New Zealand Veterinary Journal
ISSN: 0048-0169 (Print) 1176-0710 (Online) Journal homepage: http://www.tandfonline.com/loi/tnzv20
Surgical management of small intestinal intussusception associated with jejunal adenocarcinoma in a dairy cow EL Milnes & A McLachlan To cite this article: EL Milnes & A McLachlan (2015) Surgical management of small intestinal intussusception associated with jejunal adenocarcinoma in a dairy cow, New Zealand Veterinary Journal, 63:5, 288-290, DOI: 10.1080/00480169.2014.999843 To link to this article: http://dx.doi.org/10.1080/00480169.2014.999843
Accepted author version posted online: 20 Dec 2014.
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Date: 06 November 2015, At: 03:33
288
New Zealand Veterinary Journal 63(5), 288–290, 2015
Peer-reviewed Correspondence
Downloaded by [York University Libraries] at 03:33 06 November 2015
Surgical management of small intestinal intussusception associated with jejunal adenocarcinoma in a dairy cow
Neoplasia of the gastrointestinal tract is considered to be rare in cattle (Bertone 1990). Sporadic reports of bovine intestinal adenocarcinoma have been recorded in surveys of material from New Zealand slaughterhouses (Ross 1984), but there are few reports of diagnosis and management of this disease in living animals. Presented here is a case of small intestinal intussusception associated with jejunal adenocarcinoma in an adult dairy cow, and its successful surgical management. A 4-year-old mid-lactation Friesian cow on a dairy farm in the Waikato region of the North Island of New Zealand presented with acute onset of abdominal pain. The cow was tachycardic and tachypnoeic with heart rate of 120 beats per minute and respiratory rate of 40 breaths per minute. Rectal temperature was 38.3°C. Rectal examination revealed dilated loops of small intestine, a distended atonic rumen, and scant mucoid faeces in the rectum. A presumptive diagnosis of acute intestinal obstruction was made on the basis of these clinical signs, and the decision was made to proceed immediately to surgery in the field. The animal was restrained by the head, and the right paralumbar fossa was clipped and aseptically prepared for a standing exploratory right flank laparotomy. Local analgesia was achieved by infiltrating 150 mL of 2% lignocaine in an inverted L field block. A 20 cm vertical skin incision was made in the mid flank 10 cm caudal to the last rib and starting 10 cm ventral to the transverse lumbar processes, followed by a modified grid incision through the muscle layers and peritoneum (Kersjes et al. 1985). Exploration of the abdomen identified a jejunojejunal intussusception involving a segment of intestine approximately 30 cm in length located in the proximal jejunum. The intussusception was bright pink in colour and firm on palpation, with no visible sign of compromised circulation or injury to the intestinal wall. The jejunum distal to the intestine was empty of ingesta but distended with gas, with flaccid pale pink walls showing weak peristaltic activity. The large intestines were also distended with gas but appeared normal in colour and on palpation. Further exploration of the accessible abdominal cavity revealed no other abnormalities. Exteriorisation of the intussusception was attempted, but the resulting traction on the mesenteric root caused a severe pain response and collapse. The animal was encouraged to stand and a sling was constructed using two 5 m ropes criss-crossed between the horizontal bars of the race to support the abdomen and thorax. This sling supported the animal in a standing position for the duration of surgery. Approximately 50 mL of 2% lignocaine was infiltrated into the mesenteric root and the affected segment of intestine was exteriorised. The intussusception was easily reduced and an intraluminal mass was palpated at the proximal margin of the intussusception. The serosal
http://dx.doi.org/10.1080/00480169.2014.999843 © 2015 New Zealand Veterinary Association
surface of the intestine immediately adjacent to the mass appeared grossly normal in colour and texture, with weak but normal motility. Bowel clamps were placed to isolate the lesion, and incision into the intestinal lumen revealed a 50 × 40 × 20 mm proliferative tan-coloured mass protruding from the mucosal surface. The affected section of jejunum, which had been isolated with bowel clamps, and the mass were removed by enterectomy including 10 cm margins of normal intestine proximally and distally. A V-shaped segment of the adjacent mesentery was included in the resection, taking care not to compromise blood flow to the remaining wound edges. After resection, the viable ends of jejunum were flushed with sterile physiologic saline and an end-to-end anastomosis was performed. The abdominal incision was closed using a routine three layer repair (Kersjes et al. 1985). Eighteen litres of warm electrolyte