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Mortality Patterns Associated with Poult Enteritis Mortality Syndrome PEMS and Coronaviral Enteritis in Turkey Flocks Raised in PEMS Affected Regions Author s Donna K Carver Jean Pierre Vaillancourt Michael Stringham James S Guy and H John Barnes Source Avian Diseases Vol 45 No 4 Oct Dec 2001 pp 985 991 Published by American Association of Avian Pathologists Stable URL http www jstor org stable 1592878 Accessed 23 06 2014 07 45 Your use of the JSTOR archive indicates your acceptance of the Terms IFAT indirect fluorescent antibody technique PBS phosphate buffered saline PEMS poult enteritis mortality syndrome PEMS flocks positive for poult enteritis mortality syndrome SMT spiking mortality of turkeys TCV turkey coronavirus TCV flocks positive for turkey coronavirus TCV PEMS flocks positive for both turkey coronavirus and poult enteritis mortality syndrome Poult enteritis mortality syndrome PEMS is an economically devastating disease 1 2 To date many questions about the syndrome remain unanswered including its cause 3 4 5 7 8 11 12 13 14 transmission of causa tive agent s and control methods Because there is no specific diagnostic test PEMS is identified by a characteristic mortality pattern 2 The clinical syndrome associated with the two forms of PEMS has been characterized as excess mortality of turkeys EMT and spiking mortality of turkeys SMT 2 EMT is de fined as mortality greater than 2 for any 3 wk period excluding the first week during the brooding phase of production and SMT is de fined as mortality greater than 9 for any 3 wk period excluding the first week during the brooding phase of production PEMS has been associated with turkey coronavirus TCV in fections Areas having a higher incidence of TCV infection also typically have an increased incidence of PEMS Understanding the rela tionship of TCV to PEMS is important in or der to better understand the natural history of PEMS and to establish and maintain control efforts for PEMS The objectives of this study were to determine mortality patterns for flocks experiencing PEMS and or TCV infection in PEMS affected regions and to delineate the role of TCV in PEMS affected flocks MATERIALS AND METHODS Study design A prospective longitudinal study was conducted with commercial turkey flocks reared in two areas of North Carolina Both areas had his toric evidence of PEMS and TCV PEMS occurred in these areas starting in mid May and continuing through October Flocks were selected for the study on the basis of placement dates Flocks placed be tween May 15 and July 15 were eligible for inclusion in the study so they could be closely monitored for at least 6 wk with mortality data collection continu ing until processing Previous disease status with re gard to PEMS and TCV for individual farms was not revealed to investigators prior to flock selection Flocks from four commercial companies were mon itored Mortality Mortality was monitored daily and was reported as number of birds dead each day including cull birds Weekly mortality was used for the analysis 986 This content downloaded from 62 122 73 86 on Mon 23 Jun 2014 07 45 59 AM All use subject to JSTOR Terms and Conditions Mortality patterns associated with PEMS and TCV Table 1 Mortality for the different health status groups DifferenceA DifferenceA Health status Weeks 2 6 Weeks 7 13 Total weeks 2 6 weeks 7 13 Healthy 4 6 1 9 6 5 TCV 7 3 2 9 10 2 2 7 1 0 PEMS 12 0 2 6 14 6 7 4 0 7 TCV PEMS 10 3 4 5 14 8 5 7 2 6 ADifference in mortality percentage between infected group and healthy group and was calculated as the number of birds that died over a 7 day period This number was then divided by the number of birds placed and multiplied by 100 to obtain weekly mortality percentage TCV status TCV status was monitored for each flock by obtaining six blood samples per turkey house on each farm Age at first testing varied from 6 to 14 wk of age Serum collected from each flock was tested by an indirect fluorescent antibody test If any one serum sample tested positive for TCV antibodies the flock was called positive Flocks that tested neg ative were retested approximately 4 wk after the ini tial test and again before processing TCV antibody titers were determined for each serum by an indirect fluorescent antibody