Evaluation of the validity of the double two-thirds rule for diagnosing hemangiosarcoma in dogs with nontraumatic hemoperitoneum due to a ruptured splenic mass: a systematic review

Ashley R. Schick Department of Small Animal Medicine and Surgery, College of Veterinary Medicine, University of Georgia, Athens, GA

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Janet A. Grimes Department of Small Animal Medicine and Surgery, College of Veterinary Medicine, University of Georgia, Athens, GA

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Abstract

OBJECTIVE

To evaluate the validity of the double two-thirds rule for a diagnosis of splenic hemangiosarcoma in dogs with nontraumatic hemoperitoneum due to a ruptured splenic mass.

SAMPLE

Systematic literature review.

PROCEDURES

3 databases (PubMed, CAB abstracts, and World of Science) were searched in November 2020. Articles were included if data on dogs with nontraumatic hemoperitoneum due to a splenic mass were included and subsequent pathologic diagnosis could be determined.

RESULTS

In total, 2,390 unique articles were identified, with 66 articles meeting the criteria for full-text review and 14 articles included for analysis. A total of 1,150 dogs were evaluated, with 73.0% (840/1,150) of dogs being diagnosed with a malignant splenic lesion and 27.0% (310/1,150) being diagnosed with a benign splenic lesion. Of the malignancies, 87.3% (733/840) were hemangiosarcoma. Levels of evidence were low, and bias was high as most included studies were retrospective case series.

CLINICAL RELEVANCE

The double two-thirds rule should be refined when evaluating dogs with nontraumatic hemoperitoneum from a ruptured splenic mass, with more dogs being diagnosed with a malignancy and hemangiosarcoma specifically than the double two-thirds rule indicates. These findings may be useful in an emergency setting to guide owners on potential diagnoses for dogs with nontraumatic hemoperitoneum due to a ruptured splenic mass. However, there remains a portion of these dogs with benign conditions and nonhemangiosarcoma malignancies that may have a good long-term prognosis compared to dogs with hemangiosarcoma. Studies with higher levels of evidence, lower risks of bias, and large case numbers are needed in the literature.

Abstract

OBJECTIVE

To evaluate the validity of the double two-thirds rule for a diagnosis of splenic hemangiosarcoma in dogs with nontraumatic hemoperitoneum due to a ruptured splenic mass.

SAMPLE

Systematic literature review.

PROCEDURES

3 databases (PubMed, CAB abstracts, and World of Science) were searched in November 2020. Articles were included if data on dogs with nontraumatic hemoperitoneum due to a splenic mass were included and subsequent pathologic diagnosis could be determined.

RESULTS

In total, 2,390 unique articles were identified, with 66 articles meeting the criteria for full-text review and 14 articles included for analysis. A total of 1,150 dogs were evaluated, with 73.0% (840/1,150) of dogs being diagnosed with a malignant splenic lesion and 27.0% (310/1,150) being diagnosed with a benign splenic lesion. Of the malignancies, 87.3% (733/840) were hemangiosarcoma. Levels of evidence were low, and bias was high as most included studies were retrospective case series.

CLINICAL RELEVANCE

The double two-thirds rule should be refined when evaluating dogs with nontraumatic hemoperitoneum from a ruptured splenic mass, with more dogs being diagnosed with a malignancy and hemangiosarcoma specifically than the double two-thirds rule indicates. These findings may be useful in an emergency setting to guide owners on potential diagnoses for dogs with nontraumatic hemoperitoneum due to a ruptured splenic mass. However, there remains a portion of these dogs with benign conditions and nonhemangiosarcoma malignancies that may have a good long-term prognosis compared to dogs with hemangiosarcoma. Studies with higher levels of evidence, lower risks of bias, and large case numbers are needed in the literature.

Introduction

Splenic masses are common in dogs and can be of malignant or benign etiologies. The most common malignant diagnoses include hemangiosarcoma, lymphoma, and other sarcomas, while the most common benign diagnoses include hematoma, hyperplasia, and hemangioma.13 Diagnosis of the etiology of a canine splenic mass lesion prior to surgical excision via splenectomy and pathologic evaluation is currently not possible, as benign lesions are grossly indistinguishable from malignant lesions and no preoperative factors have been found to be sufficiently accurate for diagnosis. Although many clinical variables on their own are nonspecific for a diagnosis, 2 groups have reported on a combination of clinical variables that may be more specific for a diagnosis.4,5 The hemangiosarcoma likelihood score was developed for dogs with spontaneous hemoperitoneum by using patient body weight, total protein, platelet count, and thoracic radiographic findings to determine a patient’s risk of having a diagnosis of hemangiosarcoma.4 A second group developed a prediction tool for malignant or benign splenic masses by using information on serum total protein, nucleated RBC count, amount of abdominal effusion, number of splenic nodules, inhomogeneity of the splenic mass, diameter of the splenic mass, number of liver nodules, and whether mesenteric, omental, or peritoneal nodules were present.5 Although these models can be used to help owners understand the risk of a diagnosis of a malignant lesion, they are not definitive for any particular diagnosis.