solution with 2 L of liquid paraffin were given by stomach tube immediately after surgery. Post-surgical aftercare included 2.2 mg/kg I/V flunixin meglumine (Flunixin, Norbrook NZ Ltd, Auckland, NZ) every 24 hours for 3 days, 5 mg/kg I/M oxytetracycline (Engemycin, MSD Animal Health NZ, Wellington, NZ) every 24 hours for 5 days, and a diet of hay. The cow passed soft dark faeces within 24 hours of surgery and recovery continued uneventfully. The cow was 6 weeks pregnant at the time the surgery was performed. The pregnancy continued uneventfully and the cow produced a live calf unassisted at term with a subsequently normal lactation. The resected section of small intestine was fixed in 4% neutral buffered formalin and a representative section of the mass and adjacent intestinal wall was cut, routinely processed and stained with H&E. A mass of neoplastic intestinal epithelial cells had replaced the mucosa and infiltrated the smooth muscle of the intestinal wall (Figure 1a). The neoplastic cells were arranged in stratified cords and sometimes rudimentary glands. The cells were polygonal, differed three-fold in size, had pink-purple cytoplasm and indistinct cell borders. Nuclei were oval, 15–30 µm in diameter, with speckled chromatin and a nucleolus. There were scattered mitoses and areas of tumour necrosis (Figure 1b). Due to the tortuous nature of the specimen, margins could not be assessed, but the neoplastic cells appeared to be confined to the mass so the gross margins observed during surgery were probably representative. Based on these findings a diagnosis was made of jejunal adenocarcinoma. To the authors’ knowledge, this is the first report of successful surgical management of small intestinal adenocarcinoma in a bovine animal in New Zealand. Previous reports of intestinal neoplasia in cattle in New Zealand are rare, although in some geographical locations the reported prevalence of carcinoma/adenocarcinoma of the small intestine in cattle and sheep is high. Carcinoma of the small intestine was reported to be common in sheep in New Zealand (Simpson and Jolly 1974). A high prevalence of bovine intestinal adenocarcinoma has been reported to occur in northern England and Scotland, where disease is associated with ingestion of an environmental carcinogen
Milnes and McLachlan
New Zealand Veterinary Journal, 2015
289
Downloaded by [York University Libraries] at 03:33 06 November 2015
adenocarcinoma of the small intestine in 32 cattle (0.91% of all bovine neoplasms diagnosed during the 10-year period) but diagnosis could not be confirmed due to lack of data; a further eight cases of bovine intestinal adenocarcinoma (0.23%) were confirmed on histopathology (Ross 1984). True prevalence rates for the disease in New Zealand cannot be calculated from these data because cases were submitted from slaughterhouses and farms with no particular requirements placed on submitters. Six cases of adenocarcinoma of the bovine small intestine examined at Massey University veterinary school were described by Johnstone et al. (1983). Historical information was available for five animals which were all Jersey, Friesian, or Jersey/Friesian crossbreed animals aged between 8 and 10 years, and which had all shown an insidious and progressive loss of condition over several weeks necessitating euthanasia. All but one of these animals had histopathological evidence of tumour metastasis post mortem (Johnstone et al. 1983). Bovine small intestinal neoplasia is reported to metastasise early, with spread commonly occurring to the mesenteric lymph nodes, liver and lung (Bertone 1990). In the current case, the mesenteric lymph nodes appeared macroscopically normal. Wedge biopsy specimens from the lymph nodes draining the affected section of intestine would have been useful to assist in determining whether metastasis had occurred, but this was not done. A case report of ileal adenocarcinoma in an 11- year-old Pinzgauer cow described a 6-day history of anorexia and abdominal pain, with generalised peritonitis and multifocal abdominal metastases diagnosed on necropsy (Floeck et al. 2008). It is likely that healthy animals with small intestinal adenocarcinomas found incidentally at post-mortem examination are in the pre-metastatic stage of disease.
Figure 1. Photomicrographs of sections of small intestine from a cow diagnosed with jejunal adenocarcinoma. (a) A mass of neoplastic epithelial cells replaces the mucosa, extends through the muscularis mucosa, expands the submucosa and infiltrates the smooth muscle of the intestinal wall (H&E, bar=500 µm). (b) Pleomorphic neoplastic epithelial cells are arranged in rudimentary stratified cords and sheets. The neoplastic cells are polygonal, differ three-fold in size and have indistinct cell borders. Nuclei are oval, 15–30 µm diameter and have speckled chromatin. There are scattered mitoses and necrotic cells (H&E, bar=40 µm).
