| J37(8) | 11/21/03 | 160 (80–320) | 87.5 | 131 (80–320) | 87.5 | 87.5 |
| J38(10) | 11/24/03 | 215 (80–320) | 70.0 | 173 (40–320) | 90.0 | 90.0 |
| J39(5) | 11/26/03 | 226 (160–320) | 80.0 | 381 (320–640) | 80.0 | 80.0 |
| J45(4) | 12/4/03 | 113 (40–160) | 100.0 | 226 (80–320) | 100.0 | 100.0 |
| J48(9) | 12/8/03 | 173 (40–320) | 100.0 | 173 (40–320) | 100.0 | 100.0 |
| J54(7) | 12/22/03 | 184 (40–640) | 71.4 | 279 (40–640) | 71.4 | 71.4 |
| J55(6) | 12/31/03 | 184 (40–640) | 83.3 | 279 (80–640) | 83.3 | 83.3 |
| J56(5) | 10/23/03 | 113 (80–160) | 80.0 | 226 (160–320) | 80.0 | 80.0 |
| J57(7) | 1/22/04 | 95 (40–320) | 57.1 | 113 (80–320) | 57.1 | 57.1 |
| J60(6) | 2/25/04 | 320 (320–320) | 83.3 | 368 (320–640) | 83.3 | 83.3 |
| J62(8) | 2/27/04 | 190 (40–640) | 100.0 | 269 (80–640) | 100.0 | 100.0 |
| J63(5) | 3/1/04 | 121 (40–640) | 100.0 | 211 (40–640) | 100.0 | 100.0 |
| J64(6) | 3/8/04 | 243 (160–640) | 83.3 | 243 (160–640) | 83.3 | 83.3 |
| J66(5) | 3/12/04 | 226 (160–320) | 80.0 | 320 (320–320) | 80.0 | 80.0 |
| J67(6) | 3/31/04 | 160 (80–320) | 100.0 | 285 (160–320) | 100.0 | 100.0 |
| J68(5) | 4/14/04 | 269 (160–640) | 80.0 | 381 (320–640) | 80.0 | 80.0 |
| J69(5) | 4/22/04 | 320 (160–640) | 80.0 | 538 (320–640) | 80.0 | 80.0 |
| J70(5) | 4/26/04 | 190 (40–320) | 80.0 | 269 (80–640) | 80.0 | 80.0 |
| J71(5) | 5/4/04 | 279 (80–640) | 100.0 | 320 (160–640) | 100.0 | 100.0 |
| J72(5) | 5/21/04 | 135 (40–320) | 80.0 | 135 (40–320) | 80.0 | 80.0 |
Note:
The 40 farms listed were selected randomly from 73 farms we sampled in Nebraska;
only those sera with a HI titer of 1:40 or more are used to calculate the GMT and the lowest and highest titers are measured from those sera with a HI titer of 1:40 or more;
seropositive rate was calculated based on those samples whose HI titers ≥1:40 for either D/13N or D/46N;
overall seropositive rates was calculated based on those samples whose HI titers ≥1:40 for D/13N, D/46N, or both.
Table 2.
Neutralization assays for the highest and lowest HI titer samples.
