Surgical findings and outcome for dairy cattle with jejunal hemorrhage syndrome: 31 cases (2000–2007)

Simon F. Peek Department of Medical Sciences, School of Veterinary Medicine, University of Wisconsin, Madison, WI 53706.

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Elizabeth M. Santschi Department of Surgical Sciences, School of Veterinary Medicine, University of Wisconsin, Madison, WI 53706.

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Michael A. Livesey Department of Surgical Sciences, School of Veterinary Medicine, University of Wisconsin, Madison, WI 53706.

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Mike A. Prichard Department of Surgical Sciences, School of Veterinary Medicine, University of Wisconsin, Madison, WI 53706.

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Sheila M. McGuirk Department of Medical Sciences, School of Veterinary Medicine, University of Wisconsin, Madison, WI 53706.

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Sabrina H. Brounts Department of Surgical Sciences, School of Veterinary Medicine, University of Wisconsin, Madison, WI 53706.

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Ryland B. Edwards III Department of Surgical Sciences, School of Veterinary Medicine, University of Wisconsin, Madison, WI 53706.

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Abstract

Objective—To describe signalment; surgical findings; short-, medium-, and long-term outcome; and recurrence rate for cattle undergoing celiotomy because of jejunal hemorrhage syndrome (JHS) and to analyze risk factors associated with outcome and recurrence.

Design—Retrospective case series.

Animals—31 dairy cattle with JHS.

Procedures—Medical records were analyzed. Follow-up information was obtained from owners of cattle surviving until discharge.

Results—18 of 31 (58%) cattle undergoing celiotomy survived to initial discharge. Fifteen (48%) and 13 (42%) were alive 6 and 12 months after discharge, respectively. All 5 deaths within 12 months after discharge were attributed to JHS recurrence. Survival time was 12 to 85 months for the 13 long-term survivors. Six of 7 that died > 12 months after celiotomy did so for reasons unrelated to JHS. Recurrence rate among short-term survivors was 7 of 18; 1 of these survived long-term. A significant proportion of affected cattle were Brown Swiss, compared with proportions for other breeds. Manual massage of the bowel to break down clots was associated with a significantly higher short-term survival rate than was en-terectomy or enterotomy. Medium- and long-term survival rate was higher in cattle referred 24 to 48 hours after onset of signs. Length of obstructing blood clots was not associated with outcome. Other factors were not significantly associated with recurrence.

Conclusions and Clinical Relevance—Survival rates were higher than those in other reports. Prompt celiotomy and resolution by use of manual massage were associated with higher survival rates. In this population, JHS recurred in 7 of 18 short-term survivors.

Abstract

Objective—To describe signalment; surgical findings; short-, medium-, and long-term outcome; and recurrence rate for cattle undergoing celiotomy because of jejunal hemorrhage syndrome (JHS) and to analyze risk factors associated with outcome and recurrence.

Design—Retrospective case series.

Animals—31 dairy cattle with JHS.

Procedures—Medical records were analyzed. Follow-up information was obtained from owners of cattle surviving until discharge.

Results—18 of 31 (58%) cattle undergoing celiotomy survived to initial discharge. Fifteen (48%) and 13 (42%) were alive 6 and 12 months after discharge, respectively. All 5 deaths within 12 months after discharge were attributed to JHS recurrence. Survival time was 12 to 85 months for the 13 long-term survivors. Six of 7 that died > 12 months after celiotomy did so for reasons unrelated to JHS. Recurrence rate among short-term survivors was 7 of 18; 1 of these survived long-term. A significant proportion of affected cattle were Brown Swiss, compared with proportions for other breeds. Manual massage of the bowel to break down clots was associated with a significantly higher short-term survival rate than was en-terectomy or enterotomy. Medium- and long-term survival rate was higher in cattle referred 24 to 48 hours after onset of signs. Length of obstructing blood clots was not associated with outcome. Other factors were not significantly associated with recurrence.

Conclusions and Clinical Relevance—Survival rates were higher than those in other reports. Prompt celiotomy and resolution by use of manual massage were associated with higher survival rates. In this population, JHS recurred in 7 of 18 short-term survivors.