technique IFAT This test has proved reliable over the years in determining TCV status for turkeys and has been used as a gold stan dard in development of another serologic test for TCV 9 10 Antigen for the IFAT consisted of epi thelial cells exfoliated from the bursae of Fabricius of turkeys experimentally infected with TCV 6 TCV infected epithelial cells were spotted onto glass mi croscope slides air dried and fixed in cold 4 C absolute acetone for 10 min Twofold serum dilutions were prepared in phosphate buffered saline PBS starting at a 1 20 dilution Diluted sera were overlaid onto cells and incubated at 37 C for 15 min Slides were washed briefly in two changes of PBS and cells were overlaid with a 1 40 dilution of fluorescein iso thiocyanate labeled rabbit anti chicken immuno globulin G ICN Biomedicals Inc Costa Mesa CA Slides were incubated at 37 C for 15 min washed twice with PBS and examined by epifluores cence PEMS status PEMS status was determined with the use of clinical definitions previously provided by Barnes and Guy combining EMT and SMT into one category referred to as PEMS Mortality experienced the first week after placement was not included in the analysis because of possible effects of hatchery holding shipment and placement on mortality Mortality rates from weeks 2 6 8 42 days of age were analyzed and those flocks experiencing unex plained 3 wk cumulative mortality greater than 2 in weeks 2 4 3 and 4 or 4 6 were considered pos itive for PEMS A chi square test was used to determine if the oc currence of PEMS affected the timing of the first test for TCV Health status Flocks were categorized as healthy TCV positive TCV PEMS positive PEMS and TCV and PEMS positive TCV PEMS Healthy flocks were defined as those that experienced neither TCV nor PEMS throughout the life of the flock TCV flocks were those that tested positive for TCV but did not experience PEMS PEMS flocks were those that experienced PEMS but never tested positive for TCV Flocks that experienced PEMS and tested positive for TCV were classified as TCV PEMS RESULTS Healthy flocks Twenty four of the 54 tur key flocks remained healthy and did not sero convert to TCV or experience PEMS Healthy flocks had cumulative mortality rates Table 1 of 4 6 at 6 wk of age and 6 5 at 13 wk of age These rates equate to a cumulative mor tality increase of 1 9 between 6 and 13 wk of age in healthy flocks TCV Seventeen flocks tested positive for TCV antibodies TCV flocks had detectable antibodies on the first test at an average of 7 7 wk of age Of the 17 flocks with TCV anti bodies 10 experienced PEMS and are referred to as TCV PEMS flocks No correlation was found between age of first test and presence or absence of PEMS P 0 82 The seven remaining flocks with no evidence of PEMS are referred to as TCV TCV flocks experi enced greater mortality than did healthy flocks Mortality patterns differed for TCV flocks relative to healthy flocks Fig 1 Mortality in TCV flocks was essentially the same as in healthy flocks from week 2 through week 5 At week 6 mortality in TCV flocks started to increase above that for healthy flocks and re mained higher throughout the remainder of the 987 This content downloaded from 62 122 73 86 on Mon 23 Jun 2014 07 45 59 AM All use subject to JSTOR Terms and Conditions D K Carver et al 3 5 3 0 2 5 2 0 1 5 1 0 A TCV N 7 A Healthy N 24 A ALA A 0 5 0 0 1 2 3 4 5 6 7 8 9 10 11 12 13 Weeks Fig 1 Weekly mortality patterns of healthy and TCV positive turkey flocks growout period Cumulative mortality Table 1 was greater at 6 wk of age in TCV flocks mean 7 3 relative to healthy flocks mean 4 6 Cumulative mortality continued to diverge from the pattern seen in healthy flocks and averaged 10 2 in TCV flocks com pared with 6 5 in healthy flocks at 13 wk of age The cumulative mortality increase in TCV flocks between weeks 6 and 13 was 2 9 This increase was 1 greater than that expected for a healthy flock 3 5 3 0 II t 0 0 C 0 a L 4 CL 2 5 2 0 1 5 1 0 PEMS A total of 23 flocks experienced PEMS Of these 10 tested positive for anti bodies to TCV and are referred to as TCV PEMS flocks The remaining 13 flocks that experienced PEMS with no serocon version to TCV are referred to as PEMS flocks PEMS flocks experienced greater mortality than did healthy flocks Mortality patterns differed in PEMS