(bracken fern; Pteridium esculentum) and infection with a papillomavirus (Jarrett et al. 1978). No such disease aetiology has yet been elucidated for the disease in grazing ruminants in New Zealand (Johnstone et al. 1983). Clinical signs associated with intestinal neoplasia are variable, ranging from acute abdominal crisis due to intestinal obstruction to chronic debilitation and progressive loss of condition (Bristol et al. 1984). Examination using ultrasonography may help to support a diagnosis of intestinal neoplasia prior to surgical intervention or euthanasia. In the current case ultrasonography would have been useful to confirm this diagnosis before surgical intervention, but equipment was unavailable at the time. Animals presenting with an acute abdominal crisis may die on farm or be subject to euthanasia without diagnosis. Definitive diagnosis of intestinal adenocarcinoma requires exploratory surgery or necropsy and histopathology, which may not be undertaken by clinicians in general practice. A 1984 report of a retrospective search of the files of the Animal Health Laboratories of the Ministry of Agriculture and Fisheries in New Zealand for the period 1973–1982 revealed a tentative diagnosis of
There are few published reports of surgical management and post-surgical survival for this type of tumour in cattle. It has been reported that palliative surgery for focal small intestinal tumours may be rewarding in individual cases, but that death from metastatic disease occurs within 1 year (Bertone 1990). Successful surgical resection of a jejunal adenocarcinoma was described in an aged Holstein cow which recovered well from surgery and produced milk and embryos to expectation; however during the seventh month after surgery this cow developed pneumonia and was subject to euthanasia, with disseminated abdominal and thoracic neoplasia observed at necropsy (Archer et al. 1988). In conclusion, this report describes an unusual presentation of intestinal neoplasia in a relatively young cow. The history and clinical signs of this case suggested acute intestinal obstruction. Surgical intervention has so far been worthwhile, with the cow appearing healthy and productive at 12 months post-surgery. Lymph node biopsies taken at the time of surgery would have been useful to assist in determining whether metastasis had occurred.
Acknowledgements We would like to thank Isobel Gibson, New Zealand Veterinary Pathology, Hamilton for taking the digital photomicrographs.
References Archer RM, Cooley AJ, Hinchcliff KW, Smith DF. Jejunojejunal intussusception associated with a transmural adenocarcinoma in an aged cow. Journal of the American Veterinary Medical Association 192, 209–11, 1988
290
New Zealand Veterinary Journal, 2015
EL Milnes Veterinary Enterprises Group 18 Tuhoro Street Otorohanga 3900 New Zealand Email: [email protected] EL Milnes http://orcid.org/0000-0002-7797-2217 A McLachlan New Zealand Veterinary Pathology Cnr. Anglesea and Thackeray Streets Hamilton New Zealand
Submitted 19 May 2014 First published online 20 December 2014
Downloaded by [York University Libraries] at 03:33 06 November 2015
Bertone AL. Neoplasms of the bovine gastrointestinal tract. Veterinary Clinics of North America: Food Animal Practice 6, 515–24, 1990 Bristol DG, Baum KH, Mezza LE. Adenocarcinoma of the jejunum in two cows. Journal of the American Veterinary Medical Association 185, 551–3, 1984 Floeck M, Hoegler S, Krametter-Froetscher R. Ileal adenocarcinoma in a cow: a case report. Veterinarni Medicina 53, 221–3, 2008 Jarrett WFH, McNeil PE, Grimshaw TR, Selman IE, McIntyre WIM. High incidence area of cattle cancer with a possible interaction between an environmental carcinogen and a papillomavirus. Nature 274, 215–7, 1978 Johnstone AC, Alley MR, Jolly RD. Small intestinal carcinoma in cattle. New Zealand Veterinary Journal 31, 147–9, 1983 *Kersjes AW, Nemeth F, Rutgers LJE. Atlas of Large Animal Surgery. Pp 36–7. Williams & Wilkins, Baltimore, USA, 1985 Ross AD. Small-intestinal adenocarcinoma in cattle. New Zealand Veterinary Journal 32, 98–9, 1984 Simpson BH, Jolly RD. Carcinoma of the small intestine in sheep. The Journal of Pathology 112, 83–92, 1974
Milnes and McLachlan
*Non-peer-reviewed
ISSN: 0048-0169 (Print) 1176-0710 (Online) Journal homepage: http://www.tandfonline.com/loi/tnzv20
Surgical management of small intestinal intussusception associated with jejunal adenocarcinoma in a dairy cow EL Milnes & A McLachlan To cite this article: EL Milnes & A McLachlan (2015) Surgical management of small intestinal intussusception associated with jejunal adenocarcinoma in a dairy cow, New Zealand Veterinary Journal, 63:5, 288-290, DOI: 10.1080/00480169.2014.999843 To link to this article: http://dx.doi.org/10.1080/00480169.2014.999843
Accepted author version posted online: 20 Dec 2014.