Hemorrhagic bowel syndrome, also known as bloody gut syndrome or JHS, has emerged as an economically important, sporadic, acute disease of adult dairy cattle. The first account of the disease was published in 1992,1 and in the intervening years, the condition has been reported in dairy cows in the United States,2 Europe,3,4 and the Middle East5 and beef cows6 and dairy and beef cows7 in Canada. Studies8,9 have shed light on risk factors, such as high milk production and consumption of high-energy diets, that may be associated with the condition in dairy cows in the United States. However, a common theme of all the retrospective studies of cattle from the United States,2 Europe,4 and Canada6,7 is an extremely high mortality rate (77%2 and 100%4,6,7). The only report of successful treatment was in a study2 of 22 cases in which there were 4 short-term survivors that underwent laparotomy with resection of affected intestinal segments or clot removal via enterotomy or intraluminal lavage. In that same study,2 1 animal survived with medical treatment alone.

The purposes of the study reported here were to identify surgical procedures and intraoperative findings in cattle with JHS and to determine short- and long-term survival rates in a veterinary hospital–based population. The timing of surgery relative to the onset of clinical signs of cattle on farms and subsequent examination and treatment at our veterinary hospital as well as the length of intraluminal blood clots were examined as risk factors for survival. Several clinical and clinicopathologic variables were also evaluated to better identify risk factors that may be important in predicting a successful outcome.

Materials and Methods

Case selection—Medical records of cattle that underwent celiotomy from 2000 through 2007 at the veterinary medical teaching hospital at the University of Wisconsin, Madison, were accessed. An additional selection criterion was visual or palpable evidence of blood clots causing intraluminal obstruction within the jejunum during surgery.

Medical records review—Signalment data obtained from the medical records included age, breed, sex, number of days in lactation, and pregnancy status. Additional information obtained from the medical records included the interval from when the owner first noticed clinical signs (hypophagia, hypogalactia, abdominal distention, colic, or a combination of these) to referral to our veterinary hospital as well as the amount of time that elapsed between admission at our veterinary hospital and celiotomy. Duration of clinical signs prior to referral was categorized as < 24 hours, 24 to 48 hours, 48 to 72 hours, or > 72 hours. The amount of time from admission at our veterinary hospital to celiotomy was categorized as < 3 hours, 3 to 12 hours, 12 to 24 hours, or > 24 hours. Specific physical examination findings (rectal temperature as well as heart and respiratory rates at initial examination and 24 hours after celiotomy) were obtained from each record. Furthermore, clinicopathologic variables (fibrinogen, total protein, sodium, potassium, chloride, and bicarbonate concentrations; Hct; and total WBC count) were also obtained from hematologic examinations performed on samples obtained at the time of admission to our veterinary hospital. When cattle died or were euthanized, gross pathologic information relating to the abdominal cavity and potential cause of death was also obtained.

Surgical information—Surgical information obtained from the medical records of eligible cattle included data pertaining to the type of intraoperative procedure performed (specifically, whether blood clots were manually massaged, removed by enterotomy, or removed by enterectomy). An approximation of the length of the obstructing jejunal blood clots was available for all cattle and was categorized as < 10 cm, 10 to 20 cm, 20 to 30 cm, or > 30 cm.

Survival information—Short-term survival was defined as survival until discharge from the veterinary hospital. Medium- and long-term survival was defined as survival until 6 and 12 months after discharge from the veterinary hospital, respectively. Owners of animals discharged from the veterinary hospital were contacted by telephone in March 2008 to obtain additional follow-up information regarding long-term survival and final outcome. Recurrence rates were also established for short-, medium-, and long-term survivors.

Statistical analysis—Signalment information (age, breed, and number of days in lactation) was initially evaluated to determine Gaussian or non-Gaussian distribution. On the basis of those results, descriptive statistics appropriate for non-Gaussian data were used for analysis. The Fisher exact test was used to compare the frequency of celiotomy for JHS in Brown Swiss cattle, compared with the frequency in other breeds of cattle in the hospital population. Short-, medium-, and long-term survival were analyzed by use of the Fisher exact test with respect to surgical procedure performed (manual massage, enterectomy, or enterotomy), interval from when clinical signs were first noticed in cattle on a farm to referral to our veterinary hospital (< 24 hours, 24 to 48 hours, 48 to 72 hours, or > 72 hours), time elapsed from admission at our veterinary hospital to onset of surgery (< 3 hours, 3 to 12 hours, 12 to 24 hours, or > 24 hours), and length of obstructing blood clot (< 10 cm, 10 to 20 cm, 20 to 30 cm, or > 30 cm). For cattle that survived to discharge but that had recurrence of JHS, the type of surgical procedure performed, length of obstructing blood clot found during the initial surgery, interval from onset of clinical signs to referral, and amount of time elapsed from admission at our veterinary hospital to surgery were also examined as potential risk factors by use of the Fisher exact test. The Mann-Whitney U test was used to compare median values of the continuous physical examination and clinicopathologic variables between cattle that survived or died in the short-term period. Significance was defined as values of P < 0.05 for all statistical analyses.