flocks relative to healthy flocks Fig 2 Mortality in PEMS flocks was greater than in healthy flocks from PEMS N 13 Healthy N 24 i Xm vk 0 0 5 0 0 1 2 3 4 5 6 7 8 9 10 11 12 13 Weeks Fig 2 Weekly mortality patterns of healthy and PEMS positive turkey flocks 988 I 0 c L I I I I I I I I I I I I I I I This content downloaded from 62 122 73 86 on Mon 23 Jun 2014 07 45 59 AM All use subject to JSTOR Terms and Conditions Mortality patterns associated with PEMS and TCV TCV PEMS N 10 Healthy N 24 1 2 3 4 5 6 7 8 9 10 11 12 13 Weeks Fig 3 Weekly mortality patterns of healthy and PEMS and TCV positive turkey flocks placement and remained much higher until week 9 At weeks 6 and 7 the mortality began to approach that of healthy flocks By week 10 mortality patterns of PEMS and healthy flocks were essentially the same Cumulative mortality Table 1 was greater at 6 wk of age in PEMS flocks mean 12 relative to healthy flocks mean 4 6 Cumulative mortality was also greater at 13 wk of age in PEMS flocks mean 14 6 when com pared with healthy flocks mean 6 5 The cumulative mortality increase in PEMS flocks between weeks 6 and 13 was 2 6 This increase was 0 7 greater than expected for healthy flocks Flocks positive for PEMS and TCV Ten flocks were positive for both PEMS and TCV and are referred to as TCV PEMS flocks These flocks also experienced greater mortality than healthy flocks Mortality patterns differed in TCV PEMS flocks relative to healthy flocks Fig 3 Like the PEMS flocks mor tality in TCV PEMS flocks was greater than that in healthy flocks from placement then approached mortality levels for healthy flocks by week 8 Like the TCV flocks the mortality pattern for the TCV PEMS flocks started to diverge from the pattern of the healthy flocks at 9 wk of age and remained el evated throughout the remainder of the gro wout period in these flocks Cumulative mor tality Table 1 was greater at 6 wk of age in TCV PEMS flocks mean 10 3 rel ative to healthy flocks mean 4 6 Cu mulative mortality was also greater at 13 wk of age in TCV PEMS flocks mean 14 8 compared with healthy flocks mean 6 5 The cumulative mortality increase in TCV PEMS flocks between weeks 6 and 13 was 4 5 This increase was 2 6 greater than that in healthy flocks DISCUSSION Three basic mortality patterns were evident in clinically affected flocks One was associated with the brooding phase of production 6 wk of age one with the growout phase of pro duction 6 wk of age and one occurred in both brooding and growout periods Early in the brooding phase a mortality pattern started very high and remained relatively elevated for several weeks then gradually declined Fig 2 Once birds were moved to the growout phase of production the daily mortality curve was similar to that of healthy flocks This mortality pattern had only one peak and was typical for flocks that experienced PEMS The second mortality pattern was one that occurred later in the production phase and was persistent This 3 5 3 0 2 5 t 2 0 0 o r 1 5 0 1 0 0 5 0 0 I I 989 s o 4e v A This content downloaded from 62 122 73 86 on Mon 23 Jun 2014 07 45 59 AM All use subject to JSTOR Terms and Conditions D K Carver et al pattern began to diverge from the healthy flock curve after 6 wk of age Fig 1 This mortality pattern did not have a distinct peak and con tinued to slowly diverge from that of the healthy flocks throughout the remainder of the growout period Unlike the previous pattern this pattern did not approximate that of healthy flocks late in the production phase Birds in these flocks continued to experience increased mortality until market TCV flocks exhib ited this mortality pattern A third mortality pattern that was apparent in TCV PEMS flocks involved an increase in mortality very early followed by a merging with the healthy flock curve Fig 3 This brief merging was fol lowed by another increase during the growout phase This bimodal distribution was the ap parent result of both disease patterns occurring within the same flocks Cumulative mortality Table 1 for clinically affected flocks quantifies losses due to mortality Though the overall cumulative mortality clearly showed an increase in mortality for all health status groups again there were differences in mortality specific to health status and phase of production The role of TCV in PEMS and the existence