Although blood tests such as flow cytometry for endothelial precursor cells and measurement of plasma vascular endothelial growth factor and thymidine kinase have been evaluated for ability to diagnose hemangiosarcoma, none of these tests are both sensitive and specific enough for a diagnosis of hemangiosarcoma.68 Other groups have evaluated circulating microRNAs for the diagnosis of hemangiosarcoma in dogs,912 but more work is needed in this area before this is useful clinically. Splenic aspirates may be unrewarding in attempts to achieve a diagnosis, as focal sampling may miss an area of interest, tissue architecture cannot be assessed with cytology, and blood contamination is common.3,13 Accuracy of cytology compared to histopathology for splenic lesions is 60% to 61%, although accuracy may be improved when evaluating nonneoplastic lesions.3,13 Mass rupture with subsequent hemorrhage and tumor seeding is a concern when aspirating splenic masses, although this complication was not reported in 1 study13 of splenic aspiration. Diagnostics such as contrast harmonic ultrasound, CT, and MRI may show characteristics that can differentiate malignant from benign lesions, but the availability of these techniques is limited and cost can be prohibitive in some cases.1418 Another group found that smaller masses compared to splenic volume were more likely to be hemangiosarcoma than benign lesions, but numerous factors can alter the size of the spleen, which could affect these measurements, and no optimal cutoffs for size were determined.19

In the absence of more definitive diagnostics prior to surgery, veterinarians frequently rely on the double two-thirds rule to guide owners on the probability of a malignant versus benign lesion and a diagnosis of hemangiosarcoma. This rule states that two-thirds of splenic masses will be malignant, and of those malignancies, two-thirds will be hemangiosarcoma.20 Although this rule seems to have originated for all splenic masses independent of the presence of hemoperitoneum, the double two-thirds rule more closely applies to dogs with hemoperitoneum due to their splenic mass based on the literature. Previous groups have identified that approximately 62.5% to 84.3% of dogs with hemoperitoneum due to a ruptured splenic mass have a malignancy, and of those, 85.1% to 100.0% have hemangiosarcoma.2,19,2124 A more favorable prognosis has been found for dogs with incidentally identified, nonruptured splenic masses, with 70.5% of dogs with nonruptured masses having benign lesions and only 17.1% having splenic hemangiosarcoma in 1 study.25 The objective of the current study was to systematically examine the peer-reviewed veterinary literature to assess the validity of the double two-thirds rule for dogs with hemoperitoneum due to a splenic mass. The hypothesis was that the double two-thirds rule would be accurate, with two-thirds of dogs with hemoperitoneum due to a splenic mass having a malignant lesion and two-thirds of those dogs having splenic hemangiosarcoma.

Materials and Methods

This systematic review was performed following Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines.26

Eligibility criteria

Peer-reviewed veterinary publications providing information on dogs with nontraumatic hemoperitoneum due to a splenic mass with subsequent information on pathologic diagnosis were evaluated. Publications were excluded if they were case reports, letters to the editor, abstracts without subsequent publication, conference proceedings notes, or book chapters or if the report was not in English. If information on the number of dogs with hemoperitoneum with each diagnosis could not be determined, the article was also excluded.

Information sources

One author (ARS) searched 3 databases (PubMed, CAB abstracts, and World of Science Core Collection) for relevant publications on November 24, 2020. Publication dates from January 1, 1905, to November 24, 2020, were considered for inclusion.

Search strategy

The following search terms were used: “hemoabdomen dog,” “hemoperitoneum dog,” “hemangiosarcoma dog,” “splenic mass dog,” “splenectomy dog,” “hemoabdomen canine” “hemoperitoneum canine,” “hemangiosarcoma canine,” “splenic mass canine,” and “splenectomy canine.”

Selection process

After identification of candidate articles, both authors (ARS and JAG) independently screened all results via evaluation of titles and abstracts for relevance. In cases of disagreement, discussion was used to reach a consensus on inclusion or exclusion in the full-text screening step. After this initial screening phase, both authors (ARS and JAG) independently screened full-text articles for inclusion or exclusion. If there was disagreement between the 2 authors, discussion was used to reach a consensus on inclusion or exclusion in the study.

Data collection process

Data extraction from included records was performed independently by both authors (ARS and JAG). After extraction, data were compared between authors and discussion was used to resolve any discrepancies. If data were unclear in the article, corresponding authors were contacted to request clarification.