Results

Thirty-one cattle with JHS met the criteria for inclusion. Affected cattle comprised 30 lactating dairy cows and 1 mature breeding bull. Three of the cows were in their first lactation, and the remaining 27 were multiparous cows. The cattle originated from 28 farms (1 farm had 3 affected cattle, and another farm had 2 affected cattle). Four cows were pregnant, and the median number of days in lactation at the time of admission to our veterinary hospital was 150. Median age at time of admission was 3 years. Cattle comprised 18 (58%; 17 cows and 1 bull) Brown Swiss, 12 (39%) Holsteins, and 1 (3%) Jersey. During that same time period, there were 2,863 bovine admissions to our large animal clinic, of which 156 (5%) were Brown Swiss. There were 712 adult cattle that underwent celiotomy, of which 63 (9%) were Brown Swiss. Use of the Fisher exact test revealed a significantly (P < 0.001) higher frequency for JHS in Brown Swiss cattle, compared with the frequency in other breeds. There was no difference in the physical examination variables at initial examination or 24 hours after surgery between short-term survivors and nonsurvivors. Similarly, no significant differences were detected between short-term survivors and non-survivors for any clinicopathologic variables evaluated in samples obtained at admission.

Twenty cattle were referred within 24 hours after the onset of clinical signs, 8 were referred between 24 and 48 hours after onset, and 3 had clinical signs that had been detected > 72 hours prior to admission. The majority of cattle (n = 27) underwent celiotomy within 3 hours after admission, 1 animal underwent celiotomy between 3 and 12 hours after admission, and 3 cattle underwent celiotomy between 12 and 24 hours after admission to our veterinary hospital. Two cattle had obstructing blood clots < 10 cm in length, 7 had clots between 10 and 20 cm in length, 4 had clots between 20 and 30 cm in length, and 18 had obstructing blood clots < 30 cm in length.

Surgical procedures—Of the 31 cattle that had an initial celiotomy, manual massage of the blood clot or clots in an aborad direction was performed in 17, enterectomy and anastomosis were performed in 9, and an enterotomy was performed in 1; 4 cattle were euthanized during surgery. In all 31 cattle, obstructing blood clots were limited to the jejunum. Of the 18 short-term survivors, manual massage alone was performed in 13 and enterectomy was performed in 5. Twenty-nine cattle underwent a single surgery for JHS in our veterinary hospital; 1 animal had a second celiotomy 61 days after the initial surgery, and 1 animal had 2 additional surgeries (42 and 72 days after the initial celiotomy, respectively). Both cows with multiple surgical interventions were of the Brown Swiss breed. Treatment by use of manual massage alone resulted in short-term survival for 13 of 17 cattle, compared with short-term survival for 5 of 9 cattle treated by use of an enterectomy. Of the 7 short-term survivors that had subsequent recurrence of JHS, 5 had been treated by use of manual massage alone and 2 had undergone an enterectomy.

Pathologic findings—Postmortem information was available for all 13 cattle that did not survive until discharge from the veterinary hospital and 2 of 3 cattle that survived to discharge but died within 6 months after discharge. Four of the 13 cattle that did not survive until discharge were euthanized during surgery. All 4 cattle euthanized during surgery had jejunal obstruction of various lengths. In addition, 2 had jejunal perforation within the obstructed section with subsequent diffuse peritonitis, and 2 had mild to severe peritonitis with no evidence of intestinal perforation but substantial amounts of ischemic jejunum.

The remaining 9 cattle were euthanized (n = 4 cattle) or died (5) within 96 hours after surgery. The 4 cattle were euthanized within 96 hours after surgery because of clinical reasons (increasing abdominal distention and lack of fecal output [n = 2] or recumbency and inability to stand in addition to increasing abdominal distention and lack of fecal output [2]), rather than purely economic ones.

