Skip to main content

Main menu

  • Home
  • Current Issue
  • Content
    • Current Issue
    • Early Access
    • Multimedia
    • Podcast
    • Collections
    • Past Issues
    • Articles by Subject
    • Articles by Type
    • Supplements
    • Plain Language Summaries
    • Calls for Papers
  • Info for
    • Authors
    • Reviewers
    • Job Seekers
    • Media
  • About
    • Annals of Family Medicine
    • Editorial Staff & Boards
    • Sponsoring Organizations
    • Copyrights & Permissions
    • Announcements
  • Engage
    • Engage
    • e-Letters (Comments)
    • Subscribe
    • Podcast
    • E-mail Alerts
    • Journal Club
    • RSS
    • Annals Forum (Archive)
  • Contact
    • Contact Us
  • Careers

User menu

  • My alerts

Search

  • Advanced search
Annals of Family Medicine
  • My alerts
Annals of Family Medicine

Advanced Search

  • Home
  • Current Issue
  • Content
    • Current Issue
    • Early Access
    • Multimedia
    • Podcast
    • Collections
    • Past Issues
    • Articles by Subject
    • Articles by Type
    • Supplements
    • Plain Language Summaries
    • Calls for Papers
  • Info for
    • Authors
    • Reviewers
    • Job Seekers
    • Media
  • About
    • Annals of Family Medicine
    • Editorial Staff & Boards
    • Sponsoring Organizations
    • Copyrights & Permissions
    • Announcements
  • Engage
    • Engage
    • e-Letters (Comments)
    • Subscribe
    • Podcast
    • E-mail Alerts
    • Journal Club
    • RSS
    • Annals Forum (Archive)
  • Contact
    • Contact Us
  • Careers
  • Follow annalsfm on Twitter
  • Visit annalsfm on Facebook
Research ArticleOriginal Research

Potential for Reducing Time to Referral for Colorectal Cancer Patients in Primary Care

Nicole F. van Erp, Charles W. Helsper, Saskia M. Olyhoek, Ramon R. T. Janssen, Amber Winsveen, Petra H. M. Peeters and Niek J. de Wit
The Annals of Family Medicine September 2019, 17 (5) 419-427; DOI: https://doi.org/10.1370/afm.2446
Nicole F. van Erp
Julius Centre for Health Sciences and Primary Care, University Medical Centre Utrecht, Utrecht University, Utrecht, The Netherlands
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Charles W. Helsper
Julius Centre for Health Sciences and Primary Care, University Medical Centre Utrecht, Utrecht University, Utrecht, The Netherlands
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: C.W.Helsper-2@umcutrecht.nl
Saskia M. Olyhoek
Julius Centre for Health Sciences and Primary Care, University Medical Centre Utrecht, Utrecht University, Utrecht, The Netherlands
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Ramon R. T. Janssen
Julius Centre for Health Sciences and Primary Care, University Medical Centre Utrecht, Utrecht University, Utrecht, The Netherlands
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Amber Winsveen
Julius Centre for Health Sciences and Primary Care, University Medical Centre Utrecht, Utrecht University, Utrecht, The Netherlands
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Petra H. M. Peeters
Julius Centre for Health Sciences and Primary Care, University Medical Centre Utrecht, Utrecht University, Utrecht, The Netherlands
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Niek J. de Wit
Julius Centre for Health Sciences and Primary Care, University Medical Centre Utrecht, Utrecht University, Utrecht, The Netherlands
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • Article
  • Figures & Data
  • eLetters
  • Info & Metrics
  • PDF
Loading

Article Figures & Data

Figures

  • Tables
  • Additional Files
  • Figure 1
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure 1

    Flowchart for CRC patient selection.

    CRC = colorectal cancer; GP = general practitioner.

  • Figure 2
    • Download figure
    • Open in new tab
    • Download powerpoint
    Figure 2

    Factors contributing to longest duration (≥219 days) for symptomatic CRC patients.a

    CRC = colorectal cancer; RBL = rectal blood loss.

    aThe Venn diagram circles do not illustrate the relative sizes of groups.