Data items

Both authors (ARS and JAG) assessed each article for quantitative data relevant to the review. Requirements included dogs with a diagnosis of nontraumatic hemoperitoneum due to a splenic mass and information on the histopathologic diagnoses of the splenic mass lesions. The histopathologic diagnoses were categorized into benign lesions, hemangiosarcoma, and other malignancies (malignant tumors other than hemangiosarcoma). The numbers of dogs with each diagnosis were recorded. Studies were excluded that only reported dogs with certain diagnoses and/or were not all-inclusive in terms of possible diagnoses (eg, studies that only evaluated dogs with a certain malignancy or compared only hemangiosarcoma to hematoma without including other diagnoses).

Level of evidence

Each article was then assessed for level of evidence and classified on a scale of I to V using a previously defined, modified Oxford classification scheme.27,28 Grades were defined as grade I (randomized control trial, systematic review [grade Ia] or individual study [grade Ib]), grade II (cohort study, systematic review [grade IIa] or individual study [grade IIb]), grade III (case-control study, systematic review [grade IIIa] or individual study [grade IIIb]), grade IV (cohort or case-control study, lower-quality prospective study [grade IVa], retrospective study [grade IVb], or case series [grade IVc]), or grade V (expert opinion).

Study risk of bias assessment

The Cochrane Handbook for Systematic Reviews of Interventions29 was used as a guide to assess for overall risk of bias. Each of the following components was analyzed and categorized into low risk, moderate risk, high risk, and unclear risk for bias: selection bias, performance bias, attrition bias, and reporting bias. Following categorization, the overall risk for bias for each article was determined as either low, moderate, or high. For studies with a level of evidence of grade IV, overall risk bias was categorized as high.

Effect measures

The raw numbers and percentages for each diagnosis (hemangiosarcoma, benign lesion, and other malignancy) were calculated for each study.

Synthesis methods

Raw numbers for each included study were added together to determine overall raw numbers and percentages for each diagnosis across all included literature.

Results

Study selection

The initial database search yielded a total of 7,611 articles with 2,390 unique records and 66 articles meeting the inclusion criteria for full-text review (Supplementary Figure 1). In total, 14 studies2,19,2124,3037 were included and 52 studies were excluded (Supplementary Table S1).

Study characteristics

The characteristics and level of evidence of each included study were recorded. Twelve studies2,19,2224,3034,36,37 were retrospective case series assigned a level of evidence of grade IVc. Two studies21,35 were prospective studies assigned a level of evidence of grade IIb.

Risk of bias in studies

All retrospective studies had a high or uncertain risk of bias for all components. For the 2 prospective studies,21,35 selection bias was low risk, as case selection occurred consecutively in each study. Investigators were not blinded to diagnoses (high risk); however, all animals received the intervention (low risk) and the study protocol was adhered to for all enrolled patients (low risk), leading to a moderate risk of performance bias. Attrition bias was low risk as all animals completed the study protocol. Reporting bias was moderate for both studies due to lack of blinding. Overall bias for these 2 prospective studies was determined to be moderate.

Results of individual studies

For each included article, dogs diagnosed with hemoperitoneum secondary to a ruptured splenic mass were evaluated and diagnoses of a benign splenic lesion, hemangiosarcoma, or other malignancy were recorded (Table 1).

Table 1

Summary of diagnoses for splenic lesions in dogs presenting with nontraumatic hemoperitoneum due to a ruptured splenic mass from 14 articles included in the systematic review.

Article No. of dogs included Malignant mass Benign mass Hemangiosarcoma Other malignancy
Aronsohn23 44 63.6% (28/44) 36.4% (16/44) 100.0% (28/28) 0.0% (0/28)
Corbin30 23 56.5% (13/23) 43.5% (10/23) 69.2% (9/13) 30.8% (4/13)
Davies31 78 87.2% (68/78) 12.8% (10/78) 91.2% (62/68) 8.8% (6/68)
Fernandez32 115 66.1% (76/115) 33.9% (39/115) 78.9% (60/76) 21.1% (16/76)
Fleming24 210 84.3% (177/210) 15.7% (33/210) 88.7% (157/177) 11.3% (20/177)
Hammond22 71 76.1% (54/71) 23.9% (17/71) 92.6% (50/54) 7.4% (4/54)
Johnson33 39 94.9% (37/39) 5.1% (2/39) 89.2% (33/37) 10.8% (4/37)
Levinson34 28 78.6% (22/28) 21.4% (6/28) 81.8% (18/22) 18.2% (4/22)
Mallinckrodt19 40 65.0% (26/40) 35.0% (14/40) 92.3% (24/26) 7.7% (2/26)
Marino35 23 52.2% (12/23) 47.8% (11/23) 100.0% (12/12) 0.0% (0/12)
Sherwood36 91 76.9% (70/91) 23.1% (21/91) 82.9% (58/70) 17.1% (12/70)
Stewart21 40 62.5% (25/40) 37.5% (15/40) 96.0% (24/25) 4.0% (1/25)
Vnuk37 19 52.6% (10/19) 47.4% (9/19) 90.0% (9/10) 10.0% (1/10)
Wendelburg2 329 67.5% (222/329) 32.5% (107/329) 85.1% (189/222) 14.9% (33/222)
Total 1,150 73.0% (840/1,150) 27.0% (310/1,150) 87.3% (733/840) 12.7% (107/840)