The 9 cattle that died or were euthanized within 96 hours after surgery had a variety of pathologic changes, including reobstruction of the jejunum (n = 7), jejunal perforation with diffuse peritonitis (3), and moderate to severe localized peritonitis without perforation (2) but no other relevant abdominal lesions. The 2 cattle that did not have recurrent obstruction had mild localized peritonitis but no other relevant abdominal lesions.

The 2 cattle that survived to discharge but that died within 6 months after discharge from the veterinary hospital and for which postmortem information was available were readmitted to the hospital for recurrent obstruction, but surgical intervention was declined. In both of those cattle, there was extensive reobstruction with localized peritonitis and jejunal ulcers but no intestinal perforation. One of these animals had undergone an enterectomy for the initial treatment, but the reobstruction was at a site distal to the original enterectomy site.

Short-term outcome—Eighteen (58%) cattle survived to discharge from the veterinary hospital. Statistical analysis by use of the Fisher exact test revealed that the proportion of cattle with short-term survival was significantly (P = 0.01) higher for cattle treated by use of manual massage, compared with the proportion for cattle undergoing enterectomy or enterotomy. Short-term survival was not significantly associated with the duration of signs prior to referral, the time that elapsed from admission at the veterinary hospital to surgery, or the length of blood clots identified during celiotomy.

Medium-term outcome—Fifteen (48%) cattle survived until 6 months after discharge. The 3 cattle that died or were euthanized after initial discharge had JHS recurrence at 5 days, 1 month, and 4 months after discharge, respectively. Statistical analyses revealed that the proportion of cattle with medium-term survival was significantly (P = 0.01) higher for cattle that had been referred to our veterinary hospital 24 to 48 hours after onset of clinical signs at the farm. However, the elapsed time from admission at the hospital to the commencement of surgery and the length of obstructing blood clot were not associated with medium-term outcome.

Long-term survival—Follow-up conversations with the owners of the 15 cattle that had long-term survival revealed that 2 additional cattle had a fatal recurrence of JHS (died 7 months and 11 months, respectively, after discharge from the veterinary hospital). One cow had 2 more recurrences of JHS that were treated medically on the farm, and she was still alive 5 years after discharge. The 12 other cattle had not had any additional episodes of JHS. Of these 12, 6 were still alive (survival time from discharge varied from 12 months to 58 months), 5 died or had been culled for other reasons not related to JHS, (survival time varied from 25 months to 85 months), and 1 had been sold 14 months after discharge. Animals died or were euthanized > 12 months after the initial JHS event as a result of events unrelated to JHS or the gastrointestinal tract.

Of the 18 short-term survivors, 7 had at least 1 additional episode of JHS. Recurrence of JHS was not significantly associated with surgical procedure performed, length of obstructing blood clots, or interval from onset of clinical signs on the farm to referral to our veterinary hospital or amount of time elapsed from admission to surgery. The proportion of cattle with long-term survival was again significantly (P = 0.043) higher for cattle that had been referred within 24 to 48 hours after detection of onset at the farm.

Discussion

In the study reported here, we described results for 31 mature dairy cattle with JHS treated surgically during a 7-year period. There were no cattle with this condition examined at our veterinary hospital prior to that time, which, in conjunction with the available literature, suggests that this is a relatively new syndrome in cattle. In contrast to another study,2 no cattle with presumptive JHS were treated medically in our veterinary hospital during this period, although the authors are aware of a few successful outcomes with nonsurgical management of cattle with JHS. Indeed, one of the long-term survivors in our study had 2 more episodes of abdominal distention, colic, and poor fecal output; after cathartics and antimicrobials were administered to the cow at the farm, she passed feces with numerous blood clots. Contrary to reports for other case-based retrospective studies and case reports, we had higher short-term (18/31 [58%]), medium-term (15/31 [48%]), and long-term (12/31 [39%]) survival rates.