Tables

  • Figures
  • Additional Files
    • View popup
    Table 1

    Disease Characteristics of Symptomatic CRC Patients Referred by GP (N = 309)

    CharacteristicNo. (%)
    TNM stage at diagnosis
     01 (0.3)
     I41 (13.3)
     II83 (26.9)
     III114 (36.9)
     IV65 (21.0)
     Unknown5 (1.6)
    Tumor location
     Proximal colon90 (29.1)
     Distal colon20 (6.5)
      (Recto)sigmoid99 (32.0)
     Rectal97 (31.4)
     Colon unspecified3 (1.0)
    • CRC = colorectal cancer; GP = general practitioner; TNM = tumor, nodes, metastases.

    • View popup
    Table 2

    Patient and Presentation Characteristics of Symptomatic CRC Patients, Duration of Primary Care Interval, and Log-Binomial Regression Analysis for 75th Percentile (N = 309)

    CharacteristicNo.Duration, d, Median (IQR)P ValueaP90bUnivariable RR (95% CI)Multivariable RR (95% CI)
    Age, y
    ≤503534 (1-233)4911.5 (0.8-3.0)
    51-60473 (1-15)4080.6 (0.3-1.4)
    61-7010014 (1-47)940.8 (0.4-1.4)
    71-80916 (1-61)2040.9 (0.5-1.7)
    81-90368 (1-68).1541501 (ref)
    Sex
    Male1554 (1-47)1011 (ref)1 (ref)
    Female15413 (1-78).0043211.6 (1.1-2.4)1.4 (0.9-2.1)
    SES 2010c
    Low8112 (1-72)2401 (ref)
    Medium-low799 (1-63)2390.9 (0.5-1.5)
    Medium-high737 (1-51)1180.7 (0.4-1.3)
    High766 (1-47).5512230.7 (0.4-1.2)
    Registered comorbidityd
    Chronic somatic
     No625 (1-48)3261 (ref)
     Yes24710 (1-61).3171981.1 (0.7-1.9)
     ≥21819 (1-58)2031.1 (0.6-1.8)
     ≥4708 (1-43)980.9 (0.5-1.7)
    Gastrointestinal
     No2568 (1-63)2191 (ref)
     Yes5315 (2-48).6221190.7 (0.4-1.3)
    Psychiatric
     No2908 (1-58)2041 (ref)
     Yes1922 (2-84).2035381.1 (0.5-2.3)
    Registered family history of CRCe
    Not registered26711 (1-65)2331 (ref)
    Negative301 (1-13)870.5 (0.2-1.3)
    Positive122 (1-34).003870.3 (0.1-2.0)
    Consultation frequency for year prior to first CRC consultation
    ≤2562 (1-29)1171 (ref)
    3-1118811 (1-64)2351.4 (0.8-2.5)
    ≥126512 (1-54).0931201.2 (0.6-2.3)
    History of malignancy
    No2677 (1-50)2191 (ref)1 (ref)
    Yes4218 (2-84).1011781.7 (1.1-2.6)1.5 (0.9-2.2)
    Main registered symptom at first CRC consultationf
    Alarm GI symptom(s)1682 (1-28)1231 (ref)1 (ref)
    Nonalarm GI symptom(s)11326 (5-87)2571.9 (1.2-2.8)1.7 (1.1-2.6)
    Other symptom(s)2813 (2-43).0002730.9 (0.4-2.2)0.9 (0.4-2.1)
    Hemorrhoids at physical examinationg
    No2988 (1-54)2191 (ref)
    Yes1169 (1-115).1922132.3 (1.3-4.1)
    TNM stage at diagnosis
    0187……
    I412 (1-42)831 (ref)
    II837 (1-48)2131.1 (0.5-2.3)
    III1147 (1-48)1591.1 (0.5-2.2)
    IV6523 (3-92)5021.9 (0.9-3.8)
    Unknown55 (1-246).013……
    • CRC = colorectal cancer; GI = gastrointestinal; GP = general practitioner; IPC = primary care interval; IQR = interquartile range; P75 = 75th percentile value of the duration distribution; P90 = 90th percentile value of the duration distribution; RR = relative risk; SES = socioeconomic status score; TNM = tumor, nodes, metastases.