Submit your article to this journal
Article views: 53
View related articles
View Crossmark data
Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=tnzv20 Download by: [York University Libraries]
Date: 06 November 2015, At: 03:33
288
New Zealand Veterinary Journal 63(5), 288–290, 2015
Peer-reviewed Correspondence
Downloaded by [York University Libraries] at 03:33 06 November 2015
Surgical management of small intestinal intussusception associated with jejunal adenocarcinoma in a dairy cow
Neoplasia of the gastrointestinal tract is considered to be rare in cattle (Bertone 1990). Sporadic reports of bovine intestinal adenocarcinoma have been recorded in surveys of material from New Zealand slaughterhouses (Ross 1984), but there are few reports of diagnosis and management of this disease in living animals. Presented here is a case of small intestinal intussusception associated with jejunal adenocarcinoma in an adult dairy cow, and its successful surgical management. A 4-year-old mid-lactation Friesian cow on a dairy farm in the Waikato region of the North Island of New Zealand presented with acute onset of abdominal pain. The cow was tachycardic and tachypnoeic with heart rate of 120 beats per minute and respiratory rate of 40 breaths per minute. Rectal temperature was 38.3°C. Rectal examination revealed dilated loops of small intestine, a distended atonic rumen, and scant mucoid faeces in the rectum. A presumptive diagnosis of acute intestinal obstruction was made on the basis of these clinical signs, and the decision was made to proceed immediately to surgery in the field. The animal was restrained by the head, and the right paralumbar fossa was clipped and aseptically prepared for a standing exploratory right flank laparotomy. Local analgesia was achieved by infiltrating 150 mL of 2% lignocaine in an inverted L field block. A 20 cm vertical skin incision was made in the mid flank 10 cm caudal to the last rib and starting 10 cm ventral to the transverse lumbar processes, followed by a modified grid incision through the muscle layers and peritoneum (Kersjes et al. 1985). Exploration of the abdomen identified a jejunojejunal intussusception involving a segment of intestine approximately 30 cm in length located in the proximal jejunum. The intussusception was bright pink in colour and firm on palpation, with no visible sign of compromised circulation or injury to the intestinal wall. The jejunum distal to the intestine was empty of ingesta but distended with gas, with flaccid pale pink walls showing weak peristaltic activity. The large intestines were also distended with gas but appeared normal in colour and on palpation. Further exploration of the accessible abdominal cavity revealed no other abnormalities. Exteriorisation of the intussusception was attempted, but the resulting traction on the mesenteric root caused a severe pain response and collapse. The animal was encouraged to stand and a sling was constructed using two 5 m ropes criss-crossed between the horizontal bars of the race to support the abdomen and thorax. This sling supported the animal in a standing position for the duration of surgery. Approximately 50 mL of 2% lignocaine was infiltrated into the mesenteric root and the affected segment of intestine was exteriorised. The intussusception was easily reduced and an intraluminal mass was palpated at the proximal margin of the intussusception. The serosal
http://dx.doi.org/10.1080/00480169.2014.999843 © 2015 New Zealand Veterinary Association
surface of the intestine immediately adjacent to the mass appeared grossly normal in colour and texture, with weak but normal motility. Bowel clamps were placed to isolate the lesion, and incision into the intestinal lumen revealed a 50 × 40 × 20 mm proliferative tan-coloured mass protruding from the mucosal surface. The affected section of jejunum, which had been isolated with bowel clamps, and the mass were removed by enterectomy including 10 cm margins of normal intestine proximally and distally. A V-shaped segment of the adjacent mesentery was included in the resection, taking care not to compromise blood flow to the remaining wound edges. After resection, the viable ends of jejunum were flushed with sterile physiologic saline and an end-to-end anastomosis was performed. The abdominal incision was closed using a routine three layer repair (Kersjes et al. 1985). Eighteen litres of warm electrolyte solution with 2 L of liquid paraffin were given by stomach tube immediately after surgery. Post-surgical aftercare included 2.2 mg/kg I/V flunixin meglumine (Flunixin, Norbrook NZ Ltd, Auckland, NZ) every 24 hours for 3 days, 5 mg/kg I/M