The nature of an uncontrolled, retrospective study makes it difficult to precisely pinpoint factors in case management or clinical features at the time of admission that are predictive of a successful outcome. Although we were most hopeful of identifying factors of predictive importance prior to surgery, as well as surgical and postsurgical factors that may have influenced outcome, we were hindered by the limitations of a post hoc retrospective study. There was inconsistent anamnestic information on medical treatments administered to affected cattle prior to referral, which limited us to an analysis of the time from detection of onset of the illness at the farm until admission to our veterinary hospital. It also would have been of interest to examine whether intramural hemorrhage in the region of intraluminal obstruction was associated with short-term survival because many of the cattle in this report had obvious extension of the hemorrhagic lesion into the jejunal wall. However, the presence or absence of intramural hemorrhage was not consistently recorded, which precluded an accurate analysis. Postsurgical medical treatment with administration of crystalloid solutions, antimicrobials, anti-inflammatories, and cathartics was extremely variable so that an analysis of postsurgical medical treatment and its potential influence on outcome was also unrewarding. However, we did detect that there was a significantly higher proportion of cattle with medium- and long-term survival, but not short-term survival, for cattle referred to our veterinary hospital between 24 and 48 hours after the estimated onset of clinical signs, compared with results for cattle referred at shorter or longer intervals. The fact that survival to discharge was not influenced by the interval from detection of initial clinical signs to referral or time elapsed from admission to surgery is probably a relevant observation for practitioners and referral hospital clinicians in terms of case management, and it is hard to explain this outcome for later time frames (ie, medium- and long-term survival). There may have been some component of onfarm treatment (antimicrobials, anti-inflammatories, or fluids) for cattle referred between 24 and 48 hours after detection of the onset of clinical signs that positively influenced medium- and long-term outcome but not short-term survival. Because 5 of 6 short-term survivors died or were euthanized because of a subsequent recurrence of JHS, it is tempting to hypothesize that this survival effect was mediated through a prevention of recurrence. However, it is hard to encourage a delay in referral or surgery for cattle with potential obstructive small bowel lesions, so the practical relevance of this finding is dubious.

Worthy of mention in this study was the observation that manual massage alone (without enterectomy or enterotomy) was significantly associated with short-term survival and was associated (but not significantly) with medium-term survival. It is important to place this finding in the context of a retrospective study in which subjective intraoperative decisions about the severity of the lesion and the most appropriate course for correction influenced the analysis in ways that would not be possible in a double-blinded prospective study. It is probably best to state that short-term survival was significantly improved in those cattle for which the jejunal blood clots could be successfully massaged in an aborad direction without intraoperative reformation of the obstruction, compared with results for cattle whose jejunal obstruction and intestinal compromise were so severe or recalcitrant that enterectomy or enterotomy was deemed necessary. In cattle that underwent manual massage alone without an enterectomy or enterotomy, the procedure was always performed via a conventional right-sided abdominal approach with the patient in a standing position and administered local anesthetics. Some, but not all, cows on which enterectomy was performed had first undergone celiotomy in the right flank (cows restrained in a standing position with local anesthesia) immediately prior to undergoing induction for general anesthesia to facilitate the resection and anastomosis.

Follow-up information obtained on the cattle of this study revealed a recurrence rate of 39% (7/18) among those that survived to initial discharge. The high mortality rates reported in other studies2,4,6,7 have obviously precluded any observation as to recurrence for JHS, but our findings will likely not be surprising to practitioners who have dealt with the condition on dairies with recurring JHS. The JHS recurred in 6 cattle during the 12-month period following the initial event and was fatal in 5 of the 6 cattle (in the 1 cow that did not die, the condition resolved with medical treatment on the farm). Only 1 cow had presumptive recurrence of JHS > 12 months after the initial event; in that cow, the condition was successfully treated medically on the farm. It should be pointed out that cattle with recurrence were not always treated as aggressively as during the initial event, and financial factors played a part in several of the decisions to euthanize animals (n = 3 cattle) or to not refer cattle for additional surgical treatment. Our findings suggested that most recurrences of JHS were within the first 12 months after the initial event and that cattle that survived > 12 months after celiotomy because of JHS eventually left the herd for reasons unrelated to JHS or complications of the surgery.

Analysis of signalment data for our study suggested a breed predilection for JHS within Brown Swiss cattle, at least within our hospital population. In other case-based retrospective studies2,4 evaluating JHS in dairy cattle, investigators focused on dairy cattle from only 1 farm, which would thus prevent any comparison among breeds. Interestingly, there is evidence from the literature that Brown Swiss cattle are predisposed to intussusception,10 although any explanation for this apparent predilection to intestinal disease is lacking. Gross pathologic information was available for all cattle that died or were euthanized in this study, and it was consistent with that in other reports2,6,7 in which investigators described jejunal obstruction, ulcers, and necrosis with fibrinous peritonitis that varied from mild to severe. We also identified full-thickness perforation of obstructed jejunum in several cattle that inevitably led to gross contamination of the abdominal cavity.