| Farm IDa | Sample IDb | HI titerc
|
NI titer d
|
|
|---|---|---|---|---|
| D/13N | D/46N | D/46N | ||
| J5(10) | 150 | 640 | 640 | 80 |
| 104 | 10 | 20 | 20 | |
| J6(10) | 51 | 320 | 160 | 160 |
| 110 | 20 | 20 | 10 | |
| J7(6) | 23 | 320 | 160 | 40 |
| 177 | 10 | 20 | 10 | |
| J8(6) | 169 | 160 | 320 | 80 |
| 30 | <10 | 10 | 10 | |
| J9(6) | 28 | 160 | 160 | 40 |
| 1 | 10 | 20 | 10 | |
| J10(8) | 229 | 320 | 320 | 160 |
| 116 | <10 | <10 | <10 | |
| J14(10) | 85 | 320 | 320 | 160 |
| 33 | 20 | 20 | 10 | |
| J17(10) | 52 | 320 | 320 | 320 |
| 94 | <10 | <10 | <10 | |
| J18(10) | 311 | 320 | 320 | 160 |
| 127 | 160 | 160 | 80 | |
| J19(8) | 156 | 640 | 640 | 160 |
| 85 | 20 | 20 | <10 | |
| J20(8) | 143 | 640 | 320 | 160 |
| 64 | 160 | 160 | 80 | |
| J23(7) | 129 | 320 | 320 | 80 |
| 71 | 40 | 40 | <10 | |
| J25(10) | 2 | 1280 | 640 | 320 |
| 119 | <10 | <10 | <10 | |
| J26(10) | 98 | 640 | 640 | 160 |
| 110 | <10 | <10 | <10 | |
| J28(7) | 116 | 320 | 320 | 80 |
| 117 | 20 | 20 | 10 | |
| J31(10) | 230 | 160 | 320 | 80 |
| 217 | <10 | <10 | 20 | |
| J33(5) | 128 | 80 | 320 | 80 |
| 6 | 20 | 20 | 20 | |
| J34(10) | 136 | 320 | 320 | 320 |
| 179 | <10 | <10 | <10 | |
| J35(10) | 110 | 640 | 320 | 80 |
| 59 | <10 | 20 | 10 | |
| J36(10) | 93 | 160 | 320 | 160 |
| 26 | <10 | <10 | <10 | |
| J37(8) | 93 | 320 | 320 | 80 |
| 122 | <10 | <10 | <10 | |
| J38(10) | 76 | 320 | 320 | 80 |
| 26 | 20 | 40 | <10 | |
| J39(5) | 7 | 160 | 320 | 160 |
| 11 | 10 | 20 | 20 | |
| J45(4) | 70 | 160 | 320 | 160 |
| 71 | 40 | 80 | 10 | |
| J48(9) | 208 | 320 | 320 | 160 |
| 180 | 40 | 40 | 20 | |
| J54(7) | 275 | 640 | 640 | 160 |
| 92 | 20 | 10 | <10 | |
| J55(6) | 39 | 640 | 640 | 160 |
| 26 | <10 | <10 | <10 | |
| J56(5) | 19 | 160 | 320 | 80 |
| 97 | 20 | 20 | 10 | |
| J57(7) | 140 | 320 | 320 | 80 |
| 23 | <10 | <10 | <10 | |
| J60(6) | 27 | 320 | 640 | 160 |
| 55 | 10 | 20 | <10 | |
| J62(8) | 5 | 640 | 640 | 320 |
| 33 | 40 | 80 | 20 | |
| J63(5) | 133 | 640 | 640 | 80 |
| 130 | 40 | 40 | 20 | |
| J64(6) | 14 | 640 | 640 | 320 |
| 101 | 10 | 20 | 20 | |
| J66(5) | 316 | 320 | 320 | 80 |
| 278 | 10 | 20 | 20 | |
| J67(6) | 110 | 320 | 320 | 320 |
| 88 | 80 | 160 | 160 | |
| J68(5) | 9 | 640 | 640 | 160 |
| 133 | 10 | 20 | 10 | |
| J69(5) | 26 | 640 | 640 | 80 |
| 28 | 20 | 20 | 20 | |
| J70(5) | 82 | 320 | 640 | 160 |
| 96 | <10 | <10 | <10 | |
| J71(5) | 72 | 640 | 640 | 320 |
| 15 | 80 | 160 | 40 | |
| J72(5) | 95 | 320 | 320 | 160 |
| 274 | <10 | <10 | <10 | |
Note:
The 46 farms listed were selected randomly from 73 farms in Nebraska;
Two samples with the highest and lowest HI titers were selected for neutralization inhibition assays;
HI assays were performed against two prototype viruses D/13N and D/46N using 0.5% turkey red blood cells;
NI assays were performed in human rectal tumor (HRT-18G) cells against the prototype virus D/46N.
Cattle from all of the 40 farms had evidence of IDV exposure in the period between September 2003 to May 2004, and these farms were geographically located across Nebraska (Figure 1). By assuming these herds to be representative of those in Nebraska at the time, we would have 95% confidence that the state prevalence of seropositive herds was 91% to 100%. The seropositive rates varied among farms from 16.7% to 100% against D/13N and from 33.3% to 100% against D/46N.