    • ↵a P values based on Mann-Whitney U tests for variables with 2 categories and Kruskall-Wallis tests for variables with 3 or more categories.

    • ↵b P90 value = 90th percentile value of the duration distribution; that is the IPC duration time in days where 90% of the population was below and 10% above.

    • ↵c Socioeconomic status scores 2010 were retrieved from publicly available data from the Netherlands Institute for Social Research.16 Lowest SES score was defined as: SES score of <1 SD than the Dutch mean of 2010, Medium-low: 1 SD to mean SES score, Medium-high: mean SES score to +1 SD and Highest: > +1 SD higher than Dutch mean.

    • ↵d Chronic somatic comorbidities were defined according to O’Halloran et al.17 Gastrointestinal comorbidities were all relevant GI-related registered comorbidities or conditions in either episode list or mentioned during GP consultations: irritable bowel syndrome, reflux disease, esophagitis, dyspepsia, abdominal pain, peptic ulcer, hiatus or abdominal hernia, benign GI neoplasms/polyps, constipation, chronic diarrhea, cholelithiasis, diverticulosis, anal fissures. Psychiatric comorbidities were all chronic psychiatric comorbidities according to O’Halloran et al.17

    • ↵e Registered occurrence of colorectal cancer in a first degree family member.

    • ↵F Alarm symptoms for colorectal cancer were defined as rectal blood loss, unintended weight loss, anemia, and a palpable tumor. GI symptoms include all GI-related, nonalarming symptoms. Other symptoms are all remaining, nonalarming, non-GI symptoms.

    • ↵g Multivariable model excludes this factor due to low patient numbers.

Additional Files

  • Figures
  • Tables
  • Supplemental Appendix

    Supplemental appendix

    Files in this Data Supplement:

    • Supplemental data: Appendix - PDF file
  • The Article in Brief

    Potential for Reducing Time to Referral for Colorectal Cancer Patients in Primary Care

    Charles W. Helsper , and colleagues

    Background Delay in referral to specialty care for patients who have symptoms of colorectal cancer may lead to poor health outcomes. While the current median duration from first consultation with cancer related complaints to referrals is approximately one week for colorectal cancer patients in the UK and the Netherlands, time to referral varies strongly. Some cases document months and even years before referral, and explanations for suboptimal referral is often incomplete or oversimplified.

    What This Study Found A retrospective cohort study in the Netherlands reviewed the time to specialty referral for a group of 309 patients with colorectal cancer who initially presented with symptoms to their primary care doctor. A multivariable analysis narrowed down the factors associated with delays in referrals to specialty care. Those who initially presented with red flag symptoms, such as rectal bleeding or unintended weight loss, experienced shorter wait time than those who presented with non-alarming gastrointestinal symptoms. Univariable analysis showed that female patients and patients without a registered family history of the disease were also more likely to have a longer wait period. Of the 10% of patients with the longest wait times for referral to specialty care all patients had received an alternative initial diagnosis from their primary care physicians. These patients usually presented with conditions that obscured concern for colorectal cancer, such as hemorrhoids, fissures and inflammatory bowel disease. Initial diagnoses were not always reconsidered when complaints persisted and follow-up consultations were sometimes omitted.