Although we did not specifically address the issue of risk factors on the farms of origin for the development of JHS, this is an obvious area of interest for veterinarians and producers and has been the focus of at least 1 large multistate, cross-sectional study.9 In that study,9 it was found that management practices designed to achieve high milk production may increase the risk of cows developing JHS, and the dairy cows in the study reported here would have been exposed to such management practices on their farms of origin. The 1 mature bull in our retrospective study represented a different scenario in terms of management. As has been mentioned in other reports2,4,11 on JHS in dairy cattle, it is typical for multiple cattle to be affected on dairy farms, either as clusters of cases or as sporadic cases over longer time frames on the same dairy farms. Indeed, multiple cattle came from 2 farms in our study, and several of those owners that provided follow-up information regarding long-term survival indicated that they had other cattle with presumed JHS in the interim.

We did not consistently address possible infectious etiologic causes for JHS by use of microbiologic culture; we only submitted intestinal contents or feces for anaerobic culture from 9 of the 31 affected cattle (data not reported). Of those 9 submissions, 3 anaerobic cultures did not yield growth, 3 yielded Clostridium perfringens type A α-toxin–producing strain, 2 yielded C perfringens type A α- and β2-toxin–producing strain, and 1 yielded an unspeciated Clostridium organism. Much interest in the dairy industry has centered on possible roles for C perfringens or Aspergillus fumigatus as etiologic causes for JHS, but we did not pursue the latter in any of the cattle. Although C perfringens type A appears to be frequently cultured from feces or intestinal contents of affected cattle2,6,12 and α-toxin–producing and α- and β2-toxin–producing strains are more likely to be obtained from cattle with JHS than from cattle with abomasal displacement, it has not been possible to experimentally induce the disease with a β2-toxin–producing organism isolated from a field case,13 which suggests a multifactorial aspect to the disease.

In the study reported here, we provided a hospital-based retrospective study that revealed survival rates for cattle with JHS after surgical treatment in our referral veterinary hospital population can be much higher than those reported elsewhere. At our facility, surgical exploration in standing cattle via right-flank celiotomy when the jejunal obstruction could be successfully alleviated by use of manual massage alone was associated with a significant improvement in short-term survival. Cattle that required enterotomy or enterectomy had poorer survival rates. Additional studies to characterize the cause of JHS and to evaluate its prevention are warranted.

ABBREVIATIONS

JHS

Jejunal hemorrhage syndrome

References

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    Ruggles AJ, Sweeney RW, Freeman DE, et al. Intraluminal hemorrhage from small intestinal ulceration in two cows. Cornell Vet 1992;82:181186.

    • Search Google Scholar
    • Export Citation
  • 2.

    Dennison AC, Van Metre DC, Callan RJ, et al. Hemorrhagic bowel syndrome in dairy cattle: 22 cases (1997–2000). J Am Vet Med Assoc 2002;221:686689.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3.

    von Rademacher G, Lorenz I, Haenichen T. Jejunumanschoppung mit koaguliertem Blut infolge blutender Darmulzera bei Kuehen. Sonderdruck Aus Tierärztliche Umsch 2002;57:399411.

    • Search Google Scholar
    • Export Citation
  • 4.

    Muskens J, Veldhorst GJ, Snoep JJ, et al. High mortality in a herd with signs of jejunal hemorrhage syndrome [in Dutch]. Tijdschr Diergeneeskd 2007;132:116119.

    • Search Google Scholar
    • Export Citation
  • 5.

    Brenner J, Orgad U, Tiomkin D, et al. Adult jejunal hemorrhage syndrome—an emerging dairy cow disease. Isr J Vet Med 2002;57:41.

  • 6.

    Abutarbush SM, Carmalt JL, Wilson DG, et al. Jejunal hemorrhage syndrome in 2 Canadian beef cows. Can Vet J 2004;45:4850.

  • 7.

    Abutarbush SM, Radostits OM. Jejunal hemorrhage syndrome in dairy and beef cattle: 11 cases (2001 to 2003). Can Vet J 2005;46:711715.

  • 8.

    Godden S, Frank R, Ames T. Survey of Minnesota dairy veterinarians on the occurrence and potential risk factors for jejunal hemorrhage syndrome in adult dairy cattle. Bovine Pract 2001;35(2):97103.

    • Search Google Scholar
    • Export Citation
  • 9.