oxytetracycline (Engemycin, MSD Animal Health NZ, Wellington, NZ) every 24 hours for 5 days, and a diet of hay. The cow passed soft dark faeces within 24 hours of surgery and recovery continued uneventfully. The cow was 6 weeks pregnant at the time the surgery was performed. The pregnancy continued uneventfully and the cow produced a live calf unassisted at term with a subsequently normal lactation. The resected section of small intestine was fixed in 4% neutral buffered formalin and a representative section of the mass and adjacent intestinal wall was cut, routinely processed and stained with H&E. A mass of neoplastic intestinal epithelial cells had replaced the mucosa and infiltrated the smooth muscle of the intestinal wall (Figure 1a). The neoplastic cells were arranged in stratified cords and sometimes rudimentary glands. The cells were polygonal, differed three-fold in size, had pink-purple cytoplasm and indistinct cell borders. Nuclei were oval, 15–30 µm in diameter, with speckled chromatin and a nucleolus. There were scattered mitoses and areas of tumour necrosis (Figure 1b). Due to the tortuous nature of the specimen, margins could not be assessed, but the neoplastic cells appeared to be confined to the mass so the gross margins observed during surgery were probably representative. Based on these findings a diagnosis was made of jejunal adenocarcinoma. To the authors’ knowledge, this is the first report of successful surgical management of small intestinal adenocarcinoma in a bovine animal in New Zealand. Previous reports of intestinal neoplasia in cattle in New Zealand are rare, although in some geographical locations the reported prevalence of carcinoma/adenocarcinoma of the small intestine in cattle and sheep is high. Carcinoma of the small intestine was reported to be common in sheep in New Zealand (Simpson and Jolly 1974). A high prevalence of bovine intestinal adenocarcinoma has been reported to occur in northern England and Scotland, where disease is associated with ingestion of an environmental carcinogen
Milnes and McLachlan
New Zealand Veterinary Journal, 2015
289
Downloaded by [York University Libraries] at 03:33 06 November 2015
adenocarcinoma of the small intestine in 32 cattle (0.91% of all bovine neoplasms diagnosed during the 10-year period) but diagnosis could not be confirmed due to lack of data; a further eight cases of bovine intestinal adenocarcinoma (0.23%) were confirmed on histopathology (Ross 1984). True prevalence rates for the disease in New Zealand cannot be calculated from these data because cases were submitted from slaughterhouses and farms with no particular requirements placed on submitters. Six cases of adenocarcinoma of the bovine small intestine examined at Massey University veterinary school were described by Johnstone et al. (1983). Historical information was available for five animals which were all Jersey, Friesian, or Jersey/Friesian crossbreed animals aged between 8 and 10 years, and which had all shown an insidious and progressive loss of condition over several weeks necessitating euthanasia. All but one of these animals had histopathological evidence of tumour metastasis post mortem (Johnstone et al. 1983). Bovine small intestinal neoplasia is reported to metastasise early, with spread commonly occurring to the mesenteric lymph nodes, liver and lung (Bertone 1990). In the current case, the mesenteric lymph nodes appeared macroscopically normal. Wedge biopsy specimens from the lymph nodes draining the affected section of intestine would have been useful to assist in determining whether metastasis had occurred, but this was not done. A case report of ileal adenocarcinoma in an 11- year-old Pinzgauer cow described a 6-day history of anorexia and abdominal pain, with generalised peritonitis and multifocal abdominal metastases diagnosed on necropsy (Floeck et al. 2008). It is likely that healthy animals with small intestinal adenocarcinomas found incidentally at post-mortem examination are in the pre-metastatic stage of disease.
Figure 1. Photomicrographs of sections of small intestine from a cow diagnosed with jejunal adenocarcinoma. (a) A mass of neoplastic epithelial cells replaces the mucosa, extends through the muscularis mucosa, expands the submucosa and infiltrates the smooth muscle of the intestinal wall (H&E, bar=500 µm). (b) Pleomorphic neoplastic epithelial cells are arranged in rudimentary stratified cords and sheets. The neoplastic cells are polygonal, differ three-fold in size and have indistinct cell borders. Nuclei are oval, 15–30 µm diameter and have speckled chromatin. There are scattered mitoses and necrotic cells (H&E, bar=40 µm).