Results of syntheses

In total, 1,150 dogs were diagnosed with hemoperitoneum secondary to a ruptured splenic mass. Overall, 73.0% (840/1,150) of dogs were diagnosed with a malignancy and 27.0% (310/1,150) were diagnosed with a benign lesion. Of the malignancies, 87.3% (733/840) were hemangiosarcoma.

Discussion

To the authors’ knowledge, this study was the first to systematically review the validity of the double two-thirds rule in dogs with nontraumatic hemoperitoneum from a ruptured splenic mass. Across the 1,150 dogs included in this review, 73.0% were diagnosed with a malignancy and, of those malignancies, 87.3% were hemangiosarcoma; therefore, the hypothesis that the double two-thirds rule would be accurate was rejected. The double two-thirds rule seems to have originated from all dogs presenting with a splenic mass, regardless of the presence of a concurrent hemoperitoneum.20 The authors chose to analyze cases diagnosed specifically with hemoperitoneum secondary to a ruptured splenic mass due to recent studies that report improved odds of a benign diagnosis in dogs without hemoperitoneum.25 It is possible that the double two-thirds rule may have been found to be more accurate if dogs without hemoperitoneum were included. However, these are 2 distinct populations of dogs and it may be preferable to be more specific because the influence of hemoperitoneum on the odds of diagnosis of hemangiosarcoma is well-known. Previous research has shown that 76.4% to 80.0% of dogs with malignant masses present with nontraumatic hemoperitoneum due to rupture of the mass, compared to only 29.6% to 56.0% of dogs with benign splenic masses.19,38 Previous studies have confirmed an association between hemoperitoneum,19,24,38 anemia,5,36 and thrombocytopenia4,5,22,36 and a diagnosis of hemangiosarcoma or splenic malignancy, consistent with dogs with hemangiosarcoma being more likely to present with hemoperitoneum.

No preoperative test has been identified that is both sensitive and specific enough for definitive diagnosis of a splenic mass prior to surgery. Because of this, the double two-thirds rule is one of the most helpful tools veterinarians have in guiding owners faced with pursuing surgery for or euthanasia of their dog with hemoperitoneum due to a ruptured splenic mass. These dogs are frequently presented on an emergent basis, displaying clinical signs associated with hypovolemic shock, and owners must make quick decisions about pursuing treatment. Therefore, it is important to be accurate in the prediction. Although the findings of this systematic review indicate that the risk of both malignant disease and hemangiosarcoma specifically are higher than previously thought, it is important to remember that there is still a percentage of dogs that will have benign disease or malignancies other than hemangiosarcoma, which may have a good long-term prognosis.

Limitations of this systematic review included that, even though a thorough, controlled electronic search of articles and manuscripts was performed using the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines, it is possible that some valuable reports were unknowingly excluded. Articles may also have been omitted if the title did not contain the specified search term. Only 14 reports over the chosen 115-year period met the final inclusion criteria despite the large number of publications identified with the search terms. Cases required histopathology postoperatively or following necropsy, and the report also needed to specify that the ruptured mass originated from a primary splenic lesion. In several reports, hemoperitoneum from nonsplenic causes were included and if the final diagnoses could not be specifically associated with the spleen, the report was excluded. Additionally, specifics on histopathologic assessment, such as evaluation of a sufficient number of sections39 or use of immunohistochemistry, could not be determined. Some of the studies had small case numbers, which could have affected final percentages for both benign and malignant lesions and resulted in bias. Twelve of the 14 reports included in the final systematic review were retrospective in nature, which increased the overall bias and decreased the level of evidence. Therefore, higher-quality studies with larger case numbers may be needed to establish the true likelihood of a particular diagnosis.

The double two-thirds rule may need to be refined when evaluating dogs with nontraumatic hemoperitoneum from a ruptured splenic mass. Results of this study showed that 73.0% of dogs with a nontraumatic hemoperitoneum due to rupture of a splenic mass were diagnosed with a malignancy, and of the malignancies, 87.3% were hemangiosarcoma. This information can be used by veterinarians to help guide owners for treatment decisions in dogs with nontraumatic hemoperitoneum due to a ruptured splenic mass.

Supplementary Materials

Supplementary materials are posted online at the journal website: avmajournals.avma.org

Acknowledgments

No third-party funding or support was received in connection with this study or the writing or publication of the manuscript. The authors declare that there were no conflicts of interest.

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