    Berghaus RD, McCluskey BJ, Callam RJ. Risk factors associated with hemorrhagic bowel syndrome in dairy cattle. J Am Vet Med Assoc 2005;226:17001706.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10.

    Constable PD, St Jean G, Hull BL, et al. Intussusception in cattle: 336 cases (1964–1993). J Am Vet Med Assoc 1997;210:531536.

  • 11.

    Kirkpatrick MA, Timms LL, Kersting KW, et al. Case report— jejunal hemorrhage syndrome of dairy cattle. Bovine Pract 2001;35(2):104116.

    • Search Google Scholar
    • Export Citation
  • 12.

    Dennison AC, Van Metre DC, Morley PS, et al. Comparison of the odds of isolation, genotypes and in vivo production of major toxins by Clostridium perfringens obtained from the gastrointestinal tract of dairy cows with hemorrhagic bowel syndrome or left-displaced abomasum. J Am Vet Med Assoc 2005;227:132138.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13.

    Ewoldt JM, Anderson DE. Determination of the effect of single abomasal or jejunal inoculation of Clostridium perfringens type A in dairy cows. Can Vet J 2005;46:821824.

    • Search Google Scholar
    • Export Citation
  • 1.

    Ruggles AJ, Sweeney RW, Freeman DE, et al. Intraluminal hemorrhage from small intestinal ulceration in two cows. Cornell Vet 1992;82:181186.

    • Search Google Scholar
    • Export Citation
  • 2.

    Dennison AC, Van Metre DC, Callan RJ, et al. Hemorrhagic bowel syndrome in dairy cattle: 22 cases (1997–2000). J Am Vet Med Assoc 2002;221:686689.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3.

    von Rademacher G, Lorenz I, Haenichen T. Jejunumanschoppung mit koaguliertem Blut infolge blutender Darmulzera bei Kuehen. Sonderdruck Aus Tierärztliche Umsch 2002;57:399411.

    • Search Google Scholar
    • Export Citation
  • 4.

    Muskens J, Veldhorst GJ, Snoep JJ, et al. High mortality in a herd with signs of jejunal hemorrhage syndrome [in Dutch]. Tijdschr Diergeneeskd 2007;132:116119.

    • Search Google Scholar
    • Export Citation
  • 5.

    Brenner J, Orgad U, Tiomkin D, et al. Adult jejunal hemorrhage syndrome—an emerging dairy cow disease. Isr J Vet Med 2002;57:41.

  • 6.

    Abutarbush SM, Carmalt JL, Wilson DG, et al. Jejunal hemorrhage syndrome in 2 Canadian beef cows. Can Vet J 2004;45:4850.

  • 7.

    Abutarbush SM, Radostits OM. Jejunal hemorrhage syndrome in dairy and beef cattle: 11 cases (2001 to 2003). Can Vet J 2005;46:711715.

  • 8.

    Godden S, Frank R, Ames T. Survey of Minnesota dairy veterinarians on the occurrence and potential risk factors for jejunal hemorrhage syndrome in adult dairy cattle. Bovine Pract 2001;35(2):97103.

    • Search Google Scholar
    • Export Citation
  • 9.

    Berghaus RD, McCluskey BJ, Callam RJ. Risk factors associated with hemorrhagic bowel syndrome in dairy cattle. J Am Vet Med Assoc 2005;226:17001706.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10.

    Constable PD, St Jean G, Hull BL, et al. Intussusception in cattle: 336 cases (1964–1993). J Am Vet Med Assoc 1997;210:531536.

  • 11.

    Kirkpatrick MA, Timms LL, Kersting KW, et al. Case report— jejunal hemorrhage syndrome of dairy cattle. Bovine Pract 2001;35(2):104116.

    • Search Google Scholar
    • Export Citation
  • 12.

    Dennison AC, Van Metre DC, Morley PS, et al. Comparison of the odds of isolation, genotypes and in vivo production of major toxins by Clostridium perfringens obtained from the gastrointestinal tract of dairy cows with hemorrhagic bowel syndrome or left-displaced abomasum. J Am Vet Med Assoc 2005;227:132138.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13.

    Ewoldt JM, Anderson DE. Determination of the effect of single abomasal or jejunal inoculation of Clostridium perfringens type A in dairy cows. Can Vet J 2005;46:821824.

    • Search Google Scholar
    • Export Citation

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