    Implications

    • This study points to a relationship between long time to referral of colorectal cancer in primary care and low cancer suspicion. There is potential for reducing longest times to referral of colorectal cancer patients in primary care by earlier reconsideration of the initial hypothesis and implementing strict follow-up consultations.
  • Visual Abstract

    Files in this Data Supplement:

    • Adobe PDF - visual_abstract_van_erp_sept_2019.png.pdf
PreviousNext
Back to top

In this issue

The Annals of Family Medicine: 17 (5)
The Annals of Family Medicine: 17 (5)
Vol. 17, Issue 5
September/October 2019
  • Table of Contents
  • Index by author
  • Back Matter (PDF)
  • Front Matter (PDF)
  • In Brief
Print
Download PDF
Article Alerts
Sign In to Email Alerts with your Email Address
Email Article

Thank you for your interest in spreading the word on Annals of Family Medicine.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
Potential for Reducing Time to Referral for Colorectal Cancer Patients in Primary Care
(Your Name) has sent you a message from Annals of Family Medicine
(Your Name) thought you would like to see the Annals of Family Medicine web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
12 + 8 =
Solve this simple math problem and enter the result. E.g. for 1+3, enter 4.
Citation Tools
Potential for Reducing Time to Referral for Colorectal Cancer Patients in Primary Care
Nicole F. van Erp, Charles W. Helsper, Saskia M. Olyhoek, Ramon R. T. Janssen, Amber Winsveen, Petra H. M. Peeters, Niek J. de Wit
The Annals of Family Medicine Sep 2019, 17 (5) 419-427; DOI: 10.1370/afm.2446

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Get Permissions
Share
Potential for Reducing Time to Referral for Colorectal Cancer Patients in Primary Care
Nicole F. van Erp, Charles W. Helsper, Saskia M. Olyhoek, Ramon R. T. Janssen, Amber Winsveen, Petra H. M. Peeters, Niek J. de Wit
The Annals of Family Medicine Sep 2019, 17 (5) 419-427; DOI: 10.1370/afm.2446
Twitter logo Facebook logo Mendeley logo
  • Tweet Widget
  • Facebook Like
  • Google Plus One

Jump to section

  • Article
    • Abstract
    • INTRODUCTION
    • METHODS
    • RESULTS
    • DISCUSSSION
    • Acknowledgments
    • Footnotes
    • References
  • Figures & Data
  • eLetters
  • Info & Metrics
  • PDF

Related Articles

  • PubMed
  • Google Scholar

Cited By...

  • Exploring why European primary care physicians sometimes do not think of, or act on, a possible cancer diagnosis. A qualitative study
  • Measurement of clinical delay intervals among younger adults with colorectal cancer using health administrative data: a population-based analysis
  • Role of primary care physician factors on diagnostic testing and referral decisions for symptoms of possible cancer: a systematic review
  • Factors affecting the decision to investigate older adults with potential cancer symptoms: a systematic review
  • Multilevel Approaches to Reducing Diagnostic and Treatment Delay in Colorectal Cancer
  • Google Scholar

More in this TOC Section

  • Shared Decision Making Among Racially and/or Ethnically Diverse Populations in Primary Care: A Scoping Review of Barriers and Facilitators
  • Convenience or Continuity: When Are Patients Willing to Wait to See Their Own Doctor?
  • Feasibility and Acceptability of the “About Me” Care Card as a Tool for Engaging Older Adults in Conversations About Cognitive Impairment
Show more Original Research

Similar Articles

Subjects

  • Domains of illness & health:
    • Acute illness
    • Chronic illness
    • Disease pathophysiology / etiology
    • Prevention

Keywords

  • colorectal cancer
  • delayed diagnosis
  • early diagnosis
  • general practice
  • primary health care

Content

  • Current Issue
  • Past Issues
  • Early Access
  • Plain-Language Summaries
  • Multimedia
  • Podcast
  • Articles by Type
  • Articles by Subject
  • Supplements
  • Calls for Papers

Info for

  • Authors
  • Reviewers
  • Job Seekers
  • Media

Engage

  • E-mail Alerts
  • e-Letters (Comments)
  • RSS
  • Journal Club
  • Submit a Manuscript
  • Subscribe
  • Family Medicine Careers

About

  • About Us
  • Editorial Board & Staff
  • Sponsoring Organizations
  • Copyrights & Permissions
  • Contact Us
  • eLetter/Comments Policy

© 2025 Annals of Family Medicine