of PEMS as a separate clinical disease are con troversial This study showed that TCV does play a role in some but not all cases of PEMS Of those flocks experiencing PEMS almost half did not have TCV Similarly about one fourth of TCV flocks did not experience PEMS Additionally this study provides evidence of mortality patterns that differ by health status PEMS flocks experienced mortality in the early phase of production and eventually exhib ited mortality equal to that of healthy flocks TCV flocks experienced mortality during growout and the mortality continued until pro cessing These mortality patterns are distinct and suggest that TCV can be a disease entity separate from PEMS The mortality of TCV PEMS flocks suggest that these were flocks that experienced PEMS in conjunction with TCV Mortality during brooding was similar to the that of PEMS flocks and mortality dur ing growout was similar to though more ex treme than that of TCV flocks Data from this study suggest that there are instances when TCV infection is superimposed on PEMS These data also show that there are situations when TCV plays no role in PEMS TCV appears to be neither necessary nor suf ficient to cause PEMS REFERENCES 1 Barnes H J and J S Guy Spiking mortality of turkeys SMT and related disorders an update In Proc 19th Annual North Carolina Turkey In dustry Days Conference North Carolina State Uni versity Raleigh NC pp 16 21 1995 2 Barnes H J and J S Guy Poult enteritis mortality syndrome spiking mortality of turkeys In Diseases of poultry 10th ed B W Calnek H J Barnes C W Beard L R McDougald and Y M Saif eds Iowa State University Press Ames IA pp 1025 1031 1997 3 Brown T P D R Howell A P Garcia and P Villegas Histological lesions of spiking mortality of turkeys SMT comparison of lesions induced by SMT organ suspension and cell culture J Am Vet Med Assoc 209 373 1996 4 Edens E W C R Parkhurst M A Qureshi I A Casas and G B Havenstein Atypical Esche richia coli strains and their association with poult en teritis and mortality syndrome Poult Sci 76 952 960 1997 5 Edens E W R A Qureshi C R Parkhurst M A Qureshi G B Havenstein and I A Casas Characterization of two Escherichia coli strains as sociated with poult enteritis and mortality syndrome PEMS Poult Sci 76 1665 1673 1997 6 Guy J S New methods for diagnosis of tur key coronavirus infections In Proc 49th North Central Avian Disease Conference and Symposium on Enteric and Emerging Diseases Indianapolis IN pp 8 10 1998 7 Guy J S Virus infections of the gastrointes tinal tract of poultry Poult Sci 77 1166 1175 1998 8 Guy J S L G Smith J J Breslin J P Vaillancourt and H J Barnes High mortality and growth depression experimentally produced in young turkeys by dual infection with enteropathogenic Escherichia coli and turkey coronavirus Avian Dis 44 105 113 2000 9 Loa C C T L Lin C C Wu T A Bryan H L Thacker T Hooper and D Schrader Detec tion of antibody to turkey coronavirus by antibody capture enzyme linked immunosorbent assay utiliz ing infectious bronchitis virus antigen Avian Dis 44 498 506 2000 10 Patel B L B S Pomeroy E Gonder and C E Cronkite Indirect fluorescent antibody test for diagnosis of coronaviral enteritis of turkeys blue comb Am J Vet Res 37 1111 1112 1976 11 Qureshi M A M Yu and Y M Saif A novel small round virus inducing poult enteritis 990 This content downloaded from 62 122 73 86 on Mon 23 Jun 2014 07 45 59 AM All use subject to JSTOR Terms and Conditions Mortality patterns associated with PEMS and TCV and mortality syndrome and associated immune al terations Avian Dis 44 275 283 2000 12 Schultz Cherry S D R Kapczynski V M Simmons M D Koci C Brown and H J Barnes Identifying agent s associated with poult enteritis mortality syndrome importance of the thymus Avi an Dis 44 256 265 2000 13 Yu M R N Dearth M A Qureshi and Y M Saif Viral agents associated with poult enteritis and mortality syndrome In Proc 79th Annual Con ference of Research Workers in Animal Diseases Chi cago IL p 42 1998 14 Yu M M M Ismail M A Qureshi R N Dearth H J Barnes and Y M Saif Viral agents associated with poult enteritis and mortality syn drome the role of a small round virus and a turkey coronavirus Avian Dis 44 297 304 2000 991 This content downloaded from 62 122 73 86 on Mon 23 Jun 2014 07 45 59 AM All use subject to JSTOR Terms and Conditions