To confirm the HI titers, neutralization inhibition (NI) assays were performed against two serum samples from each farm, one with the highest HI titer and one with the lowest. Results showed that 44 out of 50 samples with an HI titer ≥ 1:40 also had a NI titer ≥ 1:40 and that only two samples with a HI titer ≥ 1:40 against D/13N and/or D/46N had a NI titer <1:10 against D/46N (Table 2). Results further confirmed the samples seronegative against D/13N and/or D/46N were seronegative against D/46N in NI assays.
To evaluate the current situation of IDV in cattle of Nebraska, we tested the presence of IDV antibody in paired sera from 242 calves in 2014. These sera were collected from the same animals at 1 week post-birth, and again at approximately 3 months later. HI results showed that 98% of sera samples collected from 1-week-old calves were seropositive against D/46N with a GMT of 1:648, ranging from <1:10 to 1:1280. Three months later, 76% calves remained seropositive against D/46N with a GMT of 1:127, ranging from <1:10 to 1:640. For most calves, the HI titers decreased between one week and three months. Only one calf had an increase in HI titer, which rose from 1:10 to 1:40. These results suggest that these newborn calves have high levels of maternal antibodies against IDV and that IDV is likely to still be prevalent in the beef cattle population in Nebraska.
In addition to the state of Mississippi (MS) (Ferguson et al., 2015) and Oklahoma (OK) (Hause et al., 2013), IDV seems to be present across a number of states in the United States. A serological surveillance study using 141 bovine sera from 8 different farms, from each of which 11 to 27 serum samples were collected, from South Dakota (SD), Vermont (VT), Pennsylvania (PA), Idaho (ID), and California (CA) in the United States, reported 7 out of 8 tested farms were IDV positive (Hause et al., 2014). In addition, IDVs were detected using quantitative PCR in nasal swabs, pharyngeal swabs, or lung tissue samples collected from sick cattle in Kansas (KS), Nebraska (NE), and Texas (TX) (Collin et al., 2015). In addition to beef cattle (Ferguson et al., 2015), using metagenomic approaches, IDV was detected in 62% of 50 samples collected from California dairy calves between 27 and 60 days of age (Ng et al., 2015). This study found that 100% of the beef cattle farms tested in Nebraska had IDV exposure, further demonstrating the high prevalence of IDV infections in the bovine herds in the United States.
Similar to a previous study in Mississippi beef cattle (Ferguson et al., 2015), this study confirmed that Nebraskan beef calves had high levels of maternal antibodies against IDV, which gradually diminished with age. It seems likely that cattle are often seronegative by six months of age, the age when beef cattle are traded and transported to order-buyer facilities or feedlots. The waning of maternal antibodies can allow for a susceptible population of young beef cattle creating a permissive environment for IDV infection at a critical time. Thus, a susceptible population of young beef cattle in the order-buyer facilities or feedlots would allow active IDV transmission and generate the infection cycle and ecology for IDV infection. However, there is still a lack of knowledge regarding the transmission within the cattle herds on individual farms. The virus detection rate using quantitative PCR on the cattle with signs of respiratory disease from individual farms (208 samples from 12 states, primarily those in the Midwest; age unknown) was 4.8% (Collin et al., 2015), which is much lower than in order-buyer facilities (up to 23.8%), where cattle aged 6 to 9 months were sampled (Ferguson et al., 2015).
4. Conclusions
This study demonstrates that IDV was prevalent in Nebraskan cattle herds as early as 2003 and continues to circulate in Nebraska cattle. An earlier report of IDV was able to document the presence of IDV as far back as 2004 in two herds of Mississippi beef cattle, this study demonstrated serologic evidence of IDV in all 40 Nebraska beef herds tested as far back as 2003. Further risk assessment is needed to confirm the impacts of ubiquitous IDV exposure in bovine production, given the fact that bovine respiratory disease is the leading cause of economic loss to the beef industry in the United States, and to clarify what, if any, the potential risk IDV may pose to public health.
Acknowledgments
We are grateful to Kaijian Luo and Hailiang Sun for technical supports. We are also grateful to Liesel Schneider, Kathleen Barton, Bianca Quade, and Hui Wang for helping procure the archived samples. Lucas Ferguson is supported by NIH NIAID 1R15AI107702A-01.
Footnotes
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