(bracken fern; Pteridium esculentum) and infection with a papillomavirus (Jarrett et al. 1978). No such disease aetiology has yet been elucidated for the disease in grazing ruminants in New Zealand (Johnstone et al. 1983). Clinical signs associated with intestinal neoplasia are variable, ranging from acute abdominal crisis due to intestinal obstruction to chronic debilitation and progressive loss of condition (Bristol et al. 1984). Examination using ultrasonography may help to support a diagnosis of intestinal neoplasia prior to surgical intervention or euthanasia. In the current case ultrasonography would have been useful to confirm this diagnosis before surgical intervention, but equipment was unavailable at the time. Animals presenting with an acute abdominal crisis may die on farm or be subject to euthanasia without diagnosis. Definitive diagnosis of intestinal adenocarcinoma requires exploratory surgery or necropsy and histopathology, which may not be undertaken by clinicians in general practice. A 1984 report of a retrospective search of the files of the Animal Health Laboratories of the Ministry of Agriculture and Fisheries in New Zealand for the period 1973–1982 revealed a tentative diagnosis of
There are few published reports of surgical management and post-surgical survival for this type of tumour in cattle. It has been reported that palliative surgery for focal small intestinal tumours may be rewarding in individual cases, but that death from metastatic disease occurs within 1 year (Bertone 1990). Successful surgical resection of a jejunal adenocarcinoma was described in an aged Holstein cow which recovered well from surgery and produced milk and embryos to expectation; however during the seventh month after surgery this cow developed pneumonia and was subject to euthanasia, with disseminated abdominal and thoracic neoplasia observed at necropsy (Archer et al. 1988). In conclusion, this report describes an unusual presentation of intestinal neoplasia in a relatively young cow. The history and clinical signs of this case suggested acute intestinal obstruction. Surgical intervention has so far been worthwhile, with the cow appearing healthy and productive at 12 months post-surgery. Lymph node biopsies taken at the time of surgery would have been useful to assist in determining whether metastasis had occurred.
Acknowledgements We would like to thank Isobel Gibson, New Zealand Veterinary Pathology, Hamilton for taking the digital photomicrographs.
References Archer RM, Cooley AJ, Hinchcliff KW, Smith DF. Jejunojejunal intussusception associated with a transmural adenocarcinoma in an aged cow. Journal of the American Veterinary Medical Association 192, 209–11, 1988
290
New Zealand Veterinary Journal, 2015
EL Milnes Veterinary Enterprises Group 18 Tuhoro Street Otorohanga 3900 New Zealand Email: [email protected] EL Milnes http://orcid.org/0000-0002-7797-2217 A McLachlan New Zealand Veterinary Pathology Cnr. Anglesea and Thackeray Streets Hamilton New Zealand
Submitted 19 May 2014 First published online 20 December 2014
Downloaded by [York University Libraries] at 03:33 06 November 2015
Bertone AL. Neoplasms of the bovine gastrointestinal tract. Veterinary Clinics of North America: Food Animal Practice 6, 515–24, 1990 Bristol DG, Baum KH, Mezza LE. Adenocarcinoma of the jejunum in two cows. Journal of the American Veterinary Medical Association 185, 551–3, 1984 Floeck M, Hoegler S, Krametter-Froetscher R. Ileal adenocarcinoma in a cow: a case report. Veterinarni Medicina 53, 221–3, 2008 Jarrett WFH, McNeil PE, Grimshaw TR, Selman IE, McIntyre WIM. High incidence area of cattle cancer with a possible interaction between an environmental carcinogen and a papillomavirus. Nature 274, 215–7, 1978 Johnstone AC, Alley MR, Jolly RD. Small intestinal carcinoma in cattle. New Zealand Veterinary Journal 31, 147–9, 1983 *Kersjes AW, Nemeth F, Rutgers LJE. Atlas of Large Animal Surgery. Pp 36–7. Williams & Wilkins, Baltimore, USA, 1985 Ross AD. Small-intestinal adenocarcinoma in cattle. New Zealand Veterinary Journal 32, 98–9, 1984 Simpson BH, Jolly RD. Carcinoma of the small intestine in sheep. The Journal of Pathology 112, 83–92, 1974
Milnes and McLachlan
*Non-peer-reviewed
